Carbon and nitrogen dynamics in a Brazilian soil-pasture system ...

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Aug 1, 2009 - sewage effluent. ADRIEL FERREIRA DA FONSECA,a,* RAFAEL MARQUES PEREIRA LEAL,b UWE HERPIN,c AND ADOLPHO JOSÉ MELFId.


Israel Journal of Plant Sciences

Vol. 59

2011

DOI: 10.1560/IJPS.59.2-4.147

pp. 147–157

Carbon and nitrogen dynamics in a Brazilian soil–pasture system irrigated with treated sewage effluent

a

Adriel Ferreira da Fonseca,a,* Rafael Marques Pereira Leal,b Uwe Herpin,c and Adolpho José Melfid Department of Soil Science and Agricultural Engineering, State University of Ponta Grossa, Av. General Carlos Cavalcanti, 4748-Campus Uvaranas, Ponta Grossa (PR) 84030-900, Brazil b Ecotoxicology Laboratory, Center of Nuclear Energy in Agriculture, University of São Paulo, Piracicaba (SP) 13400-970, Brazil c Research Center of Geochemistry and Geophysics of Lithosphere (NUPEGEL), University of São Paulo, Piracicaba (SP) 13418-900, Brazil d Soil Science Department, ‘Luiz de Queiroz’ College of Agriculture (ESALQ),University of São Paulo, Piracicaba (SP) 13418-900, Brazil (Received August 1, 2009; accepted in revised form April 6, 2010)

ABSTRACT The use of treated sewage effluents for agricultural irrigation represents a promising agronomic–environmental–economic practice; however, little is known about its effects on chemical attributes of tropical soils. This research project aimed at evaluating the effects of irrigation with secondary-treated sewage effluent (STSE) and various application rates of mineral-N fertilizer (MNF) on total carbon (TC) and nitrogen (TN) contents, and ammonium (NH4+-N) and nitrate (NO3–-N) concentrations in a tropical soil–pasture system. The experimental field was cropped with Tifton 85 bermudagrass, over two years. The treatments were: T1 (control), irrigation with potable water and addition of MNF, 520 kg ha–1 year–1; T2–T5, irrigation with STSE (31.9 mg L–1 of total-N) and addition of MNF: 0, 171.6, 343.2, and 520 kg ha–1 year–1, respectively. Soil TC and TN concentrations normally decreased over the experimental period. In general, higher NO3–-N concentrations in the soil solution were found for treatments receiving higher rates of MNF plus TSE irrigation. Compared to fresh water irrigation, STSE caused no changes in soil TC and TN concentrations, and it resulted in slightly higher mineral N concentrations in the soil solution, but without environmental risk. N concentrations in the soil solution were directly influenced by the high N uptake capacity of the Tifton 85 bermudagrass. Keywords: bermudagrass, tropical soil, organic matter, wastewater, recycling

INTRODUCTION The use of treated sewage effluent (TSE) for agricultural irrigation is an old and popular practice worldwide (Feigin et al., 1991), used in dry as well as in humid regions (Bouwer and Chaney, 1974). However, the utilization of TSE for agricultural irrigation is still a recent and limited practice in Brazil (da Fonseca et al., 2005). Ir-

rigation with TSE may be beneficial, reducing demands of natural fresh water resources for crop irrigation and avoiding negative impacts of nutrient-rich effluent input to surface waterbodies. However, it may also result in environmental risks such as salt and trace contaminants *Author to whom correspondence should be addressed. E-mail: [email protected]

© 2011 Science From Israel / LPPltd., Jerusalem

148 accumulation in the soil, and nitrate leaching (da Fonseca et al., 2007a). If adequately managed, the soil–plant system encourages the retention of effluent components (such as macro- and micronutrients) mainly due to their incorporation into dry matter (DM) of plants (Bouwer and Chaney, 1974), leading to a decreasing potential of ground and surface water contamination (Feigin et al., 1978). Crop irrigation with TSE was found to change chemical (Bond, 1998), physical (Balks et al., 1998), microbiological (Friedel et al., 2000), and biochemical attributes of soils (Speir, 2002). The magnitude of these changes in the soil–water–plant system varies considerably depending on soil type, plant species, climate, water sources, and quality/quantity of applied TSE (Hayes et al., 1990; Bond, 1998; da Fonseca et al., 2007a). Regarding total carbon (TC) and total nitrogen (TN) contents in soils, Quin and Woods (1978), Mancino and Pepper (1992), and Friedel et al. (2000) verified increasing concentrations due to high nitrogen (N) and carbon (C) input by TSE. These increases were mainly found in long-term experiments (Quin and Woods, 1978; Friedel et al., 2000; Ramirez-Fuentes et al., 2002). On the other hand, decreases in soil TC and TN concentrations were also reported, and attributed to one or more of the following factors: (i) predominance of effluent-N in the mineral form (Bouwer and Chaney, 1974; Feigin et al., 1991; da Fonseca et al., 2007b); (ii) fast mineralization of the effluent organic N fraction, consisting predominantly of dead algae (Snow et al., 1999); (iii) maintenance of ideal humid conditions (Myers et al., 1982), temperature (Artiola and Pepper, 1992), and re-supply of O2 (Stanford and Smith, 1972) for the mineralization of soil organic matter; (iv) low C/N ratio of TSE (Bouwer and Chaney, 1974; Feigin et al., 1991; da Fonseca et al., 2007c); and (v) increase of microbial activity encouraging soil organic matter (SOM) decomposition (Barton et al., 2005) associated with a priming effect due to high input of effluent-N (da Fonseca et al., 2007c), mainly in tropical soils generally with low organic matter content (De Paula et al., 2010). It is hypothesized that TSE application in a tropical soil–pasture system can result in decreased soil TC and TN concentrations in the short term, also affecting the dynamics of mineral N in soil solution. This is a critical aspect for highly weathered tropical soils, showing variable pH-dependent charge, in which soil organic matter may be responsible for as much as 90% of the total cation exchange capacity of superficial soil layers (Da Silva and Mendonça, 2007). This work aimed at evaluating soil TC and TN contents, as well as mineral N [ammonium (NH4+-N) and nitrate (NO3–-N)] concentrations in soil solution after secondary-treated sewage effluent (STSE) irrigation Israel Journal of Plant Sciences 59

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and addition of various rates of mineral-N fertilizer (MNF) in a tropical soil-pasture system during a 24 month period. The authors are unaware of any other study conducted in Brazil for a soil–pasture system, that evaluated the effects of effluent irrigation on these variables. Previous studies evaluated the influence of effluent irrigation on plant dry matter yield and crude protein content (da Fonseca et al., 2007c), and also soil microbial metabolic potential (De Paula et al., 2010). MATERIAL AND METHODS The experiment was carried out at the municipal district of Lins, State of São Paulo, Brazil (49º50¢W; 22º21¢S; 440 m above sea level; average slope 10%), close to the sewage treatment plant (STP) which is operated by Sabesp (company for basic sanitation of the State of São Paulo). The regional climate is characterized as mesothermic with a dry winter, mean temperatures between 18 and 26 °C, and an annual rainfall level from 1,100 to 1,300 mm (Ciiagro, 2009). The soil of the experimental area is a typic-haplustult, sandy clay loam, cropped with ‘Tifton 85’ hybrid bermudagrass (Cynodon dactylon Pers. ´ C. niemfuensis Vanderyst). Prior to the experiment, the area was fallow land. Four months before grass planting, the area was limed with 2.0 Mg ha–1 of dolomitic limestone in order to raise base saturation to 60% in the 0–20 cm soil layer. The experiment started when the grass was 12 months old. At this time, soil chemical and granulometric analyses of the 0–20 cm layer showed the following results: pH (1:2.5 soil:0.01 CaCl2 mol L–1 suspension) of 4.73; exchangeable aluminum (Al), calcium (Ca), magnesium (Mg), potassium (K), and sodium (Na) contents of 1.40, 10.40, 5.79, 1.12 and 0.45 µm) were 49.44 ± 7.95 and 8.85 ± 1.62 mg L–1, respectively; NH4+-N, NO3–-N, NO2–-N, phosphorus (as orthophosphate, H2PO4–-P), sulfur (as sulfate, SO42–-S), Ca, Mg, K, Na, and alkalinity (as bicarbonate) contents were 22.37 ± 3.52, 0.61 ± 0.53, < 0.02, 4.30 ± 1.11, 4.93 ± 1.36, 8.06 ± 1.07, 1.89 ± 0.46, 16.62 ± 1.81, 145.79 ± 31.33, and 301.41 ± 60.75 mg L–, respectively. More detailed information on STSE composition, soil characterization and crop fertilization and management are available in da Fonseca et al. (2007c). Soil samples were randomly collected using a stainless steel sampler in April, July, and October, 2003; January and July, 2004; and January, 2005. Twelve and six sub-samples were taken forming composite samples from the surface (0–10 and 10–20 cm) and sub-surface layers (20–40, 40–60, 60–80, and 80–100 cm), respectively. Samples were air dried, crushed, and passed through a 2-mm screen. TC and TN determinations were carried out according to the method proposed by Nelson and Sommers (1996). Soil solution and soluble NH4+-N and NO3–-N + NO2–-N concentrations were obtained using saturation extracts, according to Rhoades (1996). Each sample was filtered through a 0.22 µm pore diameter ester-cellulose membrane. Mercuric chloride was added (30 mmol L-1) in order to preserve the samples, which were kept refrigerated at 4 ºC prior to analysis. NH4+-N and NO3--N + NO2--N were determined using conductivity and colorimetric methods, respectively, by means of molecular absorption spectroscopy in a continuous flow injection analysis system (Ruzicka and Hansen, 1975). Once NO2–-N concentrations were below the detection limit (5 µg L–1), mineral N was considered only as the sum of NH4+-N plus NO3–-N. All data were submitted to analyses of variance. The analyses presented a uniform covariance matrix, a necessary condition—according to Huynh–Feldt (H–F)—to carry out univariate statistical analyses for da Fonseca et al. / Carbon and nitrogen dynamics

150 a randomized complete block design, considering time (period of each sampling) as subplot. The variables which showed significant F test (p < 0.05) were submitted to mean comparisons by the Tukey test (p < 0.05). All statistical analyses were carried out using the SAS program, version 9.1 (SAS System, 2004). RESULTS AND DISCUSSION Soil total carbon and total nitrogen contents No changes in soil TC (Fig. 1) and TN (Fig. 2) concentrations were found between treatments, despite the different types of irrigation water applied and the varying quantities of effluent-N input; this disagrees with several other studies. Quin and Woods (1978) observed increasing concentrations of soil TC and TN concentrations in a perennial ryegrass (Lolium perenne L.) pasture irrigated over 16 years with TSE. Latterell et al. (1982) reported higher concentrations of soil TC and TN in a maize (Zea mays L.) crop irrigated with TSE during five years. Mancino and Pepper (1992) found increased soil TC in a bermudagrass pasture (Cynodon dactylon  L.) after TSE irrigation over 3.2 years. Zekri and Koo (1994) observed decreased TN concentrations in sandy soils (Florida region, USA) cultivated with citrus (Citrus sp.) and submitted to TSE irrigation for five years. Falkiner and Smith (1997) verified increased decomposition rates of SOM in forest plantations irrigated with TSE, which decreased soil TC and TN concentrations.

Paliwal et al. (1998) reported increasing TN concentrations in soils under forest plantations submitted to TSE irrigation. Agunwamba (2001) found an increase of approximately 100% of TN in soil cultivated with a maize crop after four years of TSE application. Also in an area cropped with maize, Mohammad and Mazahreh (2003) observed increased soil TC concentrations after TSE irrigation. Madyiwa et al. (2002) found an increase of 2.6% in TC concentration in a soil cropped with star (Cynodon nlemfuensis Vanderyst) and Kikuyu (Pennisetum clandestinum Chiov.) grasses and irrigated with TSE over 29 years. Ramirez-Fuentes et al. (2002) found small effects over 1, 2, 22, 33, 73, and 86 years of TSE irrigation in different agro-systems, leading to increased concentrations in soil TC and TN. However, our results (Figs. 1–2) agree with Ross et al. (1978), who found no changes in the concentrations of TC and TN in ten New Zealand soils cropped with different pastures [perennial ryegrass, Paspalum sp., white clover (Trifolium repens L.), and native grasses from the region] irrigated with 1700 to 2400 mm of TSE for 16 months. Cromer et al. (1984) found no changes in TN concentrations in Australian forest soils subjected to irrigation with TSE. Also, Agunwamba (2001) observed no effects of TSE irrigation with TSE on TC concentrations in Nigerian agricultural soils. Da Fonseca et al. (2005, 2007b) found no changes in TC concentrations after STSE irrigation in Brazilian soils that were similar to the soil used in the present study.

Fig. 1. Effect of irrigation water sources (potable water and secondary-treated sewage effluent, STSE) and rates of mineral-N fertilizer (MNF) application on total carbon (TC) contents in a tropical soil-pasture system. T1: irrigation with potable water and addition of MNF, 520 kg N ha–1 year–1. T2: irrigation with STSE, without MNF. T3: irrigation with STSE and addition of 171.6 kg N ha–1 year–1. T4: irrigation with STSE and addition of 343.2 kg N ha–1 year–1. T5: irrigation with STSE and addition of 520 kg N ha–1 year–1. Within a soil layer means marked by the same letter do not differ according to Tukey test at p < 0.05. Israel Journal of Plant Sciences 59

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Fig. 2. Effect of irrigation with different water qualities (potable water and secondary-treated sewage effluent, STSE) and rates of mineral-N fertilizer (MNF) application on total nitrogen (TN) contents in a tropical soil-pasture system. T1: irrigation with potable water and addition of MNF, 520 kg N ha–1 year–1. T2: irrigation with STSE, without MNF. T3: irrigation with STSE and addition of 171.6 kg N ha–1 year–1. T4: irrigation with STSE and addition of 343.2 kg N ha–1 year–1. T5: irrigation with STSE and addition of 520 kg N ha–1 year–1. Within a soil layer, means marked by the same letter do not differ according to Tukey test at p < 0.05.

Compared to the initial conditions, soil TC concentrations decreased along the soil profile during the experimental period (Table 1). On the other hand, the concentrations of soil TN decreased throughout the experimental period only in the 20–40 cm layer, showing small fluctuations in the other layers (Table 1). Although no variations were found between the treatments (Figs.  1, 2), the mean C/N ratio of the soil (ranging from 11.2 to 12.2) decreased over time for almost all layers. Results indicated that irrigation plus mineral N fertilization provided no soil input of organic wastes in sufficient quantity and quality to promote an increase in concentrations of SOM, although it promoted greater grass DM yield (as reported by da Fonseca et al., 2007c). In a study comparing different sources of irrigation water (potable water and TSE), Zekri and Koo (1994) found decreased soil TN over time after irrigation with both types of water. The mineralization of SOM is highly dependent on the soil water potential (Myers et al., 1982) associated with other factors such as temperature, O2, pH, and the amount and quality of the native organic material (Stanford and Smith, 1972). By promoting changes in microbial activity, particularly in pasture agro-systems, irrigation can affect nutrient cycling, causing higher SOM mineralization (Dubeux Jr. et al., 2004) and subordinately a reduction in soil TC and TN concentrations.

Moreover, the decreases over time in soil TC and TN (Table 1) may have been caused by: (i) priming effect due to MNF and effluent N inputs, causing mineralization of the native humus N, (ii) external inputs of N into the system (effluent-N and/or MNF), promoting better conditions for the growth and development of the shoot and root systems, followed by a higher N use efficiency (Stevenson, 1986). Barton et al. (2005) studied four New Zealand soils cultivated with perennial ryegrass and white clover over a two-year irrigation period with TSE. The authors found that (i) a priming effect occurred in two soils (one rich in alophane material and the other with sandy texture), and (ii) the amount of N recovered (N leached and N accumulation in grassland) exceeded the N input of 180 kg ha–1 (by means of fertilizer and effluent), indicating that mineralization of native soil N took place. From these data it is expected that the priming effect was also significant in this study, because the efficiency of conversion of applied N (MNF and effluent-N) was considerable higher (60–70 kg of DM per kg of N) than the average values presented in the review of Martha Júnior et al. (2004). The N conversion efficiency in tropical grasses (without irrigation) generally ranges from 15 to 45 kg of DM per kg of N, and may reach up to 83 kg of DM per kg of N (Martha Júnior et al., 2004). From this it follows that irrigation can increase N uptake da Fonseca et al. / Carbon and nitrogen dynamics

152 Table 1 Temporal evolution of total carbon (TC) and total nitrogen (TN) contents in a tropical soil-pasture system, following the application of different irrigation water qualities (potable water and secondary-treated sewage effluent, STSE) and rates of mineral nitrogen fertilizer (MNF). CV is coefficient of variation Soil attribute

Soil layer, cm



3

TC (CV = 8.4%) 0–10 TN (CV = 8.4%) TC (CV = 7.0%) 10–20 TN (CV = 7.0%) TC (CV = 10.9%) 20–40 TN (CV = 9.5%) TC (CV = 7.0%) 40–60 TN (CV = 11.4%) TC (CV = 8.7%) 60–80 TN (CV = 29.4%) TC (CV = 7.6%) 80–100 TN (CV = 14.4%)

7.23A 0.53B 6.60A 0.49AB 6.18A 0.47A 5.22A 0.39A 4.16A 0.29AB 3.41A 0.26BC

Time from the beginning of the experiment (months) 6

9

6.62B 0.55AB 5.88B 0.50AB 5.31B 0.46AB 4.45B 0.38A 3.63B 0.32A 2.88B 0.27AB

12

mg kg–1 6.32B 6.19B AB 0.57 0.54AB B 6.06 5.98B 0.53A 0.51AB 5.30B 5.41B 0.48A 0.47A B 4.44 4.36B 0.41A 0.40A 3.46BC 3.33C 0.32A 0.30AB A 2.89 2.85A 0.30A 0.30A

18

6.38B 0.56AB 5.28 C 0.48B 4.51C 0.41C 3.98C 0.32B 3.24C 0.29B 2.74A 0.23C

24 6.56B 0.59A 5.37C 0.48B 4.96BC 0.42BC 4.26BC 0.37A 3.33C 0.31AB 2.79A 0.24BC

Within a row, means followed by the same letters do not differ according to Tukey test at p < 0.05.

efficiency and utilization by the grass (Marcelino et al., 2003), but this fact is not enough to explain the effects occurring in the present study. In agro-systems irrigated with TSE, changes in the concentrations of TC and TN may vary along the soil profile. In pasture soils irrigated with TSE for 11 years, Sommers et al. (1979) found increased and decreased concentrations of TC in the 0–15 cm and 15–60 cm layers. In several cropped soils in Florida (USA), including bermudagrass pastures, Allhands et al. (1995) observed decreased and increased SOM concentrations in the 0–15 cm and 15–120 cm layers after eight years of irrigation. In TSE irrigated forest soils in New Zealand, Speir (2002) reported no changes in soil TC and TN concentrations in the 0–5 cm layer and increased total concentrations of these elements in the 5–15 cm soil layer. As mentioned above, results presented here of soil TC and TN (Table 1) disagree with the majority of published reports, possibly due to the following factors: a. The highly weathered local soils are different compared to the less weathered soils of regions also used for effluent disposal. In this study, the soil displays low natural fertility and low SOM contents (da Fonseca et al., 2007c); and receives large amounts of solar energy throughout the year. These factors, associated with appropriate conditions of soil moisture and aeration and proper irrigation management, foster rapid mineralization of SOM (Mielniczuk et al., 2003). Israel Journal of Plant Sciences 59

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b. The supply of organic C and organic N by TSE is mainly originated from dead algae, which have a rapid decomposition rate (Snow et al., 1999). In soils with low natural fertility, the input of nutrients (especially N and P) due to TSE irrigation, associated with low concentrations of effluent-C, may enhance mineralization and nitrification processes (Speir et al., 1999), which may cause a decrease of soil TC concentrations over the long term (Speir, 2002). c. Although STSE application induced a high N input to the soil–plant system, an increase in soil TN concentrations was not observed (Fig. 2, Table  1). This might be attributed to the high degree of N extraction by grass (data shown in da Fonseca et al., 2007c), which was also reported by Mancino and Pepper (1992) and Barton et al. (2005). d. In several long-term studies the increase in concentrations of TC and/or TN after TSE irrigation was associated with increasing heavy metals concentrations in the soil (Quin and Woods (1978), Madyiwa et al. (2002), and Ramirez-Fuentes (2002)). The accumulation of heavy metals in the soil can alter the enzymatic activities of the microorganisms, modifying C, N, P, and S cycling (Kandeler et al., 1996) and causing increased concentrations of TC in the soil (Valsecchi et al., 1995), but not necessarily in humified C (Stevenson, 1986). At high concentrations, heavy metals may affect growth, morphology, and metabolism of microganisms working on SOM mineralization, causing functional disorders, dena-

153 turation of proteins, and destruction of the integrity of cell membranes (Leita et al., 1995). Because the TSE used in the present study showed low heavy metal contents (da Fonseca et al., 2007c), all conditions favored an increased degradation of soil-C and effluent-C. Mineral nitrogen in soil solution The applied treatments caused alterations in (i) NO3–N concentrations in the 0–10 cm and 60–80 cm layers (Fig.  3), and (ii) NH4+-N concentrations in the 0–10 cm and 40–60 cm layers (Fig. 4). In the 0–10 cm layer, lower concentrations of NO3–-N were found for T1 and T2 compared to treatments T4 and T5, which presented higher concentrations (Fig. 3). In the 60–80 cm layer, the NO3–-N concentrations were lower at T2 and T3 and higher at T1 and T5; while treatment T4 was not different from any of the others (Fig. 3). In general, higher NO3–N concentrations were found for treatments receiving higher rates of MNF plus TSE irrigation (Fig.  3). The fact that the TSE irrigation promotes increased NO3–-N concentrations in soil solution has widely been reported for agricultural systems (Feigin et al., 1978), grasslands

(Quin and Forsythe, 1978), and forests (Speir et al., 1999). However, the increases in NO3–-N concentrations observed in this study were not of major concern, because subsurface NO3–-N concentrations were always below 10 mg L–1 (maximum concentration tolerated for potable water, according to Stevenson, 1986). Quin and Forsythe (1978) found similar results in a study on perennial ryegrass irrigated annually with 840 mm of TSE (containing 13.8–41.0 mg total-N L–1). In the 0–10 cm layer, higher NH4+-N concentrations were measured for T2 compared to T1, T4, and T5, while for T3 NH4+-N concentrations were not different from the other treatments (Fig. 4). In the 40–60 cm layer, treatment T2 showed higher NH4+-N concentration than treatment T5, but these treatments were not different from the others (Fig. 4). Lower NH4+-N concentrations were generally obtained for treatments receiving higher rates of irrigation and/or MNF, indicating no positive relationship between levels of MNF or effluent-N and NH4+-N concentrations in soil solution. This may be attributed to: (i) uptake of NH4+-N by the plants, (ii) retention of NH4+-N to the negatively charged surfaces of clay minerals and soil organic matter, (iii) use of

Fig. 3. Effect of irrigation with different water qualities (potable water and secondary-treated sewage effluent, STSE) and rates of mineral-N fertilizer (MNF) application on nitrate (NO3–-N) concentration in a tropical soil-pasture system. T1: irrigation with potable water and addition of MNF, 520 kg N ha–1 year–1. T2: irrigation with STSE, without MNF. T3: irrigation with STSE and addition of 171.6 kg N ha–1 year–1. T4: irrigation with STSE and addition of 343.2 kg N ha–1 year–1. T5: irrigation with STSE and addition of 520 kg N ha–1 year–1. Within each soil layer, means marked by the same letter do not differ according to Tukey test at p < 0.05. da Fonseca et al. / Carbon and nitrogen dynamics

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Fig. 4. Effect of irrigation with different water qualities (potable water and secondary-treated sewage effluent, STSE) and rates of mineral-N fertilizer (MNF) application on ammonium (NH4+-N) concentration in a tropical soil-pasture system. T1: irrigation with potable water and addition of MNF, 520 kg N ha–1 year–1. T2: irrigation with STSE, without MNF. T3: irrigation with STSE and addition of 171.6 kg N ha–1 year–1. T4: irrigation with STSE and addition of 343.2 kg N ha–1 year–1. T5: irrigation with STSE and addition of 520 kg N ha–1 year–1. Within a soil layer, means marked by the same letter do not differ according to Tukey test at p < 0.05. Table 2 Temporal evolution of nitrate (NO3–-N) and as ammonium (NH4+-N) concentration in the soil solution in a tropical soil-pasture system, following the application of different irrigation water qualities (potable water and secondary-treated sewage effluent, STSE) and rates of mineral nitrogen fertilizer (MNF). CV is coefficient of variation Soil solution attribute

Layer, cm



3

NO3–-N (CV = 32.8%) 0–10 NH4+-N (CV = 25.5%) NO3–-N (CV = 36.0%) 10–20 NH4+-N (CV = 27.6%) NO3–-N (CV = 87.4%) 20–40 NH4+-N (CV = 27.9%) NO3–-N (CV = 90.1%) 40–60 NH4+-N (CV = 25.2%) NO3–-N (CV = 82.8%) 60–80 NH4+-N (CV = 24.1%) NO3–-N (CV = 85.7%) 80–100 NH4+-N (CV = 27.6%)

Time from the beginning of the experiment (months) 6

9

mg L

12

18

24

5.86B 1.84BC 4.07CD 1.18D 1.90B 1.30C 0.68BC 1.28CD 0.42C 1.31BC 0.36C 1.17AB

1.84D 1.36C 8.50A 1.47CD 4.44A 1.92B 4.66A 1.82B 4.27A 1.68A 3.08A 1.22A

4.56BC 1.72C 8.18A 1.29D 4.64A 1.37C 1.62BC 1.08D 2.76B 1.01D 1.93B 0.81C

–1

5.73B 2.24B 5.47BC 2.33B 4.45A 2.01AB 2.05B 1.44CD 1.21C 1.04CD 0.82C 0.93BC

9.78A 3.78A 7.19AB 3.11A 1.30B 2.50A 0.94BC 1.58BC 0.59C 0.92D 0.48C 0.95BC

3.69C 1.63C 2.35D 1.87BC 1.16B 2.49A 0.53C 2.47A 0.37C 1.41B 0.26C 1.08AB

Within the row, means followed by the same letters do not differ according to Tukey test at p < 0.05.

NH4+-N for soil microbiota growth, once NH4+-N is the preferred N form of microbial N immobilization, (iv) fixing NH4+-N in clay interlayer spaces, (v) use of NH4+N to form complex quinone-NH2, which is an important reaction of the stabilization of SOM, (vi) volatilization of NH4+-N as ammonia NH3, and (vii) use of NH4+-N as Israel Journal of Plant Sciences 59

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an energy source for bacteria during the quimioautotrophic process of nitrification (Paul and Clark, 1989). The effects of applied treatments on the concentrations of mineral N in soil solution were equivalent to those reported for NO3–-N concentrations due to the predominance of the latter in the soil solution. The

155 predominance of NO3–-N in soil solution is a common fact in oxidizing environments without limitations in terms of temperature, moisture, aeration, and substrate NH4+ (Stevenson, 1986; da Fonseca et al., 2007b; Quin and Forsythe, 1978). NO3–-N and NH4+-N in soil solution changed over the experimental period in all layers (Table 2). However, average mineral N concentrations obtained at the last sampling period (24 months) were similar to those of the first sampling (3 months) throughout the soil profile (Table 2). These changes may be related to periods of higher or lower demands of N by plants (da Fonseca et al., 2007c). The grass governed mineral N concentrations in the soil-solution system. Through cutting and export of DM and nutrients, the soil–plant system maintained its capacity of polishing (equivalent to tertiary treatment) applied STSE. These findings agree with Barton et al. (2005) and da Fonseca et al. (2007a), who indicated that (i) plants are the main factor governing N losses and leaching of nutrients from the soil–plant system irrigated with TSE, (ii) the rate of effluent application has to be related to the variable plant water requirement (considering seasonal differences in crop production and water demand), (iii) losses of effluent-N by volatilization, denitrification, as well as the increased storage of N in soil are variable and difficult to predict and measure in the short term, and (iv) the N requirements of plants, especially of tropical grasses, are “known” and easier to monitor. When compared to fresh water irrigation, STSE caused (i) no changes in soil TC and TN concentrations; (ii) slightly higher mineral N concentrations in the soil solution, but without environmental risk. Mineral N concentrations were directly influenced by the high N uptake capacity of ‘Tifton 85’ bermudagrass. ACKNOWLEDGMENTS The authors are grateful to the financial support of the “Fundação de Amparo à Pesquisa do Estado de São Paulo” (FAPESP), the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), and to the logistic support of the Sabesp. The authors also thank Prof. Klaus Reichardt of the University of São Paulo for his kind assistance with language review. Finally, we thank the anonymous reviewers for their helpful comments to the paper. REFERENCES Agunwamba, J.C. 2001. Analysis of socioeconomic and environmental impacts of waste stabilization pond and unrestricted wastewater irrigation: interface with maintenance. Environ. Manage. 27: 463–476.

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