Driving Factors of Temporal Variation in Agricultural Soil Respiration Yang Wangabc, Manfred Bölterd, Qingrui Changa, Rainer Duttmannb, Annette Scheltzd, James F

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Acta Agriculturae Scandinavica, Section B — Soil & Plant Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/sagb20 Driving factors of temporal variation in agricultural soil respiration Yang Wangabc, Manfred Bölterd, Qingrui Changa, Rainer Duttmannb, Annette Scheltzd, James F. Petersene & Zhanli Wangcf a College of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China b Department of Geography, Division of Physical Geography: Landscape Ecology and Geoinformation Science (LGI), Christian-Albrechts-University Kiel, Ludewig-Meyn-Str. 14, 24098 Kiel, Germany c Click for updates State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China d Institute for Ecosystem Research, Christian-Albrechts-University Kiel, Olshausenstr. 75, 24118 Kiel, Germany e Geography Department, Texas State University, San Marcos, TX 78666, USA f Institute of Soil and Water Conservation, Chinese Academy of Science and Ministry of Water Resources, Yangling, Shaanxi 712100, P.R. China Published online: 27 Apr 2015.

To cite this article: Yang Wang, Manfred Bölter, Qingrui Chang, Rainer Duttmann, Annette Scheltz, James F. Petersen & Zhanli Wang (2015) Driving factors of temporal variation in agricultural soil respiration, Acta Agriculturae Scandinavica, Section B — Soil & Plant Science, 65:7, 589-604, DOI: 10.1080/09064710.2015.1036305 To link to this article: http://dx.doi.org/10.1080/09064710.2015.1036305

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ORIGINAL ARTICLE

Driving factors of temporal variation in agricultural soil respiration

Yang Wanga,b,c, Manfred Bölterd, Qingrui Changa, Rainer Duttmannb, Annette Scheltzd, James F. Petersene and Zhanli Wangc,f*

aCollege of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China; bDepartment of Geography, Division of Physical Geography: Landscape Ecology and Geoinformation Science (LGI), Christian-Albrechts-University Kiel, Ludewig-Meyn-Str. 14, 24098 Kiel, Germany; cState Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China; dInstitute for Ecosystem Research, Christian-Albrechts-University Kiel, Olshausenstr. 75, 24118 Kiel, Germany; eGeography Department, Texas State University, San Marcos, TX 78666, USA; fInstitute of Soil and Water Conservation, Chinese Academy of Science and Ministry of Water Resources, Yangling, Shaanxi 712100, P.R. China (Received 21 January 2015; accepted 26 March 2015)

Investigations of diurnal and seasonal variations in soil respiration support modeling of regional CO2 budgets and therefore in estimating their potential contribution to greenhouse gases. This study quantifies temporal changes in soil respiration and their driving factors in grassland and arable soils located in Northern Germany. Field –2 –1 measurements at an arable site showed diurnal mean soil respiration rates between 67 and 99 mg CO2 m h with a hysteresis effect following changes in mean soil temperatures. Field soil respiration peaked in April at 5767 –2 –1 –2 –1 mg CO2 m day , while values below 300 mg CO2 m day were measured in wintertime. Laboratory incubations were carried out in dark open flow chambers at temperatures from 5°C to 40°C, with 5°C intervals, and soil moisture was controlled at 30%, 50%, and 70% of full water holding capacity. Respiration rates were higher in grassland soils than in arable soils when the incubating temperature exceeded 15°C. The respiration rate difference between them rose with increasing temperature. Monthly median values of incubated soil –1 –1 respiration rates ranged from 0 to 26.12 and 0 to 7.84 µg CO2 g dry weight h , respectively, in grassland and arable land. A shortage of available substrate leads to a temporal decline in soil respiration rates, as indicated by a decrease in dissolved organic carbon. Temporal Q10 values decreased from about 4.0 to below 1.5 as Downloaded by [Zhanli Wang] at 02:40 27 July 2015 temperatures increased in the field. Moreover, the results of our laboratory experiments confirmed that soil temperature is the main controlling factor for the Q10 values. Within the temperature interval between 20°C and 30°C, Q10 values were around 2 while the Q10 values of arable soils were slightly lower compared to that of grassland soils. Thus, laboratory studies may underestimate temperature sensitivity of soil respiration, awareness for transforming laboratory data to field conditions must therefore be taken into account.

Keywords: soil respiration; temperature sensitivity of soil respiration; bacterial biomass; dissolved organic carbon; diurnal change; seasonal change

Introduction ecosystems play critical roles in affecting the chemical and microbial properties of soil and they further Research on soil respiration in agricultural ecosystems and its controlling factors is of growing import- regulate the patterns of soil respiration (Merino et al. ance (Li et al. 2010), as the IPCC estimated that 2004; Wang et al. 2011). Different limiting factors agriculture contributed 10–12% of the global anthro- exist for soil respiration in grasslands and arable pogenic greenhouse gas emissions; a rate of 5.1–6.1 lands, related to different plant biomass inputs, tillage Gt CO2-eq/year in 2005 (Smith et al. 2007). Different methods, and fertilizer applications (Iqbal et al. 2010; land use and management practices in agricultural Koga et al. 2011). Higher CO2 emissions are

*Corresponding author. Email: [email protected]

generally observed from soils in grasslands compared provide an estimate of additional temperature-related to those of arable lands. This is interconnected with carbon release from soils. the development of soil microbial communities, their To characterize the soil respiration of an ecosys- activities, and soil nutrient availability (Insam & tem, temporal variability is a critical factor (Vargas Haselwandter 1989; Murugan et al. 2014). As et al. 2011; Moriyama et al. 2013). During the reported by De Vries et al. (2013), production of growing season, changes in plant growth and carbon CO2 in situ was significantly greater in grassland inputs from plants occur, both of which are pivotal –2 –1 (median value was around 3 g CO2 m day ) than driving factors of soil respiration (Yang & Cai 2006; in arable land (median value was around 1.5 g CO2 Jia & Zhou 2009). Diurnal and seasonal soil respira- – – m 2 day 1) due to higher soil carbon content and tion variability have been intensively reported in increased earthworm biomass. temperate forests and other dominantly natural Conversion from grasslands into biofuel croplands environments; however, limited research has been has been increasing in recent years for a substantial performed in agricultural soils derived from glacial reduction of greenhouse gas emissions (Hertel et al. tills (Jarosz et al. 2008; Schaefer et al. 2009; Han et al. 2010; Vázquez-Rowe et al. 2014). In order to comply 2014). Moreover, in northern temperate grasslands, with the “20–20–20” targets of the European Union, soil respiration patterns are inconsistent as reported – – renewable sources should provide 20% of energy between 1090 and 1752 g C m 2 year 1 during six production by 2020 (European Commission 2009). continuous years of the study by Peichl et al. (2012). Between 2005 and 2011 in Germany, there was an Thus, there is a need for addressing temporal changes increase of 0.53 million hectares acreage of silage in biotic and abiotic factors relative to soil respiration maize despite expecting a continuous expansion by in temperate agricultural soils. 2020, for biogas production (Duttmann et al. 2013). Our study investigated diurnal and seasonal varia- In the past decade, arable land in the state of tions in soil respiration and the driving factors in Schleswig-Holstein increased by nearly 43.1 thou- arable and in grassland soils derived from glacial till sand hectares (667.0 thousand hectares in total in Northern Germany. The specific objectives of this estimated in 2012), while in contrast grassland areas study were to: (1) compare temporal variations in decreased by 64.5 thousand hectares (317.4 thou- agricultural soil respiration under both field and sand hectares in total; Statistisches Amt für Hamburg laboratory conditions; (2) elucidate responses of soil und Schleswig-Holstein, 2013). respiration to soil temperature and moisture changes Soil temperature and moisture are recognized as in grasslands and arable lands; (3) quantify the the dominant controlling factors for soil respiration, temporal Q10 changes and the effects of soil temper- and can be regarded as an overall driver and indicator ature and moisture on Q10; (4) identify the driving for soil biological processes (Paul & Clark 1989; Jia & chemical and microbial factors related to temporal variations in agricultural soil respiration. In order to Zhou 2009). The reactions of soil respiration to detect the basic patterns mentioned above, we chose temperature and moisture are affected by thresholds two different agricultural land use types, an arable

Downloaded by [Zhanli Wang] at 02:40 27 July 2015 which act as switches for biochemical processes; soil and a grassland soil, during long-term analyses of however, there are several other influential factors soil respiration as related to accompanying environ- which cannot be identified in detail. These factors are mental parameters. especially important for the actual contents of low

molecular weight organic matter. The Q10 values of biochemical processes and relationships to other Materials and methods environmental properties can serve as a tool for descriptions of soil respiration (Gaumont-Guay et al. Study sites and sampling 2006). There is a considerable bias in the application The study area is near the city of Kiel, Schleswig- of constant Q10 values in biogeochemical models Holstein, Germany. Annual precipitation and mean especially when describing soil respiration at low air temperature registered by the weather station Kiel- temperatures (Bond-Lamberty & Thomson 2010). Holtenau weather station (54°22′33″ N, 10°8′35″ E) The Q10 values vary widely among different ecosys- for the period 1981–2010 are 778.0 mm and 8.9°C, tems, in addition to their temporal variability. The respectively (German Weather Service, www.dwd. Q10 values mainly depend on soil temperature, soil de). Soil types in the research area are mainly Luvisols moisture, and litter quality (Kirschbaum 1995; Zhou and Stagnic Luvisols at higher locations, and Gleysols et al. 2009; Oechel et al. 2014). In response to global dominate the lower areas. The dominant soil textures climate change, Q10 values may indicate to what are loamy sand and sandy loam, with sand con- extent warming could stimulate stronger soil respira- tents ranging from 49% to 77% and clay content tion in grassland and arable land and thus, could from 7% to 24%. The soils contain 36.0 mg g–1 and Acta Agriculturae Scandinavica, Section B — Soil & Plant Science 591

17.6 mg g–1 organic matter in grassland and arable L.). Mineral fertilizers including urea and in some land, respectively. Soil pH (A. dest.) varied between sites ammonium sulfate or calcium ammonium 4.9 and 7.4, while pH (0.01 m CaCl2) ranged between nitrate were mainly applied in March and May 2012 4.2 and 6.9, respectively. in the arable sites. Grassland sites received one or two times of mowing or cattle grazing during the sampling period. For lab analyses, topsoil samples (soil depth Measurement of soil respiration 0–5 cm) were taken in November 2011 and from April to July 2012 in a monthly interval from Soil respiration in the field randomly selected sites. Nine grassland sites and The field study on CO2 evolution was carried out from nine arable land sites were selected. Each soil an arable site on the experimental farm of Kiel sample was retrieved by mixing five subsamples University, Hohenschulen (54°19′ N, 10°0′ E), from within a 1 m2 sample area. Freshly sampled soil was October 2010 to July 2011. During the experiment, kept in zipper plastic bags and transported to labor- rape seed (Brassica napus L.) was grown on the test atory in a cooling box. The soil was stored unsieved field. Gas flux measurements in the field were per- while maintaining field moisture at 4°C and were formed by a Minicuvette System (Walz Co., Effeltrich, analyzed within six weeks of collection. Only the Germany). Soil CO2 emission was sampled by a samples taken in November 2011 were stored for 12 plexiglass cuvette, which covers an area of 55 cm2 weeks in freezer (–18°C) before taking soil respiration with a height of 12 cm. The plexiglass cuvette was measurements (Stenberg et al. 1998). At least three mounted on an aluminum frame installed at a soil consistent samples from each land use type were depth of 10 cm. The aluminum frame was a perman- measured for all of the chemical and microbial ent installation since the beginning of the measure- properties examined in this study. ment, while the plexiglass cuvette was separately Soil respiration was analyzed in the laboratory demounted regularly to prevent the disturbance of according to the method of Bölter et al. (2003). In photosynthesis by growth of plant shoots. Ambient air brief, subsamples equivalent to 20 g wet weight were –1 (gas flow 0.5 L min ) passed the cuvette and CO2 incubated in dark, open flow chambers. After passing contents (ppm) were measured against outside air by a a sealed tube partially filled with water, normal differential channel Infrared Gas Analyser (Binos, atmospheric air flowed through the closed water- Fisher-Rosemount, Hanau, Germany). Standard bathing chamber at the rate of 0.5 L min–1 and then gases (Messer-Griesheim, Germany) were used for reached the CO2-Analyser, an infrared gas analyser calibration. (BINOS, Rosemount Co./originally invented by Ley- The registration of CO2-concentrations was per- bold-Heraeus, Germany). Soil respiration rates were formed in a time interval of 10 min. Thus, generally calculated by subtracting the CO2 emission rate in 130 ± 1 records were stored per day. Due to technical control (without subsamples) from the value obtained problems, resulting from the loggers, external power from a soil sample in an incubating chamber. To get sources, or weather conditions, the full data-set (at quasi-constant records, pre-incubation was carried

Downloaded by [Zhanli Wang] at 02:40 27 July 2015 least 126 records per day) comprised 196 full days out for around 30 min for each incubating temperat- and another 68 sets of incomplete daily data (21–125 ure to let the CO2 concentration in the outflow reach records per day). Temperature inside the cuvette was an equilibration. The data used for calculation were regulated by the outside temperature to prevent a the mean value of at least 10 quasi-constant records localized “greenhouse” effect. Temperature sensors of soil respiration rate at each incubating temperature and data loggers (Squirrel, Grant Co., UK) were considering every moisture condition. installed to control air temperature (2 m high) and Incubation temperature was increased from 5°C to soil temperatures (–1 cm, –5 cm). The mini-cuvette 40°C, using a stepwise interval of 5°C. The time for data were converted to 1 m2, and ppm changes were measurement was set at two hours. The water content –1 converted to mg CO2 h using the gas flow data (0.5 of soil subsamples for incubation was separately set to – L min 1). 30%, 50%, and 70% of water holding capacity (WHC) by adding sterile water. WHC was determined previously on a mass basis by saturating and Soil sampling and respiration measurements in the draining soil subsamples until equilibrium and then laboratory drying them at 105°C for 24 hours. Air drying was For the laboratory study of soil respiration, disturbed only required for incubation subsamples if their in situ soil samples taken from grassland and arable soils of soil moisture exceeded the preset soil water content. 41 km2 catchment area (54°24′22″–54°27′48″ N and After adding water until reaching the preset soil 9°55′36″–10°5′55″ E) were used. The arable sites moisture, one hour of pre-incubation was carried were covered with winter wheat (Triticum aestivum out with tinfoil cover. Pre-incubation allowed the 592 Y. Wang et al.

sterile water to permeate the subsample and to avoid soil respiration rate and soil temperature were used to the flush of rewetting. calculate Q10 due to a better correlation compared to all records of a day. Specifically, daily maximum soil respiration rate and soil temperature were selected Soil chemical properties and microbial and linear regression analysis was perform with them. descriptors For each month, T1 and T2 were the minimum and Dissolved organic carbon (DOC) is regarded as a maximum of the daily maximum values, respectively, glucose equivalent, measured by a photometer (CE while R1 and R2 were calculated based on T1, T2, and 1011, CECIL, England) at a wavelength of 625 nm. the linear model. The procedure followed the recommendations of For laboratory measurements, median values and Neumann (1954). The C/N ratios were calculated ranges were shown of the non-normal distributed from data measured with an elemental analyser data and rank-transformation was applied to the data- (EURO EA3000, EURO VECTOR, Italy) with set prior to the regression analysis (Conover & Iman combustion at 1000°C and corrections for carbonate 1981). Statistical analyses were conducted using the + – – free software environment R, Version 2.15.0. content. Contents of NH4 ,NO2 ,NO3 , and avail- 3– able phosphorous (AP), which presents PO4 , were measured by analytical test kits (Nitrite, Nitrate, Results Ammonium, Phosphate, Cell Tests, Spectroquant Nova 60, Merck, Germany). Temporal changes in agricultural soil Descriptors of the microbes included total bacterial properties number (TBN), bacterial biomass (BBM), mean Environmental property changes of the sample site in values of surface and volume (MBS and MCV) of the field the community. Biovolume estimates were based on epifluorescence microscopy. The microscope was During the field measurement recording period linked to a digital image analysis system (Image (Table 1), mean soil temperature in the arable site Access easyLab8, Imagic Bildverarbeitung AG, Swit- decreased from October to its lowest value in Decem- zerland). Length and width measurements of cocci ber and maintained around 0°C in the following two and rods were carried out by geometrical terms months. From March to July, mean soil temperature (Bölter et al. 2002). Subsamples for microscopy progressively increased from 3.38°C to 17.41°C. were taken from an ultrasound-treated and centri- Mean air temperature recorded by the meteorological fuged soil suspension, which consisted of 1 g fresh station showed the same trend as the mean soil soil and 10 ml sterile particle-free distilled water, temperature recorded by the cuvette. During the where 100 μl were filtered onto a polycarbonate recording period, minimum mean precipitation membrane (pore size 0.2 µm), extenuated with 5 ml occurred in April and rose to maximum in July distilled water and stained with 200 μl acridine (Table 1). orange solution (1:1000). TBN and linear dimen- Downloaded by [Zhanli Wang] at 02:40 27 July 2015 sions of individual bacterial cells were determined by Soil property changes of samples under laboratory the mean count of at least 14 random fields (50 × 50 incubation μm). BBM-C was calculated following the assump- tion that 20% of the wet bacterial biovolume was dry During the sampling for laboratory measurements, weight containing 50% carbon (Bloem et al. 1995). field soil temperature increased progressively from April to July in both the grassland and arable land sites (Tables 2 and 3). For both sites, field soil Data analyses moisture was lowest in May, while the median values Temperature sensitivity of soil respiration was pre- from May to July were lower in grassland compared to arable land (Tables 2 and 3). sented by Q10 values, and calculation was performed In terms of the soil chemical properties (Tables 2 with the following equation (Hochachka & Som- – ero 1984): and 3), the median grassland soil NO3 content experienced an increasing trend from 70.6 µg g–1 in 10 –1 R2 T2T1 November up to 178 µg g in July. The runaway Q10 ¼ –1 R1 value in June (122.2 µg g ) might be due to mowing that occurred in May. In arable soil, an increase from –1 – Here, R1 and R2 are the measured rates at temperat- 65.3 to 251 µg g of the NO3 content was observed ure T1 and T2 (where T1 < T2), respectively. To after the application of fertilizer in May; however, in laboratory data, R1 and R2 were the median values at June it declined rapidly to the same low level as –1 T1 and T2, respectively. To field data, daily maximum in April (65 µg g ). The median AP concentrations in Acta Agriculturae Scandinavica, Section B — Soil & Plant Science 593

Table 1. Monthly weather records at the field site.

Temperature (°C) Precipitation (mm)

Cuvette Cuvette Cuvette Station Station Station Date for precipitation Year/month (mean) (min) (max) (mean) (mean) (total) >10 mm

October/ 8.21 –1.6 21.00 8.66 1.77 54.80 21st 2010 November/ 3.49 –10.3 13.00 3.78 3.75 112.50 4th, 12th, 19th and 2010 29th (snow) December/ –1.91 –3.3 2.50 –4.60 0.94 29.20 2nd, 6th–27th (snow) 2010 January/ –0.34 –7.9 7.20 0.42 1.21 37.40 14th 2011 February/ 0.35 –5.0 11.10 –0.08 1.38 38.50 4th 2011 March/2011 3.38 –4.0 19.00 3.21 0.61 19.00 April/2011 11.77 –1.1 29.60 10.43 0.11 3.30 May/2011 14.38 –3.6 35.50 12.22 1.17 36.30 June/2011 17.26 4.9 31.80 15.23 3.11 93.20 8th, 18th, 19th and 22nd July/2011 17.41 10.3 30.00 15.73 4.66 150.20 6th, 8th, 14th and 22nd

Note: The records from cuvette in July lasted only until 15th. For November 2010, January 2011 and February 2011, the lowest recordable temperature at the cuvette was –5°C, thus it is substituted by data from an air temperature sensor from a location close to this, as only few records showed this low temperature, the mean value was not significantly influenced.

3– −1 grassland decreased from 3.26 to 1.17 µg PO4 g . noon around 12:00 hours. It fluctuated between 83 and –2 –1 In comparison, higher median AP concentrations in 90 mg CO2 m h during afternoon from 13:00 to 3– –1 arable soil were maintained above 3.96 µg PO4 g 21:00 hours. The monthly diurnal variations in soil except for the drop in May. Grassland DOC contents respiration (Figure 2) showed similar responses to greatly exceeded the arable land values. Nevertheless, variations in soil temperature compared to the mean both values were highest in April (respectively, 1457.2 value of all data (Figure 1), except that in April and and 448.1 19 µg glucose g–1 dry weight) and declined May. In April, the soil temperature peaked around noon dramatically to 25.2 and 9 µg glucose g–1 dry weight time, while the soil respiration rate fluctuated around –2 –1 from May to June. The grassland soil tended to have a 180 mg CO2 m h .InMay,therewasapeakofsoil slightly higher C/N ratio in contrast to that of the respiration around 22:00 hours, although temperature arable soil, ranging from 12.4 to 13.8 and from 10.6 to peaked at 12:00 hours. 12.7 of the median values, respectively. At the seasonal scale (Figure 3), the highest soil According to the microbial properties of grassland respiration rate appeared in late April (5767 mg CO2 soil (Table 2), the median value of BBM declined m–2 day–1). The records of soil respiration rate from 1 – Downloaded by [Zhanli Wang] at 02:40 27 July 2015 from 4.38 µg C g 1 dry weight in November 2011 to October to 30 November fluctuated at a median level –1 –2 –1 the monthly minimum of 1.77 µg C g dry weight in between 990 and 2906 mg CO2 m day . It then –2 May 2012 and increased in the following two months. maintained at the lowest level below 300 mg CO2 m In contrast, the much lower median BBM value in day–1 from December to early March, despite a sharp the arable land (Table 3), ranging from 0.72 to1.58 increase in early February. Soil respiration rates rose µg C g–1 dry weight, appeared stable after the decline from 5 March to late April and then started a –2 –1 from November 2011 to April 2012. declining trend to 3076 mg CO2 m day until the end of the record in July 2011.

Temporal changes in soil respiration Monthly changes in soil respiration according to Diurnal and seasonal changes in arable soil respiration in incubation in the laboratory the field The laboratory measurements of soil respiration Temporal variations were determined for soil respira- (Figure 4; Appendix Tables A1 and A2) indicated tion rates in the arable field. At the diurnal scale, mean that the rates were higher in grassland soil than in soil respiration for the whole research period (Figure 1) arable soil when the incubating temperature exceeded –2 –1 maintained at the lowest level below 77 mg CO2 m h 15°C, and this difference increased directly with from 22:00 to 08:00 hours during night-time and the temperature. At the temporal scale, median grassland early morning. An increase began at 08:00 and reached soil respiration rate decreased from April to July 2012 –2 –1 the highest soil respiration rate (99 mg CO2 m h )at with most temperature levels between 5°C and 40°C, 594 Y. Wang et al.

Table 2. Monthly variations in soil properties at the grassland sites for laboratory measurements.

Parameter November 2011 April 2012 May 2012 June 2012 July 2012

T Median – 8.4 14.0 14.4 18.5 Range – 5.3–10.3 11.2–15.9 13.3–15.3 15.9–19.7 WHC Median 58 69 24 46 34 Range 32–76 51–129 20–29 36–52 24–38 DOC Median 1119.1 1457.2 1095.6 25.2 41.0 Range 559.5–2690.5 879.1–2060.8 702.5–1544.6 15.7–26.3 21.8–48.8 C/N Median 13.8 13.4 12.4 12.7 13.1 Range 12.2–17.0 12.5–14.3 11.5–15.1 11.6–13.7 11.6–14.5 – NO2 Median 0.04 0.32 0.22 0.17 0.44 Range 0.00–0.18 0.01–0.36 0.19–0.46 0.16–0.20 0.34–1.00 – NO3 Median 70.6 72.6 140.1 122.2 178.0 Range 40.0–215.7 45.5–342.3 29.2–165.3 62.8–227.6 72.0–227.3 AP Median 3.22 3.26 1.55 1.17 1.52 Range 0.59–8.42 1.42–6.61 0.94–6.47 1.14–6.65 1.05–11.70 BBM Median 4.38 2.45 1.77 2.77 3.62 Range 1.97–12.29 0.94–6.93 0.91–2.32 1.56–3.41 2.35–4.88 MCV/MBS Median 0.078 0.074 0.066 0.071 0.069 Range 0.073–0.079 0.068–0.077 0.065–0.069 0.067–0.071 0.069–0.070

T, field soil temperature (°C); WHC, field soil moisture as percentage of water holding capacity (%); DOC, dissolved organic carbon (µg –1 – –1 – –1 3– –1 –1 glucose g ); NO2 , soil nitrite (µg g ); NO3 , soil nitrate (µg g ); AP, available phosphate (µg PO4 g ); BBM, bacterial biomass (µg C g ); MCV/MBS, mean cell volume to mean bacterial surface ratio (µm); C/N, soil total carbon to soil total nitrogen ratio; numbers of measurements are between 3 and 9.

while no clear temporal trend was observed from the October to December and dramatically increased to the arable land during the growing season except for July maximum (5.49) in January and remained above 4.0 in when median values were relatively lower (Appendix the following two months. In April, the Q10 value Tables A1 and A2). Soil respiration rates of grassland dropped back to a low level (1.48) again and kept and arable land (Figure 4d) increased as temperatures declining. An ascending trend occurred in the Q10 Downloaded by [Zhanli Wang] at 02:40 27 July 2015 increased from 5°C to 40°C. In both grassland and values from May (1.29) to July (1.45); however, they arable land, the increase in soil respiration rates with did not exceed the April value. rising temperatures were greater from April to July According to laboratory measurements (Table 5), 2012 compared to November 2011 (Figures 4d,4D).A the Q10 values in grassland were much higher than that similar temporal trend and relation to temperature of the arable land in most temperature classes. Apart existed with variations in soil respiration when the from the effect of soil moisture, the temperature incubating soil moisture was at 30% WHC (Figures 4a, sensitivity of grassland soil respiration rates peaked at 4A), 50% WHC (Figures 4b, 4B), and 70% WHC 2.69 when the incubating temperature class was (Figures 4c, 4C) separately. Compared to the soil between 15°C and 25°C and continuously decreased respiration rate during the growing season, the soil to 1.59 as the temperature increased. The Q10 values in respiration rates of samples taken in November arable land also decreased from 2.00 to 1.03 as increased much slower with increasing temperature in temperature increased from 20°C to 40°C. At temper- grassland and even decreasing trends were observed ature class 10–20°C, arable Q10 value reached the with increasing temperature in arable soils (Figure 4). minimum at 1.00 while the grassland Q10 value was 2.03 considering all soil moisture conditions. Soil moisture and temperature interactions influenced the Temperature sensitivity of soil respiration Q values in both grassland and arable land. Although measured in the field and laboratory 10 the temperature sensitivity of soil respiration fluctuated, The field data of the arable sites (Table 4) indicated that the Q10 values at all temperature classes were generally Q10 values were at the minimum level below 1.2 from highest at 70% WHC (Table 5). Acta Agriculturae Scandinavica, Section B — Soil & Plant Science 595

Table 3. Monthly variations in soil properties at the arable sites for laboratory measurements.

Parameter November 2011 April 2012 May 2012 June 2012 July 2012

T Median – 8.6 15.0 13.8 17.6 Range – 6.5–9.7 12.7–15.8 13.2–14.6 15.8–19.7 WHC Median 58 68 37 59 43 Range 42–70 41–83 21–55 44–69 35–53 DOC Median 357.1 448.1 434.4 9.0 8.6 Range 153.7–545.1 376.7–560.3 257.6–729.7 7.2–10.4 8.2–11.7 C/N Median 12.2 12.7 10.6 11.4 11.4 Range 11.0–13.0 11.7–13.1 10.4–11.1 10.7–11.5 10.8–12.2 – NO2 Median 0.02 0.29 0.30 0.20 0.26 Range 0.00–0.03 0.04–0.39 0.10–0.42 0.10–0.23 0.12–0.28 – NO3 Median 50.9 65.3 251.1 65.0 43.3 Range 40.7–77.6 54.8–167.8 27.9–533.9 57.0–157.6 26.5–72.4 AP Median 4.76 3.96 2.30 4.17 4.13 Range 1.48–7.59 0.77–7.47 0.88–3.64 2.13–4.55 2.30–5.80 BBM Median 1.58 0.96 0.77 0.72 0.76 Range 1.08–2.95 0.79–2.01 0.57–0.81 0.59–1.17 0.51–0.92 MCV/MBS Median 0.078 0.073 0.070 0.070 0.068 Range 0.075–0.080 0.071–0.080 0.069–0.073 0.068–0.075 0.066–0.074

Factors that influenced temporal changes in soil arable land (laboratory incubation). Soil moisture respiration only had limited effects on soil respiration. Moreover, Temporal changes in soil respiration largely depended the laboratory data indicated that changes in soil on soil temperature in both field and laboratory respiration were also partly dependent on DOC and measurements (Table 6). According to the coefficient the MCV/MBS ratio under both pasture and arable Downloaded by [Zhanli Wang] at 02:40 27 July 2015 of determination, variations in soil respiration were managements (Table 7). The C/N ratio only affected best explained by temperature in the field conditions, grassland soil respiration, while BBM only affected followed by grassland (laboratory incubation) and arable soil respiration.

–2 –1 Figure 1. The daily variations in mean soil respiration rate (mg CO2 m h ) and mean soil temperature (°C) of ﬁeld measurements. The data cover all 264 recording days. 596 Y. Wang et al.

–2 –1 Figure 2. The daily variations in mean soil respiration rate (mg CO2 m h ) and mean soil temperature (°C) of ﬁeld measurements for each month (a, October 2010; b, November 2010; c, December 2010; d, January 2011; e, February 2011; f, March 2011; g, April 2011; h, May 2011; i, June 2011; j, July 2011). The data cover all 264 recording days. Downloaded by [Zhanli Wang] at 02:40 27 July 2015

–2 –1 Figure 3. Time course of integrated mean soil respiration rate (mg CO2 m day ) and mean soil temperature (°C). The course covers 196 days of full data records in the ﬁeld without breaks of incomplete days.

Discussion chemical and microbial properties of typical grass- Temporal changes of soil properties land and arable soils developed on Weichselian glacial deposits. Soil nitrate content increased from We compared temporal variations in soil respiration November 2011 to July 2012 in grassland (Table 2) and its driving factors concerning the environmental, mainly resulted from higher nitrogen mineralization Acta Agriculturae Scandinavica, Section B — Soil & Plant Science 597

–1 –1 Figure 4. The seasonal variations in soil respiration rate (µg CO2 g dry weight h ; median value in each month) and temperatures at different soil moisture conditions in grassland (left column: a, at 30%WHC; b, at 50%WHC; c, at 70%WHC; d, at all 30% to 70% WHC condition) and arable land (right column: A, at 30%WHC; B, at 50%WHC; C, at 70%WHC; D, –1 at all 30–70% WHC condition). (The system error may disturb the values when soil respiration rate is below 2.8 µg CO2 g dry weight h–1). Downloaded by [Zhanli Wang] at 02:40 27 July 2015

Table 4. Mean Q10 values of the months from October 2010 to July 2011 measured at a winter rape field.

Month/year Q10 T span T span (°C) Days (n) r Significance level (%)

October/2010 1.18 8.7 to 21.0 12.3 23 0.7739 0.1 November/2010 1.17 –1.4 to 13.0 14.4 30 0.5784 1 December/2010 1.14 –1 to 2.5 3.5 31 0.0964 none January/2011 5.49 –1.1 to 7.2 8.3 26 0.4884 1 February/2011 4.05 –1.7 to 11.1 12.8 28 0.7124 0.1 March/2011 4.23 0.4 to 19.0 18.6 31 0.9422 0.1 April/2011 1.48 11.3 to 29.6 18.3 25 0.8315 0.1 May/2011 1.29 16.8 to 35.5 18.7 30 0.5474 0.1 June/2011 1.36 15.8 to 31.8 16.0 26 0.5806 0.1 July/2011 1.45 15.2 to 30.0 14.8 14 0.6560 1

Note: r, correlation coefficient between soil temperature and soil respiration rate.

and subsequent nitrification. Stronger microbial aggregated the increase of nitrate content in grassland activities with increasing temperature also contribu- because defoliation often results in higher available ted to this trend (Wang et al. 2006; Gelfand & Yakir nitrogen content by improving soil nitrogen cycling 2008). The mowing in May 2012 may have further and mineralization (Gavrichkova et al. 2010). The 598 Y. Wang et al.

Table 5. Q10 values at different temperature classes at various soil moisture conditions under laboratory conditions.

Grassland Arable land

Temperature 30% 50% 70% Mixed 30% 50% 70% Mixed range WHC WHC WHC moisture WHC WHC WHC moisture

10–20°C 1.90 2.05 2.15 2.03 ––– – 15–25°C 2.59 2.74 2.28 2.69 ––– – 20–30°C 2.26 2.14 2.06 2.14 1.96 1.65 2.06 2.00 25–35°C 1.71 1.78 1.92 1.73 1.40 1.65 1.94 1.92 30–40°C 1.30 1.64 1.66 1.59 1.01 1.50 1.15 1.03

Note: There are no Q10 values calculated in the temperature range 10–20°C and 15–25°C for arable soil. With respect to the error level of soil –1 respiration rate measured in the laboratory, Q10 values are mainly calculated when the median values are higher than 2.8 µg CO2 g dry weight h–1. WHC, water holding capacity. Mixed moisture included 30% WHC, 50% WHC, 70% WHC, and soil moisture under field condition.

increase of nitrate in arable land (Table 3) in May disturbance during the decomposition period (Poeplau 2012 was mainly caused by applications of fertilizers, &Don2013). Plants are the primary sources of DOC, while fertilization is regarded leading higher gross especially sugars such as fructose and glucose (Medeiros nitrification rate (Stange & Neue 2009). The sharp et al. 2006). During the period from November 2011 to decrease of nitrate content in arable land shortly after April 2012, more carbohydrates could be transferred to the application of chemical nitrogen fertilizer is the surrounding soil body by higher plant roots due to consistent with other research findings because of the recovery of plant growth (Wilson et al. 2001). nitrate leaching from topsoil and utilization of avail- Therefore, DOC contents rose as carbohydrates accu- able nitrogen by crops in order to support plant mulated in both land use types. The dramatic decrease growth (Carranca et al. 1999; Merino et al. 2004; of soil DOC content reported in this study has also been Steenwerth & Belina 2008). observed in other studies (e.g., Murata et al. 1999). According to Tables 2 and 3, higher AP content in Reasons for this DOC decrease include its utilization by arable soil compared to that of grassland soil was microbes during decomposition and also the transport observed here. Lower acidity values in the arable land of sugars to other plant parts during vigorous growth contribute to more AP in the soil. The AP content (van Doorn 2004;Medeirosetal.2006). decreased in both grassland and arable land mainly Elevated amounts of BBM are often observed in because of the uptake by plant roots and usage by grassland compared to arable land (Wallenius et al. microbes during the growing season (Zhao et al. 2009). 2011) and can be attributed to a greater biologically However, application of mineral nitrogen fertilizer in available fraction of total SOM (Štursová & Baldrian arable soil results in an increasing AP content by 2011). In November 2011, a higher amount of BBM stimulating soil microbial mineralization activity (Song was observed in both grassland and arable land

Downloaded by [Zhanli Wang] at 02:40 27 July 2015 et al. 2013). Maintenance of relatively high values in despite less favorable soil temperatures and low labile arable AP concentration after fertilizer application can C content (Tables 2 and 3). A high amount of BBM be due to the immobility of phosphorus in soil. Low in winter was also reported by Yao et al. (2011), and crop utilization efficiencies may further enhance the explained by higher N availability. Soil microbes accumulation of residue P (Aulakh et al. 2003). benefit from the absence of growing plants in winter- In line with earlier studies, significantly higher SOC time that would compete for the same available contents as well as DOC contents were observed in nitrogen content (Yao et al. 2011). grassland compared to arable land (Tables 2 and 3) An increasing trend of BBM in grassland during the credits by a higher input of biomass and less physical growing season was also observed by others (Patra et al.

Table 6. Rank-based linear regression coefficients between soil respiration rate and soil temperature as well as soil moisture in grassland and arable land.

Grassland (lab) Arable land (lab) Arable land (field)

Influencing factors Adjusted R2 Adjusted R2 Adjusted R2

Soil temperature 0.579* 0.182* 0.706* Soil moisture (lab)/precipitation (field) 0.005** 0.014* 0.004*

Note:

Table 7. Rank-based linear regression coefficients between shown due to strong effects of temperature on the soil respiration rate and individual influencing factors in variations in soil respiration. grassland and arable land. However, soil respiration measured in the arable field in April 2011 did not change in the same pattern Grassland Arable land as soil temperature (Figure 2). The growth of young Influencing factors Adjusted R2 Adjusted R2 plants and possible effects of exudates of them on the soil microbes should be considered. The exudates DOC 0.286* 0.342** may be different in quantity and quality, and thus C/N 0.341* NS BBM NS 0.292* relationships of microbial activity with temperature MCV/MBS 0.394** 0.221* may be overridden by factors of sufficient or pulsed nutrient shots. A shortage of precipitation (Table 1) Note: Soil samples (without samples taken in November 2011) were incubated at 50% water holding capacity and 25°C. may have also restricted the increase of soil respira- DOC, dissolved organic carbon; BBM, bacterial biomass; MCV/ tion rate. Reasons for that soil respiration and soil MBS, mean cell volume to mean bacterial surface ratio. temperature peaked at different times in May 2011 *P <0.05;**P < 0.01; NS, not significant at 95% confidence by T-test. (Figure 2) can be seen in some hysteresis. That may be caused by the reactions of the microbial commu- 1990; Yao et al. 2011), created by the flush of labile C nities on effects of the availability of oxygen, available supplied from fine root turnover and root exudates (Yao nutrients or other factors. Previous field studies have et al. 2011). Defoliation also stimulates microbial also reported delays of soil respiration changes activity and microbial biomass by improving the avail- following soil temperature variations as was observed ability of carbon in the rhizosphere (Butenschoen et al. in this study (Gaumont-Guay et al. 2006). Hysteresis 2008). In this study, a slight decrease in grassland BBM in the diurnal relationship of soil respiration to soil content in May 2012 was observed (Table 2). This may temperature was indicated by delayed declines of soil have resulted from the low soil moisture caused by in situ respiration both in the morning and again in the water stress. After shrinking the total bacterial surface afternoon along with changes in temperature (Figures during a drought, less water is available and a decrease in 1 and 2). The hysteresis effect is mainly attributed to microbes has been described by Pesaro et al. (2004). CO2 diffusion through soil and variations in rhizo- The slightly larger MCV of soil bacteria in grassland soil spheric respiration due to assimilates transported (Tables 2 and 3) was likely the result of higher amounts from leaves to roots, release of root exudates and of available nutrition for microbial cell growth. During uptake by microorganisms (Darenova et al. 2014; the growing season, except for May 2012, the observed Han et al. 2014). A CO2 peak was observed in early decrease of MCV, while TBN increased is consistent February 2011 when mean soil temperature in‐ with the conclusions of Erlinger and Saier (1982), that creased from minus to above 0°C in the cuvette cell volume is inversely correlated with cell density. (Figure 3; Table 1). It indicated that the sharp increase of soil respiration rate may be caused by a Soil respiration and its driving factors freezing and thawing effect. In line with other studies, Downloaded by [Zhanli Wang] at 02:40 27 July 2015 It is commonly accepted that soil respiration is significant increase of soil CO2 emission rate was temperature-dependent as are other chemical and usually observed following thawing event (Priemé & biochemical reactions (Davidson & Janssens 2006). Christensen 2001). The sudden flush of water and Darenova et al. (2014) also pointed out that estimating nutrients during thawing is generally considered to soil CO2 efflux based on continuously measured soil induce rapid shifting of microbial activities after the temperatures is sufficient with less than 7.2% differ- stop during freezing (Wang et al. 2013). In this ences between modeled rates and those measured in research, the estimated coefficients of linear equa- the field. Although soil moisture typically plays an tions are generated by rank regression analysis. important role in controlling soil respiration rates, this However, the coefficient of determination indicates relationship was not necessarily present in this study the fitness of the models used here. The coefficient of according to very small coefficient of determination determination can also be accounted for providing (Table 6). Precipitation in the field and soil water the proportion of variations in soil respiration, even content determined in the laboratory each showed though they show a smaller sensitivity to values limited effects on variations in soil respiration rates. generated by parametric regression analysis. This finding may be a result of microbial communities Soil respiration rate in the arable field is consistent not being exposed to water stress during the research with other studies conducted in situ that represented soil period, thus the adequate soil moisture conditions that heterotrophic activity and root respiration (De Vries existed did not restrict the soil respiration rate et al. 2013). The amounts of CO2 emissions measured (Williamson & Wardle 2007). Therefore, we consid- in other European countries with comparable soil and ered that the effects of soil moisture were not obviously vegetation types as well as environmental and soil 600 Y. Wang et al.

nutrition conditions were reported as ranging from of DOC concentration explained the decreasing –2 –1 about 0.5 to 3.5 g CO2 m day and from about 1 to temporal trends of soil respiration rate. –2 –1 8gCO2 m day in arable land and grassland, About 34% of the total variation in grassland soil respectively. De Vries et al. (2013)reportedthatin respiration was explained by C/N ratio when incu- different agricultural soils in Europe CO2 productions bated at 25°C and 50%WHC; however, no signific- –2 –1 were between 2 and 4 g CO2 m day .Fieldmeasure- ant correlation was found between arable soil ments of soil respiration rates have shown significant respiration and C/N ratio (Table 7). This may be correlations with soil temperature during both diurnal related to the higher C/N ratios in grassland com- (Figure 1 and 2) and seasonal (Figure 3) time scales. It is pared to arable land that were found in this research. further supported by a regression analysis (Table 6), Manzoni et al. (2008) suggested that with high C/N where 70.6% of the variations in soil respiration rate ratio (low initial N concentration), microbes intend were explained by field soil temperature measurements to enhance the decomposition of plant residues by using the full recorded dataset. Soil respiration rate exploiting substrates. In contrast, with low C/N ratio measured in the laboratory consists of both microbe (high initial N concentration), decomposers increase respiration and plant root respiration by incubating soil their carbon-use efficiencies to support cell growth samples without picking out the roots. For laboratory (Manzoni et al. 2008). But changes in C/N are only measurements, an increasing soil respiration rate is minor and are not effective for changes in soil activity. observed as soil temperatures rise in the incubating The MCV/MBS ratio played an important role in chamber, both for grassland and arable land (Figure 4; affecting soil respiration in both grassland and arable Table 6; Appendix Tables A1 and A2). land according to the regression analysis (Table 7). In From April to July 2011 soil temperature kept the view of individual microbes, MCV/MBS ratio increasing, however, there was a noticeable decline of follows the principle that the smaller the cell volume soil respiration in the field (Figure 3). We also found is, the higher of the surface area to volume ratio a decrease in the soil respiration rate from April to (Thomas & Madigan 1991). It partly depends on the MCV/MBS ratio, that microbes can effectively use July 2012 in the laboratory when soil samples were organic and inorganic soil nutrition to provide energy incubated at the same soil temperature and moisture and material for microbial activities. Concerning the (Figure 4). This observed downward trend concurs soil taken in November 2011 which reacted differ- with the findings of other studies and a substrate ently compared to the soil taken in the growing limitation mainly accounts for the changing temporal season, we conclude 12 weeks over storage as the respiration pattern (Kirschbaum 2013). The amount major source of error (Černohlávková et al. 2009). of SOC and its soluble components play critical roles Moreover, the system error may disturb the values in affecting soil respiration. They control substrate when soil respiration rate is relatively low. According availability and thus explain a considerable propor- to other studies, the error may come from dissolution tion of changes in soil respiration (Liu et al. 2006; of CO2 in soil water when the pH in the range of 7 Laganière et al. 2012). (Martens 1987; Lin & Brookes 1999; Oren &

Downloaded by [Zhanli Wang] at 02:40 27 July 2015 The coefficient of determination (Table 6) shows a Steinberger 2008). To avoid that, we have carried better fit for grassland soil compared to arable soil in out pre-incubation to let the CO2 concentration in predicting laboratory soil respiration from soil tem- the outflow become quasi-constant. perature. This study shows when soil temperatures In summary, according to our field measurements are not a limiting factor, higher soil respiration rates in arable soil (Figure 1), diurnal soil respiration rates in grassland than in arable land occur resulting from peak around 12:00 and generally fluctuate following higher availability of substrates like glucose in soils changes in soil temperature while differences in (Iqbal et al. 2010; Uchida et al. 2012). A regression precipitation only explain a negligible proportion of analysis of soil respiration rate and DOC in two land variations in soil respiration rates (Table 6). Based on use types in this research (Table 7) indicated that soil results both measured in the field and in the laborat- respiration in arable land was regulated by DOC ory, seasonal changes in soil respiration rates show a more than in grassland soil. A nutrition or energy decreasing trend from April to July and values in shortage leads to an inhibition of soil respiration by winter are significantly lower than those of the growing restricting mineralization and microbial metabolic season (Figures 3 and 4). Laboratory incubation activities (Yoshitake et al. 2007; Hill et al. 2008). revealed that variations in DOC play a critical role in Hence, the soil respiration rate is more sensitive to driving the declining trend during the growing season DOC changes in arable land compared to grassland. as well as causing significant differences between soils Also arable soil respiration is regulated by BBM in grassland and arable land (Table 7). However, soil concentration (Table 7) while grassland soil respira- temperature remains the main factor leading to variation is not sensitive to changes in BBM. The decline tions in soil respiration rates observed in this study Acta Agriculturae Scandinavica, Section B — Soil & Plant Science 601

(Table 6). Soil moisture, in spite of being regarded as laboratory data. Concerning all moisture conditions, an important factor in many studies, had a limited it shows that incubation of soil samples in the effect on variations in soil respiration rates in Northern laboratory may mostly (except in the temperature German agricultural soils (Table 6). Additionally, C/ class 20–30°C and 25–35°C) underestimate the N ratios and MCV/MBS ratios also influence changes temperature sensitivity of soil respiration compared in soil respiration rates in grassland; while in contrast, to the values derived from the natural environment. it is BBM and MCV/MBS ratios that show positive effect on arable soil respiration (Table 7). Acknowledgments

Temperature sensitivities of soil respiration We are thankful to the technical assistants of the Division of Physical Geography – Landscape Ecology and Geoinfor- According to field results (Table 4), the occurrence of mation Science (LGI), Institute of Geography and of the Institute of Polar Ecology (IPÖ) of Kiel University for lab extremely high Q10 values in winter has mainly been attributed to low variations in soil temperature. Mean analyses. We especially acknowledge the farmers of the Danish Wahld region for supporting our fieldwork. Further Q10 values from a global database are 3.3 ± 1.5 when thanks go to Ms. Kirstin Marx, who contributed a lot to the soil temperature ranges from 0°C to 10°C (Bond- first draft. The LGI student assistants Katrin Schünemann, Lamberty & Thomson 2010). Smaller Q10 values are Nicole Wilder and Wolfgang Hamer kindly helped with observed in other months with higher ranges of soil collecting soil samples and lab work. The first author is very grateful to an overseas visiting PhD scholarship from the temperature because Q10 values decrease with increasing temperature (Kirschbaum 1995). Stange China Scholarship Council (CSC), Ministry of Education, PR China to study and develop research collaborations at and Neue (2009) pointed out in their research, that Christian-Albrechts-University Kiel, Germany. the variation of Q10 values under field condition usually are attributed to a combination of changes in the surrounding soil properties. When soil tem- Disclosure statement perature increases in the field, many progresses react No potential conflict of interest was reported by the simultaneously, such as stimulating more active authors. microbial activities, stronger photosynthesis and higher root exudations. That is, a combined effect instead of a single enzymatic reaction has leaded the Funding Q10 values deviate from two under field condition. We are also grateful to partially financial support for this According to laboratory results (Table 5), soil research provided by the National Natural Science Founda- respiration rate increased with temperature rising in tion of China funded project (41471230, 41171227). grassland while it only showed limited responses to temperature increase in arable land (Fang & Mon- References crieff 2001; Liu et al. 2006; Karhu et al. 2010). This Aulakh MS, Kabba BS, Baddesha HS, Bahl GS, Gill MPS. research shows that a lower temperature sensitivity in 2003. Crop yields and phosphorus fertilizer transfor- arable land, however, can be proved. More available mations after 25 years of applications to a subtropical Downloaded by [Zhanli Wang] at 02:40 27 July 2015 substrate usually stimulates stronger microbial activ- soil under groundnut-based cropping systems. Field – ities in the organic matter decomposition progress. If Crops Res. 83:283 296. Bloem J, Bolhuis PR, Veninga MR, Wieringa J. 1995. there is only limited substrate, the rise of soil Microscopic methods for counting bacteria and fungi respiration rate would be restricted even when soil in soil. In: Alef K, Nannipieri P, editors. Methods in temperature increases. That may be the reason why applied soil microbiology and biochemistry. New the temperature sensitivity of soil respiration is higher York: Academic Press; p. 162–173. in grassland compared to the values in arable land. Bölter M, Bloem J, Meiners K, Möller R. 2002. Enumera- tion and biovolume determination of microbial cells – The Q10 values increased at temperature classes a methodological review and recommendations for below 25°C probably because of the different optimal applications in ecological research. Biol Fertil Soils. temperatures for the variable mixes of microbe 36:249–259. species existing in the soil. For example, even facul- Bölter M, Müller-Lupp W, Takata K, Yabuki H, Moller R. tative psychrophiles, which can be isolated from soils 2003. Potential CO2-production in aerobic conditions from a Siberian tundra environment. Polar Biosci. in temperate climates, grow best when the temperat- 16:70–85. ure is between 25 and 30°C (Thomas & Madigan Bond-Lamberty B, Thomson A. 2010. A global database of 1991). Another optimal temperature range (25–35° soil respiration data. Biogeosciences. 7:1915–1926. C) is reported for one species of atrazine-degrading Butenschoen O, Marhan S, Scheu S. 2008. Response of Arthrobacter, strains of which are often isolated from soil microorganisms and endogeic earthworms to cutting of grassland plants in a laboratory experiment. agricultural soils (Wang & Xie 2012). In our study, Appl Soil Ecol. 38:152–160. arable Q10 values derived from the field measurement Carranca C, de Varennes A, Rolston DE. 1999. Variation varied in a larger range than that derived from the in N-recovery of winter wheat under Mediterranean 602 Y. Wang et al.

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Appendix

–1 –1 Table A1. Grassland soil respiration rate (µg CO2 g dry weight h ) at all (30%, 50% and 70%WHC) soil moisture conditions.

Temperature (°C) Parameter November 2011 April 2012 May 2012 June 2012 July 2012

5 Median 5.63 0.00 0.00 0.00 0.00 Range 0.00–12.59 0.00–4.96 0.00–5.84 0.00–2.87 0.00–6.38 10 Median 5.04 3.44 2.84 2.80 1.44 Range 0.00–14.76 0.00–8.31 0.00–8.75 0.00–6.53 0.00–5.87 15 Median 4.60 6.50 4.04 3.08 2.90 Range 0.00–16.87 0.00–14.69 0.00–8.74 0.00–8.96 0.00–8.8 20 Median 5.97 9.46 5.64 5.84 3.08 Range 0.00–14.54 3.07–14.69 0.00–11.67 0.00–11.01 0.00–11.74 25 Median 6.47 14.00 10.85 9.01 8.70 Range 0.00–17.6 7.03–21.47 0.00–19.26 3.20–15.03 0.00–17.61 30 Median 11.27 19.87 14.42 12.05 10.52 Range 0.00–21.05 7.03–32.21 8.31–26.26 5.99–22.02 0.00–23.48 35 Median 11.00 21.15 18.64 15.61 15.73 Range 0.00–21.81 7.03–34.60 11.08–32.10 10.77–33.03 2.80–29.35 40 Median 12.57 26.12 22.4 20.85 22.12 Range 0.00–25.66 3.52–42.29 16.34–38.52 8.24–40.37 11.21–32.28 All N 26 26 18 18 18

–1 –1 Note: The system error may disturb the values when soil respiration rate is below 2.8µg CO2 g dry weight h . N, number of measured results.

–1 –1 Table A2. Arable land soil respiration rate (µg CO2 g dry weigh h ) at all (30%, 50% and 70%WHC) soil moisture conditions.

Temperature (°C) Parameter November 2011 April 2012 May 2012 June 2012 July 2012

5 Median 5.18 0.00 2.51 0.00 0.00 Range 0.00–32.57 0.00–5.84 0.00–5.41 0.00–3.01 0.00–2.93 10 Median 4.56 2.81 2.70 2.77 0.00 Range 0.00–20.47 0.00–5.84 0.00–20.38 0.00–5.74 0.00–5.50 Downloaded by [Zhanli Wang] at 02:40 27 July 2015 15 Median 3.97 2.83 2.70 2.77 0.00 Range 0.00–13.46 0.00–8.88 0.00–7.34 0.00–6.00 0.00–5.74 20 Median 0.00 2.87 2.73 2.75 0.00 Range 0–15.06 0–8.88 0–7.34 0–5.83 0–13.58 25 Median 0.00 5.75 4.89 2.93 2.62 Range 0.00–5.75 0.00–11.84 0.00–8.18 0.00–8.94 0.00–8.15 30 Median 4.56 5.75 5.34 5.61 2.87 Range 0.00–13.46 2.66–14.19 0.00–8.22 0.00–9.01 0.00–10.87 35 Median 4.56 6.08 6.77 5.85 5.24 Range 0.00–11.94 0.00–17.76 0.00–12.20 0.00–11.82 0.00–16.19 40 Median 0.00 7.50 5.76 7.84 5.48 Range 0.00–11.64 0.00–17.76 2.51–10.96 0.00–14.89 2.61–26.22 All N 25 23 21 21 21

–1 Note: N, number of measured results. The system error may disturb the values when soil respiration rate is below 2.8 µg CO2 g dry weight h–1.