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Biol Fertil Soils (1999) 30 : 1–6

Q Springer-Verlag 1999

ORIGINAL PAPER

J.A. Pascual 7 C. García 7 T. Hernandez

Lasting microbiological and biochemical effects of the addition of municipal solid waste to an arid soil

Received: 3 July 1998

Abstract This paper reports the effect of the addition of the organic fraction of municipal solid waste at two different rates on the microbiological and biochemical properties of an arid soil after 8 years. The vegetation that appeared spontaneously just after the amendment was still present 8 years later. The organic matter fractions were higher in the amended soil than in the control soil. Amended soil showed higher values of microbial biomass C, soil basal respiration and dehydrogenase activity than control soil, which reached values near to those of the natural soils in the area. The organic amendment had a positive effect on the activity of enzymes related with C, N, P cycles, particularly when the amendment was at the highest dose. This effect could be also observed on the activity of extracted enzymes. The results indicated that the addition of urban waste could be a suitable technique with which to restore soil quality. Key words Arid soil 7 Biomass carbon 7 Basal respiration 7 Soil enzyme 7 Dehydrogenase activity

Introduction Soils from many parts of the Mediterranean region are subjected to progressive degradation and desertification (Albaladejo and Diaz 1990) and, consequently, their level of fertility declines. One method of reversing the degradation and improving the quality of soils with low organic matter content, such as those of the semiarid regions of southeast Spain, involves the addition of municipal solid wastes (MSW; Garcia et al. 1992). In this way, the additional benefit of reducing waste disposal costs is also obtained. These residues are rich in orJ.A. Pascual 7 C. García 7 T. Hernandez (Y) Department of Soil and Water Conservation and Organic Waste Management, CEBAS-CSIC, P.O. BOX 4195, E-30080, Murcia, Spain Fax: c34-968-266613

ganic compounds that stimulate natural soil microorganisms, and thus reactivate biogeochemical nutrient cycles (Garcia et al. 1996; Pascual et al. 1997). Chemical and physical soil parameters have been used to measure soil quality in long-term experiments (Albaladejo and Diaz 1990; Parr and Papendick 1997). Many authors have described the influence of organic amendment on soil quality by using chemical parameters (Pagliai and Vittori Antisari 1993). Soil organic matter content changes very slowly, and therefore, many years are required to measure significant changes. Furthermore, the content of soil organic matter cannot be used as a simple criterion for soil quality since it is not a sensitive indicator of changes in soil activity (Sparling 1992). On the other hand, there is growing evidence that soil microbiological and biochemical parameters (biomass C, enzyme activities, etc.) may hold potential as early and sensitive indicators of soil ecological stress or restoration in long-term experiments (Jenkinson and Ladd 1981; Paul 1984; Dick 1992, 1994). Several authors have suggested that trends in microbial parameters can be used to predict long-term trends in the fertility and quality of soils (Powlson et al. 1987; Sparling 1992). The microbial biomass content of soils has been used to reveal effects of forest management (Diaz-Ravina et al. 1995; Hossain et al. 1995) and ecosystem functioning (Paul and Voroney 1989). It is not possible to evaluate the ecological significance of a microorganism in a given ecosystem simply by knowing its number; it is more important to obtain information on its activity (Alexander 1977). Basal respiration and the metabolic quotient (qCO2) have been defined as good bioindicators of soil microbial activity (Pascual et al. 1997). Some authors criticise the use of the qCO2 in particular situations since it can be insensitive to disturbance and ecosystem development, confounding the effects of disturbance (rapidly changing environmental conditions) with those of stress (non-changing consistently harsh conditions; Wardle and Ghani 1995). There has been increasing interest in soil enzymes as indicators of soil

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fertility, as soil enzyme activity reflects numerous factors such as climate, amendment type, cultivation techniques, crop type and edaphic properties (Skujins 1976; Naseby and Lynch 1997). However, Nannipieri et al. (1990) pointed out that enzymatic activities are substrate specific and therefore related to a specific reaction. For this reason, it is difficult to obtain an overall picture of soil status from one enzymatic activity value alone. The simultaneous measurement of various enzymes can be useful as a marker of the bioactivity of a soil (Nannipieri et al. 1990; Gil-Sotres et al. 1992; Nannipieri 1994). Naseby and Lynch (1997) considered enzymatic determinations more useful than microbial measures, since they can be made with high precision. A possible solution is to combine the information offered by several parameters (Frankenberger and Dick 1983; Nannipieri et al. 1990). An index which comprises both soil biological and biochemical parameters has been defined as a good quality indicator (Trasar-Cepeda et al. 1998). In this paper, we report the maintenance of the improvement in the microbiological and biochemical characteristics of a degraded soil 8 years after the addition of the organic fraction of a municipal solid waste. Parameters related to the organic matter, microbiological and biochemical processes were evaluated, i.e. biomass C, basal respiration, oxidoreductases, and hydrolases involved in the N, C and P cycles. Total and extracted urease and phosphatase were studied due to their role in the cycles of two important elements (N and P) for soil fertility.

Materials and methods The study area was located in Murcia (southeast Spain) in a semiarid Mediterranean area with average annual rainfall of 300 mm, which occurs mostly in autumn and spring. The mean annual temperature is 19.2 7C and the potential evapotranspiration reaches 900–1000 mm year –1 (Diaz 1992). The predominant soil is Xeric Torriortents (Soil Survey Staff 1975). In October 1988, three plots of 87 m 2 (one for each treatment) were set up on an east-facing hill slope (10% gradient). The main experimental factor was the amendment with the organic fraction of a MSW from Murcia which had been stored for 15 days. The soil was amended at two different rates: 6.5 kg m –2 and 26.0 kg m –2. The organic amendment was incorporated into the top 20 cm using a rotovator. Soil was sampled from each plot 8 years after the incorporation of the waste. For sampling, eight subsamples were taken randomly from the surface soil (0–20 cm) of each plot, mixed, grounded and sieved (0.5 mm) before analysis. The main characteristics of the soil and waste are shown in Tables 1 and 2, and have been described in a previous paper (Garcia et al. 1992). The total organic C (TOC) content was determined by oxidation with potassium dichromate in a sulphuric medium and evaluation of the excess of dichromate with Mohr’s salt (Yeomans and Bremner 1989). Humic substances were extracted with 0.1 M sodium pyrophosphate, pH 7.1, for 24 h at 37 7C. The suspension was centrifuged at 18 000 g and the supernatant passed through a 0.22-mm Millipore membrane. Identical volumes of these extracts were dialysed in dialysis tubes against distilled water for 10 days, changing the distilled water every day. After dialysis, the extracts were made up to the same volume (Nannipieri et al. 1983). Humic

Table 1 Characteristics of the soil. (atm Atmospheres, TOC total organic C) Clay (%) Silt (%) Fine sand (%) Coarse sand (%) pH (H2O) Electrical conductivity (S m P1) Water holding capacity (1/3 atm; %) Water holding capacity (15 atm; %) TOC (g kg P1) Total N (g kg P1) Total P (g kg P1) Total K (g kg P1)

48.6 40.1 5.0 6.3 7.8 0.18 31.5 14.1 5.41 0.41 0.58 8.10

Table 2 Characteristics of the municipal solid waste pH Electrical conductivity (s m P1) TOC (g kg P1) Humic substances (g kg P1) Total N (g kg P1) Total P (g kg P1) Available P (g kg P1) Total K (g kg P1) Available K (g kg P1) Cu (mg kg P1) Zn (mg kg P1) Cr (mg kg P1) Cd (mg kg P1) Ni (mg kg P1) Pb (mg kg P1)

6.5 0.4 242.0 26.0 13 5.5 0.6 4.2 3.0 237 650 365 2 328 235

substances, soluble and precipitated C from the organic matter extract and water-soluble C were analysed by the method of Yeomans and Bremner (1989). Microbial biomass C was determined by a fumigation-extraction method (Vance et al. 1987). Respiration rates were determined by placing 50 g of dry soil in hermetically sealed flasks, moistened at 65% of field capacity and incubated in the dark at 28 7C. The CO2 emitted was collected in 10 ml of 0.1 M NaOH, and at appropriate times the resulting CO3 2– was measured by tritation with 0.1 M HCl; the value of the CO2 emitted in a glass flask without soil (controls) was subtracted from the value for CO2 emitted from the soil sample (Parr and Smith 1969). The qCO2 was calculated by dividing the CO2–C released from the sample in 1 h by the biomass C content (Anderson and Domsch 1990). Dehydrogenase activity was determined by the reduction of 2-p-iodo-3-nitrophenyl 5-phenyl tetrazolium chloride to iodonitrophenylformazan by the method of Skujins (1976) modified by Garcia et al. (1993). Urease activity and protease activity on Na-benzoil-L-argininamide (BAA protease) were measured following the method proposed by Nannipieri et al. (1980). Phosphatase and b-glucosidase activities were determined using p-nitrophenyl phosphate disodium (0.115 M) and p-nitrophenyl-b-Dglucopiranoside (0.05 M) as substrates, respectively (Tabatabai 1982). Urease and phosphatase activities extracted from the soil were measured using 1 ml of the organic matter extract following the methods described above. Biomass C, CO2–C emission and dehydrogenase activity were determined immediately after sampling, while the other analysis were carried out after storage at 4 7C. All analysis were done in triplicate and data were submitted to an ANOVA test; the differences between treatments were tested by a protected least significant difference test, using the Statgraph version 4.1 program.

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Results and discussion Plant cover Vegetation is an important factor that can modify soil characteristics (Albaladejo and Diaz 1990; Brockway et al. 1998), mainly due to maintaining a stable microbial population in soil by supplying easily biodegradable C compounds through root exudates and plant remains (Balloni and Favilli 1987; Dick 1992; Garcia et al. 1998). The percentage of plant cover was estimated by a grid-line intersect method. One year after the soil organic amendment, treated plots were covered with spontaneous vegetation in contrast with the control plot, in which very scarce vegetation was observed. After 8 years, the percentage of plant cover decreased in the following order: plot treated at high dose (62% of plant cover) 1 plot treated at low dose (25% of plant cover) 1 control plot (5% of plant cover). The amended plots also showed a higher diversity of plant species, Artemisia herba-alba, Moricandia arvensis, Plantago albicans, Piptatherum miliaceum, Rapistrum rugosum and Thimelacea hirsuta being the most abundant.

Organic C fractions Eight years after the amendment was applied, even at the low dose, the TOC content in the amended soils was higher than in the control (Table 3). According to Pascual et al. (1999), half of the organic matter added as MSW is mineralised after 12 months, thus it was reasonable to consider that the increase in organic C content after 8 years was mainly due to the supply of plant remains since, 1 year after amendment, the treated Table 3 C fractions of the soils 8 years after organic amendment. LSD Least significant difference

Parameters

TOC (g kg P1) Humic substances (mg kg P1) Fulvic acids (mg kg P1) Humic acids (mg kg P1) Water-soluble C (mg kg P1) a

Table 4 Biological characteristics of the soils 8 years after organic amendment. CO2 Metabolic quotient, INTF iodonitrotetrazoliumformazan

plots were already covered with autochtonous vegetation. The humic and fulvic acid content and the watersoluble C fraction were also higher in the amended plots than in the control plot (Table 3). Water-soluble compounds are easily degraded by microorganisms (Cook and Allan 1992); the higher content observed in the soil amended at the high dose than in the control soil after 8 years probably reflected the contribution of root exudates from the vegetation which had established on the amended soil (Campbell and Zentner 1993). This confirmed the hypothesis mentioned above on the influence of plant cover rather than the direct effect of the MSW addition. All this indicated that the soil had improved as regards the higher levels of soil organic matter maintained after 8 years. Microbiological and biochemical soil characteristics Soil amendment with MSW resulted in a significant increase in microbial biomass C (Table 4), which reached values near those of the natural soils in the area (without any anthropogenic effects in the last 50 years; 425 mg C g –1 soil). If we accept that biomass C gives an idea of the potential microbial activity of a soil (Nannipieri et al. 1990), then the soil under study showed very low biological activity, the values being lower than those found in the literature for natural and agricultural soils (Dick et al. 1988). The incorporation of the organic fraction of a MSW improved the microbial activity, being noticeable 8 years after the amendment, due to the contribution of root exudates generated by the vegetation. In short-term laboratory experiments without vegetation, the microbial biomass C decreased with incubation time to initial values, because of the decline in the easily biodegradable organic compounds which Control

5.4 710 410 300 180

Low dose

High dose

12.4 1200 610 590 290

20.8 1900 1100 800 610

0.6 140 123 180 40

LSD at P^0.05

Parameters

Biomass C (mg C g P1 soil) Biomass C/TOC ratio (%) Basal respiration (mg CO2-C g P1 soil day P1) qCO2 (mg CO2-C g P1 h P1 mg C biomass) Dehydrogenase activity (mg INTF g P1 h P1) a

LSD a

Amended soil

LSD at P^0.05

Control

280 5.18 24 3.10 0.41

Amended soil Low dose

High dose

586 4.72 53 3.73 1.03

1053 5.06 86 3.52 2.06

LSD a

53 0.43 12 1.0 0.12

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had been incorporated, which were used by microorganisms (Pascual et al. 1997). The percentage of microbial biomass C of TOC ranged from 4.7% to 5% in the control and amended soils (Table 4). These values were in the range reported in the literature (Anderson and Domsch 1980, 1989; Jenkinson and Ladd 1981), and 8 years after the amendment, the ratio of microbial biomass C to TOC was similar in amended and unamended soils. Soil basal respiration is a widely used parameter to monitor microbial activity and soil organic matter break down (Anderson 1982). It is obtained by dividing the CO2–C evolved during a respiration experiment by the duration of the experiment. The soil basal respiration was higher in the amended soils with respect to the control after 8 years (Table 4). Taking into account that in a laboratory experiment the CO2–C emitted in amended soil increased with respect to the control and then decreased with time (Pascual et al. 1998a), the higher respiration values in the amended soils could have been due to the higher level of water-soluble C of the amended soils. It could be concluded that not only was the microbial activity encouraged just after the amendment was applied, as has been demonstrated in previous studies (Pascual et al. 1997), but that this activity was maintained 8 years after the soil was amended, thus indicating soil restoration. The basal respiration value of the soil amended at the high rate was similar to those of the natural soils of the area (80 mg CO2–C g –1 soil day –1). The qCO2, usually expressed as mg CO2–C g h –1 –1 mg microbial biomass C, is used to investigate soil development, substrate quality, ecosystem development and microbial response to adverse environmental conditions (Insam and Haselwandter 1989; Anderson and Domsch 1990; Wardle and Ghani 1995). This index has valuable applications as a relative measure of how efficiently the soil biomass is utilizing C resources, and the degree of substrate limitation for the soil microbial biomass (Wardle and Ghani 1995). The values of qCO2 tend to increase immediately after soil amendment, due to the response to the microbial biomass to the new environmental conditions, and then decrease (Pascual et al. 1997). Eight years after amendment, the qCO2 values were similar in amended and unamended soils (Table 4), indicating a reduction in adverse environmental conditions (Wardle and Ghani 1995). Dehydrogenase activity has been generally used as a measure of microbial activity in soil, although this application has been criticised (Nannipieri et al. 1990; Beyer et al. 1992). According to Garcia et al. (1994), dehydrogenase activity can be used as indicator of microbial activity in semiarid soils. Eight years after amendment, the dehydrogenase activity was higher in the amended soils than in the control (Table 4). It was reasonable to hypothesise that there was a positive effect of water-soluble organic C from plant remains on the amended soils as a consequence of the vegetation which established spontaneously.

The study of different hydrolase enzyme activities is important since these activities indicate a soil’s potential to carry out specific reactions important in nutrient cycling. Urease and BAA protease are involved in the N cycle. The organic amendment had a positive effect on the activity of these enzymes, particularly when the amendment was at the high dose (Fig. 1), probably due to the higher microbial biomass produced in response (Garcia et al. 1994; Pascual et al. 1998b). Phosphatase catalyses the hydrolysis of organic P compounds to PO4 3–. Hence, the activity of these en-

Fig. 1 Hydrolase activities of the soils 8 years after organic amendment (bars with the same letter are not significantly different at P^0.05). BAA protease N-a-benzoil-L-argininamide, PNP p-nitrophenyl

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chemical cycles of the soil (Pascual et al. 1998b). The initial reactivation of the different cycles as a consequence of the introduction of easily biodegradable compounds with the organic waste (Pascual et al. 1997) encouraged the spontaneous establishment of vegetation that led to the long-term bioremediation of the arid soil. The addition of urban waste to the soil improved the soil quality for a long period after the amendment was applied, and, therefore, this is considered a suitable technique for the regeneration of soils in semiarid regions. The continued study of biological and biochemical parameters help in the exact diagnosis of a soil’s status and its capacity to be regenerated.

References

Fig. 2 Urease (mmol NH4 c ml –1 h –1) and phosphatase (mmol PNP ml –1 h –1) of soil extracts 8 years after organic amendment (bars with the same letter are not significantly different at P^0.05)

zymes is related to P availability from organic matter. According to Dick (1992), we found that phosphatase activity was higher in the amended soils than in the control (Fig. 1). The higher phosphatase activity values probably depended on the microbial activity rather than the available P content of soil. b-glucosidase hydrolyses b-glucosides in soil or in decomposing plant residues (Hayano and Tubaki 1985), an important reaction making easily degradable substrates available to soil microorganisms (Eivazi and Tabatabai 1990). The addition of the MSW encouraged soil b-glucosidase activity, probably as a result of the increase in microbial activity (Fig. 1). According to Burns (1982), the enzymatic activities determined in soil may be the result of different activities associated with biotic and abiotic factors. The enzymes linked to humic colloids (immobilised enzymes) are resistant to high temperatures, proteolysis, etc. (Mayaudon 1986; Nannipieri et al. 1996). Extracted urease and phosphatase activities were studied due their biotechnological and agronomic interest (Ladd 1985). The activities of extracted enzymes from the amended soils were significantly higher than those of the control (Fig. 2). This indicated that 8 years after soil amendment, the amended soils had greater overall enzymatic activities than the control. The biogeochemical cycles of N, P and C had been reactivated, thus the fertility of the amended soil had improved (Ladd 1985). In conclusion, the addition of organic waste not only increased the organic matter content of the arid soil (Pascual et al. 1998a), but also led to an increase in the microbial biomass and maintained the important bio-

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