Dynamics of soil microbial biomass C, soluble organic C and CO 2. evolution after three years of manure application
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1 Dynamics of soil microbial biomass C, soluble organic C and evolution after three years of manure application P. Rochette 1 and E. G. Gregorich 2 1 Agriculture and Agri-Food Canada, Soils and Crops Research and Development Centre, 2560, Hochelaga Blvd., Ste-Foy, PQ, Canada G1V 2J3, rochettep@em.agr.ca; and 2 Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, Neatby Bldg., Central Experimental Farm, Ottawa, Ontario, Canada K1A 0C6, GregorichE@em.agr.ca. Received 15 July 1997, accepted 14 January Rochette, P. and Gregorich, E. G Dynamics of soil microbial biomass C, soluble organic C and evolution after three years of manure application. Can. J. Soil Sci. 78: Application of manure and fertilizer affects the rate and extent of mineralization and sequestration of C in soil. The objective of this study was to determine the effects of 3 yr of application of N fertilizer and different manure amendments on evolution and the dynamics of soil microbial biomass and soluble C in the field. Soil respiration, soluble organic C and microbial biomass C were measured at intervals over the growing season in maize soils amended with stockpiled or rotted manure, N fertilizer (200 kg N ha 1 ) and with no amendments (control). Manure amendments increased soil respiration and levels of soluble organic C and microbial biomass C by a factor of 2 to 3 compared with the control, whereas the N fertilizer had little effect on any parameter. Soil temperature explained most of the variations in flux (78 to 95%) in each treatment, but data from all treatments could not be fitted to a unique relationship. Increases in emission and soluble C resulting from manure amendments were strongly correlated (r 2 = 0.75) with soil temperature. This observation confirms that soluble C is an active C pool affected by biological activity. The positive correlation between soluble organic C and soil temperature also suggests that production of soluble C increases more than mineralization of soluble C as temperature increases. The total manure-derived -C was equivalent to 52% of the applied stockpiled-manure C and 67% of the applied rotted-manure C. Estimates of average turnover rates of microbial biomass ranged between 0.72 and 1.22 yr 1 and were lowest in manured soils. Manured soils also had large quantities of soluble C with a slower turnover rate than that in either fertilized or unamended soils. Key words: Soil respiration, greenhouse gas, soil carbon Rochette, P. et Gregorich, E. G Cinétique du C de biomasse microbienne, du C organique soluble et du après 3 années d épandage de fumier de ferme. Can. J. Soil Sci. 78: L épandage de fumier et d engrais chimique, influe sur le taux et sur l étendue de la minéralisation et de la séquestration de C dans le sol. L objet de nos travaux était de dégager, au champ, les effets de 3 années de fumure minérale N et d apports de fumier frais ou plus ou moins décomposé sur l évolution du et sur la cinétique du C d origine microbienne et du C soluble du sol. La respiration du sol, le C organique soluble et le C de biomasse microbienne étaient mesurés à diverses reprises durant la période de végétation dans des champs de maïs ayant reçu du fumier frais ou décomposé, un engrais azoté minéral (200 kg N ha 1 ) ou aucun amendement (témoin). Par rapport à ce dernier traitement, les fumiers accroissaient de 2 à 3 fois la respiration du sol et les niveaux des deux formes de C, mais l engrais azoté minéral n avait que peu d effet sur ces paramètres. Dans chaque traitement, la température du sol justifiait la quasi-totalité des variations du flux de, mais les données obtenues pour l ensemble des traitements ne pouvaient pas être ramenées à une relation unique. Les accroissements des émissions de ou des teneurs en C soluble résultant des apports de fumier étaient fortement corrélés (r 2 = 0,75) avec la température du sol, ce qui confirme que le C soluble constituer un réservoir actif de C sensible à l activité biologique. Les corrélations positives observées entre le C organique soluble et la température du sol font voir qu il se produit plus de C soluble qu il ne s en minéralise à mesure que la température s élève. Le C sous forme total issue du fumier correspondait à 52 % du C du fumier, dans le cas du fumier frais et à 67 % dans le cas du fumier décomposé. Le taux de renouvellement moyen de la biomasse microbienne était estimé entre 0,72 et 1,22 par année, les valeurs les plus basses s appliquant aux sols amendés au fumier. Ces derniers révélaient également de fortes quantités de C soluble avec un taux de renouvellement plus lent que dans les sols recevant la fumure minérale ou que dans les sols témoins. Mots clés: Respiration du sol, gaz à effet de serre, carbone du sol Large quantities of readily decomposable organic matter are added to agricultural soils every year as crop residues or animal wastes and have a significant effect on soil microbial activity. The rate at which organic matter is decomposed by microorganisms is related to the chemical composition of the material as well as the environmental conditions. Predicting the rate of decomposition requires that the availability of the C substrates be measured and the role of controlling factors, such as soil temperature and water content, be quantified under field conditions. McGill et al. (1981) 283 proposed that the soluble organic C in soils is an immediate source of C for soil microorganisms. Several incubation studies have shown that mineralizable C was directly related to soluble C. Gilmour and Gilmour (1985) reported that the decrease in soluble C correlated well with C assimilated in microbial biomass. Reinertsen et al. (1984) observed that soil microbial biomass C and the decomposition of straw were largely dependent on the quantity of soluble C at early stages of decomposition. Soluble C has been reported to be a good indicator of the availability of C to sustain denitrifi-
2 284 CANADIAN JOURNAL OF SOIL SCIENCE cation activity (Burford and Bremner 1975; Davidson et al. 1987; Paul and Beauchamp 1989). However, other studies have found that not all of the soluble C is readily decomposable (Horwath and Elliott 1996) and that the recalcitration fraction increases with incubation time (Cook and Allan 1992). It is not clear to what extent these findings can be applied to field conditions under which the continuous inputs of C from root exudates and root turnover occur simultaneously with decomposition processes. The objective of this study was to determine the effects of 3 yr of application of N fertilizer and different manure amendments on evolution and the dynamics of soil microbial biomass and soluble C in the field. MATERIALS AND METHODS The study was conducted in 1994 at the Central Experimental Farm of Agriculture and Agri-Food Canada in Ottawa, Ontario (latitude N, longitude W, 79 m above sea level), on plots that were part of an experiment on the effects of agricultural practices on soil C and N dynamics. The experiment was initiated in 1992 and the same treatments were applied to the same plots every year. The soil was classified as a Brandon loam soil (Orthic Humic Gleysol), contained 20.5 g kg 1 organic C, 176 g kg 1 organic N, 374 g kg 1 sand, 364 g kg 1 silt and 262 g kg 1 clay, and had a ph of 5.4 (in 0.01 M CaCl 2 ). The experimental design consisted of randomized blocks with three replicates of 100 Mg ha 1 (wet weight) of stockpiled and 100 Mg ha 1 of rotted dairy cattle manure, 200 kg N ha 1 of ammonium-nitrate fertilizer and a control receiving no amendments. The manure consisted of dairy cow faeces and a large amount of straw because the dairy herd and barn were in a public area and used for demonstration purposes. Manure was collected in the summer and fall of 1993 and either stockpiled on a concrete slab or placed on slotted concrete slabs for aeration in an attempt to compost the manure. The stockpiled manure was relatively unchanged prior to application in the spring of 1994, and the appearance of the second manure suggested that it had undergone some decomposition but was not fully composted. The composition of the manures was similar but indicated that nitrification had also occurred in the rotted manure (Table 1). The 12 plots (9.15 m by 7.62 m each) were plowed on day 322 in Soil cores were obtained for bulk density measurements on day 115 in Mean bulk density values for the surface layer (0 15 cm) were 1.18 Mg m 3 for the unamended plots, 1.24 Mg m 3 for the plots receiving N fertilizer, 1.10 Mg m 3 for plots receiving stockpiled manure and 1.03 Mg m 3 for plots receiving rotted manure. Fertilizer phosphorus and potassium ( at 67 kg ha 1 ) were applied to all plots on day 122. Manure was applied and incorporated to a depth of 0.20 m on days 130 and 131 using a moldboard plow. Fertilizer N (ammonium nitrate ) was broadcast and incorporated on day 139. Grain maize was planted (38 plants row 1 ; row spacing, 0.75 m) on day 145, emerged on day 154 and was harvested on day 300. Herbicide applications in the spring of 1994 included 1.6 L ha 1 Frontier (dimethenamid), 3.43 L ha 1 Bladex (cyanazine) and 2.5 L ha 1 Atrazine (2-chloro-4-ethylamino-6-isopropylamino-1,3,5-triazine). The method for measuring soil surface fluxes is described by Rochette et al. (1997) and used a dynamic closed system in which air was circulated between an acrylic plastic (thickness = 6.35 mm) chamber and a portable analyser (LI-6200, LI-COR Inc, Lincoln, NE, USA). During the measurement, the cylindrical chamber (height = 0.15 m; cross section = m 2 ) was clamped on collars previously installed in the soil. The collars were 0.14-m sections of the same acrylic plastic cylinder used to build the chamber. They were inserted 0.10 m into the soil. During the measurement, a good seal between the chamber and the collar was achieved using a closed-cell foam gasket. For each measurement, the chamber was placed on the collar and the rate of change concentration in the system was measured for two 30-s periods. The measurement was considered valid if the two successive flux computations were within 10% of each other, thereby implying steadystate conditions. Three collars were installed on each plot, for a total of 36 collars on day 322 and 323 in The collars were removed for the application of the amendments and for planting, and put back in the soil after each operation. The flux was measured on each collar between 1000 and 1400 EST on 27 d between days 108 and 325. Soil temperature (copper-constantan thermocouples with digital thermometers; model HH23, Omega Inc., Stamford, CT, and model , Barnant Co., Barrington, IL) and water content (time domain reflectometry probes) were measured at depths of 0.5, 0.10, 0.20 and 0.40 m on each plot simultaneously with the flux measurements. Three replicate soil samples were taken at each sampling depth ( and m) in each plot at different times through the season. Within 48 h of sampling, soil microbial biomass C was determined using the fumigationextraction technique described by Voroney et al. (1993). About 25 g of field-moist soil was fumigated with chloroform for 24 h. The fumigated and nonfumigated soils were extracted with 0.5 M K 2 SO 4, filtered and the soluble organic C measured on a Shimadzu TOC-5050 analyser (Shimadzu Inc., Tokyo, Japan). Soluble organic C in the extracts was determined as the difference between total soluble C and inorganic C, which were measured directly on the TOC-5050 analyser. A k EC factor of 0.38 (Vance et al. 1987) was used to estimate microbial biomass C from extractable C. Soluble organic C in the nonfumigated extracts was used as an estimate of soluble organic C in soil (Deluca and Keeney 1994). Estimates of manure-induced quantities of emissions ( RESP), microbial biomass C ( MBC) and soluble C ( SOC) were made by subtracting values measured on the fertilized treatment from those measured on manure treatments. Treatment effects on fluxes were examined for each sampling day using the interaction between block and treatment as the error term in the General Linear Models procedure in SAS (SAS Institute, Inc. 1990). RESULTS AND DISCUSSION The average daily air temperature was 19.6 C, and total precipitation was 354 mm during June, July and August. These
3 ROCHETTE AND GREGORICH SOIL C DYNAMICS IN MANURED SOILS 285 Table 1. Composition of stockpiled and rotted manure (dry-weight basis) Moisture Total N Total C NH 4 -N NO 3 -N Soluble C Manure type (g g 1 ) ph (g g 1 ) (g g 1 ) (mg kg 1 ) (mg kg 1 ) (g kg 1 ) Stockpiled Rotted values are 0.3 C and 104 mm higher than average values since 1890, respectively. Soil temperature and moisture were not significantly different among treatments. Soil temperature at 0.10 and 0.20 m, averaged across treatments, peaked at 28 and 24 C, respectively (Fig. 1a). Except for a brief period at the time of pre-planting tillage (day 130), soil moisture in the top 0.2 m remained 0.25 m 3 m 3 until day 240 in response to the relatively abundant rainfall, after which it fluctuated between 0.20 and 0.25 m 3 m 3 (Fig. 1b). Soil Surface Fluxes Rates of soil flux from the control and fertilized plots were not significantly different. Average (Table 2) and maximum flux values (Fig. 2a) from these treatments were similar to those measured in mineral soils under grain crops in previous years in Ottawa (Rochette et al. 1992). The observation of equal values of flux on fertilized and control plots has practical significance, because the level of mineral N in soil is expected to have an effect on the respiration processes in the soil ecosystem. Nitrogen fertilization has little effect on the total root biomass of maize (Anderson 1987; Eghball and Maranville 1993), but maize plants grown at high-n levels lose a larger portion of the C transferred to the roots as root-rhizosphere repiration (R rr ) than plants grown at low-n levels (Liljeroth et al. 1994). In this experiment we did not observe any differences in evolution between the control and fertilized treatments, indicating that N addition did not appear to increase decomposition rates. The influence of N fertilizer on the decomposition of soil organic matter is complex. In the absence of fresh plant residues, it has been reported that the addition of NO 3 reduces evolution (Kowalenko et al. 1978; Puig- Gimenez and Chase 1984). Green et al. (1995) confirmed this effect on native soil organic matter but also showed that NO 3 increased the rate of decomposition of stover added to the soil. Our measurements indicate that the net result of these opposite effects of N fertilizer on the decomposition of soil organic matter was small under the conditions of this study. Similar decomposition rates of soil organic matter in the fertilized treatment and the control, combined with the Fig. 1. Seasonal variations of a) soil temperature and b) soil water content from April to November Values were averaged over four treatments, each of which were replicated three times. Error bars indicate standard deviations. increased return of plant residues (Table 2) in the fertilized treatment, suggest that the fertilized soil was gaining C in 1994 compared with the control. These results are in agreement with the observation by Gregorich et al. (1996) that >30 yr of fertilization of maize had no effect on the level of native organic C but increased the amount of maize-derived C in soil. The addition of stockpiled and rotted manure increased flux by a factor of 2.2 and 2.6, respectively, compared Table 2. Soluble organic C (SOC) and microbial biomass C (MBC), and cumulated soil-surface flux (RESP) in soils receiving fertilizer (ammonium nitrate), stockpiled and rotted manure, and in unamended control. Values are averages for the growing season SOC RESP MBC SOC z RESP z MBC z ADM y Treatment (mg C kg 1 ) (g C m 2 d 1 ) (mg C kg 1 ) (mg C kg 1 ) (g C m 2 d 1 ) (mg C kg 1 ) (kg C m 2 ) Control Fertilizer Stockpiled Rotted z values are observed values minus control values for the fertilizer treatment, and minus Fertilizer values for manure treatments. y Aboveground dry matter of maize at harvest.
4 286 CANADIAN JOURNAL OF SOIL SCIENCE Fig. 2. Seasonal variations of a) soil-surface flux (RESP), b) soluble organic carbon (SOC), and c) microbial biomass carbon (MBC) from April to November 1994 in maize soils amended with 100 t ha 1 of stockpiled or rotted manure, 200 kg ha 1 NH 4 -NO 3 -N and an unamended soil (control). Error bars indicate standard deviations. with values on fertilized plots (Table 2). Values of flux were similar on both manure treatments except for a 3-wk period in June and one sampling date in mid-august (Fig. 2a). Differences between the manured and nonmanured treatments were small or non-existant early and late in the snow-free period but were at a maximum in the summer months. The seasonal pattern was governed by soil temperature which explained between 78 and 95% of the variation in flux (Fig. 3a). This exceptionally close relationship between soil respiration and soil temperature is likely the result of optimum soil water contents during most of the season (Fig. 1b) and to the abundance of readily decomposable C in manure treatments. Fig. 3. Relationships between soil temperature in the top 0.2-m layer and a) soil-surface flux (RESP), and b) manure-induced RESP ( RESP). Equations presented in a) refer to the treatments listed in b) in the same vertical order. Treatments are described in Fig. 2. The increased flux in manure treatments was due to the input of additional available C substrates to the soil. Isolating the influence of manure on soil C dynamics under field conditions is difficult. In this study, we subtracted the flux values obtained on fertilized plots from those on manured plots to account for the effect of all factors other than the addition of the manure on flux. This approach has a weakness in that it is not known if the effects of N on the decomposition of soil organic matter (Green et al. 1995) are the same with organic and mineral N sources. However, the aboveground plant biomass was the same on manure and fertilized treatments (Table 2), and thus any effects related to the root activity were assumed to be similar. Manure-induced changes in flux ( RESP) were near zero early and late in the season, and were highest between days 160 and 220 (Fig. 4a). Values of RESP were about the same on both manure treatments from the start of when measurements were taken until day 160. The seasonal peak was lower in stockpiled (23.6 g m 2 d 1 ) than in rotted manure (31.6 g m 2 d 1 ). This pattern is the result of a higher response of RESP to temperature at temperatures 15 C on rotted than on stockpiled manure plots. (Fig. 3b). Therefore, factors other than temperature are responsible for the slower mid-season decomposition rates in stockpiled manure plots. The fact that losses of -C were higher on soils amended with rotted manures than those amended with
5 ROCHETTE AND GREGORICH SOIL C DYNAMICS IN MANURED SOILS ). Total RESP for the season was 5.7 Mg C ha 1 on stockpiled and 7.0 Mg C ha 1 on rotted manure. These losses accounted for 52% of the C in the applied stockpiled manure and 67% of the C in the applied rotted manure. Therefore, it appears that the C dynamics in these plots were still not in equilibrium after 3 yr of heavy manure application. The calculated soil C gain in 1994 was 5.3 Mg ha 1 in the stockpiled manure treatment and 3.4 Mg ha 1 in the rotted manure treatment. Fig. 4. Seasonal variations of manure-induced a) soil-surface flux ( RESP), b) soluble organic carbon ( SOC), and c) microbial biomass carbon ( MBC) from April to November Treatments are described in Fig. 2. stockpiled manure (Table 2; Fig. 4a, b) suggests there was a difference in the amount of readily decomposable C in the two manures. Following a change in farming practices that increases the return of organic residues to the soil, the rates of the decomposition processes gradually increase until the -C losses equal the new C input (Janzen et al. 1997). During this adjustment period, soil C increases by the difference between organic input and gaseous output, assuming no losses of soil by erosion. The cumulative -C losses induced by manure application were integrated by linearly interpolating RESP values between the sampling dates. Measured values were considered representative of mean daily fluxes because the m soil temperature at 12:00 h was close to its daily mean value (Lessard et al. Microbial Biomass C The seasonal average for microbial biomass C in control plots (Table 2) is consistent with values reported by McGill et al. (1986) on unfertilized plots in various crop rotations (389 mg C kg soil 1 ). Biomass C in the fertilized treatment was higher than in fertilized third-year maize in Ontario (70 to 125 mg C kg soil 1 ; Drury et al. 1991) but lower than in fertilized continuous barley in Québec (321 mg C kg soil 1 ; Angers et al. 1993) and in various fertilized crop rotations in Alberta (431 mg C kg soil 1 ; McGill et al. 1986). The ratio of microbial biomass C to total soil organic C was about 1.5% in control and fertilized treatments and 3.5% in manure treatments. If the microbial biomass content of soils is used as an early indicator of changing soil organic matter contents, then the larger proportion of total organic C as microbial biomass in manured soils indicates that the C levels in soils receiving manure will increase. The ratio of microbial biomass C to total soil C measured in this study was lower than average values reported for a range of fertilized soils under monoculture (2.36%) but higher than average values in manured soils (2.57%; Anderson and Domsch 1989). The microbial biomass C in the top 0.20 m of the soil was significantly (P < 0.01) increased by the application of manure but not by the application of NH 4 -NO 3 (Fig. 2c). The microbial biomass C remained relatively steady during the growing season in control and fertilized treatments whereas the highest values were observed in June in the manure treatments. Paul and Beauchamp (1996) also observed that microbial biomass concentration increased following spring application of dairy cattle manure. The high values in the spring prior to the application of the manure are a residual effect of the manure applied in the 2 previous years. This is in agreement with the observation that microbial biomass C reflects the cumulative rather than the current-year input of C in the soil (McGill et al. 1986). Microbial biomass C was positively correlated to soil water content in the rotted (r = 0.84) and stockpiled (r = 0.68) manure treatments but not in the control (r = 0.22) and fertilized (r = 0.22) treatments. McGill et al. (1986) and Perfect et al. (1990) have also observed that seasonal dynamics of microbial biomass C were related to soil water status. However, this relationship between soil moisture and microbial biomass can also result from the greater efficiency of the fumigation as the water content increases (Sparling and West 1989). The microbial biomass C was not correlated with the seasonal dynamics of soil respiration. However, the specific
6 288 CANADIAN JOURNAL OF SOIL SCIENCE respiration of the manure-induced microbial biomass C ( RESP/ MBC; soil bulk density = 1.2 Mg m 3 ; m soil layer) was similar on stockpiled (0.084 g g 1 microbial biomass C d 1 ) and rotted (0.097 g g 1 microbial biomass C d 1 ) manure treatments. This indicates that the mean increases in microbial biomass C and flux resulting from the addition of manure are related, but that the seasonal pattern of flux is controlled by the fluctuations of environmental factors rather than solely by microbial biomass C. The maintenance energy requirements of microbial populations are needed to understand and predict C and N dynamics in soils. Maintenance energy data obtained from pure culture have yielded high values that are not compatible with C inputs and microbial biomass in agricultural soils (McGill et al. 1981). Smith et al. (1986) calculated the specific maintenance rate of microbial biomass (rate of utilization of biomass C for energy production) using the product formation ( ) instead of the substrate use. Their calculations were based on the released during the incubation at 22 C of soil samples in which microbial biomass C was constant. A yield of product of 0.6 per unit of biomass formed and a 0.4 fraction of active biomass were also assumed. Since the MBC was constant during the second half of the season (days ; Fig. 4c), we used our data to make a similar calculation under field conditions. We obtained specific maintenance rates of 4.6 and h 1 for the microbial biomass induced by the addition of stockpiled and rotted manure ( MBC), respectively when cumulated -C (stockpiled = 3640 kg -C ha 1 ; rotted = 4619 kg -C ha 1 ) and mean MBC over the 148-d period (stockpiled = 1080 kg C ha 1 ; rotted = 1133 kg C ha 1 ) were fed into the Eq. 15 of Smith et al. (1986). Values for the other factors used in the equation were the same as in Smith et al. (1986). These values are slightly higher that those reported by Smith et al. (1986) for five soils from eastern Washington (3.0 to h 1 ) despite a lower average soil temperature (17.3 C) in our study than in the incubations of Smith et al. (1986). Assuming that the field and laboratory calculations are comparable, the relatively high maintenance rates of microbial populations sustained by the addition of manure could be explained by a lower yield of product or a larger fraction of active biomass than in non-manured soils. Fig. 5. Relationships between manure-induced soluble organic carbon ( SOC) and a) manure-induced soil surface flux ( RESP), and b) soil temperature. Dark squares represent observations on soils amended with stockpiled or rotted manures. Open circles represent observations made in the 4 wk following manure application, and were not included in the regression analysis. Soluble Organic Carbon Ammonium nitrate fertilizer had no effect on soluble C (extracted using K 2 SO 4 ) levels but stockpiled and rotted manures increased it by a factor of 2.7 and 3.2, respectively, (Table 2) relative to the unamended soil. In manured soils, soluble C increased sharply after manure application and gradually decreased during the season. The concentration of soluble C in control and fertilized soils ranged from 40 to 100 mg C kg soil 1 during the growing season (Fig. 2b). Levels of soluble organic C in these soils remained remarkably steady at about their seasonal average ( 60 mg C kg soil 1 ) during most the season except for an increase in June. Variations of K 2 SO 4 soluble C between 42 and 88 mg C kg soil 1 in fertilized continuous moldboardplowed barley during a 2-yr period in Normandin, Québec (D. A. Angers, personal communication) compare well with those observed in our fertilized soil. McGill et al. (1986) reported water-soluble organic C levels in long-term plots in northern Alberta. Their values on control and fertilized treatments are about half the soluble C levels of measured on the same treatments in this study. However, comparisons of soluble C are difficult because of the different extractants used (cold-water vs. K 2 SO 4 ) in the two studies. Values of SOC were not correlated to RESP when measurements for both manure treatments and all sampling dates were used (Fig. 5a). However, if the group of five data points from the period of time shortly after the application of manure and corresponding to SOC > 150 mg C kg soil 1 are removed, a highly significant correlation is obtained (Fig. 5a). The same observation is also valid for the relationship between SOC and soil temperature (Fig. 5b). The lack of fit for the soluble organic C measured in the first few weeks following manure application could result from several factors. These include the natural physiological limitations of the microorganisms to utilization of the substrate or the presence of recalcitrant forms of soluble C that are either subsequently decomposed or leached from the surface soil. Also, large quantities of manure may have temporarily disrupted microbial activity because of increased soil osmotic
7 ROCHETTE AND GREGORICH SOIL C DYNAMICS IN MANURED SOILS 289 Table 3. Flow and turnover rate of C through the microbial biomass and soluble organic fractions in the m layer of soil under different treatments Microbial biomass C Soluble organic C Biomass C z Turnover y Flow x Soluble C z Turnover w Flow v Treatment (mg C kg 1 ) (yr 1 ) (mg C kg 1 yr 1 ) (mg C kg 1 ) (yr 1 ) (mg C kg 1 yr 1 ) Control Fertilized Stockpiled manure Rotted manure z Average value. y Summation of measured losses in biomass C/average biomass C. x Turnover biomass. w Flow of soluble organic C/average soluble organic C. v Biomass C flow/50% C utilization efficiency. potential resulting from high concentrations of anions in the manure (data not shown). Before and after that period, the decomposition processes are in balance and the microbial activity (as expressed by RESP) is related to the SOC pool and soil temperature. Under the optimal water content conditions experienced during our study, temperature was the main controlling environmental factor, as indicated by its strong relationship with RESP and SOC. The increase in SOC that occurs as soil temperature increases suggests that the processes that solubilize soil C are more sensitive to a change in temperature than the processes that mineralize soluble C. Also, all of the data, with the exception of those for the period shortly after manure application, could be described by the same linear relationship, suggesting that the manure-derived soluble C remained equally available for the microbes throughout most of the growing season. A minimum estimate of the turnover of microbial biomass was made by dividing the summation of biomass losses measured over the season by the seasonal average amount of biomass present as proposed by McGill et al. (1986). Such estimates indicate that biomass was recycled between 0.72 and 1.22 times a year in the soils under the different treatments (Table 3). Average biomass levels were higher and turnover rates were lower on the manured soils than on the unamended control and fertilized soils. McGill et al. (1986) also reported that soils receiving manure amendments had higher levels of biomass with a slower turnover than fertilized soils. The quantity of biomass and the flow of C through the biomass were similar in the two manured treatments. The average quantity of soluble C was more than three times greater on the manured plots than on the unamended control and fertilized soils (Table 3). The annual flow of C through this soluble component supplies substrate for biomass turnover and ranged from 470 mg kg 1 in the fertilized soil to more than 1000 mg kg 1 in the manured soils. CONCLUSIONS Application of 200 kg N ha 1 of ammonium nitrate fertilizer to a maize crop had little effect on soil surface emissions, microbial biomass C and soluble C compared with an unfertilized control. Equal soil -C losses from fertilizer treatment and control, combined with larger return of crop residue-c to the fertilized soil, indicate that total soil C was increasing in the fertilized treatment relative to the control. The addition of manure to the soil for a third consecutive year markedly changed the dynamics of soil C relative to that in the unamended soil. Soil surface emissions were more than doubled compared with the fertilizer treatment (200 kg N ha 1 ). Despite these increased oxidative losses, it was estimated that approximately half of the added manure- C was retained in the soil at the end of the season. Levels of microbial biomass C early in the season, prior to the 1994 application of manure, were higher in manure treatments than in the control, indicating that microbial biomass responded to cumulative annual additions of manure. The 1994 addition of manure had a much smaller effect on microbial biomass C. Soil temperature explained most of the variations in flux (78 to 95%) in each treatment, but data from all treatments could not be fitted to a unique relationship. Increases in emission and soluble C resulting from manure amendments were strongly correlated (r 2 = 0.75) with soil temperature. This observation confirms that soluble C is an active C pool affected by biological activity. The positive correlation between soluble organic C and soil temperature also suggests that production of soluble C increases more than mineralization of soluble C as temperature increases. ACKNOWLEDGEMENTS We thank Mrs. A Barbeau and Mssrs. R. Lessard, S. Millette and Dr. B.C. Liang for their assistance in the data collection and laboratory analysis. We also thank Dr. B.L. Ma for providing the yields of aboveground dry matter. Anderson, E. L Corn root growth and distribution as influenced by tillage and nitrogen fertilization. Agron. J. 79: Anderson, T. H. and Domsch, K. H Ratios of microbial biomass carbon to total organic carbon in arable soils. Soil Biol. Biochem. 21: Angers, D. A., Bissonnette, N., Légère, A. and Samson, N Microbial and biochemical changes induced by rotation and tillage in a soil under barley production. Can. J. Soil Sci. 73: Burford, J. R. and Bremner, J. M Relationships between the denitrification capacities of soils and total, water soluble and readily decomposable soil organic matter. Soil Biol. Biochem. 7: Cook, B. D. and Allan, D. L Dissolved organic carbon in
8 290 CANADIAN JOURNAL OF SOIL SCIENCE old field soils: total amounts as a measure of available resources for soil mineralization. Soil Biol. Biochem. 24: Davidson, E. A., Galloway, L. F. and Strand, M. K Assessing available carbon: comparison of techniques across selected forest soils. Comm. Soil Sci. Plant Anal. 18: Deluca, T. H. and Keeney, D. R Soluble carbon and nitrogen pools of prairie and cultivated soils: seasonal variation. Soil Sci. Soc. Am. J. 58: Drury, C. F., Stone, J. A. and Findlay, W. I Microbial biomass and soil structure under corn, grasses and legumes on a clay loam soil. Soil Sci. Soc. Am. J. 55: Eghball, B. and Maranville, J. W Root development and nitrogen influx of corn genotypes grown under combined drought and nitrogen stresses. Agron. J. 85: Gilmour, C. M. and Gilmour, J. T Assimilation of carbon by soil biomass. Plant Soil 86: Green, C. J., Blackmer, A. M. and Horton, R Nitrogen effects on conservation of carbon during corn residue decomposition in soil. Soil Sci. Soc. Am. J. 59: Gregorich, E. G., Ellert, B. H., Drury, C. G. and Liang, B. C Fertilization effects on soil organic matter turnover and corn residue C storage. Soil Sci. Soc. Am. J. 60: Horwath, W. R. and Elliott, L. F Microbial C and N dynamics during mesophilic and thermophilic incubations of ryegrass. Biol. Fertil. Soils 22: 1 9. Janzen, H. H., Campbell, C. A., Gregorich, E. G. and Ellert, B. H Soil carbon dynamics in Canadian agroecosystems. In R. Lal, J. Kimble, and R. Follet, eds. Soil processes and the carbon cycle. Advances in soil science. Lewis Publishers, CRC Press, Boca Raton, FL. Kowalenko, C. G., Ivarson, K. C. and Cameron, D. R Effect of moisture content, temperature and nitrogen fertilization on carbon dioxide evolution from field soils. Soil Biol. Biochem. 10: Lessard, R., Rochette, P., Gregorich, E. G., Pattey, E. and Desjardins, R. L N 2 O fluxes from manure-amended soil under maize. J. Environ. Qual. 25: Liljeroth, E., Kuikman, P. and Van Veen, J. A Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant Soil 161: McGill, W. B., Cannon, K. R., Robertson, J. A. and Cook, F. D Dynamics of soil microbial biomass and water-soluble organic C in Breton L after 50 years of cropping to two rotations. Can. J. Soil Sci. 66: McGill, W. B., Hunt, H. W., Woodmansee, R. G. and Reuss, J. O PHOENIX. A model of the dynamics of carbon and nitrogen in grassland soils. In F. E. Clark and T. Rosswall, eds. Terrestrial nitrogen cycles. Ecol. Bull. (Stockholm) 33: Paul, J. W. and Beauchamp, E. G Effect of carbon constituents in manure on denitrification in soil. Can. J. Soil Sci. 69: Paul, J. W. and Beauchamp, E. G Soil microbial biomass C, N mineralization, and N uptake by corn in dairy cattle slurryand urea-amended soils. Can. J. Soil Sci. 76: Perfect, E., Kay, B. D., van Loon, W. K. P., Sheard, R. W. and Pojasok, T Factors influencing soil structural stability within a growing season. Soil Sci. Soc. Am. J. 54: Puig-Gimenez, M. H. and Chase, F. E Laboratory studies of factors affecting microbial degradation of wheat straw residues in soil. J. Soil Sci. 64: Reinertsen, S. A., Elliott, L. F., Cochran, V. L. and Campbell, G. S Role of available carbon and nitrogen in determining the rate of wheat straw decomposition. Soil Biol. Biochem. 16: Rochette, P., Desjardins, R. L., Gregorich, E. G., Pattey, E. and Lessard, R Soil respiration in barley and fallow fields. Can. J. Soil Sci. 72: Rochette, P., Ellert B., Gregorich, E. G., Desjardins, R. L., Lessard, R., Pattey, E. and Johnson, B. J Techniques for measuring the soil surface emissions. Can. J. Soil Sci. 77: SAS Institute, Inc SAS user s guide: Statistics, Version 6. 5th ed. SAS Institute, Inc., Cary, NC. Smith, J. L., McNeal, B. L., Cheny, H. H. and Campbell, G. S Calculation of microbial maintenance rates and net nitrogen mineralization in soil at steady-state. Soil Sci. Soc. Am. J. 50: Sparling, G. P. and West, A. W Importance of soil water content when estimating soil microbial C, N and P by the fumigation-extraction methods. Soil Biol. Biochem. 21: Vance, E. D., Brookes, P. C. and Jenkinson, D. S An extraction method for measuring soil microbial biomass. Soil Biol. Biochem. 19: Voroney, R. P., Winter, J. P. and Beyaert, R. P Soil microbial biomass C and N. Pages in M. R. Carter, ed. Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, FL.
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