As crucial terrestrial ecosystems, temperate forests play an important role in global soil carbon dioxide flux and this process can be sensitive to atmospheric nitrogen deposition. It is often reported that the nitrogen addition induces a change in soil carbon dioxide emission in growing season. However, the important effects of interactions between nitrogen deposition and the freeze-thaw-cycle have never been investigated. Here we show nitrogen deposition delays spikes of soil respiration and weaken soil respiration. We found the nitrogen addition, time and nitrogen addition×time exerted the negative impact on the soil respiration of spring freeze-thaw periods due to delay of spikes and inhibition of soil respiration (p < 0.001). The values of soil respiration were decreased by 6% (low-nitrogen), 39% (medium-nitrogen) and 36% (high-nitrogen) compared with the control. And the decrease values of soil respiration under medium- and high-nitrogen treatments during spring freeze-thaw-cycle period in temperate forest would be approximately equivalent to 1% of global annual C emissions. Therefore, we show interactions between nitrogen deposition and freeze-thaw-cycle in temperate forest ecosystems are important to predict global carbon emissions and sequestrations. We anticipate our finding to be a starting point for more sophisticated prediction of soil respirations in temperate forests ecosystems.
Carbon (C) cycles are increasingly paid attention under global climate change. Freeze-thaw-cycle (FTC) significantly affects soil C cycles as a crucial ecological process1,2,3 due to its more frequent appearance under global climate change4,5,6. Therefore FTC is recognized as crucial ecological processes and has received increased attention. Studying on the impacts of FTC on soil C dynamic is beneficial to the further understanding of soil C cycle and their feedback to climate change.
Many previous studies have pointed out that the FTC-induced enhancement of carbon dioxide (CO2) emission was often observed7,8,9,10,11,12,13,14,15,16,17,18. Wang et al.16 showed that the ephemeral burst of CO2 occurred at the early stage of spring FTC period in a temperate forest. Song et al.15 found the high emission peaks of CO2 during FTC period in a freshwater marsh. Wang et al.17 suggested that FTC play an important role in soil CO2 emissions in a wet meadow. In addition, the CO2 emission peaks during the FTC period were also detected in some laboratory incubations10,19, which are consistent with most of the field studies. However, different conclusions have been also reported. For example, the FTC had no a significantly impact on CO2 emission in broadleaf forests or it reduced the release of CO2 in grassland20,21. The emission of CO2 from soil is one of major C exchanges between terrestrial ecosystems and the atmosphere22. With global climate change, less snowfall and warming may lead to increasing the frequency and intensity of FTC and then may cause the increase of CO2 emission from soil to atmosphere. Sullivan et al.23 suggested that the pulses of CO2 caused by FTC are jointly driven by biological and physical factors. Several potential mechanisms have been proposed to clarify the FTC-induced enhancement of CO2 emissions: (1) burst of CO2 during the FTC period largely resulted from the release of trapped CO2 in the winter7; (2) increased CO2 emissions may be due to enhancing microbial metabolism by substrate supply in the FTC period21; (3) increased substrates leaching from the litter layer accumulated during the winter might lead to CO2 burst24. Currently, there are still many uncertainties in the mechanisms of these increased CO2 fluxes25. The first objective of our study was to examine the impact of spring FTC on the soil CO2 emissions in the temperate forest and then to investigate the mechanisms potentially inducing FTC period CO2 emissions.
In addition, atmospheric nitrogen (N) deposition is another important factor to soil C cycle, because the cycles of soil C and N are closely coupled26,27,28. Some previous studies showed that simulated N addition had significantly increase release of CO2 29. Nevertheless, other studies found controversial affecting soil CO2.fluxes in terrestrial ecosystem30,31. The different responses of soil CO2 fluxes to N addition have been reported in the different ecosystem, including increases26, decreases32 and no significant differences33,34. Summary, most of the high concentration N deposition may limit CO2 release and low concentration may promote or no changes. Several potential mechanisms have been proposed to clarify the N-induced change of CO2 emissions: (1) N inhibition of lignin degradation largely resulted from change of microbial composition35; (2) change of CO2 emissions may be due to ecological shifts in the soil microbiota under N deposition36; (3) the coupling of soil carbon and nitrogen was broken due to N deposition, which might lead to change of CO2 emission37. Although the effect of FTC on C cycles and the effect of atmospheric N deposition on C cycles have been investigated, respectively28,38,39, the effect of FTC together with atmospheric N deposition on C cycles has never been reported. We hypothesized that soil respiration (Rs) could have a special response pattern to N deposition due to the changes of soil physicochemical properties and microbial characteristic in the FTC period. The second objective of our study was to examine the impact of simulated N deposition together with spring FTC on soil CO2 fluxes in temperate forest.
The major objective of this paper was to evaluate the change quantities of CO2 due to N deposition addition in FTC period in temperate forests which cover 9.7% of the earth’s continental surface40. We hypothesized that N deposition would inhibit CO2 emissions via delay burst or decrease fluxes in spring FTC period in temperate forest. In addition, previous studies did not show an understandable mechanism regarding impact of FTC and N deposition on CO2 fluxes. The FTC and N deposition could affect the soil biological and physicochemical processes leading to C dynamic change. Therefore, we conducted a simulated N deposition experiment from May 2010 to present and investigated the interactive effects of N deposition and spring FTC on soil C fluxes in a temperate forest and the potential mechanisms in 2015.
Materials and Methods
This study was conducted at the Fenglin Natural Reserve of Lesser Khingan Mountains in Heilongjiang province, Northeast China (48°02′–48°12′ N, 128°58′–129°15′ E). The climate is continental monsoon climate, with dry, cold winters and humid, warm summers. The forests had a mean annual temperature of −0.5 °C from 1959 to 2013, with the lowest and highest monthly mean air temperature being −25.6 °C in January to 23.8 in July, respectively. The mean annual precipitation is 728 mm, of which approximately 75% falls between July and August. The snowpack lasted for 148 days with the snow depth ranging from 0 to 42 cm during the measurement years (Nov, 2014–Mar, 2015). The soil is classified as a dark brown forest soil41. The vegetation type is a cold-temperate spruce-fir Korean pine forest with the age of exceeded 200 years. The community is dominated by Picea koraiensis, Abies nephrolepis and Pinus koraiensis. The mean stand density is 972 ± 96 trees ha−1, the mean diameter at breast height is 13.7 ± 7.5 cm and the mean tree height is 16.7 ± 5.3 m. The major species in the canopy layer are Pinus koraiensis, Abies nephrolepis, Picea koraiensis, Picea jezoensis var. microsperma, Larix gmelini, Betula platyphylla, Acer mono, Fraxinus mandshurica and Betula costata.
To investigate changes in soil CO2 fluxes (Rs) following N application, we established three random blocks in May 2010 and each consisting of four research plots measuring 20 m × 20 m. The plots were separated by 10 m wide buffer strips to avoid horizontal movement of the soil N. The simulated N deposition was initiated at the onset of this experiment and included four treatments, control (no added N), low-N (5 g N.m−2.yr−1), medium-N (10 g N.m−2.yr−1) and high-N (15 g N.m−2.yr−1), with three replicates randomly distributed at each treatment. The N was applied as ammonium nitrate (NH4NO3) solution and was distributed on six occasions during annual growing season applied to the forest floor every half a month during the growing season (May to October) from 15th May 2010. In each plot, the NH4NO3 was mixed with 32 L of water (equal to 0.08 mm annual precipitation) and applied by using a backpack sprayer below the canopy. Two passes were made across each plot to ensure an even distribution of the fertilizer. The control plots received 32 L water without N addition. The simulated N deposition was applied from May 2010 to the present.
Soil CO2 fluxes measurements during spring FTC period
The spring FTC period soil CO2 fluxes (Rs) were measured every day from April 1st to May 5th 2015. For each of 12 plots, three polyvinyl Chloride (PVC) collars (20 cm inside diameter and 12 cm in height) were randomly inserted approximately 9 cm into the soil, with 3 cm left above the ground surface for Rs measurements, one week before N addition in 2010. A total of 36 soil collars were installed. The collars were left in the same place throughout the entire study period for exploring the change of the spring FTC period in Rs. The Rs was measured with a Li-8100 automated soil CO2 flux system (Li-Cor Inc, Lincoln, NE, USA) between 10:00–14:00 in spring FTC period. Each measurement was repeated 3 times for each collar to produce a collar’s mean Rs rate. Rs were calculated using exponential regression model with the LI-8100 file viewer application software (LI-8100/8150 Instruction Manual).
Soil physical and chemical properties and microbial characteristic measurements
The soil temperature at 5 cm depth (T5) and soil volumetric water content at the 5 cm depth (W5, % v/v) were monitored simultaneously with the measurement of Rs by using a soil temperature probe (Omega Engineering Inc. USA) and soil moisture probes (Deltat Devices Ltd., Cambridge, England) connected to Li-8100. The continuous soil temperature at 5 cm depth (T5cm) was monitored hourly by Em-50 data logger (Decagon Devices, Inc. USA) The air temperature (Ta) was same measured hourly by Em-50 data logger (Decagon Devices, Inc. USA).
During the measurement of Rs, because of the difficulty in collecting soil samples from frozen soil, all soil samples were collected days nearly the soil collars from a depth of 0–10 cm using a specially designed auger (2.5 cm in diameter). Three soil cores were collected and pooled to one composite sample at each plot. All of the visible extraneous materials (such as roots, stones, etc.) were removed by hand and then divided the composite sample into three sub-samples. One sub-sample was air-dried at ambient temperature and then sieved (2 mm) and ground for the analysis of soil total C and total N by using an automated TOC/TN analyzer (multi N/C3100, Analytikjene AG, Germany). In addition, soil pH values were measured by a pH meter (SX7150, China) with soil: water ratio of 1:2.5. The second sub-sample was maintained original state and taken back to laboratory. Thawed soils were mixed, whereas frozen soil was reduced to small pieces, with the pieces being homogenized to the extent possible42. Immediately following, the inorganic N concentrations were determined by extracting fresh soil with K2SO4. The extractable NH4+-N concentrations were measured by using the indophenol blue method, followed by the colorimetric analysis. The NO3−-N content was determined by using the copper-cadmium reduction method. The third sub-sample was also maintained original states and taken back to the laboratory immediately to assess microbial biomass C (MBC) and N (MBN). The MBC and MBN were measured by using a fumigation-extraction method43. The extracts of N and C from fumigated and unfumigated samples were analysed by an automated TOC/TN analyzer (multi N/C3100, Analytikjene AG, Germany). The MBN and MBC were calculated from the difference between extractable N and C contents in the fumigated and the unfumigated samples using conversion factors (kEN and kEC) of 0.45 and 0.38, respectively43. All extraction for NO3-N, NH4-N, MBC and MBN was done with K2SO4 of 0.5 mol l−1 in 25 °C and the duration of extraction was half an hour.
Dividing the year into spring FTC period and Statistical analyses
The spring FTC period was defined as the period that starts when soil surface snow is start to melt (the maximum Ta is above 0 °C) and ends when daily minimum T5cm is above 0 °C16. The spring FTC period lasted for 35 days (DOY 90–124 in 2015) in this study.
To assess the quantity of Rs under different N addition level in the FTC periods, Rs-T models were constructed. Compared to the several commonly used models, such as the modified van’t Hoff’s model44, the sigmoid-shaped Lloyd-Taylor45 and logistic models46, the Gamma model performed either better or as good as the other models47. In addition, Gamma model were tested across a wide Ts range (−18–35 °C) and can also be expanded, using simple mathematics to help researchers analyse the Rs-T relationship in the context of other environment factors, such as soil nutrients47. The Gamma model was adopted based on R2 and the Akaike Information Criterion (AIC). Therefore, Gamma model used to assess the impact of different quantities of N additions on Rs during the FTC period.
Gamma model was expressed as following:
where T is (T5cm + 40), a, b and c are regression coefficients. T5cm is measured soil temperature under 5 cm below surface. 40 °C is added to T5cm because negative T5cm results in negative or imaginary Rs (or non-meaningful Rs) and 40 °C has been chosen as the lowest T5cm where Rs continues has been measured at −39 °C. The natural logarithm (Ln) transformed version of the Rs data was applied to alleviate the heteroscedasticity problem.
Two-ways analysis of variance was used to examine the impacts of different quantities N deposition, spring FTC and their interactions on soil total C, total N, NH4+-N, NO3−-N, soil pH values, MBC, MBN. Fisher’s LSD followed the two-way analysis of variance between the N treatments. Tukey’s HSD tests were used to reveal the significant pairwise differences of the N addition. Pearson’s correlation analysis was used to determine the correlations between Rs and soil properties or microbial characteristics. Statistically significant differences were accepted at p < 0.05. All statistical analyses were performed using R 3.2.2 Version Software (R Development Core Team 2015).
Effects of spring FTC, N deposition and their interaction on Rs
At the beginning of the spring FTC period, the daily maximum Ta was above 0 °C, but all of T5cm were below 0 °C (Fig. 1(a)) and the snow was melting. However, the Rs remained at a low level (Fig. 1(b)) and the Rs under medium-N and high-N treatments was significantly lower than control and low-N treatments at the early stage of the spring FTC period (Fig. 1(b)). The significant differences in Rs were observed on next period of time and temporal peaks of Rs occurred. The ephemeral burst of Rs observed from DOY 97 to DOY 102 under control treatments and lasted for 6 days, with the maximum Rs of 0.83 μmol m−2 s−1 (Fig. 1(b)). Simultaneously, we observed the high Rs occurred from DOY 98 to DOY 102 under low-N treatments and lasted for 5 days, with the maximum Rs of 0.76 μmol m−2 s−1 (Fig. 1(b)). During the period, the daily mean of air temperature and the mean of soil temperature in 5 cm depth increased continuously (Fig. 1(a)). The snowpack had melted completely. But, the ephemeral enhancement of Rs occurred at later stage of the spring FTC and lasted for 5 days (DOY 107–111) under medium-N and high-N treatments (Fig. 1(b)). The Rs pulse lasted for a short time period and after that the rate decreased to the normal status during the spring FTC period. During most of observation period, the Rs increased with temperature.
The effects of different quantity of N addition on Rs were highly variable during spring FTC period. During the measurement period, the mean of Rs was 0.58, 0.57, 0.47, 0.48 μmol m−2 s−1 for different quantity of N addition, i.e., control, low-N, medium-N, high-N treatments, respectively (Table 1). Our results found that the simulated N deposition had significantly impact on the Rs due to inhibiting CO2 fluxes or delaying outburst event (Table 1; Fig. 1(b)). Likewise, the FTC also had a significantly impact on Rs (Table 2), which varied from 0.32 to 1.06 μmol m−2 s−1 and showed the high fluctuations under natural status (control plots) (Fig. 1(b)). In addition, Rs was also significantly affected by the interaction of the simulated N deposition and spring FTC (p < 0.001) (Table 2). In general, the two-way ANOVA analysis showed that the simulated N deposition, the spring FTC and their interaction exhibited significant effects (p < 0.001) on the Rs during the whole measurement period (Table 2).
Spring FTC period contribution of Rs to the winter and annual budget and assessing the future C dynamic in temperate forest
Applying the empirical Rs-T models assessed the quantities of Rs under different N addition levels (i.e., control, low-N, medium-N, high-N) during the spring FTC period. The ordinary least squares was used to calculate the coefficients (i.e., a, b, c), similar to what was performed in the Khomik 2009 Gamma model paper (Table 3). The predicated spring FTC period Rs was 17.53 ± 0.43 g C m−2 yr−1 in this temperate forest without N addition (Table 1). Low-N treatment exerted negative effects on spring FTC Rs and its value was 16.44 ± 0.58 g C m−2 yr−1 (Table 1). The cumulative Rs during the spring FTC period were 10.67 ± 0.75 g C m−2 yr−1 in medium-N plots and 11.24 ± 0.69 g C m−2 yr−1 in high-N plots (Table 1). In general, the N addition exerted a negative impact on spring FTC Rs and decreased it by 6% (low-N), 39% (medium-N) and 36% (high-N) compared with the control. The predicted annual Rs was 974.3 ± 67.1 g C m−2 yr−1 without N addition treatment; the values of Rs in winter were 46.8 g C m−2 yr−1 (control), 35.7 g C m−2 yr−1 (low-N), 41.89 g C m−2 yr−1 (medium-N) and 62.35 g C m−2 yr−1 (high-N)48. Under different quantities of N addition, the cumulative Rs during spring FTC period contributed 37.49% (control), 46.88% (low-N), 25.50% (medium-N) and 18.03% (high-N), respectively, to the winter Rs and contributed 1.80% (control), 1.69% (low-N), 1.10% (medium-N) and 1.15% (high-N), respectively, to the annual Rs (Fig. 2).
The Fenglin Natural Reserve (our study site) covered an area of 18165 hm2. We hypothesized that whole Reserve was used to simulate the impact of N addition on Rs. The Rs in the study area was reduced by 1.97 × 10−4 Tg C yr−1 (low-N), 1.25 × 10−3 Tg C yr−1 (medium-N) and 1.14 × 10−3 Tg C yr−1 (high-N) during the spring FTC period. The temperate forest covers 9.7% of the earth’s continental surface40. The temperate forest covered an area of 14.5 million km2. The Rs in whole temperate forest would be reduced by 15.81 Tg C yr−1 (low-N), 99.47 Tg C yr−1 (medium-N) and 91.21 Tg C yr−1 (high-N) during the spring FTC period. Global total CO2 emission (excluding Land-use Change and Forestry) cumulative value was 33843.05 Mt (about 9229.92 Tg C) in 2012 49. The decrease values of Rs under medium- and high-N treatments during spring FTC period in temperate forest would be approximately equivalent to 1% of global annual C emissions.
Relationships between spring FTC Rs and soil biochemical property
The mean values of soil biochemical property were summarized in Table 4. The correlation analyses between Rs and soil biochemical property were performed to attempt to explain the observed changes in Rs during spring FTC period. But we only found the Rs and the soil NH4+-N, the soil NO3−-N, the soil MBC and the soil MBN are related. The Rs was positively correlated with the soil MBC and MBN during the spring FTC period (Fig. 3a,b). But, the Rs was positively correlated with the lower concentrations of the soil NH4+-N and the soil NO3−-N and negatively correlated with the higher concentrations of the soil NH4+-N and the soil NO3−-N during spring FTC period (Fig. 3c,d). We made the best fitting equation of the Rs and the soil biochemical property. The Rs increased linearly with the soil MBC (y = 0.47x − 0.21, R2 = 0.75, p < 0.01, y was defined as Rs values, x was defined as MBC values) and the soil MBN (y = 4.07x − 1.83, R2 = 0.74, p < 0.01, y was defined as Rs values, x was defined as MBN values). The Rs decreased exponentially with the soil NO3−-N concentrations (y = 0.70e−0.03x, R2 = 0.63, p < 0.01, y was defined as Rs values, x was defined as soil NO3−-N concentrations). The Rs changed irregularly with the soil NH4+-N concentrations (y = 139.55x2−139.89x + 64.82, R2 = 0.33, p < 0.05, y was defined as Rs values, x was defined as soil NH4+-N concentrations).
We found that the ephemeral spikes of Rs occurred in control plots (without N addition) at the early stage of the spring FTC period, which was consistent with some previous observation16,19,25. At the beginning of the outburst, the snow was completely melted. And, the soil microbes can recover rapidly from disturbance resulting from freezing50. Therefore, we conjectured that microbial activity and biomass may increase via enhanced substrate supply and available water (liquid water) result in Rs emission pulses. Wang et al.16 also suspected that Rs pulses might be related to the soil hydrology changes in the spring FTC period. Priemé and Christensen51 pointed out that the mechanisms for Rs pulses during the FTC period were stimulated by microbial metabolism via the enhanced substrate supply, which was also consistent with our results. During the outburst period, we measured the MBC and the MBN that were significantly difference among all treatments (Table 4) and the results supported our conjecture. However, the rate of Rs gradually decreased to a normal level after short time pulses. We considered that the soil microbial activity or biomass were higher in the early stage of spring FTC and decreased in the following cycles, indicating that successive FTCs might lead to the decrease of the microbial biomass in the soil examined. There are some consistent explanations for the phenomenon10,51,52. Schimel and Clein’s53 study shown that the successive FTCs might lead to the lysis of microbial cells and followed by the decrease of Rs. In addition, Haei et al.54 suggested that the change of dissolved organic carbon (DOC) might also impact on Rs during FTCs and the decreased rate of Rs after the pulses could be due to change of DOC utilization.
We also found the nitrogen addition exerted the negative impact on the soil respiration of spring freeze-thaw periods due to delay of spikes and inhibition of soil respiration. The mechanisms for impact of N addition on Rs during the spring FTC period are complicated. In our study, the mechanism for FTC-induced enhancement of Rs is not consistent with the conjecture of Elberling and Brandt7 that a pulse during the FTC period resulted from the release of trapped CO2 in the winter. We suggested that a relatively high microbial biomass is more likely to release a pulse of CO2 during FTC than a relatively low microbial biomass. With respect to the delay under N addition, we hypothesized N and salt in high concentrations inhibited microbial activity and biomass during the early period of FTC so that pulse of Rs did not occur in this period. After this period of FTC, the pulse of Rs was observed, because the continuous FTC promoted N leaching losses55, which decreased the inhibition of microbial activity and biomass. Simultaneously, when most of the extrinsic inhibitor can be removed, the microbial activity and the biomass may rapidly increase resulting in the Rs emission pulses in treatments plots. The hypothesis is also supported by the results of others56,57,58,59,60,61.
The contributions of Rs during the spring FTC period to the annual Rs were 1.80%, 1.69%, 1.10% and 1.15% for control, low-N, medium-N and high-N treatment, respectively (Table 1, Fig. 3). Our results suggested that response of Rs to simulated N deposition in temperate forests is a decline and it may vary depending on the level of N deposition during the spring FTC periods. In the previous studies, the decrease in Rs occurred in the warm and wet growing season in the N addition plots62,63,64 and not occurred in winter among treatment63. In addition, our results also suggested that contribution of Rs during the spring FTC period to the annual Rs will vary when the global N deposition are greatly altered with the atmospheric N levels rise64. We suspected that the decline of Rs due to N addition may be an improvement in the C use efficiency of the soil microbial community and might impact on the global C cycle. However, N deposition may enhance soil carbon storage via decrease of Rs during spring FTC period. Therefore, more attention should be paid to the impact of N deposition on soil respiration in the spring FTC period.
The simulated N addition delayed the outburst of Rs compared with control (no N addition). The soil spring FTC decreased the soil C that releases into atmosphere under N deposition. The relative diminution of Rs induced by N addition may potentially affect C cycle in temperate forest. In general, the effects of N addition and spring FTC on Rs are very important to accurately predict soil CO2 flux in cold region forest ecosystems under a changing climate.
How to cite this article: Yan, G. et al. Nitrogen deposition may enhance soil carbon storage via change of soil respiration dynamic during a spring freeze-thaw cycle period. Sci. Rep. 6, 29134; doi: 10.1038/srep29134 (2016).
Cooley, K. R. Effects of CO2-induced climatic changes on snowpack and streamflow. Hydrolog Sci J. 35, 511–522 (1990).
Kunkel, K. E. et al. Trends in Twentieth-Century US Extreme Snowfall Seasons. J Climate 22(23), 6204–6216 (2009).
IPCC. The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. ( Stocker, T. F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S. K., Boschung, J., Nauels, A., Xia, Y., Bex, V. & Midgley, P. M. eds). Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA (2013).
Freppaz, M., Williams, B. L., Edwards, A. C., Scalenghe, R. & Zanini, E. Simulating soil freeze/thaw cycles typical of winter alpine conditions: Implications for N and P availability. Appl Soil Ecol. 35, 247–255 (2007).
Schimel, J. P. & Mikan, C. Changing microbial substrate use in Arctic tundra soils through a freeze–thaw cycle. Soil Biol Biochem. 37, 1411–1418 (2005).
Sjursen, H. S., Michelsen, A. & Holmstrup, M. Effects of freeze–thaw cycles on microarthropods and nutrient availability in a sub-Arctic soil. Appl Soil Ecol. 28, 79–93 (2005).
Elberling, B. & Brandt, K. K. Uncoupling of microbial CO2 production and release in frozen soil and its implications for field studies of Arctic C cycling. Soil Biol Biochem. 35, 263–272 (2003).
Henry, H. A. L. Soil freeze–thaw cycle experiments: trends, methodological weaknesses and suggested improvements. Soil Biol Biochem. 39, 977–986 (2007).
Holst, J. et al. Fluxes of nitrous oxide, methane and carbon dioxide during freezing-thawing cycles in an Inner Mongolian steppe. Plant Soil. 308, 105–117 (2008).
Goldberg, S. D., Muhr, J., Borken, W. & Gebauer, G. Fluxes of climate relevant trace gases between a Norway spruce forest soil and atmosphere during repeated freeze-thaw cycles in mesocosms. J Plant Nutr Soil Science 171, 729–739 (2008).
Ludwig, B., Teepe, R., de Gerenyu, V. L. & Flessa, H. CO2 and N2O emissions from gleyic soils in the Russian tundra and a German forest during freeze-thaw periods – a microcosm study. Soil Biol Biochem. 38, 3516–3519 (2006).
Monson, R. K. et al. The contribution of beneath-snow soil respiration to total ecosystem respiration in a high-elevation, subalpine forest. Global Biogeochem Cy. 20, 13 (2006).
Neilsen, C. B. et al. Freezing effects on carbon and nitrogen cycling in northern hardwood forest soils. Soil Sci Soc Am J. 65, 1723–1730 (2001).
Sharma, S., Szele, Z., Schilling, R., Munch, J. C. & Schloter, M. Influence of freeze–thaw stress on the structure and function of microbial communities and denitrifying populations in soil. Appl Environ Microbiol. 72, 2148–2154 (2006).
Song, C. C., Wang, Y. S., Wang, Y. Y. & Zhao, Z. C. Emission of CO2, CH4 and N2O from freshwater marsh during freeze-thaw period in Northeast of China. Atmos Environ. 40, 6879–6885 (2006).
Wang, C. et al. Seasonality of soil CO2 efflux in a temperate forest: Biophysical effects of snowpack and spring freeze–thaw cycles. Agr Forest Meteorol. 177, 83–92 (2013).
Wang, J. & Wu, Q. Annual soil CO2 efflux in a wet meadow during active layer freeze–thaw changes on the Qinghai-Tibet Plateau. Environ Earth Sci. 69, 855–862 (2013).
Wu, X. et al. Effects of soil moisture and temperature on CO2 and CH4 soil-atmosphere exchange of various land use/cover types in a semi-arid grassland in Inner Mongolia, China. Soil Biol Biochem. 42, 773–787 (2010).
Wu, X. et al. Environmental controls over soil-atmosphere exchange of N2O, NO and CO2 in a temperate Norway spruce forest. Global Biogeochem Cy. 24, GB2012 (2010).
Feng, X., Nielsen, L. L. & Simpson, J. Response of soil organic matter and microorganisms to freeze/thaw cycles. Soil Biol Biochem. 39, 2027–2037 (2007).
Groffman, P. M., Hardy, J. P., Driscoll, C. T. & Fahey, T. J. Snow depth, soil freezing and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Global Change Biol. 12, 1748–1760 (2006).
Schlesinger, W. H. & Andrews, J. A. Soil respiration and the global carbon cycle. Biogeochemistry 48, 7–20 (2000).
Sullivan, B. W., Dore, S., Montes-Helu, M. C., Kolb, T. E. & Hart, S. C. Pulseemissions of carbon dioxide during snowmelt at a high-elevation site in northern Arizona, USA. ArctAntarct Alp Res. 44, 247–254 (2012).
Hirano, T. Seasonal and diurnal variations in topsoil and subsoil respiration under snowpack in a temperate deciduous forest. Global Biogeochem Cy. 19 (2005).
Kim, D. G., Vargas, R., Bond-Lamberty, B. & Turetsky, M. R. Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research. Biogeosciences 9, 2459–2483 (2012).
Wang, Y. et al. Contrasting effects of ammonium and nitrate inputs on soil CO2 emission in a subtropical coniferous plantation of southern China. Biol Fert Soils 51, 815–825 (2015).
Thornton, P. E. & Rosenbloom, N. A. Ecosystem model spin-up: estimating steady state conditions in a coupled terrestrial carbon and nitrogen cycle model. Ecol Model. 189, 25–48 (2005).
Chapin, F. S. Principles of terrestrial ecosystem ecology Vol. 2 (eds Matso, P. A. et al.) (Springer, New York, 2011).
Graham, S. L. et al. Effects of Soil Warming and Nitrogen Addition on Soil Respiration in a New Zealand Tussock Grassland. PLoS ONE 9(3), e91204 (2014).
Gong, Y. M. et al. Response of carbon dioxide emissions to sheep grazing and N application in an alpine grassland—Part 2: Effect of N application. Biogeosciences 11, 1751–1757 (2014).
Wei, D., Xu-Ri., Liu, Y., Wang, Y. & Wang, Y. Three-year study of CO2 efflux and CH4/N2O fluxes at an alpine steppe site on the central Tibetan Plateau and their responses to simulated N deposition. Geoderma. 232–234, 88–96 (2014).
Jiang, C., Yu, G., Fang, H., Cao, G. & Li, Y. Short-term effect of increasing nitrogen deposition on CO2, CH4 and N2O fluxes in an alpine meadow on the Qinghai-Tibetan Plateau, China. Atmos Environ. 44, 2920–2926 (2010).
Li, K. et al. Responses of CH4, CO2 and N2O fluxes to increasing nitrogen deposition in alpine grassland of the Tianshan Mountains. Chemosphere 88, 140–143 (2012).
Krause, K., Niklaus, P. A. & Schleppi, P. Soil-atmosphere fluxes of the greenhouse gases CO2, CH4 and N2O in a mountain spruce forest subjected to long-term N addition and to tree girdling. Agr Forest Meteorol. 181, 61–68 (2013).
Berg, B. & Matzner, E. Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environmental Reviews 5, 1–25 (1997).
Fierer, N. et al. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364 (2007).
Manzoni, S. et al. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist 196, 79–91(2012).
Sun, Z. Z. et al. The effect of nitrogen addition on soil respiration from a nitrogen-limited forest soil. Agr Forest Meteorol. 197, 103–110 (2014).
Joseph, G. & Henry, H. A. L. Soil nitrogen leaching losses in response to freeze–thaw cycles and pulsed warming in a temperate old field. Soil Biol Biochem. 40, 1947–1953 (2008).
Schultz, J. The Ecozones of the World. (Springer Berlin, 1995).
Soil classification research group of Nanjing Soil Institute of Chinese Academy of Sciences & China Soil Classification Research Group. The Retrieval System for China Soil Classification Vol 3 (eds). (University of Science & Technology China, 2001) (in Chinese).
Schimel, J. P., Bilbrough, C. & Welker, J. M. Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem. 36, 217–227 (2004).
Brookes, P. C., Landman, A., Prude, N. G. & Je NkiNson, D. S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem. 17, 837–842 (1985).
Van’t Hoff, J. H. Etudes de dynamique chemique, (Frederrk Muller, Amsterdam, 1884).
Lloyd, J. & Taylor, J. On the temperature dependence of soil respiration. Funct Ecol. 8, 315–323 (1994).
Richards, F. J. A flexible growth function for empirical use. J Exp Bot. 10, 290–300 (1959).
Khomik, M., Arain, M. A., Liaw, K.-L. & McCaughey, J. H. Debut of a flexible model for simulating soil respiration–soil temperature relationship: Gamma model. J Geophys Res. 114, doi: 10.1029/2008JG000851 (2009).
Liu, B. et al. Annual soil CO2 efflux in a cold temperate forest in northeastern China: effects of winter snowpack and artificial nitrogen deposition. Sci Rep-UK. 6, 18957, doi: 10.1038/srep18957 (2016).
CAIT 2.0 Climate data explorer. World Resource Institute, Washington. http://cait2.wri.org/wri/Country%20GHG%20Emissions?indicator=Total%20GHG%20Emissions%20Excluding%20LUCF&indicator=Total%20GHG%20Emissions%20Including%20LUCF&year=2010&sortIdx=&sortDir=&chartType=#CitedFAO2014, FAOSTAT Emission Database (2015).
Aanderud, Z. T., Jones, S. E., Schoolmaster, D., Fierer, N. & Lennon, J. T. Sensitivity of soil respiration and microbial communities to altered snowfall. Soil Biol Biochem. 57, 217–227 (2013).
Priemé, A. & Christensen, S. Natural perturbations, drying-wetting and freezing-thawing cycles and the emission of nitrous oxide, carbon dioxide and methane from farmed organic Soil Biol Biochem. 33, 2083–2091 (2001).
Yanai, Y., Toyota, K. & Okazaki, M. Effects of Successive Soil Freeze-Thaw Cycles on Soil Microbial Biomass and Organic Matter Decomposition Potential of Soils. Soil Sci Plant Nutr. 50(6), 821–829 (2004).
Schimel, J. P. & Clein, J. S. Microbial response to freeze–thaw cycles in tundra and taiga soils. Soil Biol Biochem. 28, 1061–1066 (1996).
Haei, M. et al. Effects of soil frost and growth, composition and respiration of the soil microbial decomposer community. Soil Biol Biochem. 43, 2069–2077 (2011).
Frey, S. D., Knorr, M., Parrent, J. L. & Simpson, R. T. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol Manag. 196(1), 159–171 (2004).
Gilliam, F. S., Cook, A. & Lyter, S. Effects of experimental freezing on soil nitrogen (N) dynamics in soils of a net nitrification gradient in an N-saturated hardwood forest ecosystem. Can J Forest Res. 40, 436–444 (2010).
Grogan, P., Michelsen, A., Ambus, P. & Jonasson, S. Freezethaw regime effects on carbon and nitrogen dynamics in sub-arctic heath tundra mesocosms. Soil Biol Biochem. 36, 641–654 (2004).
Zhao, H. T. et al. Effect of freezing on soil nitrogen mineralization under different plant communities in a semi-arid area during a non-growing season. Appl Soil Ecol. 45, 187–192 (2010).
Judd, K. E., Likens, G. E. & Groffman, P. M. High nitrate retention during winter in soils of the hubbard brook experimental forest. Ecosystems 10, 217–225 (2007).
Schmidt, S. K. & Lipson, D. A. Microbial growth under the snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil. 259, 1–7 (2004).
Tierney, G. L. et al. Soil freezing alters Wne root dynamics in a northern hardwood forest. Biogeochemistry 56, 175–190 (2001).
Mo, J. et al. Response of soil respiration to simulated N deposition in a disturbed and a rehabilitated tropical forest in southern China. Plant soil 296(1), 125–135 (2007).
Mo, J. et al. Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Global Chang Biol. 14, 403–412 (2007).
Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci. 3, 315–322 (2010).
This research was supported by grants from National Natural Science Foundation of China (31170421, 41575137, 31370494, 31070406) and the key projects of Heilongjiang Province Natural Science Foundation (ZD201406), the National Basic Research Priorities Program of the Ministry of Science and Technology of China (2014FY110600), the National Basic Research Program of China (2011CB403200).
The authors declare no competing financial interests.
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Yan, G., Xing, Y., Xu, L. et al. Nitrogen deposition may enhance soil carbon storage via change of soil respiration dynamic during a spring freeze-thaw cycle period. Sci Rep 6, 29134 (2016). https://doi.org/10.1038/srep29134
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