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Published online 13 September 2006
Published in J Environ Qual 35:1939-1947 (2006)
DOI: 10.2134/jeq2005.0482
© 2006 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
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TECHNICAL REPORTS

Waste Management

Response of Spinach and Komatsuna to Biogas Effluent Made from Source-Separated Kitchen Garbage

Yuichiro Furukawaa and Hiroshi Hasegawab,*

a International Rice Research Institute, Crop, Soil, and Water Science Division, DAPO Box 7777, Metro Manila, Philippines
b Research Team for Biomass Utilization, Tohoku National Agricultural Research Center, Aza Harajuku-Minami 50, Arai, Fukushima-shi, Fukushima 960-2156 Japan

* Corresponding author (hasegawa{at}affrc.go.jp)

Received for publication December 25, 2005.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Recycling of kitchen garbage is an urgent task for reducing public spending and environmental burdens by incineration and/or landfill. There is an interesting regional effort in Ogawa, Saitama prefecture, Japan, in which source-separated kitchen garbage is anaerobically fermented with a biogas plant and the resultant effluent is used as a quick-release organic fertilizer by surrounding farmers. However, scientific assessments of fertilizer values and risks in the use of the effluent were lacking. Thus, a field experiment was conducted from 2003 to 2004 in Tohoku National Agricultural Research Center to grow spinach (Spinacia oleracea L.) and komatsuna (Brassica rapa var. perviridis L. H. Bailey) for evaluating the fertilizer value of the kitchen garbage effluent (KGE), nitrate, coliform group (CG), Escherichia coli, fecal streptococci (FS), and Vibrio parahaemolyticus concentrations of KGE and in the soil and the plant leaves. A cattle manure effluent (CME) and chemical fertilizers (NPK) were used as controls. Total nitrogen (N) and ammonium N concentrations of the KGE were 1.47 and 1.46 g kg–1, respectively. The bacteria tested were detected in both biogas effluents in the order of 2 to 3 log CFU g–1, but there was little evidence that the biogas effluents increased these bacteria in the soil and the plant leaves. At the rate of 22 g N m–2, yield, total N uptake, apparent N recovery rate, and leaf nitrate ion concentration at harvest of spinach and komatsuna in the KGE plot were mostly comparable to those in the NPK and CME plots. We conclude that the KGE is a quick-release N fertilizer comparable to chemical fertilizers and does not cause contamination of CG, E. coli, FS, or V. parahaemolyticus in the soil and spinach and komatsuna leaves.

Abbreviations: CFU, colony forming unit • CG, coliform group • CME, cattle manure effluent • DAS, days after seeding • FS, fecal streptococci • KGE, kitchen garbage effluent


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
APPROXIMATELY 22 Tg yr–1 of kitchen garbage is incinerated and/or landfilled in Japan (Ministry of the Environment, 2005). The incineration of kitchen garbage needs large amounts of heavy oil and generates environmentally important gases and chemical waste residuals, such as NOx and dioxins. Further, landfill space is very scarce in Japan (Dijkgraaf and Vollebergh, 2004). It is urgent to establish an alternative measure to recycle kitchen garbage.

A biogas plant can generate methane as an energy resource through anaerobic fermentation from organic wastes, including kitchen garbage (Tafdrup, 1994), but the liquid phase (effluent) of biogas plant made from kitchen garbage is hardly utilized in Japan. There is a regional effort by a nonprofit organization (FOODO), however, to realize a better recycling system for kitchen garbage in Ogawa, Saitama prefecture, Japan. One of the biogas plants in Ogawa has been fermenting only kitchen garbage collected twice a week from 100 households since 2001. Up to 100 kg d–1 of kitchen garbage, completely separated from other household wastes by each household, is transported to the biogas plant by the Ogawa municipality. The local farmers report that the kitchen garbage effluent (KGE) is beneficial as a quick-release fertilizer for organic vegetable cultivation. The KGE is fully used by the farmers, and the produce grown with the KGE is consumed locally. However, there are no independent and scientific evaluations of fertilizer values or risks of KGE in agricultural use.

The KGE is basic, rich in N and K, but low in other nutrients (Table 1). There are only a few studies that evaluate the fertilizer value (primarily N and K) of KGE. Båth and Rämert (2000) found that KGE was a better N source for leek (Allium porrum L.) than plant compost or chicken manure, but no chemical fertilizer plot was included. Svensson et al. (2004) reported that KGE is not a comparable N source to chemical fertilizers for oat (Avena sativa L.) and barley (Hordeum vulgare L.) crops. Further, there is little research that investigated risks involved in the use of KGE in field conditions, such as fates of pathogenic and sanitary indicator bacteria and nitrate N concentrations in soils or plants.


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  		Table 1. Chemical properties (mean and SD) of the kitchen garbage and cattle manure effluents.

 
By contrast, more research has been conducted with livestock effluents of biogas plants. A mixed pasture of timothy (Phleum pratense L.) and legumes, sugar beet (Beta vulgaris L. subsp. vulgaris), potato (Solanum tuberosum L.), and wheat (Triticum aestivum L.) were grown with CME in combination with phosphorus fertilizers (Civil Engineering Research Institute of Hokkaido, 2003). The herbage yield of the mixed pasture and the yields of sugar beet, potato, and wheat grown with CME were similar to those grown with chemical fertilizers. The biogas effluents of swine were found as good nutrient sources as chemical fertilizes to water spinach (Ipomoea aquatica Forssk.; Lam et al., 2002), and to cucumber (Cucumis sativus L.) and tomato (Lycopersicon esculentum Mill.) in a pig-biogas-vegetable greenhouse system (Qi et al., 2005). Li et al. (2003) concluded that CME can replace N top dressing of chemical fertilizer to paddy rice.

Pathogenic and sanitary indicator bacteria such as E.coli and Salmonella spp. were studied only during the anaerobic fermentation in biogas plants (Civil Engineering Research Institute of Hokkaido, 2003; Lam et al., 2002), and little research in field conditions was found.

The objectives of this study were to evaluate the risks of contaminations of pathogenic bacteria (Vibrio parahaemolyticus) and three kinds of sanitary indicator bacteria coliform group (CG), E. coli, fecal streptococci (FS), and nitrate in the plant leaves and the soils after spinach and komatsuna were grown with the KGE, and to determine the N fertilizer value for spinach and komatsuna. In addition, heavy metal concentrations of the KGE were compared to legal regulations. The CME and chemical fertilizer plots were used as controls.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Biogas Effluents
A biogas effluent made from source-separated kitchen garbage was collected from a biogas plant in Ogawa, Saitama prefecture, Japan. After grinding the kitchen garbage, a bioreactor (6 m3) of the plant continuously fermented the kitchen garbage up to 100 kg d–1 under mesophilic conditions (35°C) for 50 d. A biogas effluent primarily made from cattle manure was used as a control biogas effluent. The CME was transported from a biogas plant in Yagi, Kyoto prefecture, Japan. A bioreactor (600 m3) of the plant continuously fermented the cattle manure up to 20 Mg d–1 under thermophilic conditions (55°C) for 25 d. The KGE and CME were collected in plastic vessels (20 L) and transported at room temperature to Tohoku National Agricultural Research Center where a field experiment was conducted. The biogas effluents were stored for up to 1 mo in the vessels at room temperature.

Field Experiment
A field experiment was conducted during 2003 to 2004 at the Department of Upland Farming, Tohoku National Agricultural Research Center, Fukushima, Japan (37°43' N, 140°23' E; elevation 176 m). The soil is classified as Typic Hapludands. The climate is humid mesothermal with hot summer (daily maximum air temperature up to 35°C) and winter snow (up to 0.2 m). Average annual precipitation and air temperatures are 1354 mm and 11.6°C, respectively. Unfertilized sorghum [Sorghum bicolor (L.) Moench] as a cleaning crop was grown before the experiment. The sorghum including root was removed. No compost other than the treatments was applied to the field through the experiment. The pH, total C, total N, NH4–N, NO3–N, Truog (available) P of the soil (0 to 0.15 m) were 6.7, 13.5 g kg–1, 1.6 g kg–1, 5.84 mg kg–1, 1.60 mg kg–1, 20.2 mg kg–1, and 1 M ammonium (NH4) acetate extractable (exchangeable) K, Ca, and Mg were 0.39, 2.34, and 0.55 g kg–1, respectively. These results indicated the soil was medium to high in exchangeable K, Ca, and Mg, but very low in available P.

Spinach (cv. Sanpia) and komatsuna (cv. Yokattana) plants were grown with the KGE and CME in the 2003 autumn and 2004 spring seasons. The KGE was applied at rates of 14, 28, and 40 g N m–2, with a 5-L watering pot. The standard rate is 20 to 25 g N m–2 in this area. Nitrogen rates of the KGE and CME treatments were increased by 21% compared to the NPK treatment, taking into account the uncertainty in ammonia volatilization loss from biogas effluents (Ruboek et al., 1996). This may be a good estimate, given that the actual amount of volatilization could vary depending on materials and environmental conditions. Individual treatments were termed as KGE-L, KGE-M, and KGE-H, respectively. The CME was applied at the rate of 28 g N m–2. Because of low P content in both the soil and the biogas effluents, calcium superphosphate was supplemented so that the P rate was 10 g m–2 in all the treatments. Potassium additions were 8, 16, 23, and 16 g K m–2, respectively, in KGE-L, KGE-M, KGE-H, and CME treatments. Potassium chloride was supplemented to the KGE and CME plots to equalize the K rate. One-half of the biogas effluents were applied a few days before seeding as basal fertilizers and the remainder just after thinning as top dressing in KGE-L, KGE-M, and CME treatments, but in the KGE-H plot two-thirds of the KGE was applied as the basal fertilizer and the other one-third as top dressing. Spinach and komatsuna plants were also grown with N, P, and K fertilizers (NPK treatment) at the rates of 22 g N m–2, 10 g P m–2, and 16 g K m–2, and with PK fertilizer (N0 treatment) at the rate of 10 g P m–2 and 16 g K m–2. Urea was used for a basal fertilizer and ammonium nitrate for top dressing in the NPK plot. These fertilizers were used because they are common N sources. Calcium superphosphate and potassium chloride were used as P and K sources. One-half of the N, P, and K fertilizers were applied a few days before seeding as basal fertilizers and the remainder as top dressing just after thinning. The soil was plowed a few days after the basal biogas effluents and chemical fertilizers were manually broadcast on the soil. The top dressing was side-dressed in furrows (0.03 to 0.04 m depth) between rows. The furrows were not covered with the soil after the top dressing. Further, the application of biogas effluents came with water. In the KGE-H treatment where most biogas effluent was applied, 27 mm of biogas effluent was applied. To equate water supply in all the treatments, additional water was furnished to the KGE-L, KGE-M, CME, NPK, and N0 treatments immediately after the fertilizations of the biogas effluents and chemical fertilizers. Plots were laid out in randomized complete blocks in a split-plot design with fertilization as main plot and spinach and komatsuna as subplots, and replicated 4 times. The plot size for each treatment was 3.6 m2 (1.2 by 3.0 m).

Spinach and komatsuna in seed tape were seeded a few days after the basal fertilization at the density of 250 m–2 with row distance 0.2 m and the plant density was reduced up to one-fourth at thinning. Alachlor (2-chloro-2',6'-diethyl-N-(methoxymethyl) acetanilide) was sprayed immediately after seeding, but no other pesticides were applied. In the 2003 autumn season, komatsuna and spinach were seeded on 6 October. Komatsuna was thinned 36 d after seeding (DAS), and harvested 65 DAS. Spinach growth was somewhat slower than komatsuna and thinned 43 DAS, and due to snow cover from late December 2003 through late February 2004, spinach plants were harvested 149 DAS (3 Mar. 2004). In the 2004 spring season, komatsuna was seeded on 5 April, thinned 31 DAS, and harvested 49 DAS. Spinach was seeded on 5 April, thinned 31 DAS, and harvested 50 DAS. Plant samples for measurements were collected from 0.8 m–2 of each plot at thinning for early growth and at harvest for fresh yield. Five subsamples from each plot were weighed wet and dried at 70°C for 2 to 3 d for total N analysis. Four plants for microbiological counting and two plants for nitrate ion (NO3–) analysis from each plot were subsampled, respectively. Soil samples for laboratory analyses were taken from 0- to 0.15-m depths using a soil probe (25-mm i.d.). Nine soil cores from each block before the field experiment and five soil cores from top-dressed plots were collected after each harvest and were composited in a sterilized plastic bag. For the NPK, KGE-M, and CME plots, microbial analyses were conducted immediately after the sampling and the remaining soil samples were kept refrigerated until chemical analyses. For the N0, KGE-L, and KGE-H plots, only chemical analyses were conducted.

Chemical Analyses and Apparent Nitrogen Recovery Rate
Biogas effluents were subsampled from 20-L plastic vessels and kept frozen until analyses. The pH and electric conductivity (EC) of the biogas effluents were directly measured by a glass electrode method (Japanese Standards Association, 1999) with a pH meter (MP 220, Mettler Toledo) and an EC meter (Ds-8F, Horiba). Total N and C were determined by the Dumas method (Bremner, 1996) with a CN analyzer (vario MAX CN, Elementar Analysensystem GmbH). Ammonium N and NO3–N were quantified by a colorimetric method with an Autoanalyzer II (Technicon Industrial Systems, 1976). Total concentrations of P, K, Ca, Mg, Na, Fe, Mn, As, Cd, Co, Cr, Cu, Mo, Ni, Pb, Se, and Zn were determined by a wet digestion method in a closed Teflon vessel (120 mL, Savillex, MN). Aliquots of biogas effluents (equivalent to 0.5 g dry matter) were dried at 70°C for 4 d to determine total solid concentrations. After 5 mL of HNO3 was added, the vessel was irradiated in a microwave oven (400W for 30 to 120 s), then cooled in an ice water bath. This step was repeated 10 times. After addition of 0.5 mL of HClO4, the irradiation-cooling procedure was repeated 10 times, followed by addition of 0.5 mL of HF and 10 repetitions of the irradiation-cooling procedure. After the digest became clear, water was added. Except for As, Se, and Hg, total elemental concentrations in the digest were analyzed by an inductively coupled plasma optical emission spectroscopy method (Japanese Standards Association, 1999) using a Vista-MPX (Varian). Total As and Se concentrations in the digest were quantified by a hydride generation atomic absorption spectrometric method (Japanese Standards Association, 1999) with a SpectrAA-220 (Varian). Total Hg concentration in the biogas effluent was determined by a cold vapor-atomic absorption spectrometric method (Japanese Standards Association, 1999) with a Mercury RA-2A20 (Nippon Instruments).

A bulk sample of wet soil was sieved through a 2-mm mesh screen. A subsample was weighed wet and dried for 24 h at 105°C to determine moisture content. Ammonium N and NO3–N in the soil were extracted with 2 M KCl in a 1:10 soil/KCl ratio and analyzed with the same method above.

Even-numbered alternate leaves along the stem of the plants and the same weight of 2 M HCl were incubated at 20°C for 15 h, and the NO3– concentrations in the HCl solution were measured using an HPLC equipped with a UV detector (SCL-10Asp, Shimadzu). Total N concentrations in spinach and komatsuna were determined with the same method as used for the effluents. Apparent N recovery rate was obtained as the difference of plant N uptake between fertilized plots and the N0 plot. In the 2004 spring season some blocks were weedy with common chickweed [Stellaria media (L.) Vill.] although herbicide had been applied. Weed N uptake was included in apparent N recovery rates.

Microbiological Enumeration
We determined the concentration of V. parahaemolyticus, one of most frequently occurring pathogens in food poisoning of Japan, and the concentrations of sanitary indicator bacteria FS (Sahlström, 2003), CG bacteria, and E. coli. These bacteria were chosen partly because they can be detected with rapid and easy methods. After the plant leaves were rinsed with sterilized water, the concentration of CG bacteria, E. coli, FS, and V. parahaemolyticus in the effluents, irrigation water, seeds, soil, and plant leaves were enumerated by dilution plate counting techniques (Zuberer, 1994). The samples of the biogas effluents were taken four times at the basal application and top dressing, and those of irrigation water 2 times at the basal fertilizer application. The leaf samples were collected at harvest, and seed samples before seeding. Soil was sampled before basal fertilization and after each harvest. X-Gal agar (Nissui Pharmaceutical) was used for CG bacteria and E. coli, Chromocult enterococci agar (Merck) for FS, and TCBS agar (Merck) for V. parahaemolyticus. Each agar plate was incubated for 20 to 48 h at 36°C. The detection limit was 1.3 log CFU g–1 dry matter in the soil and seeds, 1.3 log CFU g–1 fresh matter in plant leaves, and 0.6 log CFU g–1 fresh matter in the effluents and irrigation water.

Data Analysis
Statistical analysis was performed with SAS/STAT (1988). Heavy metal concentrations between the KGE and CME were compared with PROC TTEST. The second power regression was conducted with PROC REG for determining the dose response curve of spinach and komatsuna to the KGE (y = a+bx+cx2, where y was an independent variable of interest, x was the rate of the KGE applied, and a, b, and c were coefficients). The difference between NPK and KGE treatments at the rate of 22 g N m–2 was based on credible intervals at the 0.95 probability (P) levels of the regression curves (Sawa, 1979). The difference between the KGE-M and CME plots were tested with CONTRAST statements after analysis of variance was performed with PROC GLM as Y = µ + S + T + e, where Y was an independent variable of interest, µ was the grand average, S was season effect, T was treatment effect, and e was error.

Temperature is among the environmental factors greatly affecting the growth of spinach and komatsuna. Soil temperature affects the growth of spinach and komatsuna more than air temperature (Hamasaki and Okada, 2003). Thus, the soil temperature of the topsoil was simulated from the air temperature obtained from the on-site weather station using the soil temperature submodel of Decision Support Systems for Agrotechnology Transfer, version 3.0 (DSSAT; Jones et al., 1998). The prediction of the soil temperature submodel was found reasonably accurate (Hasegawa et al., 1999).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Chemical Properties of Biogas Effluents
Table 1 indicates pH, EC, and concentrations of total solid, total C, and major and minor elements in the KGE and CME. Standard deviations present the variations among the sampling dates of the KGE and CME. The biogas effluents were basic and their pH values were about 8. The total solid and total C concentrations of the CME were 6 times higher than those of the KGE and highly variable among the sampling dates. Ammonium N accounted for more than 99% of total N in the KGE, whereas more than 20% of the N was in organic form in the CME. The K concentration was comparable to the total N concentration in the KGE, but in the CME the K concentration was higher than the total N concentration. Phosphorus concentrations of the KGE and CME were much lower than total N concentrations. The concentrations of Na, Ca, Mg, and Fe ranged from 75 to 962 mg kg–1 except for Fe (4 mg kg–1) in the KGE. Table 2 presents the concentrations of several metals in the KGE and CME. The concentrations of Co, Cu, Ni, Pb, and Zn were lower in the KGE than in the CME (P < 0.05–0.001) and those of As, Cd, Cr, Mo, and Se did not differ between the KGE and CME. Only the Hg concentration was higher in the KGE than in CME (P < 0.01). In addition to the Japanese legal standard for heavy metal concentrations of composts and other organic sources (MAFF, 2005), the heavy metal concentrations of KGE and CME were compared to the Canadian legal standard (Standards Council of Canada, 2005) because the latter covers more kinds of heavy metals than the Japanese heavy metals and because both standards are based on total elemental digestion and analysis. Although there is no legal standard for biogas effluents in Japan and Canada, comparisons on a dry matter basis should be reasonable. All the heavy metal concentrations in the KGE and CME cleared both Japanese and Canadian legal standards.


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  		Table 2. Metal concentrations (mean and SD) in the kitchen garbage and cattle manure effluents.

 
Pathogenic and Sanitary Indicator Bacteria
Table 3 presents CG bacteria, E. coli, FS, and V. parahaemolyticus in the materials used. They were detected in both effluents in the order of 2 to 3 log CFU g–1. The E. coli and FS in the CME were about 10 times higher than those in the KGE. At the beginning of the experiment CG bacteria and V. parahaemolyticus were detected in the soil in the order of 3 and 1 log CFU g–1, respectively, but no E. coli or FS were observed. CG bacteria were also found in the seed tape. The SD values of bacteria were often as high as mean values and seemed more variable than those in Table 5 of Larsen et al. (1994), but the reason was unclear.


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  		Table 3. The concentrations (mean and SD) of coliform group bacteria, Escherichia coli, fecal streptococci, and Vibrio parahaemolyticus in materials used in this study.

 

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  		Table 5. The concentration (log CFU g–1 fresh matter) of coliform group bacteria in harvested plant leaves.{dagger}

 
Table 4 reveals the concentrations of CG bacteria, E. coli, FS, and V. parahaemolyticus in the soil after spinach and komatsuna harvest. The season effect was significant (P < 0.05) but the treatment effect was insignificant in CG bacteria, suggesting the applications of the KGE and CME did not increase CG bacteria in the soil relative to the NPK treatment. The CG bacteria concentrations after harvest ranged from 3.3 to 4.2 log CFU g–1 in the spinach soil and from 2.7 to 4.4 log CFU g–1 in the komatsuna soil and were also comparable to the CG bacteria concentration (3.8 log CFU g–1) at the beginning of the experiment (Table 3). E. coli, FS, and V. parahaemolyticus were not detected after komatsuna except for V. parahaemolyticus in the KGE-M treatment in the 2004 spring season. E. coli in the spinach soil was detected in the order of 1 log CFU g–1 in both autumn and spring seasons of the KGE-M treatment, and V. parahaemolyticus in the order of 3 and 1 log CFU g–1 only in spring in the KGE-M and CME treatments, respectively (Table 4). To determine if E. coli and V. parahaemolyticus in the spinach soil were persistent, their concentrations were enumerated 1 mo after spinach harvest in the 2004 spring season. No E. coli were detected in the soil of KGE-M treatment. The concentration of V. parahaemolyticus in the soil of the NPK and KGE-M plots were 2.1 and 1.1 log CFU g–1, and was similar to that at the beginning of the experiment (1.3 log CFU g–1; Table 3). We conclude E. coli and V. parahaemolyticus did not increase due to the application of the KGE and CME after two continuous crops.


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  		Table 4. The concentrations of coliform group bacteria, Escherichia coli, fecal streptococci, and Vibrio parahaemolyticus in the soil (0 to 0.15 m) after harvest.

 
The E. coli, FS, and V. parahaemolyticus were not detected in any harvested leaf. Table 5 presents the concentration of CG bacteria in harvested leaves. The CG bacteria were detected in all samples but no significant differences were observed among treatments. However, the concentration of CG bacteria in komatsuna leaves was significantly higher in spring than in autumn. In the spring season, komatsuna leaf surfaces were partially damaged by some insects such as striped flea beetle [Phyllotreta striolata (Fabricius)] and vegetable weevil (Listroderes costirostris Schoenherrand). This could account for the higher CG bacteria concentration in spring.

Early Nitrogen Uptake
The early N uptake determined at thinning was 2 to 6 times greater in the autumn-seeded spinach and komatsuna than in the spring-seeded ones (Fig. 1). The average simulated soil temperature of the topsoil was 17.0°C and 16.1°C in the autumn-seeded komatsuna and spinach, respectively, and was 16.1°C and 16.1°C in the spring-seeded ones, respectively. Hamasaki and Okada (2003) showed that higher soil temperature promoted komatsuna growth more at an earlier growth stage than at a later growth stage. In the autumn season the soil temperature gradually decreased, but the soil temperature gradually increased in the spring season. Given the similar average soil temperature, the temperature at early growth stages was higher in the autumn-seeded komatsuna and spinach than in the spring-seeded ones. The difference in soil temperature in the early growth stages could have caused the difference in the early N uptake. Nonetheless, the early N uptake tended to increase as the KGE rates were increased, except that the early N uptake of the autumn-seeded spinach did not increase from the KGE-M to KGE-H treatments. When the KGE treatment at the rate of 10 g N m–2 was compared with the NPK treatment, no differences were found both in the autumn-seeded and spring-seeded komatsuna and spinach. The early N uptake was 19% higher in the KGE-M plot than in the CME plot in the autumn-seeded spinach (P < 0.05), but no significant difference was observed in the spring-seeded spinach and in the autumn- and spring-seeded komatsuna (Fig. 1).


Figure 1
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  		Fig. 1. Effects of the kitchen garbage effluent (KGE), cattle manure effluent (CME), and chemical fertilizers (NPK) on the early N uptake of spinach and komatsuna in the autumn and spring seasons. The vertical bar indicates the 95% confidence interval. ** indicates that the KGE-M plot was significantly different from the CME plot at P < 0.01.

 
Fresh Yield, Nitrogen Uptake, and Apparent Nitrogen Recovery Rate
Unlike the early N uptake, fresh yield and N uptake at harvest were two- to four-fold greater in the spring-seeded spinach and komatsuna than in the autumn-seeded ones (Fig. 2). The average simulated soil temperature between thinning to harvest was 10.7 and 6.4°C in the autumn-seeded komatsuna and spinach, respectively, and was 18.0 and 17.9°C in the spring-seeded komatsuna and spinach, respectively. Thus, the differences in fresh yield and N uptake between the seasons could be attributed to favorable soil temperature in spring for spinach and komatsuna growth (Hamasaki and Okada, 2003). In the autumn season, spinach growth was prolonged relative to komatsuna, and snow cover delayed spinach harvest until 3 Mar. 2004. The minimum soil temperature for komatsuna growth is 4 to 5°C, whereas that for spinach is 9 to 10°C (M. Okada, Tohoku National Agricultural Research Center, personal communication, 2005). The requirement of higher soil temperature for spinach than that for komatsuna contributed to the initial harvest delay.


Figure 2
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  		Fig. 2. Effects of the kitchen garbage effluent (KGE), cattle manure effluent (CME), and chemical fertilizers (NPK) on the fresh yield, N uptake, and apparent N recovery rate at harvest of spinach and komatsuna in the autumn and spring seasons. The vertical bar indicates the 95% confidence interval. * and ** indicate that the KGE-M plot was significantly different from the CME plot at P < 0.05 and 0.01, respectively.

 
Nonetheless, the fresh yield of spinach and komatsuna tended to increase by 51 to 114%, as the KGE rates were increased, except that the fresh yield of the autumn-seeded komatsuna increased only by 25%. The fresh yield was 25 to 71% higher in the KGE-M plot than in the CME plot in the autumn-seeded spinach and the autumn- and spring-seeded komatsuna (P < 0.05), but no significant difference was observed in the spring-seeded spinach. At the rate of 22 g N m–2, the fresh yield between the KGE and NPK treatments was similar in the autumn- and spring-seeded spinach and komatsuna (Fig. 2 top).

The N uptake showed similar trends to the fresh yield. The only exception was the fact that the degree of increase from the KGE-M to KGE-H plots in autumn-seeded spinach and spring-seeded komatsuna was small in N uptake (Fig. 2 middle). The apparent N recovery rate decreased as the KGE rates increased in all the cases. The apparent N recovery rate in the autumn-seeded spinach was 38% lower in the CME plot than in the KGE-M plot (P < 0.01), but no difference was observed in the spring-seeded spinach. The apparent N recovery rates in the autumn- and spring-seeded komatsuna were 21 to 30% lower in the CME plot than in the KGE-M plot (P < 0.05). At the rate of 22 g N m–2 the apparent N recovery rate between the KGE and NPK treatments did not differ, and 0.4 to 0.6 of applied N was recovered (Fig. 2 bottom).

Nitrate Concentrations in the Soil and Plant Leaves
Nitrate-N concentrations in soils after harvest were significantly lower in the autumn-seeded spinach than in the spring-seeded case. The residual soil NO3–N was likely to leach after snow melt, because the harvest of the autumn-seeded spinach was delayed until March. By contrast, the residual soil NO3–N concentrations in komatsuna were higher in the autumn season than in the spring season except for the NPK and KGE-L treatments. Residual soil NO3–N concentrations increased from the KGE-L to KGE-M treatments, but increased little from the KGE-M to KGE-H treatments in all the cases except for the autumn-seeded spinach. With the autumn-seeded spinach, residual soil NO3–N concentrations increased only a little, probably due to the leaching as mentioned above. Residual soil NO3–N concentrations were not significantly different between the KGE-M and CME plots except for the spring-seeded spinach (P < 0.05). At the rate of 22 g N m–2 residual soil NO3–N concentrations in the KGE treatment were not significantly different from those in the NPK treatment (Fig. 3).


Figure 3
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  		Fig. 3. Effects of the kitchen garbage effluent (KGE), cattle manure effluent (CME), and chemical fertilizers (NPK) on the residual soil NO3–N after harvest of spinach and komatsuna in the autumn and spring seasons. The vertical bar indicates the 95% confidence interval. * indicates that the KGE-M plot was significantly different from the CME plot at P < 0.05.

 
Nitrate concentrations in the leaves were much lower in the autumn-seeded spinach and komatsuna than in the spring-seeded ones, probably reflecting the longer growth period in the autumn season. Nitrate concentrations of spinach and komatsuna leaves increased as the KGE rates increased in both seasons. Leaf NO3– concentrations were 33 to 78% lower in the CME plot than in the KGE-M plot of the autumn-seeded spinach (P < 0.01) and of the spring-seeded komatsuna (P < 0.1). No significant differences were found, however, between the KGE-M and CME plots of the spring-seeded spinach and of the autumn-seeded komatsuna. At the rate of 22 g N m–2, the NO3– concentrations of the KGE and NPK plots were not significantly different either in spinach or komatsuna (Fig. 4).


Figure 4
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  		Fig. 4. Effects of the kitchen garbage effluent (KGE), cattle manure effluent (CME), and chemical fertilizers (NPK) on leaf nitrate ion (NO3–) concentrations of spinach and komatsuna in the autumn and spring seasons. The vertical bar indicates the 95% confidence interval. Dotted lines present nitrate concentrations in standard tables of food composition in Japan (Resources Council, Science and Technology Agency, 2000) for spinach (2 g kg–1) and for komatsuna (5 g kg–1). ** indicates that the KGE-M plot was significantly different from the CME plot at P < 0.01.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Heavy Metals and Pathogenic and Indicator Bacteria
Recycling kitchen garbage to farmland is a desirable goal, but farmers and consumers are concerned about potential contamination by heavy metals and pathogens. All the heavy metals (As, Cd, Co, Cr, Cu, Hg, Mo, Ni, Pb, Se, and Zn) concentrations determined in the KGE cleared not only the legal standard of Japan but also that of Canada. In addition, the concentrations of Co, Cu, Ni, Pb, and Zn were lower in the KGE than in the CME (P < 0.05 to P < 0.001). Epstein et al. (1992) compiled heavy metals concentrations of municipal solid waste composts in USA and Europe. The concentrations of As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn ranged from1–4.8, 0.4–13.2, 0.6–130, 24–623, 0.2–3.8, 7–101, 22–913, and 125–1570 mg kg–1 dry matter, respectively. The concentrations of As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn in the KGE were lower than or close to the lower range in the municipal solid waste composts. The high quality of the KGE could be attributed to the good quality of the kitchen garbage, which had been source-separated by each household. For example, there were few visible foreign substances such as glass, plastic, and metal pieces in the kitchen garbage collected.

The concentrations of E. coli in livestock manure effluents ranged from 3 to 4 log CFU g–1 fresh matter in small-scale pig farms (Lam et al., 2002) and between 0.6 and 2 log CFU g–1 fresh matter in centralized biogas plants (Larsen et al., 1994). The concentrations of FS ranged from 2 to 4 log CFU g–1 fresh matter (Larsen et al., 1994). Thus, the concentration of E. coli and FS in the KGE was in the range of these reports. There had been few studies that investigated the fate of pathogenic and sanitary indicator bacteria under field conditions until recently. Nicholson et al. (2005) reported E. coli O157, Salmonella, Campylobactor, and Listeria survived in the soil up to 1 mo after the application of contaminated livestock manure, while Hutchison et al. (2005) found E. coli O157, Salmonella, Campylobactor, Listeria, and Cryptosporidium were detected in the soil up to 128 d. Islam et al. (2004) and Islam et al. (2005) evaluated the fate of E. coli O157 in the soil and on leaf lettuce (Lactuca sativa L.), parsley (Petroselinum crispum (Mill.) Nyman ex A. W. Hill), carrot (Daucus carota var. sativus Hoffm.), and onion (Allium cepa L.) after applications of contaminated composts and irrigation water. They found E. coli O157 persisted up to 217 d in the soil and up to 177 d on the parsley. Our study indicated that CG bacteria, E. coli and V. parahaemolyticus did not increase in the soil due to the application of the KGE (Table 4). In addition, E. coli, and V. parahaemolyticus were not detected in any leaf samples and FS was not found either in the soil or in the leaf (Tables 4 and 5). Because all the research described above was conducted in the short term, field evaluations over the long run will be needed.

Fertilizer Value of Biogas Effluent and Nitrate
Composts are the most common organic amendment in Japan, and have slow N release relative to chemical N fertilizers. The availability of applied N from composts in the first season ranges from 30% in swine and cattle composts to 50% in chicken compost, and the remaining N may be mineralized in the succeeding seasons. Thus, the applications of both chemical N fertilizers and composts are recommended to synchronize with the crop N demand. However, the overapplication of composts or ignoring carryover N after the second seasons could cause N leaching and other N losses, or the NO3– accumulation in vegetable leaves (Ushio et al., 2004).

By contrast, the KGE apparently provided N as rapidly as chemical fertilizers. At the rate of 22 g N m–2, the early N uptake, fresh yield, and N uptake at harvest of spinach and komatsuna were all comparable to those of NPK fertilizers (Fig. 1 and 2). Because the KGE was rich in NH4–N and K but low in P and the soil exchangeable K was high, the fertilizer value of the KGE was considered as primarily the N effect. The N effect of the KGE is natural because 99% of total N in the KGE was NH4–N (Table 1). By contrast, the early N uptake of the autumn-seeded spinach was lower in the CME plot than in the KGE plot (P < 0.01; Fig. 1). In addition, fresh yield and N uptake at harvest of spinach and komatsuna grown with the CME were all inferior to those grown with the KGE (P < 0.05–0.01), except for the fresh yield and N uptake of the spring-seeded spinach (Fig. 2). In the CME, 75% of the total N was the NH4–N (Table 1). The organic N in the solid fraction apparently mineralized little during the growth of spinach and komatsuna. The fertilizer value of biogas effluents in the references appears to be accounted for by the fraction of NH4–N in total N. In the report of Svensson et al. (2004), 61% of total N was NH4–N. The inferior effect of the KGE to oats and barley crops seemed reasonable if organic N in the KGE mineralized little. The comparable effect of swine biogas effluents to chemical fertilizers for water spinach could be explained by a high NH4–N fraction (94%; Lam et al., 2002). On the other hand, only 50% was NH4–N in the report of the Civil Engineering Research Institute of Hokkaido (2003), but the herbage yield of the mixed pasture and the yields of sugar beet, potato, and wheat grown with the CME were mostly comparable to those grown with chemical fertilizers. The reason for this result is unclear.

The apparent N recovery rates at the rate of 22 g N m–2 in the KGE and NPK treatments ranged from 0.28 to 0.55 for spinach and 0.19 to 0.59 for komatsuna. Most of data were unexpectedly higher than our assumption that a significant amount of applied N in the KGE would be volatilized because the KGE is basic and rich in NH4–N. There appear to be three reasons for this. First, the KGE would percolate quickly because the soil (Typic Hapludands) was characterized as quite permeable. The average saturated hydraulic conductivity of the soil was in the order of 10–5 m s–1, and the threshold of saturated hydraulic conductivity for impermeable soil is the order of 10–7 m s–1. Second, because the solid (dry matter) content of the KGE (0.7%) was much lower than that of livestock manure (3.5% for pig and 7.4% for cattle; Sommer and Hutchings, 2001) and lower than even livestock manure effluents of the biogas plant (2.2 to 6.4%; Ruboek et al., 1996), seal formation that prevents percolation (Lado et al., 2005) was likely to be small in the KGE. Third, we applied water after the application of the KGE to equate the amount of irrigation water except for the KGE-H plot. The irrigation water likely increased movement of KGE into the soil.

Chemical fertilizer N applications at the recommended rate to spinach and komatsuna often result in high levels of NO3– accumulation, such as 2 g kg–1 in spinach and in 5 g kg–1 in komatsuna (Sohn and Yoneyama, 1996) and cause high levels of residual soil NO3–N. This is because the recommended N rate is based on fresh yield, not based on leaf NO3– or residual soil NO3–N accumulations. Given that the KGE apparently provided N as rapidly as chemical fertilizers, it follows that high levels of NO3– accumulation often occurred in spinach and komatsuna grown with KGE (Fig. 4) and the residual NO3–N in the soil was significant (Fig. 3). Thus, the KGE should be considered the same as chemical N fertilizer in terms of leaf NO3– and residual soil NO3–N accumulations.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Our study indicated that the KGE, which is made from organic sources, is a rapidly available N source comparable to chemical N fertilizers. The early N uptake of spinach and komatsuna grown with the KGE was similar to that grown with N fertilizers. Fresh yield, N uptake, and apparent N recovery rate of spinach and komatsuna grown with the KGE were also comparable to those grown with N fertilizers, suggesting N loss due to NH3 volatilization might be small in a permeable soil. The total solid concentration of the KGE was constant relative to that of the CME. No visible foreign substances such as glass, plastic, and metal pieces were detected in the KGE. The concentrations of all the heavy metals measured (As, Cd, Co, Cr, Cu, Hg, Mo, Ni, Pb, Se, and Zn) in the KGE cleared the legal standards of Japan and Canada, and were generally lower than those of the CME and municipal solid waste composts in USA and Europe. The bacteria tested (CG bacteria, E. coli, FS, and V. parahaemolyticus) were detected in both biogas effluents in the orders of 2 to 3 log CFU g–1, but there was little evidence that the biogas effluents increased these bacteria in the soil and the plant leaves relative to the chemical fertilizer plot. The residual soil NO3–N and leaf NO3– of the KGE plot were comparable those of the NPK plot. During topdressing, the KGE often dropped on leaf surfaces, but no visible damage such as leaf burn was observed. Because no synthetic chemicals are required, the KGE may be the most beneficial in organic vegetable cultivation where quick release fertilizers are lacking, provided that soil available P ranges from medium to very high (Hasegawa and Furukawa, 2005).

There are some weaknesses in agricultural use of the KGE, however. The weaknesses include high water content (> 99%) and low nutrient concentrations (<0.4%) compared to chemical fertilizers (commonly used in conventional cultivation) and even to composts (commonly used in organic cultivation). To supply a given amount of N, up to 10 times as much effluent needs to be applied when compared to composts, and up to 150 times when compared to chemical N fertilizers. The application of the KGE may not practical when soil water content is high and where the soil is impermeable, such as in heavy clay soil. Another weakness is disagreeable odor during the application. The use of the KGE may not be suitable in farmland near densely populated areas, unless a measure to prevent disagreeable odor emissions is taken.

Future research directions should address the determination of N balances, including direct measurement of NH3 volatilization, the evaluation and reduction of disagreeable odors, and the assessment of long-term fates of pathogenic and sanitary indicator bacteria in the field of continuous application of the KGE.


   ACKNOWLEDGMENTS
 
We thank a nonprofit organization, FOODO, for giving us an opportunity to commence the research and for providing valuable information. We also acknowledge M. Okada, Department of Biology and Environment Sciences, Tohoku National Agricultural Research Center, for providing us unpublished data. K. Kimura, School of Food, Agriculture and Environmental Science, Miyagi University, and S. Yamazaki, Faculty of Agriculture, Tohoku University are acknowledged for their technical advice on acid digestion. Statistical analyses were performed with the assistance of Scientific Computing System of MAFFIN, Tsukuba, Japan. This study was in part supported by Grants-in-Aid for Scientific Research of the Japan Society for the Promotion of Science.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 





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