- Email: [email protected]
Responses of soil organic matter and greenhouse gas fluxes to soil management and land use changes in a humid temperate region of southern Europe
Soil Biology & Biochemistry 36 (2004) 917–925 www.elsevier.com/locate/soilbio
Responses of soil organic matter and greenhouse gas fluxes to soil management and land use changes in a humid temperate region of southern Europe Agustı´n Merino*, Pilar Pe´rez-Batallo´n, Felipe Macı´as Department of Soil Science and Agricultural Chemistry, Escuela Polite´cnica Superior, Universidad de Santiago de Compostela, Campus Universitario E-27002 Lugo, Spain Received 1 November 2002; received in revised form 27 January 2004; accepted 1 February 2004
Abstract We studied the effects of soil management and changes of land use on soils of three adjacent plots of cropland, pasture and oak (Quercus robur) forest. The pasture and the forest were established in part of the cropland, respectively, 20 and 40 yr before the study began. Soil organic matter (SOM) dynamics, water-filled pore space (WFPS), soil temperature, inorganic N and microbial C, as well as fluxes of CO2, CH4 and N2O were measured in the plots over 25 months. The transformation of the cropland to mowed pasture slightly increased the soil organic and microbial C contents, whereas afforestation significantly increased these variables. The cropland and pasture soils showed low CH4 uptake rates (,1 kg C ha21 yr21) and, coinciding with WFPS values .70%, episodes of CH4 emission, which could be favoured by soil compaction. In the forest site, possibly because of the changes in soil structure and microbial activity, the soil always acted as a sink for CH4 (4.7 kg C ha21 yr21). The N2O releases at the cropland and pasture sites (2.7 and 4.8 kg N2O-N ha21 yr21) were, respectively, 3 and 6 times higher than at the forest site (0.8 kg N2O-N ha21 yr21). The highest N2O emissions in the cultivated soils were related to fertilisation and slurry application, and always occurred when the WFPS . 60%. These results show that the changes in soil properties as a consequence of the transformation of cropfield to intensive grassland do not imply substantial changes in SOM or in the dynamics of CH4 and N2O. On the contrary, afforestation resulted in increases in SOM content and CH4 uptake, as well as decreases in N2O emissions. q 2004 Elsevier Ltd. All rights reserved. Keywords: Microbial biomass; Microbial activity; Soil respiration; Nitrous oxide; Methane; Soil organic matter; Land use
1. Introduction Soil organic C plays an essential role in determining the physical and chemical characteristics of a soil and therefore in determining its fertility. The microbial biomass is a fraction of the soil organic matter (SOM) that is actively involved in the transformation of soil organic residues and in the dynamics of N, P and S. Soil microbial biomass and its activity, especially sensitive to human activity, are suitable predictors of soil biological status in terms of soil fertility (Elliot et al., 1996). Soil respiration has received considerable attention in recent years because of the release of large quantities of CO2 from the soils to the atmosphere. Changes in land use and soil management practices (tillage, use of fertilizers, organic residues, pesticides) induce * Corresponding author. Tel.: þ 34-982-285891; fax: þ 34-982-285926. E-mail address: [email protected] (A. Merino). 0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2004.02.006
changes in soil organic C, and are largely responsible for increases in atmospheric CO2 from terrestrial ecosystems (Bouwman, 1990). Soil also plays a major role in contributing to the atmospheric concentrations of other greenhouse gases, such as CH4 and N2O. The fluxes of these gases are influenced by soil variables that influence microbial activity, such as pH þ and concentrations of NO2 3 , NH4 and O2, which, in turn, are controlled by a combination of soil properties (soil moisture, texture, structure) and soil management practices. Intensive soil management has therefore led to a considerable increase in the exchange of N2O and CH4 between soils and the atmosphere (Bouwman, 1990; IPCC, 1995). In natural upland soils, CH4 is oxidised by methanotrophic and—to a lesser extent—NH4-oxidizing bacteria. Although soil is a major sink for atmospheric CH4, methanotrophic activity is greatly affected by changes in soil properties influencing gas diffusiveness (Mosier et al.,
918
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
1991; Dobbie and Smith, 1996; Flessa et al., 1995). Cultivation of undisturbed soils has a long-term effect on the capacity of the soils to take up CH4. Although accumulated data show variable effects of N on CH4 uptake, N fertilisation rapidly reduces the capacity of CH4 uptake as a consequence of the inhibition of CH4 oxidation activity of methanotrophs, by NHþ 4 or NH3 (Steudler et al., 1989). Soil compaction by tractor traffic can also substantially reduce the uptake of CH4 (Hansen et al., 1993) and the soils can thus become a net source of atmospheric CH4 (Ruser et al., 1998). Agricultural soils are the main anthropogenic source of N2O to the atmosphere. Rates of emission of N2O and the relative proportions produced by nitrification and denitrification are influenced by environmental factors and by soil management practices (Mosier et al., 1991). Nitrous oxide dynamics are largely determined by N fertilisation, so that approximately 1.25% of fertilizer N is assumed to be lost by denitrification (IPCC, 1995). The incorporation of certain crop residues (sugar beet, potato) can also result in increased N2O emissions (Aulakh et al., 1991; Kaiser et al., 1998). Moreover, some studies carried out in Central Europe have stressed the importance of N2O emissions during winter as a consequence of daily freezing and thawing cycles (Flessa et al., 1995; Kaiser et al., 1998). In Northern Spain and many other countries arable land is increasingly used for other purposes involving less intensive management, such as pasture or newly planted forest. These changes in land use, made in response to the lower population densities in rural areas, as well as environmental or economical strategies, have noticeably increased the grassland and forest areas. Such changes can substantially alter SOM dynamics (Rodrı´guez-Murillo, 2001) thereby affecting exchanges of greenhouse gases between the soil and the atmosphere. Less intensive management improves biological properties (Emmerling et al., 2001) and conversion of agricultural land to forest usually results in considerable gains in soil organic C and reductions in CO2 fluxes (Paul et al., 2002). Furthermore, some authors have also pointed out that after ceasing cultivation and fertilisation the capacity for CH4 oxidation in soils increases, although recovery is very slow and takes place over some years (Prieme´ et al., 1997), specially in organic soils (Maljanen et al., 2001). There is a growing interest in Spain, and elsewhere, in investigating the effectiveness of afforestation in sequestering atmospheric C and improving soil properties linked to SOM (aggregate stability, water holding capacity and nutrient retention). In addition, few field measurements of greenhouse gases in southern European countries have been made and the data available are not sufficient to enable evaluation of the repercussion of soil management on the dynamics of greenhouse gases. The objective of our study was to determine the dynamics of SOM and soil greenhouse gases in a southern European region and to relate these to land use, soil management practices and abiotic factors.
Particular attention was paid to the response of these variables where arable land had been converted to uses involving less intensive management, such as pasture or forest.
2. Material and methods 2.1. Study site We studied three soils in adjacent plots under cropland, sown pasture and oak forest. The cropland selected has been under continuous cultivation of different crops for at least 200 yr, whereas the pasture and the oak forest were established in part of the former cropland, respectively, 20 and 40 yr before our study began, in 1998. The three plots are situated on a rather flat landscape (slope ranges from 0 to 5%). The altitude of the sites is 500 m a.m.s.l. The climate is temperate subtropic with humic winters. The average annual precipitation is 1022 mm and the average annual temperature, 11.7 8C. Although precipitation is distributed throughout the year, winter is the most humid season and intense rainstorms occur in spring and autumn. The general soil moisture regime in the region is Udic and the soil temperature regime is Mesic. Visual examination of the three soil profiles indicated that the soils were very similar. The soils were derived from the same parent material, acid mica-schist, and had similar morphologies. According to the FAO system (FAO-Unesco, 1998), the soils are classified as dystric Cambisol and some major properties are shown in Table 1. The forest soil has a well-developed soil profile with an O (L þ F) organic horizon of 4– 6 cm depth. It is characterized by strong acidification with a base saturation of less than 15%. The texture of the surface soil horizon is silt loam. 2.2. Soil management in the study plots During the study period (July 1998 –July 2000) the following crop rotation was used: potato—Solanum tuberosum (June 1998 –October 98), turnips—Brassica rapa (November 98– April 99), onion—Allium cepa (May 99– September 99) and rye—Secale cereale (October 99 – April 00), which is a common crop sequence in the region. Table 1 Some properties of the A horizon in the soils studied
pH (H2O) pH (KCl) Extract. P (mg kg21) CECea (cmol kg21) Al saturation (%) a
Cropland
Pasture
Forest
5.0 4.3 60 11.9 6
5.4 4.0 55 9.2 10
4.3 3.7 15 7 60
Effective cation exchange capacity.
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
In spring 2000, the rye crop was mechanically incorporated into the soil as a green amendment. Tillage and mineral fertilization (750 kg ha21 of 15-15-15 NPK) were carried out before the establishment of the next crop. The onion crop was irrigated periodically. The pasture is a mixture of ryegrass (Lolium perenne), white clover (Trifolium repens) and red clover (Trifolium pratense), which is normally renovated every 3 yr. The site had been grazed by cattle and since 1990 has become mowed pasture. The annual productivity ranges between 10 and 15 t ha21. For pasture renovation, the soil is ploughed (mouldboard ploughing at 20 cm depth followed by rolling) and mineral fertilizers and lime are added. Slurry from cows is normally applied in spring and autumn. The pasture used for this study was renovated in September 1996. During the study period new pasture was established (in October 1999); for its renovation, the soil was moldboard ploughed to a depth of approximately 0.2 m and inorganic fertilizer (750 kg ha21 of 15-15 15 NPK) and lime (3000 kg ha21) were added. Cow slurry was applied in November 1998 and June 1999 (60 and 50 m3 ha21, respectively). The pasture was mown in October 1998, April 1999, June 1999, October 1999 and June 2000. The forest site was derived from the former cropland by afforestation with English oak-Quercus robur. The average tree density and basal area are 550 ha21 and 10 m2 ha21, respectively. 2.3. Soil sampling The study was carried out over 25 months, between July 1998 and July 2000. Precipitation and air temperature measurements were provided by the nearby meteorological station at Fingoi. During this study measurements were made of soil temperature, humidity, inorganic N, total organic C and N, microbial biomass C and fluxes of CO2, N2O and CH4. These variables were determined in four replicate plots of each system, at 2 – 3 week intervals, except for microbial biomass C, which was determined every 1 – 3 months. At the pasture and the cropland sites, gases were monitored more intensively after each fertilizer application. For the determination of moisture, inorganic N and microbial biomass C, in each of the plots and at each sampling time, soil cores were collected from the upper 15 cm of the A horizon from three randomly selected points, using a PVC core (50 mm dia). The soil cores were taken to the laboratory, where composite samples for each plot were sieved (2 mm). The static chamber system, as described by Hutchinson and Mosier (1981), was used to measure surface CO2, CH4 and N2O fluxes from the soil. Dark, circular chambers with an inner diameter of 29.5 cm and height of 19.45 cm were used. A chamber base (collar) was inserted in each plot to a depth of 2 cm, and was retained in place for the entire sampling period, only being removed before soil management practices and then replaced in the same position.
919
The first measurements were made 1 month after insertion of the frame. In the arable cropland the gas fluxes were measured in the ridges (two plots) and in the interrows (two plots). Gas measurements were made every sampling day between 10:00 and 12:00 a.m. and were assumed to represent the average gas flux for that day (Larionova et al., 1998; Kessavalou et al., 1998). The surface plant cover inside the frames was cut before measurements. In order to avoid disturbance and variations in results, gas samples were collected during 30 min every 10 min in glass vacuum flasks (60 ml) sealed with a butyl rubber septum. At the end of each sampling period, the chamber was removed from the base. 2.4. Soil processing and analysis Soil temperature at a depth of 10 cm was measured at the same time as each gas sampling. Soil total C and N were determined by dry combustion, using an element analyser (LECO-2000, LECO Corporation, St Joseph, Michigan, USA). The pH was measured in H2O and 0.1 M KCl (soil:solution ratio of 1:2.5). Soil moisture was determined gravimetricaly after oven drying (105 8C; 24 h). The waterfilled pore space (WFPS) was calculated as follows: WFPS ¼ [gravimetric water content £ soil bulk density)/ total soil porosity], where soil porosity ¼ 1 2 soil bulk density/2.65 (2.65 being the assumed particle density of the soil). In the two cultivated soils, bulk density was determined frequently. Samples for determination of bulk density were taken, from four points in each plot, using a brass core (40 cm long, 55 mm inside dia). The calculated mean soil bulk densities of the upper mineral layer are given in Table 2. Ammonium and NO2 3 were extracted with 2 M KCl and measured photometrically. Microbial biomass C was measured using the method of fumigation-extraction of soil samples with chloroform (Vance et al., 1987). Moist samples of soil were incubated in desiccators for 18 h, at Table 2 Average and standard deviation (in parenthesis) values of the variables recorded in the A horizons during the period July 1998– July 2000 in the three studied soils. Significantly different means are indicated by different letters, a . b ðP , 0:05Þ
Soil temperature (8C) Soil moisture (%) Bulk density (g cm23) Organic C (g kg21) Total N (g kg21) Microbial C (mg kg21) Microbial C: org C 21 NO2 3 -N (mg kg ) 21 NHþ 4 -N (mg kg ) CO2-C (mg m22 h21) CH4-C (mg m22 h21) N2O-N (mg m22 h21)
Cropland
Pasture
Forest
12.0 (4.6) 18.2 (7.2) 1.30 (0.1)a 16.3 (0.7) b 1.2 (0.08) b 224 (137) b 1.60 (0.80) 5.3 (6.3) 4.8 (5.0) 41.6 (28.0) 20.37 (29.5) 32.5 (18.6)
11.4 (5.5) 18.6 (8.1) 1.25 (0.1)ab 17.7 (1.1) b 1.6 (0.09) b 276 (124) b 1.56 (0.67) 6.2 (5.6) 11.6 (16.1) 45.2 (29.9) 0.8 (49.1) 32.1 (26.5)
11.5 (6.1) 25.2 (6.8) 1.1 (0.1) b 37.7 (5.2) a 1.8 (0.05) a 620 (216) a 1.46 (0.50) 1.9 (1.1) 6.5 (3.8) 38.8 (25.0) 243.62 (48.0) 12.0 (12.8)
920
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
room temperature and with alcohol-free chloroform vapour. Another set of soil samples was similarly incubated but without the chloroform. Soluble C was extracted with 0.5 M K2SO4 and determined by digestion with K2Cr2O7 and titration with (NH4)2FeSO4. The difference in organic C in three fumigated and three non-fumigated samples was calculated. Concentrations of CO2 and N2O were determined using a gas chromatograph fitted with an electron capture detector (ECD), whereas CH4 was measured with a flame ionization detector (FID). A 3 m-Porapack Q (Millipore, Milford, Mass.) column was used with N2 (20 ml min21) as the carrier gas. The temperatures of the oven and ECD were 35 and 280 8C, respectively. Gas fluxes were calculated from the linear increase or decrease in gas concentrations in the chambers. All samples were analysed within 2 weeks of collection (previous tests showed that the concentration of the gases analysed did not change during this period).
Fig. 1. Water-filled pore space (WFPS) in the cropland, mowed pasture and forest soils.
3.2. Inorganic N There were large differences in the amounts of þ extractable NO2 3 and NH4 in the different soils (Fig. 2). The amounts of inorganic N in the arable land increased after addition of mineral fertiliser and tillage (November
2.5. Statistical analyses The effects of management on all the variables studied were tested using an ANOVA. The relationships among soil factors, namely WFPS, soil temperature, soil NO2 3 and microbial biomass, and the mean flux rates of CO2, CH4 and N2O were analyzed by stepwise linear and quadratic regressions. Statistical differences in soil surface gas fluxes among the three ecosystem types for each date were determined using a t-test for least significant differences (LSD). As the N2O emission rates were log-normally distributed, logarithmic (natural base) transformation were carried out to normalize the N2O data. Cumulative CH4 and N2O losses from each site were calculated from the integrated weekly fluxes of the four replicates, assuming a constant flux rate beginning with the date of each gas sampling until the next gas sampling.
3. Results 3.1. Climatic conditions Precipitation between July 1998 and July 2000 was 1640 mm. Most of the precipitation fell in winter and spring. Intense rainstorms occurred in spring 1999, October 1999, December 1999 and April 2000 (data not shown). Soils were driest in July and wettest in spring. At many sampling times the WFPSs were substantially larger in the two cultivated soils ðP , 0:05Þ; especially in the cropland soil (Fig. 1). The daily air and soil temperatures were always above freezing. In winter, the soil temperature measured at midday was approximately 0.5 8C higher in the forest plot; by contrast, during summer, the soil temperature was lower at this site.
2 Fig. 2. Changes in soil NHþ 4 (a) and NO3 (b) at the cropland, mowed pasture and forest sites.
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
1998, May 1999, October 1999) and incorporation of green plant residues of the rye crop (April 2000). In the soil under þ pasture, the amounts of NO2 3 and NH4 were low during most of the study period and increased after addition of cow slurry (November 98, May 1999), tillage and application of mineral fertiliser (October 1999). The first addition of slurry, carried out in autumn 1998, led to very high 2 quantities of NHþ 4 and NO3 , probably due to a lack of N uptake by plants. In the forest soil, the concentration of 2 NHþ 4 , which was always higher than that of NO3 , varied considerably, reaching maximum amounts of 16 mg kg21. The concentration of NO2 3 -N was always lower than 6 mg kg21. 3.3. Soil total organic C, microbial biomass and respiration Soil total organic C (in surface units) in the forest soil was almost twice that of the cropland soil ðP , 0:001Þ: The SOM in the pasture plot was slightly higher than that of the cropland plot (Table 2). Microbial biomass variations depended on seasonal changes and the type of agriculture management practice. The amounts of microbial C decreased during the driest seasons and were also low during the coldest or wettest months (Fig. 3a). The annual average concentrations of microbial C in the forest soil were 2 –3 times higher than in the agricultural soils. Differences among different sampling times within each site and among the three sites were significant ðP , 0:001Þ: In spite of the differences in land uses, the ratios of microbial C to organic C were similar in all three soils (Fig. 3b), although, in the pasture increases in this ratio were apparent in 1999 following the cow slurry application. The CO2 fluxes in the three systems (Fig. 4) were significantly different over time ðP , 0:05Þ: The ranges for the cropland and pasture soils were 5.1 – 119.0
921
Fig. 4. Soil respiration rates measured at the cropland, mowed pasture and forest sites.
and 8.4 – 179.0 mg CO2-C m22 h21, respectively. In the forest soil they ranged from 9 to 123 mg CO2-C m22 h21. The amount of CO2 released from the cropland was less than from the forest and pasture, especially during the first year. Large increases took place after land preparation, where maxima of 100 – 150 mg m22 h21 were recorded. The largest increase took place in April 2000, after the incorporation of the rye crop. During most of the study period, significantly more CO2 was released from the pasture soil than from the cropland and forest soils. The greatest differences were observed after tillage (September 1999) and application of dairy cow slurry (November 1998, May 1999), when a maximum of 100 mg CO2-C m22 h21 was measured. In these cultivated soils, the relationships between CO2 and either soil moisture or temperature were weak. However, there was a relationship between CO2 and microbial C (r ¼ 0:68 for the cropland soil; r ¼ 0:33; for the pasture soil). In the forest soil, the highest rates of soil respiration took place when the soil temperature was relatively high and the humidity moderate (October 98, October 99 and May 2000). By contrast, minimum values occurred in winter, coinciding with periods of low soil temperature (lower than 10 8C) and high soil moisture content (higher than 50% of WFPS). Low soil moisture content, corresponding to a WFPS of 10%, was important in reducing CO2 emission in summer. In the forest soil, CO2 flux correlated weakly with soil moisture (r ¼ 20:37; P , 0:05) and soil temperature (r ¼ 0:35; P , 0:05) but more strongly with soil microbial C (r ¼ 0:73; P , 0:01). 3.4. CH4 fluxes
Fig. 3. Soil microbial C (a) and ratio of microbial biomass: organic C (b) in the three systems studied.
Similar patterns of changes in CH4 fluxes were observed for the pasture and cropland soils. During most of the study period the cropland soil showed lower CH4 uptake rates and, at some times, net emissions of CH4 were observed (Fig. 5). The episodes of emission occurred during the periods of heaviest precipitation (December 1999 – March 1999, December 2000 – April 2000). By contrast, CH4 uptake was highest during the summer months, coinciding with low soil moisture content. The measured fluxes ranged from a CH4-C uptake of 50 mg m22 h21 to CH4-C emission of 125 mg m22 h21. Linear regression analysis revealed
922
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
Fig. 5. Methane fluxes from the three plots studied: cropland, mowed pasture and forest. Negative values are consumption rates of CH4, positive values are emission rates of CH4.
a weak relationship between CH4 uptake rate and both WFPS (r ¼ 20:46; P , 0:05) and temperature (r ¼ 20:32; P , 0:05) throughout the study period. The emission peak recorded in November 1998, coincided with the application of cow slurry and high soil moisture. The soil tillage carried out in October 99 apparently did produce changes in the CH4 fluxes. The measured fluxes ranged from a CH4-C uptake of 132 mg m 22 h21 to CH 4-C emission of 200 mg m22 h21. In this soil, CH4 fluxes were significantly correlated with WFPS (r ¼ 20:35; P , 0:05), NO2 3 -N (r ¼ 20:33; P , 0:05) and NHþ 4 - N (r ¼ 0:35; P , 0:05). Unlike the agricultural soils, there was a net consumption of CH4 in the forest soil, throughout most of the study. In this soil, there was seasonal variation in CH4 uptake that was similar to the changes in soil moisture content. There was only one episode of CH4 emission, which coincided with a very high soil moisture content, but which was much less than in the agricultural soils. The measured fluxes ranged from a CH4-C uptake of 116 mg m22 h21 to CH4-C emission of 3 mg m22 h21. In this forest soil, the CH4 uptake correlated significantly with the WFPS (r ¼ 20:63; P , 0:001), soil temperature (r ¼ 0:42; P , 0:01), NHþ 4 (r ¼ 0:58; P , 0:001) and C microbial biomass (r ¼ 0:55; P , 0:05). The results of stepwise multiple linear regression showed that soil moisture content and concentration of NHþ 4 accounted for up to 52% of the variation in CH4 flux.
3.5. N2O fluxes In the cropland soil, the pattern of N2O dynamics was characterised by low emission rates on most sampling dates and a few dates on which flux rates were higher than 50 mg N m22 h21 (Fig. 6). Small negative fluxes of N2O were observed at this site. The highest emissions coincided with increases in soil inorganic N concentrations brought about after soil tillage and mineral fertilisation (November 1998, May 1999 and October 1999). In spring, pulses of higher N2O emissions coincided with rewetting of the soil. The incorporation of the rye crop in April 2000 did not increase the soil inorganic N and did not affect the N2O fluxes. In this soil, significant relationships ðP , 0:05Þ among N2O fluxes, soil NO2 3 concentrations and WFPS were apparent. However, throughout the study these factors only accounted for up to 20% of the variation in N2O emission. No relationships between N2O emission and either soil or air temperature were found. In the pasture soil, the application of cow slurry and N fertilizer led to highest N2O emissions. The greatest increases took place after the first application of cow slurry (November 1998) and mineral fertilisation (October 1999), which coincided with high soil moisture contents and high concentrations of inorganic N. However, the second application of cow slurry (June 1999) led to much lower
Fig. 6. Nitrous oxide flux rates recorded at the cropland, mowed pasture and forest sites.
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
N2O increases, probably because of the lower soil moisture þ content and lower concentrations of NO2 3 and NH4 in the soil. As at the cropland, N2O emissions were significantly related to soil NO2 3 concentrations and WFPS ðP , 0:05Þ throughout the entire study period, although the relationship was also weak ðR2 ¼ 0:21Þ: In this soil, N2O emissions were also significantly correlated with microbial C (r ¼ 0:61; P , 0:05). In comparison with those in the agricultural soil, the N2O fluxes in the forest soil were very low throughout the study and exhibited weak seasonality. The highest emission rates coincided with the highest amounts of NHþ 4 (r ¼ 0:36; P , 0:05) and soil moisture (r ¼ 0:33; P , 0:05) and always took place when the soil moisture content was higher than 25%.
4. Discussion 4.1. Soil total C, microbial C and respiration The values of microbial biomass and the ratio of biomass C to organic C recorded are consistent with values reported for other arable (Wardle, 1998) and forest soils (Dı´az-Ravin˜a et al., 1995). In our study, microbial C decreased during the driest and coldest seasons, and also during prolonged periods of water saturation, which can be attributed to variations in substrate availability and to drying and re-wetting effects (Kaiser and Heinemeyer, 1993; Pe´rez-Batallo´n et al., 2001). The increase in the amount of C in the pasture soil was much smaller than in the afforested soil, probably because of the shorter period of transformation and the intensive management of this soil. Emmerling et al. (2001) have also reported slight increases in soil microbial biomass following the use of less intensive agricultural practices. The increase in the ratio of microbial C: organic C observed in the pasture during 1999 was probably due to the presence of readily available C, introduced through cow slurry application during the previous autumn. In the forest soil, in spite of the higher microbial C, the ratio of microbial C: organic C was similar to those in the agricultural soil, which may indicate adverse properties resulting from the soil acidity and low nutrient availability, as suggested by Priess and Fo¨lster (2001). The CO2 release followed the order pasture . forest . cropland. The differences among the three systems reflect differences in environmental conditions (mainly soil moisture content and temperature), input of organic residues and, in the case of the forest site, acidification, all of which influence soil organic contents, microbial activities and root densities. Seasonal variations in CO2 release mainly followed the annual changes in soil temperature and moisture, as it has also been found in other temperate forest ecosystems (Larionova et al., 1998). The poor relationship between the fluxes of this gas and both soil moisture and soil
923
temperature may be due to the antagonistic effects of soil moisture; CO2 release is enhanced during periods when soil moisture is limiting and reduced when soil moisture is in excess. Thus, CO2 release was greatly reduced during periods of heavy rain, when the WFPS was . 50%, probably as a consequence of O2 deficiency in the soil (Howard and Howard, 1993). The low rates of CO2 fluxes measured during these seasons coincided with lower CH4 uptake rates, which suggests that the lower CO2 production may also be due to a change in the metabolic pathway of the microbial community, to fermentation. The largest increases in CO2 fluxes in these soils were produced after tillage, mineral fertilization and manure application, coinciding with responses observed in other studies (Kessavalou et al., 1998; Mosier et al., 1991; Priess and Fo¨lster, 2001). The increased CO2 production observed in the pasture soil during the first 10 days following manure addition was due to mineralization of the large amount of readily oxidizable C. Flessa and Beese (2000) found that accelerated mineralization led to the respiration of 40% of the C added in manure within 9 weeks. 4.2. CH4 fluxes The average annual CH4 uptakes of 0.2 and 0.9 kg C ha21 found in the cropfield and grassland were in the lower range reported for agricultural soils from other regions (Steudler et al., 1989; Mosier et al., 1991; Flessa et al., 1995). The average annual uptake of 4.7 kg C ha21 estimated for this forest soil was similar to those reported for other mature forest soils (Dobbie and Smith, 1996; Prieme´ et al., 1997; Borken and Brumme, 1997). The fluxes of this gas depend on WFPS, therefore we must take into account that the precipitation recorded during these 2 years was lower than the annual average. In the three plots the patterns of CH4 fluxes were mainly influenced by soil moisture and NHþ 4 -N contents, whereas soil temperature was found to be a secondary factor. The lower uptake rate recorded during periods of high WFPS was caused by the reduced diffusiveness of CH4 and O2 into the soil, which produced temporary anaerobic conditions (Do¨rr et al., 1993). Net CH4 emissions from the soil to the atmosphere, such as we observed in the forest soil, are not common in upland forest soils, although they have been observed during periods of high soil moisture, following snowmelt (Yavitt et al., 1995). Most of the CH4 emission episodes observed in these soils were not only linked to management practices (Flessa and Beese, 2000), but they also took place at times when the WFPS was . 60%, even without any manure application. The release of this gas may be favoured by compaction, which is consistent with other researchers who found very low rates of CH4 uptake (Hansen et al., 1993) and net CH4 emissions (Ruser et al., 1998) in compacted, agricultural soils. The negative effect of soil NHþ 4 -N on CH4 uptake was much less evident in the two agricultural soils. This different
924
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
behaviour (between CH4 and NHþ 4 ) has also been reported by Dobbie and Smith (1996) and Flessa et al. (1995), who have suggested that in arable lands the inhibition of CH4 oxidation by NHþ 4 occurs after the initial application of fertiliser and continues for some years afterwards. Our results show that in spite of the lower intensity of tillage and N fertilization than at the cropland site, this was not sufficient to increase the CH4 uptake rate in the pasture soil. Ojima et al. (1993) also found less CH4 consumption in intensively managed grasslands in comparison with native prairie. By contrast, the conversion of cropland to forest soil carried out 40 yr ago has led to substantial increases in the CH4 oxidation rates. These findings are consistent with those of Ambus and Christensen (1995), who observed higher CH4 uptakes in abandoned farmland, and with those of Prieme´ et al. (1997), who compared the CH4 uptake in forests of different ages. Increased CH4 uptake in this soil should be produced by the increase in SOM and the subsequent higher structural stability and presence of macropores, all of which favour the diffusiveness of CH4 and O2 into the soil profile. In addition, the improved soil aeration, along with the lack of N fertilisation, may have enhanced the number and activity of methanotrophic bateria. Since methanotrophic bacteria are acid tolerant and adapt to soils with different acidities (Steudler et al., 1989; Borken and Brumme, 1997), soil acidification after afforestation probably did not affect the CH4 dynamics. 4.3. N2O fluxes The average annual N2O-N emissions from the cropland and pasture soils (2.7 and 4.8 kg ha21, respectively) were similar to those reported for agricultural soils elsewhere (Bouwman, 1990). Higher releases are normally found in more intensively fertilised fields, drained organic soils (Bouwman, 1990) and other cultivated soils from Central Europe subjected to frost-thaw events (Flessa et al., 1995; Kaiser et al., 1998). The average N2O-N emission rate recorded in the forest soil and the average annual emission (0.8 kg ha21) were similar to those reported for other temperate forests (Bouwman, 1990; Borken and Brumme, 1997). As found in other studies (Flessa et al., 1995; Kaiser et al., 1998), N2O fluxes were influenced by soil inorganic N concentrations, as well as by WFPS. In the two agricultural soils, each fertilisation was followed by increases in NO2 3 and, subsequently, N2O emissions. The low fluxes in the forest soil are related to the lower soil NO2 3 concentrations and WFPS. This suggests that in this case, N2O production was limited by anaerobic conditions and a lack of NO2 3. The losses by N2O emission made up 0.5% and 1.0% of the N added by fertilization respectively in the cropfield and grassland. However, it should been taken into account that N2O measured only constitutes a portion
of the gaseous N lost, because during periods of higher WFPS a significant fraction of the N2O can end up as N2 (Estavillo et al., 2002). The relatively low N2O emissions, as well as the occasional negative fluxes observed at the agricultural sites, may be produced by the reduction of N2O to N2 in periods of high soil moisture and low N2O production. Unlike other studies (Aulakh et al., 1991; Kaiser et al., 1998), the incorporation of crop residues by ploughing in the cropland plot did not lead to increased N2O emissions, probably because the WFPS of the soil was rather low from that time onwards. The relatively high C to N ratios, which may have impeded N losses due to denitrification, should also be taken into account (Aulakh et al., 1991). Although denitrification is controlled by the supply of readily decomposable SOM, the slight increase in SOM was not sufficient to produce a higher N2O release. On the other hand, the development of the gramineous root system in the grassland may have favoured aeration of the mineral soil, reducing the formation of this gas. However, measurements of bulk density and WFPS did not reveal substantial changes. Afforestation, on the contrary, led to decreases in N2O emission, which can be attributed to the lack of N fertilization as well as to modifications in soil properties as a consequence of the abandonment of the agricultural activity. One important change seen after afforestation was the development of an upper organic horizon. According to Borken and Brumme (1997), the contribution of the organic layer to the N2O release from the soil can be significant, although the response depends on the type of the organic horizons. It is possible that the improvement in soil structure and aeration produced conditions that were less anaerobic and subsequently, anaerobic microorganisms were less likely to be present. In addition, the progressive acidification probably reduced the net N-mineralization, although this effect does not necessarily mean a lower N2O production, because acidification also inhibits N2O reductase, resulting in a higher yield of N2O than N2 (Weier and Gillam, 1986). In boreal organic soils, however, afforestation does no necessary causes decreases in N2O fluxes because the lowering in the water table is associated with NO2 3 production (Maljanen et al., 2001).
Acknowledgements We are grateful to the staff of the Escuela Polie´cnica for their valuable support and cooperation during the field work. Ms. Pilar Pe´rez-Batallo´n also thanks the University of Santiago de Compostela for a postgraduate scholarship. We thank Ms. Maria Fe´ Lo´pez and Ms. Lucı´a Medina, for their assistance in the laboratory. We also appreciate the positive
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
and valuable suggestions given by the two anonymous referees.
References Ambus, P., Christensen, S., 1995. Spatial and seasonal nitrous oxide and methane fluxes in Danish forest-, grassland-, and agroecosystems. Journal of Environmental Quality 24, 993–1001. Aulakh, M.S., Doran, J.W., Walters, D.T., Mosier, A.R., Francis, D.D., 1991. Crop residue type and placement effects on denitrification and mineralization. Soil Science Society of America Journal 55, 1020–1051. Borken, W., Brumme, R., 1997. Liming practice in temperate forest ecosystems and the effects on CO2, N2O and CH4 fluxes. Soil Use and Management 13, 157–251. Bouwman, A.F., 1990. Exchange of greenhouse gases between terrestrial ecosystems and the atmosphere. In: Bouwman, A.F., (Ed.), Soils and the Green House Effect, Wiley, Chischester, pp. 61–127. Dı´az- Ravin˜a, M., Acea, M.J., Carballas, T., 1995. Seasonal changes in microbial biomass and nutrient flush in forest soils. Biology and Fertility of Soils 19, 220– 226. Dobbie, K.E., Smith, K.A., 1996. Comparison of CH4 oxidation rates in woodland, arable and set aside soils. Soil Biology & Biochemistry 28, 1357–1365. Do¨rr, H., Katruff, L., Levin, I., 1993. Soil texture parameterization of the methane uptake in aerated soils. Chemosphere 26, 697–713. Elliot, L.F., Lynch, J.M., Papendick, R.I., 1996. The microbial component of soil quality. In: Stozky, G., Bollag, J.-M. (Eds.), Soil Biochemistry, vol. 9. Marcel Dekker, New York, pp. 1–20. Emmerling, C., Edelhoven, T., Schro¨der, D., 2001. Response of soil microbial biomass and activity to agricultural de-intensification over a 10 year period. Soil Biology & Biochemistry 33, 2105–2114. Estavillo, J.M., Merino, P., Pinto, M., Yamulki, S., Gebauer, G., Spake, A., Corr, W., 2002. Short term effect of ploughing a permanent pasture on N2O production from nitrification and denitrification. Plant and Soil 239, 253 –265. FAO-Unesco, 1998. World reference base for soil resources. World Soil Resources Reports, 84, FAO, ISRIC and ISSS, Rome. Flessa, H., Beese, F., 2000. Laboratory estimates of trace gas emissions following surface application and injection of cattle slurry. Journal of Environmental Quality 29, 262 –268. Flessa, H., Do¨rsch, P., Beese, F., 1995. Seasonal variation of N2O and CH4 fluxes in differently managed soils in southern Germany. Journal of Geophysical Research 100, 23115–23124. Hansen, S., Maehlum, J.E., Bakken, L.R., 1993. N2O and CH4 fluxes in soil influenced by fertilization and tractor traffic. Soil Biology & Biochemistry 25, 621 –630. Howard, D.M., Howard, P.J., 1993. Relationships between CO2 evolution, moisture content and temperature for a range of soil types. Soil Biology & Biochemistry 25, 1537– 1546. Hutchinson, G.L., Mosier, A.E., 1981. Improved method for field measurement of nitrous oxide fluxes. Soil Science Society of America Journal 45, 311–316. IPCC, 1995. Climate change Scientific and Technical Analysis of Impacts, Adaptions and Mitigation. Contribution of Working Group II to the Second Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, London. Kaiser, E.-K., Heinemeyer, O., 1993. Seasonal variations of soil microbial biomass carbon within the plough layer. Soil Biology & Biochemistry 25, 1649–1655.
925
Kaiser, E.A., Kohrs, K., Ku¨che, M., Schnung, E., Munch, J.C., Heinemeyer, O., 1998. Nitrous oxide release from arable soil: importance of N fertilization, crops and temporal variation. Soil Biology & Biochemistry 30, 1553–1563. Kessavalou, A., Mosier, A.R., Doran, J.W., Drijber, R.A., Lyon, D.J., Heinemeyer, O., 1998. Fluxes of carbon dioxide, nitrous oxide, and methane in grass sod and winter wheat-fallow tillage management. Journal of Environmental Quality 27, 1094– 1104. Larionova, A.A., Yermolayev, A.M., Blagodatsky, S.A., Rozanova, L.N., Yevdokimov, I.V., Orlinsky, D.B., 1998. Soil respiration and carbon balance of gray forest soils as affected by land use. Biology and Fertility of Soils 27, 251– 257. Maljanen, M., Hyto¨nen, J., Martikainen, P.J., 2001. Fluxes of N2O, CH4 and CO2 on afforested boreal agricultural soils. Plant and Soil 231, 113– 121. Mosier, A.R., Schimel, D., Valentine, D., Bronson, K., Parton, W., 1991. Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands. Nature 350, 330–332. Ojima, D.S., Valentine, D.W., Mosier, A.R., Parton, W.J., Schimel, D.S., 1993. Effect of land use change on methane oxidation in temperate forest and grassland soils. Chemosphere 26, 675– 685. Paul, K.I., Polglase, P.J., Nyakuengama, J.G., Khanna, P.K., 2002. Change in soil carbon following afforestation. Forest Ecology Management 168, 241– 257. Pe´rez-Batallo´n, P., Ouro, G., Macı´as, F., Merino, A., 2001. Initial mineralization of organic matter in a forest plantation soil following logging residue management techniques. Annals of Forest Science 58, 807– 818. Prieme´, A., Christensen, S., Dobbie, K.E., Smith, K.A., 1997. Slow increase in rate of methane oxidation in soils with time, following land use change from arable agriculture to woodland. Soil Biology & Biochemistry 29, 1269–1273. Priess, J., Fo¨lster, H., 2001. Microbial properties and soil respiration in submontane forest of Venezuelian Guyana: characteristics and response to fertilizer treatments. Soil Biology & Biochemistry 33, 503– 509. Rodrı´guez-Murillo, J.C., 2001. Organic carbon content under different types of land uses and soil in peninsular Spain. Biology and Fertility of Soils 33, 53–61. Ruser, R., Flessa, H., Schilling, R., Steindl, H., Beese, F., 1998. Soil compaction and fertilization effects on nitrous oxide and methane fluxes in potato fields. Soil Science Society of America Journal 62, 1587–1595. Steudler, P.A., Bowden, R.D., Melillo, J.M., Aber, J.D., 1989. Influence of nitrogen fertilization on methane uptake in temperate forest soils. Nature 341, 314 –316. Vance, E.D., Brookes, P.C., Jenkinson, D., 1987. Microbial biomass measurements in forest soils: determination of Kc values and tests of hypothesis to explain the failure of the chloroform fumigation – incubation method in acid soils. Soil Biology & Biochemistry 19, 381– 386. Wardle, D.A., 1998. Control of temporal variability of the soil microbial biomass: a global scale synthesis. Soil Biology & Biochemistry 30, 1627–1637. Weier, K.L., Gillam, J.M., 1986. Effect of acidity on nitrogen mineralization and nitrification in Atlantic Coastal Plain soils. Soil Science Society of America Journal 50, 1210–1214. Yavitt, J.B., Fahey, T.J., Simmons, J.A., 1995. Methane and carbon dioxide dynamics in a Northern hardwood ecosystem. Soil Science Society of America Journal 59, 796–804.
Responses of soil organic matter and greenhouse gas fluxes to soil management and land use changes in a humid temperate region of southern Europe Agustı´n Merino*, Pilar Pe´rez-Batallo´n, Felipe Macı´as Department of Soil Science and Agricultural Chemistry, Escuela Polite´cnica Superior, Universidad de Santiago de Compostela, Campus Universitario E-27002 Lugo, Spain Received 1 November 2002; received in revised form 27 January 2004; accepted 1 February 2004
Abstract We studied the effects of soil management and changes of land use on soils of three adjacent plots of cropland, pasture and oak (Quercus robur) forest. The pasture and the forest were established in part of the cropland, respectively, 20 and 40 yr before the study began. Soil organic matter (SOM) dynamics, water-filled pore space (WFPS), soil temperature, inorganic N and microbial C, as well as fluxes of CO2, CH4 and N2O were measured in the plots over 25 months. The transformation of the cropland to mowed pasture slightly increased the soil organic and microbial C contents, whereas afforestation significantly increased these variables. The cropland and pasture soils showed low CH4 uptake rates (,1 kg C ha21 yr21) and, coinciding with WFPS values .70%, episodes of CH4 emission, which could be favoured by soil compaction. In the forest site, possibly because of the changes in soil structure and microbial activity, the soil always acted as a sink for CH4 (4.7 kg C ha21 yr21). The N2O releases at the cropland and pasture sites (2.7 and 4.8 kg N2O-N ha21 yr21) were, respectively, 3 and 6 times higher than at the forest site (0.8 kg N2O-N ha21 yr21). The highest N2O emissions in the cultivated soils were related to fertilisation and slurry application, and always occurred when the WFPS . 60%. These results show that the changes in soil properties as a consequence of the transformation of cropfield to intensive grassland do not imply substantial changes in SOM or in the dynamics of CH4 and N2O. On the contrary, afforestation resulted in increases in SOM content and CH4 uptake, as well as decreases in N2O emissions. q 2004 Elsevier Ltd. All rights reserved. Keywords: Microbial biomass; Microbial activity; Soil respiration; Nitrous oxide; Methane; Soil organic matter; Land use
1. Introduction Soil organic C plays an essential role in determining the physical and chemical characteristics of a soil and therefore in determining its fertility. The microbial biomass is a fraction of the soil organic matter (SOM) that is actively involved in the transformation of soil organic residues and in the dynamics of N, P and S. Soil microbial biomass and its activity, especially sensitive to human activity, are suitable predictors of soil biological status in terms of soil fertility (Elliot et al., 1996). Soil respiration has received considerable attention in recent years because of the release of large quantities of CO2 from the soils to the atmosphere. Changes in land use and soil management practices (tillage, use of fertilizers, organic residues, pesticides) induce * Corresponding author. Tel.: þ 34-982-285891; fax: þ 34-982-285926. E-mail address: [email protected] (A. Merino). 0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2004.02.006
changes in soil organic C, and are largely responsible for increases in atmospheric CO2 from terrestrial ecosystems (Bouwman, 1990). Soil also plays a major role in contributing to the atmospheric concentrations of other greenhouse gases, such as CH4 and N2O. The fluxes of these gases are influenced by soil variables that influence microbial activity, such as pH þ and concentrations of NO2 3 , NH4 and O2, which, in turn, are controlled by a combination of soil properties (soil moisture, texture, structure) and soil management practices. Intensive soil management has therefore led to a considerable increase in the exchange of N2O and CH4 between soils and the atmosphere (Bouwman, 1990; IPCC, 1995). In natural upland soils, CH4 is oxidised by methanotrophic and—to a lesser extent—NH4-oxidizing bacteria. Although soil is a major sink for atmospheric CH4, methanotrophic activity is greatly affected by changes in soil properties influencing gas diffusiveness (Mosier et al.,
918
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
1991; Dobbie and Smith, 1996; Flessa et al., 1995). Cultivation of undisturbed soils has a long-term effect on the capacity of the soils to take up CH4. Although accumulated data show variable effects of N on CH4 uptake, N fertilisation rapidly reduces the capacity of CH4 uptake as a consequence of the inhibition of CH4 oxidation activity of methanotrophs, by NHþ 4 or NH3 (Steudler et al., 1989). Soil compaction by tractor traffic can also substantially reduce the uptake of CH4 (Hansen et al., 1993) and the soils can thus become a net source of atmospheric CH4 (Ruser et al., 1998). Agricultural soils are the main anthropogenic source of N2O to the atmosphere. Rates of emission of N2O and the relative proportions produced by nitrification and denitrification are influenced by environmental factors and by soil management practices (Mosier et al., 1991). Nitrous oxide dynamics are largely determined by N fertilisation, so that approximately 1.25% of fertilizer N is assumed to be lost by denitrification (IPCC, 1995). The incorporation of certain crop residues (sugar beet, potato) can also result in increased N2O emissions (Aulakh et al., 1991; Kaiser et al., 1998). Moreover, some studies carried out in Central Europe have stressed the importance of N2O emissions during winter as a consequence of daily freezing and thawing cycles (Flessa et al., 1995; Kaiser et al., 1998). In Northern Spain and many other countries arable land is increasingly used for other purposes involving less intensive management, such as pasture or newly planted forest. These changes in land use, made in response to the lower population densities in rural areas, as well as environmental or economical strategies, have noticeably increased the grassland and forest areas. Such changes can substantially alter SOM dynamics (Rodrı´guez-Murillo, 2001) thereby affecting exchanges of greenhouse gases between the soil and the atmosphere. Less intensive management improves biological properties (Emmerling et al., 2001) and conversion of agricultural land to forest usually results in considerable gains in soil organic C and reductions in CO2 fluxes (Paul et al., 2002). Furthermore, some authors have also pointed out that after ceasing cultivation and fertilisation the capacity for CH4 oxidation in soils increases, although recovery is very slow and takes place over some years (Prieme´ et al., 1997), specially in organic soils (Maljanen et al., 2001). There is a growing interest in Spain, and elsewhere, in investigating the effectiveness of afforestation in sequestering atmospheric C and improving soil properties linked to SOM (aggregate stability, water holding capacity and nutrient retention). In addition, few field measurements of greenhouse gases in southern European countries have been made and the data available are not sufficient to enable evaluation of the repercussion of soil management on the dynamics of greenhouse gases. The objective of our study was to determine the dynamics of SOM and soil greenhouse gases in a southern European region and to relate these to land use, soil management practices and abiotic factors.
Particular attention was paid to the response of these variables where arable land had been converted to uses involving less intensive management, such as pasture or forest.
2. Material and methods 2.1. Study site We studied three soils in adjacent plots under cropland, sown pasture and oak forest. The cropland selected has been under continuous cultivation of different crops for at least 200 yr, whereas the pasture and the oak forest were established in part of the former cropland, respectively, 20 and 40 yr before our study began, in 1998. The three plots are situated on a rather flat landscape (slope ranges from 0 to 5%). The altitude of the sites is 500 m a.m.s.l. The climate is temperate subtropic with humic winters. The average annual precipitation is 1022 mm and the average annual temperature, 11.7 8C. Although precipitation is distributed throughout the year, winter is the most humid season and intense rainstorms occur in spring and autumn. The general soil moisture regime in the region is Udic and the soil temperature regime is Mesic. Visual examination of the three soil profiles indicated that the soils were very similar. The soils were derived from the same parent material, acid mica-schist, and had similar morphologies. According to the FAO system (FAO-Unesco, 1998), the soils are classified as dystric Cambisol and some major properties are shown in Table 1. The forest soil has a well-developed soil profile with an O (L þ F) organic horizon of 4– 6 cm depth. It is characterized by strong acidification with a base saturation of less than 15%. The texture of the surface soil horizon is silt loam. 2.2. Soil management in the study plots During the study period (July 1998 –July 2000) the following crop rotation was used: potato—Solanum tuberosum (June 1998 –October 98), turnips—Brassica rapa (November 98– April 99), onion—Allium cepa (May 99– September 99) and rye—Secale cereale (October 99 – April 00), which is a common crop sequence in the region. Table 1 Some properties of the A horizon in the soils studied
pH (H2O) pH (KCl) Extract. P (mg kg21) CECea (cmol kg21) Al saturation (%) a
Cropland
Pasture
Forest
5.0 4.3 60 11.9 6
5.4 4.0 55 9.2 10
4.3 3.7 15 7 60
Effective cation exchange capacity.
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
In spring 2000, the rye crop was mechanically incorporated into the soil as a green amendment. Tillage and mineral fertilization (750 kg ha21 of 15-15-15 NPK) were carried out before the establishment of the next crop. The onion crop was irrigated periodically. The pasture is a mixture of ryegrass (Lolium perenne), white clover (Trifolium repens) and red clover (Trifolium pratense), which is normally renovated every 3 yr. The site had been grazed by cattle and since 1990 has become mowed pasture. The annual productivity ranges between 10 and 15 t ha21. For pasture renovation, the soil is ploughed (mouldboard ploughing at 20 cm depth followed by rolling) and mineral fertilizers and lime are added. Slurry from cows is normally applied in spring and autumn. The pasture used for this study was renovated in September 1996. During the study period new pasture was established (in October 1999); for its renovation, the soil was moldboard ploughed to a depth of approximately 0.2 m and inorganic fertilizer (750 kg ha21 of 15-15 15 NPK) and lime (3000 kg ha21) were added. Cow slurry was applied in November 1998 and June 1999 (60 and 50 m3 ha21, respectively). The pasture was mown in October 1998, April 1999, June 1999, October 1999 and June 2000. The forest site was derived from the former cropland by afforestation with English oak-Quercus robur. The average tree density and basal area are 550 ha21 and 10 m2 ha21, respectively. 2.3. Soil sampling The study was carried out over 25 months, between July 1998 and July 2000. Precipitation and air temperature measurements were provided by the nearby meteorological station at Fingoi. During this study measurements were made of soil temperature, humidity, inorganic N, total organic C and N, microbial biomass C and fluxes of CO2, N2O and CH4. These variables were determined in four replicate plots of each system, at 2 – 3 week intervals, except for microbial biomass C, which was determined every 1 – 3 months. At the pasture and the cropland sites, gases were monitored more intensively after each fertilizer application. For the determination of moisture, inorganic N and microbial biomass C, in each of the plots and at each sampling time, soil cores were collected from the upper 15 cm of the A horizon from three randomly selected points, using a PVC core (50 mm dia). The soil cores were taken to the laboratory, where composite samples for each plot were sieved (2 mm). The static chamber system, as described by Hutchinson and Mosier (1981), was used to measure surface CO2, CH4 and N2O fluxes from the soil. Dark, circular chambers with an inner diameter of 29.5 cm and height of 19.45 cm were used. A chamber base (collar) was inserted in each plot to a depth of 2 cm, and was retained in place for the entire sampling period, only being removed before soil management practices and then replaced in the same position.
919
The first measurements were made 1 month after insertion of the frame. In the arable cropland the gas fluxes were measured in the ridges (two plots) and in the interrows (two plots). Gas measurements were made every sampling day between 10:00 and 12:00 a.m. and were assumed to represent the average gas flux for that day (Larionova et al., 1998; Kessavalou et al., 1998). The surface plant cover inside the frames was cut before measurements. In order to avoid disturbance and variations in results, gas samples were collected during 30 min every 10 min in glass vacuum flasks (60 ml) sealed with a butyl rubber septum. At the end of each sampling period, the chamber was removed from the base. 2.4. Soil processing and analysis Soil temperature at a depth of 10 cm was measured at the same time as each gas sampling. Soil total C and N were determined by dry combustion, using an element analyser (LECO-2000, LECO Corporation, St Joseph, Michigan, USA). The pH was measured in H2O and 0.1 M KCl (soil:solution ratio of 1:2.5). Soil moisture was determined gravimetricaly after oven drying (105 8C; 24 h). The waterfilled pore space (WFPS) was calculated as follows: WFPS ¼ [gravimetric water content £ soil bulk density)/ total soil porosity], where soil porosity ¼ 1 2 soil bulk density/2.65 (2.65 being the assumed particle density of the soil). In the two cultivated soils, bulk density was determined frequently. Samples for determination of bulk density were taken, from four points in each plot, using a brass core (40 cm long, 55 mm inside dia). The calculated mean soil bulk densities of the upper mineral layer are given in Table 2. Ammonium and NO2 3 were extracted with 2 M KCl and measured photometrically. Microbial biomass C was measured using the method of fumigation-extraction of soil samples with chloroform (Vance et al., 1987). Moist samples of soil were incubated in desiccators for 18 h, at Table 2 Average and standard deviation (in parenthesis) values of the variables recorded in the A horizons during the period July 1998– July 2000 in the three studied soils. Significantly different means are indicated by different letters, a . b ðP , 0:05Þ
Soil temperature (8C) Soil moisture (%) Bulk density (g cm23) Organic C (g kg21) Total N (g kg21) Microbial C (mg kg21) Microbial C: org C 21 NO2 3 -N (mg kg ) 21 NHþ 4 -N (mg kg ) CO2-C (mg m22 h21) CH4-C (mg m22 h21) N2O-N (mg m22 h21)
Cropland
Pasture
Forest
12.0 (4.6) 18.2 (7.2) 1.30 (0.1)a 16.3 (0.7) b 1.2 (0.08) b 224 (137) b 1.60 (0.80) 5.3 (6.3) 4.8 (5.0) 41.6 (28.0) 20.37 (29.5) 32.5 (18.6)
11.4 (5.5) 18.6 (8.1) 1.25 (0.1)ab 17.7 (1.1) b 1.6 (0.09) b 276 (124) b 1.56 (0.67) 6.2 (5.6) 11.6 (16.1) 45.2 (29.9) 0.8 (49.1) 32.1 (26.5)
11.5 (6.1) 25.2 (6.8) 1.1 (0.1) b 37.7 (5.2) a 1.8 (0.05) a 620 (216) a 1.46 (0.50) 1.9 (1.1) 6.5 (3.8) 38.8 (25.0) 243.62 (48.0) 12.0 (12.8)
920
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
room temperature and with alcohol-free chloroform vapour. Another set of soil samples was similarly incubated but without the chloroform. Soluble C was extracted with 0.5 M K2SO4 and determined by digestion with K2Cr2O7 and titration with (NH4)2FeSO4. The difference in organic C in three fumigated and three non-fumigated samples was calculated. Concentrations of CO2 and N2O were determined using a gas chromatograph fitted with an electron capture detector (ECD), whereas CH4 was measured with a flame ionization detector (FID). A 3 m-Porapack Q (Millipore, Milford, Mass.) column was used with N2 (20 ml min21) as the carrier gas. The temperatures of the oven and ECD were 35 and 280 8C, respectively. Gas fluxes were calculated from the linear increase or decrease in gas concentrations in the chambers. All samples were analysed within 2 weeks of collection (previous tests showed that the concentration of the gases analysed did not change during this period).
Fig. 1. Water-filled pore space (WFPS) in the cropland, mowed pasture and forest soils.
3.2. Inorganic N There were large differences in the amounts of þ extractable NO2 3 and NH4 in the different soils (Fig. 2). The amounts of inorganic N in the arable land increased after addition of mineral fertiliser and tillage (November
2.5. Statistical analyses The effects of management on all the variables studied were tested using an ANOVA. The relationships among soil factors, namely WFPS, soil temperature, soil NO2 3 and microbial biomass, and the mean flux rates of CO2, CH4 and N2O were analyzed by stepwise linear and quadratic regressions. Statistical differences in soil surface gas fluxes among the three ecosystem types for each date were determined using a t-test for least significant differences (LSD). As the N2O emission rates were log-normally distributed, logarithmic (natural base) transformation were carried out to normalize the N2O data. Cumulative CH4 and N2O losses from each site were calculated from the integrated weekly fluxes of the four replicates, assuming a constant flux rate beginning with the date of each gas sampling until the next gas sampling.
3. Results 3.1. Climatic conditions Precipitation between July 1998 and July 2000 was 1640 mm. Most of the precipitation fell in winter and spring. Intense rainstorms occurred in spring 1999, October 1999, December 1999 and April 2000 (data not shown). Soils were driest in July and wettest in spring. At many sampling times the WFPSs were substantially larger in the two cultivated soils ðP , 0:05Þ; especially in the cropland soil (Fig. 1). The daily air and soil temperatures were always above freezing. In winter, the soil temperature measured at midday was approximately 0.5 8C higher in the forest plot; by contrast, during summer, the soil temperature was lower at this site.
2 Fig. 2. Changes in soil NHþ 4 (a) and NO3 (b) at the cropland, mowed pasture and forest sites.
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
1998, May 1999, October 1999) and incorporation of green plant residues of the rye crop (April 2000). In the soil under þ pasture, the amounts of NO2 3 and NH4 were low during most of the study period and increased after addition of cow slurry (November 98, May 1999), tillage and application of mineral fertiliser (October 1999). The first addition of slurry, carried out in autumn 1998, led to very high 2 quantities of NHþ 4 and NO3 , probably due to a lack of N uptake by plants. In the forest soil, the concentration of 2 NHþ 4 , which was always higher than that of NO3 , varied considerably, reaching maximum amounts of 16 mg kg21. The concentration of NO2 3 -N was always lower than 6 mg kg21. 3.3. Soil total organic C, microbial biomass and respiration Soil total organic C (in surface units) in the forest soil was almost twice that of the cropland soil ðP , 0:001Þ: The SOM in the pasture plot was slightly higher than that of the cropland plot (Table 2). Microbial biomass variations depended on seasonal changes and the type of agriculture management practice. The amounts of microbial C decreased during the driest seasons and were also low during the coldest or wettest months (Fig. 3a). The annual average concentrations of microbial C in the forest soil were 2 –3 times higher than in the agricultural soils. Differences among different sampling times within each site and among the three sites were significant ðP , 0:001Þ: In spite of the differences in land uses, the ratios of microbial C to organic C were similar in all three soils (Fig. 3b), although, in the pasture increases in this ratio were apparent in 1999 following the cow slurry application. The CO2 fluxes in the three systems (Fig. 4) were significantly different over time ðP , 0:05Þ: The ranges for the cropland and pasture soils were 5.1 – 119.0
921
Fig. 4. Soil respiration rates measured at the cropland, mowed pasture and forest sites.
and 8.4 – 179.0 mg CO2-C m22 h21, respectively. In the forest soil they ranged from 9 to 123 mg CO2-C m22 h21. The amount of CO2 released from the cropland was less than from the forest and pasture, especially during the first year. Large increases took place after land preparation, where maxima of 100 – 150 mg m22 h21 were recorded. The largest increase took place in April 2000, after the incorporation of the rye crop. During most of the study period, significantly more CO2 was released from the pasture soil than from the cropland and forest soils. The greatest differences were observed after tillage (September 1999) and application of dairy cow slurry (November 1998, May 1999), when a maximum of 100 mg CO2-C m22 h21 was measured. In these cultivated soils, the relationships between CO2 and either soil moisture or temperature were weak. However, there was a relationship between CO2 and microbial C (r ¼ 0:68 for the cropland soil; r ¼ 0:33; for the pasture soil). In the forest soil, the highest rates of soil respiration took place when the soil temperature was relatively high and the humidity moderate (October 98, October 99 and May 2000). By contrast, minimum values occurred in winter, coinciding with periods of low soil temperature (lower than 10 8C) and high soil moisture content (higher than 50% of WFPS). Low soil moisture content, corresponding to a WFPS of 10%, was important in reducing CO2 emission in summer. In the forest soil, CO2 flux correlated weakly with soil moisture (r ¼ 20:37; P , 0:05) and soil temperature (r ¼ 0:35; P , 0:05) but more strongly with soil microbial C (r ¼ 0:73; P , 0:01). 3.4. CH4 fluxes
Fig. 3. Soil microbial C (a) and ratio of microbial biomass: organic C (b) in the three systems studied.
Similar patterns of changes in CH4 fluxes were observed for the pasture and cropland soils. During most of the study period the cropland soil showed lower CH4 uptake rates and, at some times, net emissions of CH4 were observed (Fig. 5). The episodes of emission occurred during the periods of heaviest precipitation (December 1999 – March 1999, December 2000 – April 2000). By contrast, CH4 uptake was highest during the summer months, coinciding with low soil moisture content. The measured fluxes ranged from a CH4-C uptake of 50 mg m22 h21 to CH4-C emission of 125 mg m22 h21. Linear regression analysis revealed
922
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
Fig. 5. Methane fluxes from the three plots studied: cropland, mowed pasture and forest. Negative values are consumption rates of CH4, positive values are emission rates of CH4.
a weak relationship between CH4 uptake rate and both WFPS (r ¼ 20:46; P , 0:05) and temperature (r ¼ 20:32; P , 0:05) throughout the study period. The emission peak recorded in November 1998, coincided with the application of cow slurry and high soil moisture. The soil tillage carried out in October 99 apparently did produce changes in the CH4 fluxes. The measured fluxes ranged from a CH4-C uptake of 132 mg m 22 h21 to CH 4-C emission of 200 mg m22 h21. In this soil, CH4 fluxes were significantly correlated with WFPS (r ¼ 20:35; P , 0:05), NO2 3 -N (r ¼ 20:33; P , 0:05) and NHþ 4 - N (r ¼ 0:35; P , 0:05). Unlike the agricultural soils, there was a net consumption of CH4 in the forest soil, throughout most of the study. In this soil, there was seasonal variation in CH4 uptake that was similar to the changes in soil moisture content. There was only one episode of CH4 emission, which coincided with a very high soil moisture content, but which was much less than in the agricultural soils. The measured fluxes ranged from a CH4-C uptake of 116 mg m22 h21 to CH4-C emission of 3 mg m22 h21. In this forest soil, the CH4 uptake correlated significantly with the WFPS (r ¼ 20:63; P , 0:001), soil temperature (r ¼ 0:42; P , 0:01), NHþ 4 (r ¼ 0:58; P , 0:001) and C microbial biomass (r ¼ 0:55; P , 0:05). The results of stepwise multiple linear regression showed that soil moisture content and concentration of NHþ 4 accounted for up to 52% of the variation in CH4 flux.
3.5. N2O fluxes In the cropland soil, the pattern of N2O dynamics was characterised by low emission rates on most sampling dates and a few dates on which flux rates were higher than 50 mg N m22 h21 (Fig. 6). Small negative fluxes of N2O were observed at this site. The highest emissions coincided with increases in soil inorganic N concentrations brought about after soil tillage and mineral fertilisation (November 1998, May 1999 and October 1999). In spring, pulses of higher N2O emissions coincided with rewetting of the soil. The incorporation of the rye crop in April 2000 did not increase the soil inorganic N and did not affect the N2O fluxes. In this soil, significant relationships ðP , 0:05Þ among N2O fluxes, soil NO2 3 concentrations and WFPS were apparent. However, throughout the study these factors only accounted for up to 20% of the variation in N2O emission. No relationships between N2O emission and either soil or air temperature were found. In the pasture soil, the application of cow slurry and N fertilizer led to highest N2O emissions. The greatest increases took place after the first application of cow slurry (November 1998) and mineral fertilisation (October 1999), which coincided with high soil moisture contents and high concentrations of inorganic N. However, the second application of cow slurry (June 1999) led to much lower
Fig. 6. Nitrous oxide flux rates recorded at the cropland, mowed pasture and forest sites.
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
N2O increases, probably because of the lower soil moisture þ content and lower concentrations of NO2 3 and NH4 in the soil. As at the cropland, N2O emissions were significantly related to soil NO2 3 concentrations and WFPS ðP , 0:05Þ throughout the entire study period, although the relationship was also weak ðR2 ¼ 0:21Þ: In this soil, N2O emissions were also significantly correlated with microbial C (r ¼ 0:61; P , 0:05). In comparison with those in the agricultural soil, the N2O fluxes in the forest soil were very low throughout the study and exhibited weak seasonality. The highest emission rates coincided with the highest amounts of NHþ 4 (r ¼ 0:36; P , 0:05) and soil moisture (r ¼ 0:33; P , 0:05) and always took place when the soil moisture content was higher than 25%.
4. Discussion 4.1. Soil total C, microbial C and respiration The values of microbial biomass and the ratio of biomass C to organic C recorded are consistent with values reported for other arable (Wardle, 1998) and forest soils (Dı´az-Ravin˜a et al., 1995). In our study, microbial C decreased during the driest and coldest seasons, and also during prolonged periods of water saturation, which can be attributed to variations in substrate availability and to drying and re-wetting effects (Kaiser and Heinemeyer, 1993; Pe´rez-Batallo´n et al., 2001). The increase in the amount of C in the pasture soil was much smaller than in the afforested soil, probably because of the shorter period of transformation and the intensive management of this soil. Emmerling et al. (2001) have also reported slight increases in soil microbial biomass following the use of less intensive agricultural practices. The increase in the ratio of microbial C: organic C observed in the pasture during 1999 was probably due to the presence of readily available C, introduced through cow slurry application during the previous autumn. In the forest soil, in spite of the higher microbial C, the ratio of microbial C: organic C was similar to those in the agricultural soil, which may indicate adverse properties resulting from the soil acidity and low nutrient availability, as suggested by Priess and Fo¨lster (2001). The CO2 release followed the order pasture . forest . cropland. The differences among the three systems reflect differences in environmental conditions (mainly soil moisture content and temperature), input of organic residues and, in the case of the forest site, acidification, all of which influence soil organic contents, microbial activities and root densities. Seasonal variations in CO2 release mainly followed the annual changes in soil temperature and moisture, as it has also been found in other temperate forest ecosystems (Larionova et al., 1998). The poor relationship between the fluxes of this gas and both soil moisture and soil
923
temperature may be due to the antagonistic effects of soil moisture; CO2 release is enhanced during periods when soil moisture is limiting and reduced when soil moisture is in excess. Thus, CO2 release was greatly reduced during periods of heavy rain, when the WFPS was . 50%, probably as a consequence of O2 deficiency in the soil (Howard and Howard, 1993). The low rates of CO2 fluxes measured during these seasons coincided with lower CH4 uptake rates, which suggests that the lower CO2 production may also be due to a change in the metabolic pathway of the microbial community, to fermentation. The largest increases in CO2 fluxes in these soils were produced after tillage, mineral fertilization and manure application, coinciding with responses observed in other studies (Kessavalou et al., 1998; Mosier et al., 1991; Priess and Fo¨lster, 2001). The increased CO2 production observed in the pasture soil during the first 10 days following manure addition was due to mineralization of the large amount of readily oxidizable C. Flessa and Beese (2000) found that accelerated mineralization led to the respiration of 40% of the C added in manure within 9 weeks. 4.2. CH4 fluxes The average annual CH4 uptakes of 0.2 and 0.9 kg C ha21 found in the cropfield and grassland were in the lower range reported for agricultural soils from other regions (Steudler et al., 1989; Mosier et al., 1991; Flessa et al., 1995). The average annual uptake of 4.7 kg C ha21 estimated for this forest soil was similar to those reported for other mature forest soils (Dobbie and Smith, 1996; Prieme´ et al., 1997; Borken and Brumme, 1997). The fluxes of this gas depend on WFPS, therefore we must take into account that the precipitation recorded during these 2 years was lower than the annual average. In the three plots the patterns of CH4 fluxes were mainly influenced by soil moisture and NHþ 4 -N contents, whereas soil temperature was found to be a secondary factor. The lower uptake rate recorded during periods of high WFPS was caused by the reduced diffusiveness of CH4 and O2 into the soil, which produced temporary anaerobic conditions (Do¨rr et al., 1993). Net CH4 emissions from the soil to the atmosphere, such as we observed in the forest soil, are not common in upland forest soils, although they have been observed during periods of high soil moisture, following snowmelt (Yavitt et al., 1995). Most of the CH4 emission episodes observed in these soils were not only linked to management practices (Flessa and Beese, 2000), but they also took place at times when the WFPS was . 60%, even without any manure application. The release of this gas may be favoured by compaction, which is consistent with other researchers who found very low rates of CH4 uptake (Hansen et al., 1993) and net CH4 emissions (Ruser et al., 1998) in compacted, agricultural soils. The negative effect of soil NHþ 4 -N on CH4 uptake was much less evident in the two agricultural soils. This different
924
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
behaviour (between CH4 and NHþ 4 ) has also been reported by Dobbie and Smith (1996) and Flessa et al. (1995), who have suggested that in arable lands the inhibition of CH4 oxidation by NHþ 4 occurs after the initial application of fertiliser and continues for some years afterwards. Our results show that in spite of the lower intensity of tillage and N fertilization than at the cropland site, this was not sufficient to increase the CH4 uptake rate in the pasture soil. Ojima et al. (1993) also found less CH4 consumption in intensively managed grasslands in comparison with native prairie. By contrast, the conversion of cropland to forest soil carried out 40 yr ago has led to substantial increases in the CH4 oxidation rates. These findings are consistent with those of Ambus and Christensen (1995), who observed higher CH4 uptakes in abandoned farmland, and with those of Prieme´ et al. (1997), who compared the CH4 uptake in forests of different ages. Increased CH4 uptake in this soil should be produced by the increase in SOM and the subsequent higher structural stability and presence of macropores, all of which favour the diffusiveness of CH4 and O2 into the soil profile. In addition, the improved soil aeration, along with the lack of N fertilisation, may have enhanced the number and activity of methanotrophic bateria. Since methanotrophic bacteria are acid tolerant and adapt to soils with different acidities (Steudler et al., 1989; Borken and Brumme, 1997), soil acidification after afforestation probably did not affect the CH4 dynamics. 4.3. N2O fluxes The average annual N2O-N emissions from the cropland and pasture soils (2.7 and 4.8 kg ha21, respectively) were similar to those reported for agricultural soils elsewhere (Bouwman, 1990). Higher releases are normally found in more intensively fertilised fields, drained organic soils (Bouwman, 1990) and other cultivated soils from Central Europe subjected to frost-thaw events (Flessa et al., 1995; Kaiser et al., 1998). The average N2O-N emission rate recorded in the forest soil and the average annual emission (0.8 kg ha21) were similar to those reported for other temperate forests (Bouwman, 1990; Borken and Brumme, 1997). As found in other studies (Flessa et al., 1995; Kaiser et al., 1998), N2O fluxes were influenced by soil inorganic N concentrations, as well as by WFPS. In the two agricultural soils, each fertilisation was followed by increases in NO2 3 and, subsequently, N2O emissions. The low fluxes in the forest soil are related to the lower soil NO2 3 concentrations and WFPS. This suggests that in this case, N2O production was limited by anaerobic conditions and a lack of NO2 3. The losses by N2O emission made up 0.5% and 1.0% of the N added by fertilization respectively in the cropfield and grassland. However, it should been taken into account that N2O measured only constitutes a portion
of the gaseous N lost, because during periods of higher WFPS a significant fraction of the N2O can end up as N2 (Estavillo et al., 2002). The relatively low N2O emissions, as well as the occasional negative fluxes observed at the agricultural sites, may be produced by the reduction of N2O to N2 in periods of high soil moisture and low N2O production. Unlike other studies (Aulakh et al., 1991; Kaiser et al., 1998), the incorporation of crop residues by ploughing in the cropland plot did not lead to increased N2O emissions, probably because the WFPS of the soil was rather low from that time onwards. The relatively high C to N ratios, which may have impeded N losses due to denitrification, should also be taken into account (Aulakh et al., 1991). Although denitrification is controlled by the supply of readily decomposable SOM, the slight increase in SOM was not sufficient to produce a higher N2O release. On the other hand, the development of the gramineous root system in the grassland may have favoured aeration of the mineral soil, reducing the formation of this gas. However, measurements of bulk density and WFPS did not reveal substantial changes. Afforestation, on the contrary, led to decreases in N2O emission, which can be attributed to the lack of N fertilization as well as to modifications in soil properties as a consequence of the abandonment of the agricultural activity. One important change seen after afforestation was the development of an upper organic horizon. According to Borken and Brumme (1997), the contribution of the organic layer to the N2O release from the soil can be significant, although the response depends on the type of the organic horizons. It is possible that the improvement in soil structure and aeration produced conditions that were less anaerobic and subsequently, anaerobic microorganisms were less likely to be present. In addition, the progressive acidification probably reduced the net N-mineralization, although this effect does not necessarily mean a lower N2O production, because acidification also inhibits N2O reductase, resulting in a higher yield of N2O than N2 (Weier and Gillam, 1986). In boreal organic soils, however, afforestation does no necessary causes decreases in N2O fluxes because the lowering in the water table is associated with NO2 3 production (Maljanen et al., 2001).
Acknowledgements We are grateful to the staff of the Escuela Polie´cnica for their valuable support and cooperation during the field work. Ms. Pilar Pe´rez-Batallo´n also thanks the University of Santiago de Compostela for a postgraduate scholarship. We thank Ms. Maria Fe´ Lo´pez and Ms. Lucı´a Medina, for their assistance in the laboratory. We also appreciate the positive
A. Merino et al. / Soil Biology & Biochemistry 36 (2004) 917–925
and valuable suggestions given by the two anonymous referees.
References Ambus, P., Christensen, S., 1995. Spatial and seasonal nitrous oxide and methane fluxes in Danish forest-, grassland-, and agroecosystems. Journal of Environmental Quality 24, 993–1001. Aulakh, M.S., Doran, J.W., Walters, D.T., Mosier, A.R., Francis, D.D., 1991. Crop residue type and placement effects on denitrification and mineralization. Soil Science Society of America Journal 55, 1020–1051. Borken, W., Brumme, R., 1997. Liming practice in temperate forest ecosystems and the effects on CO2, N2O and CH4 fluxes. Soil Use and Management 13, 157–251. Bouwman, A.F., 1990. Exchange of greenhouse gases between terrestrial ecosystems and the atmosphere. In: Bouwman, A.F., (Ed.), Soils and the Green House Effect, Wiley, Chischester, pp. 61–127. Dı´az- Ravin˜a, M., Acea, M.J., Carballas, T., 1995. Seasonal changes in microbial biomass and nutrient flush in forest soils. Biology and Fertility of Soils 19, 220– 226. Dobbie, K.E., Smith, K.A., 1996. Comparison of CH4 oxidation rates in woodland, arable and set aside soils. Soil Biology & Biochemistry 28, 1357–1365. Do¨rr, H., Katruff, L., Levin, I., 1993. Soil texture parameterization of the methane uptake in aerated soils. Chemosphere 26, 697–713. Elliot, L.F., Lynch, J.M., Papendick, R.I., 1996. The microbial component of soil quality. In: Stozky, G., Bollag, J.-M. (Eds.), Soil Biochemistry, vol. 9. Marcel Dekker, New York, pp. 1–20. Emmerling, C., Edelhoven, T., Schro¨der, D., 2001. Response of soil microbial biomass and activity to agricultural de-intensification over a 10 year period. Soil Biology & Biochemistry 33, 2105–2114. Estavillo, J.M., Merino, P., Pinto, M., Yamulki, S., Gebauer, G., Spake, A., Corr, W., 2002. Short term effect of ploughing a permanent pasture on N2O production from nitrification and denitrification. Plant and Soil 239, 253 –265. FAO-Unesco, 1998. World reference base for soil resources. World Soil Resources Reports, 84, FAO, ISRIC and ISSS, Rome. Flessa, H., Beese, F., 2000. Laboratory estimates of trace gas emissions following surface application and injection of cattle slurry. Journal of Environmental Quality 29, 262 –268. Flessa, H., Do¨rsch, P., Beese, F., 1995. Seasonal variation of N2O and CH4 fluxes in differently managed soils in southern Germany. Journal of Geophysical Research 100, 23115–23124. Hansen, S., Maehlum, J.E., Bakken, L.R., 1993. N2O and CH4 fluxes in soil influenced by fertilization and tractor traffic. Soil Biology & Biochemistry 25, 621 –630. Howard, D.M., Howard, P.J., 1993. Relationships between CO2 evolution, moisture content and temperature for a range of soil types. Soil Biology & Biochemistry 25, 1537– 1546. Hutchinson, G.L., Mosier, A.E., 1981. Improved method for field measurement of nitrous oxide fluxes. Soil Science Society of America Journal 45, 311–316. IPCC, 1995. Climate change Scientific and Technical Analysis of Impacts, Adaptions and Mitigation. Contribution of Working Group II to the Second Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, London. Kaiser, E.-K., Heinemeyer, O., 1993. Seasonal variations of soil microbial biomass carbon within the plough layer. Soil Biology & Biochemistry 25, 1649–1655.
925
Kaiser, E.A., Kohrs, K., Ku¨che, M., Schnung, E., Munch, J.C., Heinemeyer, O., 1998. Nitrous oxide release from arable soil: importance of N fertilization, crops and temporal variation. Soil Biology & Biochemistry 30, 1553–1563. Kessavalou, A., Mosier, A.R., Doran, J.W., Drijber, R.A., Lyon, D.J., Heinemeyer, O., 1998. Fluxes of carbon dioxide, nitrous oxide, and methane in grass sod and winter wheat-fallow tillage management. Journal of Environmental Quality 27, 1094– 1104. Larionova, A.A., Yermolayev, A.M., Blagodatsky, S.A., Rozanova, L.N., Yevdokimov, I.V., Orlinsky, D.B., 1998. Soil respiration and carbon balance of gray forest soils as affected by land use. Biology and Fertility of Soils 27, 251– 257. Maljanen, M., Hyto¨nen, J., Martikainen, P.J., 2001. Fluxes of N2O, CH4 and CO2 on afforested boreal agricultural soils. Plant and Soil 231, 113– 121. Mosier, A.R., Schimel, D., Valentine, D., Bronson, K., Parton, W., 1991. Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands. Nature 350, 330–332. Ojima, D.S., Valentine, D.W., Mosier, A.R., Parton, W.J., Schimel, D.S., 1993. Effect of land use change on methane oxidation in temperate forest and grassland soils. Chemosphere 26, 675– 685. Paul, K.I., Polglase, P.J., Nyakuengama, J.G., Khanna, P.K., 2002. Change in soil carbon following afforestation. Forest Ecology Management 168, 241– 257. Pe´rez-Batallo´n, P., Ouro, G., Macı´as, F., Merino, A., 2001. Initial mineralization of organic matter in a forest plantation soil following logging residue management techniques. Annals of Forest Science 58, 807– 818. Prieme´, A., Christensen, S., Dobbie, K.E., Smith, K.A., 1997. Slow increase in rate of methane oxidation in soils with time, following land use change from arable agriculture to woodland. Soil Biology & Biochemistry 29, 1269–1273. Priess, J., Fo¨lster, H., 2001. Microbial properties and soil respiration in submontane forest of Venezuelian Guyana: characteristics and response to fertilizer treatments. Soil Biology & Biochemistry 33, 503– 509. Rodrı´guez-Murillo, J.C., 2001. Organic carbon content under different types of land uses and soil in peninsular Spain. Biology and Fertility of Soils 33, 53–61. Ruser, R., Flessa, H., Schilling, R., Steindl, H., Beese, F., 1998. Soil compaction and fertilization effects on nitrous oxide and methane fluxes in potato fields. Soil Science Society of America Journal 62, 1587–1595. Steudler, P.A., Bowden, R.D., Melillo, J.M., Aber, J.D., 1989. Influence of nitrogen fertilization on methane uptake in temperate forest soils. Nature 341, 314 –316. Vance, E.D., Brookes, P.C., Jenkinson, D., 1987. Microbial biomass measurements in forest soils: determination of Kc values and tests of hypothesis to explain the failure of the chloroform fumigation – incubation method in acid soils. Soil Biology & Biochemistry 19, 381– 386. Wardle, D.A., 1998. Control of temporal variability of the soil microbial biomass: a global scale synthesis. Soil Biology & Biochemistry 30, 1627–1637. Weier, K.L., Gillam, J.M., 1986. Effect of acidity on nitrogen mineralization and nitrification in Atlantic Coastal Plain soils. Soil Science Society of America Journal 50, 1210–1214. Yavitt, J.B., Fahey, T.J., Simmons, J.A., 1995. Methane and carbon dioxide dynamics in a Northern hardwood ecosystem. Soil Science Society of America Journal 59, 796–804.