Arid Soil Research and Rehabilitation, 14 :281È292, 2000Copyright 2000 Taylor & FrancisÓ0890-3069/00 $12.00 1 .00

Potential NitriÐcation Rates of Semiarid CroplandSoils from the Central Ebro Valley, Spain

DAVID BADIAde Produccio n VegetalArea

Escuela Universitaria Polite cnicaHuesca, Spain

T he nitriÐcation capacity of agricultural soils has received little attention in semi±arid Mediterranean environments in spite of the importance of the in theNO3

]

ecosystem. In this study, a laboratory experiment was carried out to evaluate poten±

tial nitriÐcation in six agricultural soils from semiarid Central Ebro V alley(northeastern Spain). T riplicate topsoil samples (0È15 cm) were collected seasonallyover a 2± year period. T he nitriÐcation capacity was evaluated by fresh soil incu±

bation at 25°C and Ðeld capacity with a source. V erhulstÏs equation wasNH4+ ± N

used to express the accumulation of NO3 ] ± N with time. T he potential nitriÐcationrate was derived from the equation and used to quantitatively characterize(Kmax)the nitriÐcation process.

T he obtained by Ðtting a sigmoidal curve, allowed us to distinguish theKmax ,nitriÐcation capacity of each semiarid agricultural soil. T he varied betweenKmaxseasons which indicate that time± variable soil properties (such as salinity andclimate) inÑuenced the nitriÐcation rate even in an incubation experiment. On anannual average, for saline or highly gypsiferous soils ranged from 8.5 to 9.4Kmaxmg kg ] 1 d ] 1 . For the rest of the soils. ranged from 36.3 to 43.7 mgNO 3

] ± N Kmaxkg ] 1 d ] 1. Potential nitriÐcation rate was negatively correlated (P , 0.01)NO3

] ± Nwith soil salinity and positively correlated with total organic C, microbial activity,and microbial biomass. Highly gypsiferous soil showed a low (8.9 mgKmax NO 3

] ± Nkg ] 1 soil d ] 1) with the lowest content in Ðeld samplings (7 kgNO 3

] ± N NO 3] ± N

ha ] 1 as an annual average). T his fact demonstrated certain inhibition of the nitriб

cation that can be attributed to unbalanced properties in the highly gypsiferous soil.

Keywords potential nitri�cation, nitrate content, seasonal dynamics, agricultu ±

ral soils, semiarid lands, Ebro Valley

Nitri�cation is an important biological process with special signi�cance in agricultu ±

ral soils where mineral and/or organic fertilization are habitual. Urea and ammon±

ium sulfate, widely used as nitrogenous fertilizers, are oxidized and increase thecontent of agricultural soils. This process could be limited by concentra ±NO3

] NH 4+

tion but also is in�uenced by environmental factors such as temperature and mois±

ture (Malhi and McGill 1982 ; PietikaÈ inen and Fritze 1995 ; Schmidt and Belser1982 ; Yadav et al. 1987). Previous works showed that nitri�cation can also bedelayed by soil properties as salinity (Schmidt and Belser 1982 ; Gomah, Al± Naid,and Amer 1989), or favored by organic matter quantity and quality (Gispert andBad õÂ a 1988 ; Nannipieri, Greco, and Ceccanti 1990). Possible disadvantages of fast

Received 22 April 1999 ; accepted 13 August 1999.Financial support was partially provided by the Diputacioð n Provincial de Huesca (Project 96/

0237.4 on The Study of Semiarid Ecosystems). We also thank Josep Ma AlcanÄ iz, Mark Coyne, JoseðMiguel Gonzað lez and Pep PinÄ ol for their advice.

Address correspondence to Dr. David Bad�ð a, de Produccioð n Vegetal, Escuela UniversitariaAŠ reaPoliteð cnica, Crtra. Cuarte s/n, 22071-Huesca, Spain. E-mail : badia@ posta.unizar.es

281

282 D. Bad� a

nitri�cation are N ± losses by leaching and runoŒ, or movement of out of theNO3]

crop rooting zone with eventual accumulation in ground and surface waters.NO3]

Under anaerobic conditions, could be lost by denitri�cation. On the otherNO 3]

hand, a very low rate of nitri�cation encourages losses of applied throughNH4+ ± N

ammonia volatilization, an important gateway of N loss in arid and semiarid condi±tions (Praven ± Kumar and Aggarwal 1988).

With the agronomic concern for increased food production and decreasedenergy losses without negative environmental impacts, the need for more knowledgeof nitri�cation is easily evident. Most studies on nitri�cation have dealt with soilsfrom cold or temperate climates (Parker and Larson 1962 ; McCormick and Wolf1980 ; Arcara and Sparvoli 1982 ; Malhi and McGill 1982 ; Abbes, Parent, andKaram 1994), and little information is available on semiarid areas, especially incalcareous, saline, or gypsiferous soils. Because of climate and lithographic features,semiarid agricultural soils of the Central Ebro Valley (northeastern Spain) have alow organic matter content and high amounts of carbonates, gypsum or moresoluble salts (Bad õÂ a et al. 1998). The objectives of the study described here were tocharacterize nitri�cation kinetics of in six agricultural soils (with diŒer±(NH4)2SO4ent gypsum, carbonate, and salt contents) from the semiarid Central Ebro Valleyand evaluate the seasonal variation of nitri�cation, as an agroecological soil bio±

process during two years.

Materials and Methods

Site, Soils, and Crops

The experimental plots were selected from representative croplands in northeastSpain, in the Central Ebro valley (province of Huesca). This region has a semiaridMediterranean climate, with an average annual rainfall ca 350 mm, which occursmostly in autumn and spring, and an average temperature of 15°C. The potentialannual evaporative demand, estimated by the Blaney and Criddle method, was ca1300 mm (Faci and Martinez 1991). The soil temperature regime is thermic and thesoil moisture is aridic ranging to xeric. Lithology is dominated by marls, limestones,and gypsum from Oligocene or Miocene periods. Natural vegetation is dominatedby kermes oak scrub (Quercus coccifera L.). Winter barley (Hordeum vulgare L. var.Albacete) is the chief crop in the area. All selected plots had a surface of about 400m2, and their soils were classi�ed as Xeric Torriorthents. In all these soils winterbarley was sowed in October and harvested in June. Crop production for thestudied period was about 1.5 Mg ha ] 1 for soils GD, SI, and SD ; about 2.5 Mgha ] 1 for CD, and about 3.5 Mg ha ] 1 for GI and CI.

Selected chemical, physical and biological properties of the soils, as determinedby standard procedures (Page, Miller, and Keeney 1982 ; Klute 1986), are shown inTable 1. More information on these soils (properties and factors of formation) isavailable from Bad õÂ a and AlcanÄ iz (1994, 1996).

Temperature and Soil Moisture Content

Soil temperature and water content were measured in each plot, before sampling.Soil temperature was determined at 10 ± cm depth with thermocouple sensors. Soilwater content was determined at 10± cm depth with Boyoucos blocks or gravimet ±

rically (when soil moisture exceeded the range of the blocks); it is expressed as %(w/w). Additionally, rainfall collectors were installed in every plot. Soil temperature,soil water content, and monthly rainfall during the period of study are reported(Figure 1).

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284 D. Bad� a

Sampling, Incubation Procedure, and Soil Analysis

The soil samples were collected seasonally during a 2± year period (eight seasons) ineach of the six plots, leading to an analysis of nitri�cation rates in 48 sets of tripli±cate soil samples. On each seasonal sample, nitri�cation was measured as were otherstandard chemical organic C, EC, SAR) and biological (microbial activity,(NO3

] ± Nmicrobial biomass) properties. The samples were taken with aluminum rings ofknown volume to a depth of 15 cm. Three replicates were taken for each plot andstored separately in a portable refrigerator at a temperature of 4°C during the trans±

port to the laboratory. Fresh soil samples were used within 24 h of collection tobiological determinations. Stones, roots and plant debris were �rst removed bysieving through a 2± mm mesh.

To measure the nitri�cation rate, fresh soil (250 g dry weight) was placed in a300 mL Pyrex jar, moistened with 2.5 mL of solution (126 mg(NH4)2SO4 NH4

+ ± NmL ] 1) and sufficient water to bring it to the water �eld capacity (2 33 kPa). Themeasured initial ammonium concentration in the soil samples was similar to theconcentration added (1260 mg kg ] 1). Weight of the samples were measuredNH4

+ ± Ndaily and moisture losses compensated. Jars were incubated in the dark for fourweeks at 25 6 1°C, a temperature in the range of optimal activity for nitrifyingbacteria (Frederick 1956 ; West and 1978). Nitrate measurements were per±Skujins) ,formed in soil subsamples seven times during the incubation period every four or�ve days. Nitrate content of soil subsamples (7 g) was determined after(NO3

] ± N)extraction with 1N with previous elimination of chlorides by precipitationCuSO 4 ,with Nitrate content was measured spectrophotometrically by the phenol ±AgSO 4 .disulfonic acid method (Bremner 1965), using a Hitachi V± 3200 UV± Vis spectropho ±

tometer.The other standard parameters measured in this study, and its methodology,

included the following :

1. Physical and chemical parameters. Particle size distribution was determined bythe pipette method using methaphosphate as dispersing agent. Field capacity(2 33 kPa) was measured by volumetric pressure plate extractor (Soilmoisture

FIGURE 1 Soil temperature (°C) and soil water content (%, w/w) at 10 cm depthand rainfall (mm), as the mean of the six experimental plots.

NitriÐcation in Semiarid Cropland 285

Equipment). The soil pH was determined potentiometrically in a 1 : 2 ratio inTotal carbonates content was measured gas volumetrically after disinte±H2O.

gration with HCl (calcimeter). Soil organic C was obtained by wet digestion withK ± dichromate and organic matter estimated using van Bemmelen factor (1,724).Total nitrogen content was determined by Kjeldahl procedure. Gypsum wasmeasured by elementary analysis of total sulphur. Cation exchange capacity(CEC) was determined by retention after percolation with a neutral solu±NH4

+

tion of 1N The electrolytic conductivity (EC) was measured in theNH4OAc.saturated paste extract of the soil. Sodium absorption rate (SAR) was determinedfrom the soluble ions obtained in last extract. Methodological details of thesemethods can be found in Klute (1986) and Page et al. (1982).

2. Biological properties. evolved from soil was obtained as a measure of globalCO2microbial activity, using a static chamber method (Anderson 1982 ; Bad õÂ a andAlcanÄ iz 1994). In hermetically sealed 1± L glass �asks, 100 g of fresh soil (removedstones and roots) were introduced and moistened to �eld capacity. The �askswere kept in darkness at 25 6 1°C for 30 days. Carbon dioxide evolution wasmeasured, every two days, by capturing in 10 mL of 2M NaOH, placed in aCO2vial inside the �asks, adding 10 mL of 1.5N and then titrating excessBaCl2NaOH with 1M HCl. An adequate level of oxygen was maintained opening the�asks every two days until the end of the experiment. The microbial activity wasexpressed as the average of the evolved along the 30± day incubation period.CO2On the other hand, the microbial biomass was measured using the chloro±(Cmic)form fumigation ± incubation method (Powlson and Brookes 1987).

Data Analysis

Under adequate environmental conditions, the rate of nitri�cation exhibits a curvewith a lag phase during which the nitrifying population develops an exponentialphase, and a retarded rate phase due to the depletion of ammonium in soil (Abbes etal. 1994 ; Grant 1994). Sigmoidal models have been found suitable for describingnitri�cation studies by several investigators (Sabey, Frederick, and Bartholomew1959 ; Hadas et al. 1986). For this reason, the accumulation of with timeNO3

] ± Nwas expressed, quantitatively, using the Verhulst equation (Jolivet 1983). TheKaleida Graph package (version 2.0.2. Abelbeck Software Inc.) was used to �t, bythe least ± squares method, the cumulative production vs time in a sigmoidalNO3

] ± Nmodel and to determine the potential nitri�cation rate. Individual nitri�cation ratedeterminations and their interpretation were previously reported (Hadas et al. 1986 ;Bad õÂ a and AlcanÄ iz 1996). Results were expressed in mg kg ] 1 dry soilNO3

] ± Nday ] 1.

The data were analyzed using the StatView statistical package for analysis ofvariance (Abacus Concepts Inc., Berkeley, California). The separation of means wastested using the Least Signi�cance DiŒerences test with a signi�cance level ofP , 0.01. Regressions and correlations between and other soil properties wereKmaxalso determined (Spearman rank correlation test : P , 0.05 and P , 0.01).

Results and DiscussionThe accumulation of with time in the studied soils for every seasons wereNO3

] ± Nsigmoidal, showing a delay phase, a maximal rate phase and a retarded phase,similar to those of Hadas et al. (1986). The coefficient of determination (r) ofsigmoidal curve �tting ranged between values of 0.70 and 0.99 ; more than 90% ofthe data well �t sigmoidal curves (P , 0.05). As an example, and because the curvesfrom other seasons were essentially the same, the curves for January 1989 are shownin the Figure 2. Maximum values of nitrates were about 1300 mg kg ] 1 thatNO3

] ± N

286 D. Bad� a

FIGURE 2 Nitrate evolution (mg kg ] 1) in diŒerent agricultural soils,NO3] ± N

sampled in January 1989. Each value is the mean of three replicates.

indicated practically all added was available while gas losses and nitrogenNH4+

mineralization were scarce, at least in a half of the experimental soils. Because nitri±�cation was studied as an agroecological soil process, nitrate production was(Kmax)analyzed in this study.

The of the 48 samples ranged from a minimum of 1.5 to a maximum ofKmax105 mg kg ] 1 soil d ] 1 (Table 2). These values were similar to other poten ±NO 3

] ± Ntial rates reported for mineral agricultural soils, using similar techniques (Sabey etal. 1959 ; Malhi and McGill 1982 ; Hadas et al. 1986 ; Bhupinderpal ± Singh, Bijay ±

Singh, and Yadvinder ± Singh 1993) where ranged from 3 to 90 mgKmax NO3] ± N

kg ] 1 soil d ] 1. Along with soil climate (temperature, moisture), other factors (assalinity, organic matter content, or crop growth stage) changed along the period ofsoil sampling which can aŒect initial population of nitrifying organisms (Sabey et al.1959 ; Parker and Larson 1962 ; Sorensen 1974 ; Hadas et al 1986 ; Yadav et al. 1987 ;Gomah et al. 1989 ; Stark and Firestone 1995). On average, the highest values of

were obtained in spring and winter, more favorable periods for microbialKmax

TABLE 2 Potential soil nitri�cation rates, (mg kg ] 1 d ] 1), duringKmax NO3] ± N

diŒerent seasonal samplingsa

Sampling date (month/year)

Soil Oct/87 Jan/88 Apr/88 July/88 Oct/88 Jan/89 Apr/89 July/89 Average CVb

GI 12.3bc 26.1a 40.7c 34.8c 12.2b 80.0b 44.3a 40.3a 36.3a 59.6GD 3.7d 18.3b 7.1e 5.2e 17.2a 9.0d 4.3b 6.5c 8.9b 64.1SI 8.7c 16.1bc 18.7d 14.3d 8.9c 2.5e 4.1b 2.3c 9.4b 67.2SD 7.2c 13.0c 4.0e 7.7e 8.7c 20.8c 5.4b 1.5c 8.5b 70.4CI 20.0a 25.1a 52.0b 51.4a 14.7a 105.2a 45.0a 36.5a 43.7a 65.4CD 15.9ab 25.0a 61.7a 43.4b 11.1b 83.5b 39.4a 29.1b 38.7a 62.8

a Seasonal means followed by the same letter are not signiÐcantly di†erent (LSD test ; P , 0.01).b CV, Coefficient of variation (%).c Each value is the mean of three replicates.

NitriÐcation in Semiarid Cropland 287

activity in these semiarid conditions. A moderate condition (P , 0.05) was observedwith soil moisture (r 5 0.33) and temperature (r 5 2 0.29) in �eld conditions.Although large seasonal �uctuations were observed, diŒerences within soilsKmaxwere found. One group, with high values, included the soils developed onKmaxmarls (CI and CD) and gypsiferous marls (GI). A second group, with low Kmaxvalues, comprised the highly gypsiferous soil (GD) and the saline soils (SD, SI). Onan annual average (n 5 8), in the �rst group ranged from 36.3 to 43.7 mgKmax

kg ] 1 soil d ] 1. In the less active group, ranged from 9.4 to 8.5 mgNO3] ± N K max

kg ] 1 soil d ] 1 (Table 2). These values represent a potential nitri�cation ofNO3] ± N

ca 80 kg ha ] 1 d ] 1 for the �rst group and ca 20 kg ha ] 1 d ] 1 forNO3] ± N NO3

] ± Nthe second group. Although potential nitri�cation in the �rst group of soils is fourtimes higher than the second one, the transformation of toNH4

+ ± sources NO3] ± N

during the period of study was not stopped. In fact, saline soils (SD, SI) accumulate,with other ions, a higher amount of than the other soils, during the seasonsNO3

] ± Nof sampling (Table 3). Low crop production and consequent low plant absorptionand poor soil physical quality (surface soil crusting and low in�ltration rates relatedto sodicity levels) can explain why accumulated in the surface horizon ofNO3

]

saline soils (Bad õÂ a 2000). Moreover, it is known that in arid and semiarid soils NO3]

leaching and denitri�cation are restricted by low rainfall (Praven ± Kumar andAggarwal 1988). On the other hand the GD soil, with the lowest level of organic Cand CEC and the highest gypsum content, showed the lowest and the lowestKmax

content during the studied period. These facts indicate that nitri�cationNO3] ± N

processes in these soils (GD, SD, SI) could be inhibited by high gypsum content ormore soluble salts and poor physical properties (high bulk density, low soil aggre±

gate stability).Salts may interfere with one or more of the enzymes that are engaged in nitri� ±

cation (Frankenberger and Bingham, 1982). McLung and Frankenberger (1985)observed a decrease in nitri�cation as great as 75% when was applied to(NH4)2SO4calcareous soils amended with salts to 20 dS m ] 1 (NaCl). Similar or higher ECvalues than 20 dS m ] 1 were observed in some samplings for both studied salinesoils (SI, SD) when lower was measured (Bad õÂ a 2000). These observationsKmaxagree with our results and the results of earlier researchers on nitri�cation in diŒer±

ent soil types (Harada and Kai 1968 ; Laura 1974 ; McCormick and Wolf 1980). Theelectrical conductivity was negatively correlated (P , 0.01) with and withKmaxmicrobial biomass and microbial activity (Table 4). Electrical conductivity (EC)

TABLE 3 Seasonal content, in mg kg ] 1 (mean values of threeNO 3] ± N NO3

] ± Nreplicates 6 standard deviation), in the experimental soils (0È15 cm depth) duringthe studied period (1987/89)

Soils

Season GI GD SI SD CI CD

Oct/87 3.7 6 0.6 4.5 6 0.6 11.9 6 0.5 23.8 6 2.6 5.2 6 0.6 4.3 6 0.2Jan/88 6.1 6 0.4 4.4 6 0.2 10.3 6 0.2 41.7 6 5.0 5.9 6 0.7 5.6 6 1.4Apr/88 3.4 6 0.4 1.5 6 0.3 3.8 6 0.5 62.5 6 2.2 5.8 6 0.3 2.6 6 0.3July/88 15.1 6 1.1 1.2 6 0.2 13.5 6 0.3 20.8 6 1.8 5.7 6 1.0 8.0 6 1.8Oct/88 5.8 6 0.5 1.9 6 0.6 18.5 6 1.5 59.4 6 5.5 2.2 6 0.2 8.6 6 0.4Jan/89 36.9 6 0.5 7.5 6 1.3 77.8 6 6.1 71.8 6 5.4 8.1 6 0.2 13.9 6 0.6Apr/89 13.4 6 0.9 4.1 6 0.2 43.7 6 2.1 55.7 6 6.1 11.9 6 0.9 4.4 6 0.6July/89 18.2 6 1.1 1.8 6 0.1 2.2 6 0.3 53.2 6 1.6 8.2 6 0.2 4.1 6 0.2

Mean (mg N kg ] 1) 12.8 3.4 22.7 48.6 6.6 6.4

kg NO 3] -N ha ] 1 26.8 7.1 51.1 102.1 14.8 11.5

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288

NitriÐcation in Semiarid Cropland 289

TABLE 5 Simple and multiple regression equations among(mg kg ] 1 soil d ] 1), organic C (%) and electrolyticKmax NO3

] ± Nconductivity (EC, dS m ] 1) for all studied soils and seasons(n 5 48)

Regression equation r P

K max 5 36.8 (Organic C) 1 0.11 0.54 0.0001K max 5 2 1.65 (EC) 1 34.4 0.42 0.0030K max 5 29.8 (Organic C) 2 0.81 (EC) 1 9.45 0.57 0.0001

explains 18% of the overall variation and organic C content about 29%, indi±Kmaxcating that both chemical parameters have a close relationship with in theseKmaxsemiarid soils. In general, a high EC provokes stress and leads to low microbiologi±

cal activity (Garc õ a, Herna ndez, and Costa 1994) and biomass (Sarig and Steinber ±

ger 1994).Although the mechanisms by which the various solutes inhibit nitri�cation are

not well known, two eŒects can be recognized : (1) cell death or inactivation (e.g., asa result of cell disruption caused by the movement of water in response to the waterpotential gradient), and (2) a decrease in microbial activity, perhaps as a result ofintracellular inhibition of an enzyme caused by the accumulation of incompatiblesolutes. Partial recovery of nitri�cation was observed following exposure to highosmotic pressure solutions (Darrah, Nye, and White 1987), which suggests that bothreversible and irreversible mechanisms are involved in the inhibition of nitri�cation.On the other hand, organic C was positively correlated (P , 0.01) with parametersindicative of biological metabolism, such as microbial biomass and microbialKmax ,activity (Table 4). A signi�cant relation was found in a multiple regression modelamong the potential nitri�cation rate and the soil organic C and EC (Table 5). Infact, in similar semiarid soils, poor in organic matter, an increase in available Cincreased soil biomass metabolism (Al± Rashidi and Al± Jabri 1990 ; Gomah et al.1989).

Soil gypsum percentage was negatively correlated with (Table 4) althoughKmaxnot signi�cantly (P 5 0.06). Gypsum, unlike more soluble salts, did not vary withtime, which reduced its relationship with In spite of this, the GD soil, withKmax .30% gypsum content (w/w), showed both the lower and lower concen±Kmax NO3

] ± Ntration during the study period. Mashali (1996) considered that gypsiferous soilshave smaller and less active micro�ora. A high gypsum content may modify wateravailability, nutritional conditions, and free space for microbes (Herrero and Porta1987). In previous works with alkaline soils, gypsum ± amended soils released more

than unamended ones (Sindhu and Corn�eld, 1967 ; Singh and TanejaNO3] ± N

1977). Bene�cial eŒects of gypsum on soil nitri�cation were attributed to stimulationof microorganisms and/or neutralization of toxic salts, thereby creating a favourablehabitat for them. The same authors (Sindhu and Corn�eld 1967 ; Singh and Taneja1977) observed that, in the case of rates higher than the optimum, the concentrationof gypsum became sufficiently large to inhibit the function of nitrifying organisms.Thirty percent gypsum in the A± horizon of GD soil was sufficient to limit nitri�ca±

tion.

ConclusionsThe accumulation of with time in the studied soils �t sigmoidal curves well.NO3

] ± NIn general, was nitri�ed quicker in calcareous soils, with higher organic CNH4

+

290 D. Bad� a

content, than in saline or highly gypsiferous soils. On an annual average forKmaxcalcareous soils ranged from 36.3 to 43.7 mg kg ] 1 soil d ] 1. For theNO3

] ± Nremaining soils, ranged from 8.5 to 9.4 mg kg ] 1 soil d ] 1. PotentialKmax NO3

] ± Nnitri�cation rate and other biological properties (microbial activity and microbialbiomass) were negatively correlated (P , 0.01) with salinity and positively withorganic C.

Seasonal �uctuations of were observed in all soils with coefficients ofKmaxvariation about 60%È70% for the studied period. These �uctuations were related todiŒerent time± variable soil properties (salinity, soil climate) which in�uenced thenitri�cation rate even in lab± experiments. The was correlated (P , 0.05) nega ±Kmaxtively with soil temperature and positively with soil moisture.

Nitri�cation potential was not related to soil concentration during theNO3] ± N

sampling period. The content in saline soils was higher than in other soils,NO3] ± N

ranging from 51 to 102 kg ha ] 1 , as an annual average. This showed thatNO 3] ± N

when conditions are favorable, can be formed and accumulated by minimalNO3]

leaching and/or reduced plant absorption. On the other hand, highly gypsiferoussoils showed a low with the lowest content (7 kg ha ] 1, as anKmax NO3

] ± N NO3] ± N

annual average) which evidenced nitri�cation inhibition.

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