15
Carbon mineralization from organic wastes at different composting stages during their incubation with soil M.P. Bernal * , M.A. Sa ´nchez-Monedero, C. Paredes, A. Roig Department of Soil and Water Conservation and Organic Waste Management, Centro de Edafologı ´a y Biologı ´a Aplicada del Segura, CSIC, PO Box 4195, 30080 Murcia, Spain Received 24 June 1997; accepted 3 March 1998 Abstract The decomposition of seven different organic waste mixtures prepared with sewage sludges, animal manures, city refuse and industrial and plant residues, was studied during their aerobic incubation with soil. The waste mixtures were composted by the Rutgers static pile system, and four samples of each mixture were collected at various composting stages: the initial mixture, and samples taken during the thermophilic phase, at the end of the active phase and after maturation. These samples were added to a calcareous silt loam soil at a rate of 200 mg per 10 g soil, and the CO 2 –C evolution was determined during 70 days of aerobic incubation at 288C. Carbon mineralization decreased as the composting time lengthened. The lowest values of C mineralization were found for the mature samples, and only a compost which had not attained an advanced degree of maturation gave results higher than 25% of TOC. Carbon mineralization followed a combined first- and zero-order kinetic model in most of the samples, suggesting that the organic C of the composting wastes was made up of two organic pools of differing degrees of stability. However, the differences in the slow C mineralization pool at the end of the active phase and after maturation were very small, indicating that the organic matter at both stages was of a similar microbial stability. Comparing the C mineralization which takes place in soil and during composting, it can be concluded that composting is the best way of obtaining maximum C stabilization, which is an important factor in soil conservation and reclamation. # 1998 Elsevier Science B.V. All rights reserved. Keywords: Carbon mineralization; Compost maturity; Mineralization kinetic; Organic waste; Soil conservation 1. Introduction The application of organic wastes, such as animal manures, sewage sludge, city refuse, etc. to soil is a current environmental and agricultural practice for maintaining soil organic matter, reclaiming degraded soils and supplying plant nutrients. These wastes are rich in nitrogen providing high agricultural value, and in fresh organic matter which stimulates the soil microbial metabolism and soil enzymes. Their biolo- gical decomposition depends on the degradation rate of a wide range of C compounds present in the sample (carbohydrates, amino acids, fatty acids, lignin, etc.), as well as on their nutrient content. Then the amount of CO 2 –C released from organic wastes in soil has been shown to depend on the material used: plant residues, animal manures, sewage sludges, etc. (Ajwa and Tabatabai, 1994). The degradation of wastes that con- tain a high percentage of soluble organic carbon in the Agriculture, Ecosystems and Environment 69 (1998) 175–189 *Corresponding author. Tel.: +34 68 215717; fax: +34 68 266613; e-mail: [email protected] 0167-8809/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0167-8809(98)00106-6

Carbon mineralization from organic wastes at different composting stages during their incubation with soil

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Carbon mineralization from organic wastes at different

composting stages during their incubation with soil

M.P. Bernal*, M.A. SaÂnchez-Monedero, C. Paredes, A. Roig

Department of Soil and Water Conservation and Organic Waste Management, Centro de EdafologõÂa y BiologõÂa Aplicada del Segura,

CSIC, PO Box 4195, 30080 Murcia, Spain

Received 24 June 1997; accepted 3 March 1998

Abstract

The decomposition of seven different organic waste mixtures prepared with sewage sludges, animal manures, city refuse and

industrial and plant residues, was studied during their aerobic incubation with soil. The waste mixtures were composted by the

Rutgers static pile system, and four samples of each mixture were collected at various composting stages: the initial mixture,

and samples taken during the thermophilic phase, at the end of the active phase and after maturation. These samples were

added to a calcareous silt loam soil at a rate of 200 mg per 10 g soil, and the CO2±C evolution was determined during 70 days

of aerobic incubation at 288C. Carbon mineralization decreased as the composting time lengthened. The lowest values of C

mineralization were found for the mature samples, and only a compost which had not attained an advanced degree of

maturation gave results higher than 25% of TOC. Carbon mineralization followed a combined ®rst- and zero-order kinetic

model in most of the samples, suggesting that the organic C of the composting wastes was made up of two organic pools of

differing degrees of stability. However, the differences in the slow C mineralization pool at the end of the active phase and

after maturation were very small, indicating that the organic matter at both stages was of a similar microbial stability.

Comparing the C mineralization which takes place in soil and during composting, it can be concluded that composting is the

best way of obtaining maximum C stabilization, which is an important factor in soil conservation and reclamation. # 1998

Elsevier Science B.V. All rights reserved.

Keywords: Carbon mineralization; Compost maturity; Mineralization kinetic; Organic waste; Soil conservation

1. Introduction

The application of organic wastes, such as animal

manures, sewage sludge, city refuse, etc. to soil is a

current environmental and agricultural practice for

maintaining soil organic matter, reclaiming degraded

soils and supplying plant nutrients. These wastes are

rich in nitrogen providing high agricultural value, and

in fresh organic matter which stimulates the soil

microbial metabolism and soil enzymes. Their biolo-

gical decomposition depends on the degradation rate

of a wide range of C compounds present in the sample

(carbohydrates, amino acids, fatty acids, lignin, etc.),

as well as on their nutrient content. Then the amount of

CO2±C released from organic wastes in soil has been

shown to depend on the material used: plant residues,

animal manures, sewage sludges, etc. (Ajwa and

Tabatabai, 1994). The degradation of wastes that con-

tain a high percentage of soluble organic carbon in the

Agriculture, Ecosystems and Environment 69 (1998) 175±189

*Corresponding author. Tel.: +34 68 215717; fax: +34 68

266613; e-mail: [email protected]

0167-8809/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved.

P I I S 0 1 6 7 - 8 8 0 9 ( 9 8 ) 0 0 1 0 6 - 6

form of amino acids, carbohydrates, etc., leads to a

¯ush of CO2 production immediately after their addi-

tion to soil (Marstorp, 1996). This can cause a high

CO2 concentration, low O2 levels, which can lead to

O2 de®ciency in the rhizosphere, and therefore anae-

robic and reducing conditions in the soil. The strong

microbial activity could also promote the degradation

of the indigenous soil organic matter, which is known

as priming effect. Inorganic N can be immobilized

through its incorporation into microbial tissues, being

temporarily unavailable to plants. Intermediate pro-

ducts of organic waste degradation such as volatile

fatty acids, alcohols and phenols, are toxic to plants

and the reducing conditions may solubilize heavy

metals in the soil. Therefore, the usual agricultural

practice is to add organic wastes to soil some weeks

before sowing to allow the soil microorganisms to

degrade the labile organic matter, reduce phytotoxi-

city, release plant nutrients and reach a new equili-

brium in the soil microbial activity (Bernal et al.,

1998a).

The treatment of organic wastes before applying

them to soil can be aerobic (composting) or anaerobic

(fermentation, biogas digestion), which changes their

composition (Kirchmann and Witter, 1992), microbial

stability and, therefore, the proportion of C miner-

alized after their addition to soil (Bernal and Kirch-

mann, 1992). Composting is a biological process of

aerobic decomposition, which degrades labile organic

matter to carbon dioxide, water vapour, ammonia,

inorganic nutrients and a stable organic material (com-

post) containing humic-like substances (Senesi, 1989).

Composting is the most widely used treatment of

organic wastes, which is very well developed for city

refuse and the compost has been generally used in the

last years. Nowadays, the composting technology is

being updated to process organic wastes of different

origin, such as sewage sludge, animal manures, agro-

industrial wastes, etc., (Hoitink and Keener, 1993;

Paredes et al., 1996; Bernal et al., 1998b).

There are four important stages in the composting

process: (1) the initial stage, when the raw material has

not yet undergone any decomposition; (2) the thermo-

philic phase, when the material reaches its maximum

temperature (>408C) and is degraded most rapidly; (3)

the end of the bio-oxidative phase, which is marked by

a fall in temperature to values close to the external

temperature; and (4) the maturation phase, which is a

lengthy period of stabilization intended to produce a

highly stabilized and humi®ed mature compost, free of

phytotoxicity. Thus, this matured organic material or

compost can be de®ned as the stabilized and sanitized

product of composting, which has undergone decom-

position and is in the process of humi®cation. It is

therefore bene®cial to plant growth. However, depend-

ing on the composting facility and compost demand,

the material applied to soil can have different degree

of maturity, i.e., it can be taken after the biooxidative

phase before maturation, slightly transformed during

the biooxidative phase or even at the thermophilic

phase. The use of immature compost can cause phy-

totoxic effects as well as N de®ciency to plants, which

reduces plant yield (Bernal et al., 1998a)

It is necessary to know the degree of stabilization of

the organic matter in composting organic wastes and

its decomposition rate if maximum bene®t is to be

obtained from the compost after its addition to soil.

This knowledge can be achieved by studying the C

mineralization of organic wastes in incubation experi-

ments with soil. The ®tting of kinetic equations to

mineralization curves makes it possible to calculate

the fraction of potentially mineralizable C and its

mineralization rate. Several kinetic models have been

used to describe the decomposition of wastes. The

®rst-order kinetic model has been widely used in C

mineralization studies because of its versatility (Sinha

et al., 1977; Murwira et al., 1990; Ajwa and Tabatabai,

1994). Although alternatives to this model have also

been presented, most of these include several organic

pools of different degrees of stability, a combination of

two ®rst-order equations (Boyle and Paul, 1989; Mar-

storp and Kirchmann, 1991) or a combination of diffe-

rent kinetic order equations (Bernal and Kirchmann,

1992).

The main aim of the present paper was to study

the organic C mineralization rate of several organic

wastes when added to soil after undergoing varying

composting times, and to assess the best degree of

composting for soil conservation.

2. Materials and methods

2.1. Composting samples and soil used

Seven mixtures were prepared with different or-

ganic wastes at the following rates (wet weight):

176 M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189

SC 46.5% sewage sludge�53.5% cotton waste.

PCO 34.6% poultry manure�65.4% cotton waste

�1.93 l/kg olive-mill wastewater.

SCO 32.1% sewage sludge�67.9 cotton waste

�0.94 l/kg olive-mill wastewater.

SM 79.0% sewage sludge�21.0% maize straw.

SMO 52.8% sewage sludge�47.2% maize straw

�1.76 l/kg olive-mill wastewater.

PPB 27.0% pig slurry�20.0% poultry manure

�53.0% sweet sorghum bagasse.

RB 95.0% city refuse�5.0% sweet sorghum

bagasse.

About 1500 kg of each mixture was composted in a

pilot plant using the Rutgers static pile composting

system. This system maintains a temperature ceiling

in the pile, thus encouraging a high decomposition rate

through the on-demand removal of heat by ventilation

because excessively high temperatures slow down

decomposition by reducing microbial activity (Fin-

stein et al., 1985). Air was blown from the base of the

pile through the holes of three PVC tubes, 3 m in

length and 12 cm in diameter. The timer was set for

30 s ventilation every 15 min. The ceiling temperature

for continuous air blowing was 558C. The bio-oxida-

tive phase of composting (active phase) was consid-

ered ®nished when the temperature of the pile

was stable and near air temperature. This stage was

reached after 49 (SC), 49 (PCO), 84 (SCO), 56 (SM),

63 (SMO), 56 (PPB) and 77 (RB) days in the different

mixtures. Air-blowing was then stopped to allow the

compost to mature over a period of two months. Four

samples per mixture were selected at different stages

of the composting process: the initial untransformed

mixture (I), a sample taken during the thermophilic

phase (with the exception of PPB) (T), a sample from

the end of the active phase (E), and a sample from the

mature compost (M). Samples were air-dried and

ground to 0.5 mm. Table 1 presents the principal

characteristics of the mixtures at the different sam-

pling times.

The soil used for the incubation experiments was a

calcareous silt loam, classi®ed as a Typic Calciorthid

(American Soil Taxonomy; Soil Survey Staff, 1987).

Its main characteristics were 17.6% clay, 52.1% silt,

30.3% sand, 46% CaCO3, 21.3% water holding capa-

city, 7.8 pH, 0.036 S mÿ1 electrical conductivity,

0.76% organic matter, 0.46% organic C, 0.04% total

N, a C/N ratio of 11.2, and a cation exchange capacity

of 12.3 cmolc kgÿ1.

2.2. Analytical methods

The soil and composting samples were analyzed for

pH in H2O suspensions (1:10 w/v in composting

samples, saturated paste in soil). Electrical conductiv-

ity (EC) was measured in a 1:5 and 1:10 water extract

for soil and composting samples, respectively. The

organic matter (OM) of the composting samples was

estimated by loss on ignition at 4308C for 24 h

(Navarro et al., 1993) and that of the soil was calcu-

lated from the organic carbon content multiplied by

1.72. Total nitrogen and total organic carbon (TOC)

were determined by automatic microanalysis (Navarro

et al., 1991). The cation exchange capacity of the soil

was determined with BaCl2-triethanolamine following

the method of Carpena et al. (1972). The lignin

concentration of the composting samples was deter-

mined by the American National Standard methods

(ANSI and ASTM, 1977). All analyses were made at

least in duplicate. Losses of organic matter during

composting were calculated from the initial (X1) and

®nal (X2) ash contents, according to the following

equation (Viel et al., 1987),

OMÿÿÿ loss�%�� 100ÿ 100�X1�100ÿ X2��=�X2�100ÿ X1��

2.3. Incubation procedure

Carbon mineralization was studied in an aerobic

incubation experiment with soil. Ten gram samples of

soil (<2 mm) were thoroughly mixed with 200 mg

portions of the composting samples (equivalent to

48 t haÿ1) and placed in 100 ml incubation vessels.

Soil controls were run without any amendment. Dis-

tilled water was added to the soil-compost mixtures

and the soil samples (2 and 1.8 ml, respectively) in

order to bring their moisture content to 60% of their

water-holding capacity. The CO2 evolved was trapped

in 10 ml of 0.1 M NaOH in small tubes, which were

placed on top of the soil in the incubation vessels. The

incubation vessels were closed, but to maintain ade-

quate O2 levels they were opened for several minutes

every day during the ®rst week, on alternate days

during the second week and every 3 days during the

M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189 177

following weeks. Empty vessels were used as blanks.

After 1, 2, 3, 6, 10, 14 days and then weekly to 70 days,

the CO2 evolved was measured by titration of the

NaOH solution with 0.1 M HCl in an excess of BaCl2.

The incubation was carried out in a dark, temperature-

controlled incubator at 288C for 70 days.

2.4. Statistical analysis

The amount of C evolved as carbon dioxide

from the composting samples was calculated by sub-

tracting the amount produced by the control soil from

that produced by the waste-treated soil and expressed

as a percentage of the TOC concentration of the

composting samples, assuming no priming effect in

the soil (Sinha et al., 1977). Data concerning CO2±C

evolution of the composting samples were ®tted to

kinetic functions by a non-linear least-square pro-

cedure (Marquardt±Levenberg algorithm), using the

SigmaPlot computer programme. The kinetic func-

tions used were: Combined two ®rst-order kinetic

model,

Table 1

Chemical analysis of the organic wastes at different composting times

Composting

samples

pH EC (S mÿ1) OM (%) TOC

(g kgÿ1)

Total N

(g kgÿ1)

C/N Lignin(%) OM-loss

(% initial OM)

Mixture SC: sewage sludge�cotton waste

SC-I 7.6 0.39 81.5 438.6 20.8 21.1 29.4 0.0

SC-T 7.1 0.41 71.3 398.2 28.2 14.2 36.3 43.6

SC-E 8.0 0.50 64.9 359.8 36.5 9.9 37.9 58.0

SC-M 7.3 0.67 64.8 355.5 37.9 9.4 38.5 58.2

Mixture PCO: poultry manure�cotton waste�olive-mill wastewater

PCO-I 7.5 0.52 78.4 407.2 27.1 15.0 26.0 0.0

PCO-T 8.0 0.65 69.6 359.5 31.2 11.5 30.7 36.9

PCO-E 7.8 0.78 63.1 334.3 34.6 9.7 31.7 52.9

PCO-M 7.4 0.83 62.9 337.3 34.7 9.7 31.9 53.3

Mixture SCO: sewage sludge�cotton waste�olive-mill wastewater

SCO-I 7.1 0.44 80.7 405.4 19.2 21.1 23.3 0.0

SCO-T 7.8 0.60 61.5 333.1 30.4 11.0 32.0 61.9

SCO-E 7.6 0.73 56.3 300.8 29.9 10.1 31.3 69.2

SCO-M 7.8 0.77 56.4 293.7 31.1 9.4 31.8 69.1

Mixture SM: sewage sludge�maize straw

SM-I 5.6 0.77 81.0 412.7 37.5 11.0 19.1 0.0

SM-T 6.4 0.81 71.1 368.6 40.3 9.1 18.1 42.3

SM-E 6.9 0.83 55.8 305.3 31.8 9.6 15.4 70.4

SM-M 7.1 0.75 53.3 272.8 31.6 8.6 15.2 73.2

Mixture SMO: sewage sludge�maize straw�olive-mill wastewater

SMO-I 6.1 0.42 89.6 472.0 15.2 31.1 27.3 0.0

SMO-T 7.7 0.57 83.0 408.8 22.2 18.4 27.6 43.2

SMO-E 7.4 0.76 79.7 415.4 30.0 13.8 29.1 54.7

SMO-M 7.5 0.84 74.8 394.3 33.3 11.8 30.9 65.5

Mixture PPB: pig slurry�poultry manure�sweet sorghum bagasse

PPB-I 7.7 0.31 79.8 403.7 16.8 24.1 n.d 0.0

PPB-E 6.9 0.54 64.3 335.0 29.7 11.3 n.d 54.4

PPB-M 8.6 0.43 59.8 303.3 27.6 11.0 n.d 62.3

Mixture RB: city refuse�sweet sorghum bagasse

RB-I 6.7 0.46 62.5 321.4 18.2 19.5 13.2 0.0

RB-T 7.5 0.41 45.9 232.8 18.6 13.6 12.6 49.1

RB-E 7.9 0.50 28.1 161.7 17.4 9.3 12.1 76.6

RB-M 8.0 0.53 30.1 156.7 20.0 7.8 13.2 74.2

EC, electrical conductivity.

OM, organic matter.

TOC, total organic carbon.

n.d., not determined.

178 M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189

Cm � CR�1ÿ exp�ÿKRt�� � CS�1ÿ exp�ÿKSt��Combined ®rst- and zero-order kinetic model,

Cm � CR�1ÿ exp�ÿKRt�� � CSKSt

where Cm is the carbon mineralized (% of TOC) at

time t (days), CR and CS are the rapid and slow poten-

tially mineralizable carbon (% of TOC), and KR and

KS are the rapid and slow rate constants (dayÿ1). The

standard deviation of the parameters, the residual

mean square (RMS) and the F-values of the curve ®ts

were calculated. The model which gave a randomized

distribution of the residuals together with the lowest

value of RMS and high F-value was chosen as the best

®t (Little and Hills, 1975). Analysis of variance and

least signi®cant difference (LSD) at P<0.05 were used

to compare the different treatments as regards C

mineralization and C lost during C stabilization.

3. Results and discussion

3.1. Carbon mineralization

During the incubation period, the maximum C

mineralization rate in the composted samples occurred

during the ®rst day of incubation (with the exception

of sample SM-T). In the untransformed initial samples

(I) the maximum occurred between days 1 and 3 of

incubation (Fig. 1). This was because of the presence

of a high concentration of easily degradable organic

carbon in the wastes, which led to a large growth in

the microbial population in the soil. Some samples

showed a second maximum in the C mineralization

rate which occurred because of the great variety of

compounds they contained with different degrees of

degradability. After the initially high mineralization

rate there was a gradual decrease in all cases before it

became fairly constant (Fig. 1). The C mineralization

rate became constant earlier when samples in a more

transformed state (end of active phase and mature

samples) were used. The rate at the end of the incuba-

tion period was highest with the initial samples (37±

23 mg C kgÿ1 dayÿ1) and least with the mature

samples (24±12 mg C kgÿ1 dayÿ1, the greatest ®gure

being recorded in SMO-M). All rates were higher than

in the control soil (7 mg C kgÿ1 dayÿ1).

The total amount of CO2±C released after 70 days

of incubation from soil amended with the initial

organic waste mixtures ranged from 8314 to

3858 mg kgÿ1 (Table 2), decreasing in the order:

SM>SMO>SCO>PCO�SC�RB>PPB, according to

the LSD. For the samples taken at the thermophilic

stage, the C mineralized after 70 days ranged from

6324 to 1534 mg kgÿ1, statistically decreasing in the

order: SM>SMO>PCO�SC>SCO>RB. The amount

of C mineralized decreased in the samples taken after

the biooxidative phase (from 4073 to 1268 mg kgÿ1)

in the order: SMO>SM>PCO�SC>PPB�SCO>RB

(Table 2). In the mature samples the range was nar-

rower (from 3280 to 1368 mg kgÿ1), with less sig-

ni®cant differences between the mixtures, according

to LSD: SMO>PCO�SC�SM�PPB�SCO>RB. Of

all the samples taken after the maturation period, the

SMO-M showed the greatest degree of C mineraliza-

tion. This sample also showed an abnormally high rate

of CO2 production for a mature compost (34 mg C

kgÿ1 day ÿ1), because of its low degree of maturation

after composting (Bernal et al., 1998b).

The percentage of TOC mineralized from the initial

samples (I) after 30 days of incubation in soil (Fig. 2)

fell within the range expressed by Ajwa and Tabatabai

(1994) for plant materials, animal manure and sewage

sludge (21±62% of TOC). The highest proportion of C

mineralized after 70 days of incubation (Cm) was

always recorded in the untransformed samples (I).

Note the extremely high value obtained with the

SM-I sample (93.2% of TOC) and RB-I sample

(80.1% of TOC) (Table 2). These mixtures were pre-

pared, respectively, with sewage sludge and city refuse

as the principal constituents, and so both had a high

proportion of organic compounds easily degradable in

the soil. These labile compounds were also rapidly

degraded during composting, as is shown by the high

loss of organic matter in both piles (Table 1). A high

degree of organic matter degradation was also found

during the composting of city refuse and sewage

sludge by Iglesias-JimeÂnez and PeÂrez-GarcõÂa (1992).

The initial sample of the PPB mixture, which was

prepared with a high proportion of sweet sorghum

bagasse, showed the lowest degree of C mineralization

after 70 days (Table 2), because bagasse is very

resistant to decomposition (Bernal et al., 1996). The

Cm values of the other four initial mixtures ranged

from 62.3% to 70.3% of TOC. The values for PCO-I,

SCO-I and SMO-I did not differ statistically, accord-

ing to LSD. C mineralization was lower in SC-I than in

M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189 179

SCO-I, perhaps because of the presence in the latter of

soluble organic compounds, particularly sugars and

organic acids, in the olive-mill wastewater (Balis,

1994), which are easily mineralizable (Saviozzi et

al., 1993).

The C mineralized after 70 days (Cm) decreased

with the time of composting in all mixtures (Table 2).

However, no signi®cant differences were found, acc-

ording to LSD, between samples taken at the end of

the active phase and those taken after maturation of the

RB mixture. The lowest Cm values were observed in

the mature composts, where they ranged from 9.0%

to 37.9% of TOC, the highest value being found in

SMO-M. This means that this particular compost

had reached a lower degree of maturity and stability

than the others after the period allowed for matura-

tion, even though it showed the highest degree of

degradation during the maturation phase (more than

10% of OM, Table 1). This was because the maize

straw degraded slowly and incompletely during the

Fig. 1. Rate of CO2±C evolution during the incubation of soil (control) and soil amended with samples from SC (a) and PCO (b) mixtures at

different composting times. Similar CO2±C evolution dynamics occurred for the rest of the composting samples studied. Very small error are

not depicted since error bars remained within the symbol.

180 M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189

Table 2

Carbon mineralized from soil amended with several waste mixtures after 70 days of incubation (mg C kgÿ1 soil), and the proportion

mineralized from the different waste mixtures (% of waste TOC) (see Section 2)

Mixtures Cm (mg C kgÿ1 soil) Cm (% of waste TOC)

I T E M I T E M

SC 6012 d 3714 g 2322 ij 2121 jk 62.3 d 37.7 gh 22.4 jk 19.8 k

(342) (319) (349) (300) (0.34) (0.32) (0.35) (0.25)

PCO 6050 d 3848 g 2480 ij 2215 ij 68.2 c 43.8 f 28.6 i 24.3 ij

(224) (224) (34) (9) (3.30) (0.89) (0.52) (0.10)

SCO 6430 c 2467 i 1860 kl 1692 lm 68.9c 20.7 k 13.2 l 11.1 lm

(85) (222) (105) (14) (1.07) (2.74) (1.29) (0.18)

SM 8314 a 6324 cd 3067 h 1997 kl 93.2 a 77.4 b 40.1 g 23.7 ijk

(86) (140) (235) (69) (1.28) (2.33) (4.71) (1.45)

SMO 7116 b 4914 e 4073 f 3533 h 70.3 c 53.0 e 42.6 g 37.9 h

(117) (95) (36) (40) (1.55) (0.72) (0.62) (0.74)

PPB 3858 g n.d. 1977 kl 1847 kl 38.0 h n.d. 14.7 l 13.1 l

(131) (62) (82) (1.62) (0.77) (1.02)

RB 5939 d 5935 mn 1268 n 1368 n 80.1 b 11.6 lm 7.4 lm 9.0 m

(217) (58) (76) (78) (3.38) (0.91) (1.18) (1.21)

Factors Analysis of variance Analysis of variance

Mixture P<0.001 LSD�157.2 P<0.001 LSD�2.18

Stage of compost-

ing

P<0.001 LSD�128.4 P<0.001 LSD�1.78

Interaction P<0.001 LSD�314.4 P<0.001 LSD�4.36

Standard deviation in brackets (n�3).

n.d., not determined.

Values followed by the same letter are not statistically different at P<0.05, according to the least significant difference (LSD).

Fig. 2. Cumulative CO2±C mineralization of samples at different stages of the composting process of the waste mixtures: SC (a), PCO (b),

SCO (c), SM (d), SMO (e), PPB (f) and RB (g). Symbols are experimental data (n�3) and lines represent the curve-fitting result of the

combined kinetic model (Table 3). Very small error are not depicted since error bars remained within the symbol.

M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189 181

composting (Paredes et al., 1996) as a result of its large

particle size. Part of the straw would, therefore, be

physically inaccessible to the microorganisms and

only break down later in the soil after the samples

had been ground for the incubation experiment. Ajwa

and Tabatabai (1994) and Recous et al. (1995) found

that the carbon from maize straw mineralizes more

slowly in soils, than that from other plant wastes,

suggesting that the readily decomposable organic-C

fraction in maize is smaller than in other plant materi-

als. With the exception of SMO-M, the mineralized C

values did not reach 25% of TOC after 70 days of

incubation in any of the mature samples. These experi-

mental values were similar to those obtained by Serra-

Wittling et al. (1995) using a city refuse compost, but

higher than those described by Cheneby and Nicolar-

dot (1992) for a poplar bark-poultry dropping com-

post.

3.2. Mineralization kinetic

The use of kinetic models to describe the carbon

mineralization process makes it possible to ascer-

tain the potentially mineralizable C fraction and the

Fig. 2. (Continued)

182 M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189

mineralization rate. Although the ®rst-order kinetic

model is the most widely used in C mineralization

studies, the ®tting of the present results to this model

resulted in high residual mean square (RMS) values

and the distribution of the deviations was not rando-

mized in any composting sample (data not shown).

The systematic grouping of deviations led the authors

to believe that another equation would describe the

mineralization process better (Little and Hills, 1975).

Indeed, the C mineralization process observed was

best described by combined two step kinetic equa-

tions, which suggests that the organic carbon content

of the wastes was made up of two fractions of different

degree of biodegradability: labile organic compounds

which were rapidly mineralizable in soil, and com-

pounds which were resistant to microbial attack

and which broke down slowly during a second step.

The rapid step always followed a ®rst-order kinetic

model (Table 3), because the presence of available

organic C led to a substantial increase in the soil's

microbial activity. The slow step followed a zero-order

kinetic model in most of the samples studied, except

Fig. 2. (Continued)

M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189 183

SM-I and SMO-I, when both steps ®tted a ®rst-order

kinetic.

The values of rapidly mineralizable C (CR) pointed

to the existence of a large easily degradable C fraction

in the untransformed I samples. The CR values of

all the mixtures fell as the composting progressed

(Table 3), the greatest differences being between those

of the initial samples (I) and those taken during the

thermophilic phase (T). The smallest differences in

both CR and CS values were found between the

samples taken at the end of the active phase (E)

and those which had undergone a period of maturation

(M). The rate constant values (KR) were high in all E

and M samples, which indicated that the ®rst step of C

mineralization was very fast. During a second miner-

alization step rates were practically parallel in both

E and M samples of each mixture, and scant differ-

ences were observed between the values of KS. This

may indicate that both samples had organic com-

pounds of similar decomposability. Therefore, the

Fig. 2. (Continued)

184 M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189

main difference in the mineralization kinetic para-

meters of E and M were found in the CR values

referring to the ®rst days of incubation (Fig. 2).

The rate constants corresponding to the ®rst step

(KR) were generally very high, which re¯ected the

short time required to break down the most labile C

fraction (half life of CR, t(1/2)�0.62±11.63 days).

These KR values were higher than those obtained

by Gale and Gilmour (1986) and Ajwa and Tabatabai

(1994) for the C mineralization of different wastes,

and similar to those calculated by Bernal and Kirch-

mann (1992) for untreated and aerobically and anae-

robically treated pig manure (0.131±0.386 dayÿ1).

Most of the TOC of the mixtures was slowly miner-

alizable (CS), this slow step predominating in the

mineralization of E and M samples in all mixtures

with CS>88% (Table 3). According to the calculated

rate constant (KS), this step was very slow in all

samples. Except in the cases of SM-I and SMO-I,

which ®tted a combined two ®rst-order kinetic equa-

tion, the values for KS were always less than 0.0082

dayÿ1 (Table 3). These results of KS were close to

Table 3

Parameter values of the combined first-zero-order equation model, residual mean square (RMS) and F-values for carbon mineralization of the

mixtures at different times of the composting process

Composting samples CR (% of TOC) KR (dayÿ1) CS (% of TOC) KS (dayÿ1) RMS F

Mixture SC: sewage sludge�cotton waste

SC-I 38.2 (1.0) 0.115 (0.005) 61.8 (1.7) 0.0055 (0.00022) 0.433 19 628

SC-T 22.5 (1.1) 0.085 (0.006) 77.5 (6.6) 0.0029 (0.00025) 0.213 13 996

SC-E 8.4 (0.6) 0.166 (0.024) 91.6 (6.5) 0.0023 (0.00012) 0.275 3508

SC-M 6.5 (0.7) 0.128 (0.027) 93.6 (10.8) 0.0020 (0.00014) 0.266 2538

Mixture PCO: poultry manure�cotton waste�olive-mill wastewater

PCO-I 30.5 (1.4) 0.130 (0.011) 69.6 (3.2) 0.0081 (0.00023) 1.017 9146

PCO-T 15.3 (1.1) 0.151 (0.022) 84.7 (6.0) 0.0050 (0.00019) 0.799 4436

PCO-E 5.5 (0.1) 0.695 (0.060) 94.5 (2.2) 0.0031 (0.00003) 0.050 26 563

PCO-M 5.7 (0.3) 0.462 (0.069) 94.3 (4.5) 0.0029 (0.00006) 0.175 5871

Mixture SCO: sewage sludge�cotton waste�olive-mill wastewater

SCO-I a 48.9 (2.2) 0.120 (0.009) 51.1 (2.3) 0.0057 (0.00058) 1.966 5193

SCO-T 9.8 (0.2) 0.202 (0.010) 90.2 (1.9) 0.0018 (0.00004) 0.043 21 194

SCO-E 4.4 (0.1) 0.351 (0.025) 95.6 (2.4) 0.0013 (0.00002) 0.020 16 002

SCO-M 2.9 (0.1) 0.418 (0.035) 97.1 (2.7) 0.0012 (0.00002) 0.013 16 143

Mixture SM: sewage sludge�maize straw

SM-I b 32.9 (1.2) 0.317 (0.019) 67.1 (2.5) 0.0319 (0.00066) 0.460 45 740

SM-T 46.3 (1.9) 0.147 (0.012) 53.7 (2.2) 0.0088 (0.00040) 2.251 6228

SM-E 10.6 (0.8) 0.250 (0.047) 89.5 (6.7) 0.0050 (0.00015) 0.876 3309

SM-M 3.6 (0.2) 0.795 (0.144) 96.5 (4.5) 0.0030 (0.00004) 0.084 10 489

Mixture SMO: sewage sludge�maize straw�olive-mill wastewater

SMO-I b 20.6 (1.5) 0.260 (0.036) 79.4 (5.6) 0.0148 (0.00049) 0.751 13 831

SMO-T 20.7 (3.7) 0.060 (0.012) 79.3 (14.0) 0.0060 (0.00054) 0.592 8148

SMO-E 11.6 (1.0) 0.132 (0.022) 88.4 (7.8) 0.0051 (0.00017) 0.324 9444

SMO-M 8.6 (1.2) 0.097 (0.021) 91.4 (12.6) 0.0046 (0.00017) 0.205 10 945

Mixture PPB: pig slurry�poultry manure�sweet sorghum bagasse

PPB-I 22.2 (1.6) 0.068 (0.003) 77.8 (3.1) 0.0029 (0.00015) 0.060 46 152

PPB-E 5.3 (0.3) 0.314 (0.042) 94.7 (4.7) 0.0015 (0.00006) 0.107 3962

PPB-M 3.3 (0.1) 0.395 (0.042) 96.7 (3.5) 0.0015 (0.00003) 0.027 11 104

Mixture RB: city refuse�sweet sorghum bagasse

RB-I 55.5 (0.9) 0.153 (0.005) 44.5 (0.7) 0.0082 (0.00026) 0.547 29 471

RB-T 5.4 (0.4) 0.170 (0.024) 94.6 (6.4) 0.0010 (0.00007) 0.099 2848

RB-E 2.9 (0.1) 0.414 (0.060) 97.2 (4.7) 0.0007 (0.00003) 0.037 3095

RB-M 2.8 (0.1) 0.371 (0.044) 97.3 (4.0) 0.0010 (0.00003) 0.023 6526

Standard deviation in brackets (n�14).a n�15b Combined two first-order kinetic equation.

M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189 185

those calculated for the C mineralization of poultry

litter with pine shavings or wheat straw mixtures (Gale

and Gilmour, 1986), but higher than those described

for fresh wastes (Saviozzi et al., 1993; Ajwa and

Tabatabai, 1994), although Saviozzi et al. (1993) used

a different kinetic model. The mean value of KS from

the mature samples (except SMO-M) was 0.0019

dayÿ1, pointing to a t(1/2)�263 days to mineralized

one-half of CS.

3.3. Carbon conservation

To evaluate the effect of different composting stages

on organic carbon conservation, both the mineraliza-

tion which occurs during the composting process and

that occurring after addition to the soil should be

compared, and expressed as a percentage of the initial

TOC concentration of the mixtures. The higher sta-

bility of mature composts in soil suggests that these

materials will increase soil organic matter levels to a

greater extent than untransformed waste mixtures.

However, the amount of material remaining after

composting has also to be taken into account. Because

of mass losses during composting, changes in con-

centration in decomposed materials (Table 1) do not

re¯ect changes in residual amounts. Table 4 gives the

total losses of C during waste composting, in which

the length of each composting phase in the different

mixtures is also expressed. Maximum C degradation

occurred during the thermophilic phase in all mix-

tures, when almost 60% of initial C was mineralized in

the SCO mixture, but only 37.3% of initial C in PCO.

At the end of the active phase C mineralization ranged

between 48.4% of initial C in PPB and 73.8% of initial

C in RB. The lowest C losses occurred during the

maturation phase of composting, the highest value

recorded being 10.7% of initial C in SMO, whereas no

mineralization took place in PCO. Thus, the organic C

lost during the whole composting process ranged from

51.9% of initial C in PCO to 74.2% of initial C in RB.

Because the four samples taken from each mixture

represented different composting time before addition

to the soil, differences in the total decomposition time

had to be equalised in order to compare total C losses

occurring during composting and those occurring

during incubation with soil. Carbon mineralization

in soil was calculated by means of the combined C

mineralization kinetic equations (Table 3) the total

decomposition time (in composting�in soil) being

the same in all samples from each mixture (Table 4).

These C losses taking place in soil were multiplied by

the percentage of C remaining after composting in

order to express them as a percentage of the initial C of

each mixture (Table 4). The C losses in soil when the

untransformed samples were used, were generally

higher than that which had occurred during compost-

ing (except in the case of PPB). The degradation which

took place during composting was therefore less than

that occurring during incubation with soil, because

during the former process the organic matter had also

been stabilizated and humi®ed (Senesi, 1989).

The greatest losses in initial C as measured over the

total decomposition time occurred in the untrans-

formed wastes (I) (except in the case of PPB), and

were statistically different from the losses occurring in

the rest of the samples. The smallest differences in C

loss were found between the E and M samples in each

mixture, and were statistically signi®cant in all the

samples except SCO. The lowest C loss always

occurred in the M samples, according to LSD. There-

fore, composting is the most ef®cient way of stabiliz-

ing the organic C of wastes compared with the

incubation with soil.

When the decomposition time of the wastes was

extended for another 70 days in soil, most of the

untransformed samples (I) showed results close to

100% initial C or larger, which indicated priming

effect in soil. The initial assumption was that total

carbon dioxide released from amended soil should

consist of that CO2 produced from unamended soil as

a result of native soil organic matter oxidation, plus

that resulting from catabolism of the organic waste.

This apparently was not valid when the untransformed

samples were used, because the degradation of the

native soil organic matter was enhanced by the exo-

genously supplied substrate. Signi®cantly higher

values of C loss were found in T samples than in I

samples of the SM and SMO mixtures. The T samples

still contained a great proportion of the original labile

organic matter because they had not been stabilized

during the thermophilic phase of composting. Their

addition to soil leads to a growth of the soil's microbial

population, which would strongly mineralize the

organic C. When mature composts were added to

the soil, a slow C mineralization process started up

again because of the growth of the soil's microbial

186 M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189

population in the presence of a new source of organic

C. The differences in total C losses between the E and

M samples, although still statistically signi®cant, were

reduced when the decomposition time was extended

for another 70 days in soil, except in the case of the

SCO and RB mixtures (Table 4). Although these

results were obtained in disturbed soils in which no

crops were grown, they may indicate that mature

composts show the lowest loss of organic C and,

hence, the greatest degree of C conservation, as a

result of the stabilization of the organic matter during

the maturation phase of composting.

If the main concern is increasing soil organic matter

levels for soil protection, the use of a mature compost

will always be recommended over the slightly trans-

formed wastes or immature composts. In agricultural

Table 4

Losses of CO2±C during the composting process, during decomposition in soil, and total C-losses during both processes and plus 70 days of

incubation with soil

Composting samples In composting In soila Total C lossb (% initial-C)

Time

(days)

CO2±C

(% initial-C)

Time

days)

CO2±C

(% initial-C)

During

total time

During total

time�70 days

Mixture SC: sewage sludge�cotton waste

SC-I 0 0.0 105 73.9 73.9 a 97.7 a

SC-T 21 41.5 84 24.4 65.9 b 74.9 b

SC-E 49 56.8 56 8.7 65.5 b 71.9 c

SC-M 105 57.4 0 0.0 57.4 c 65.8 d

Mixture PCO: poultry manure�cotton waste�olive-mill wastewater

PCO-I 0 0.0 105 89.7 89.7 a >100 a

PCO-T 21 37.3 84 31.9 69.3 b 87.8 b

PCO-E 46 51.9 56 10.6 62.5 c 71.8 c

PCO-M 105 51.8 0 0.0 51.8 d 63.8 d

Mixture SCO: sewage sludge�cotton waste�olive-mill wastewater

SCO-I 0 0.0 140 89.7 89.7 a >100 a

SCO-T 42 58.6 98 10.7 69.3 b 74.0 b

SCO-E 84 67.2 56 3.7 70.9 b 73.8 b

SCO-M 140 67.9 0 0.0 67.9 b 71.5 b

Mixture SM: sewage sludge�maize straw

SM-I 0 0.0 112 98.1 98.1 a 99.8 b

SM-T 21 41.3 91 52.4 93.7 b >100 a

SM-E 56 68.2 56 11.3 79.5 c 89.5 c

SM-M 112 73.1 0 0.0 73.1 d 79.5 d

Mixture SMO: sewage sludge�maize straw�olive-mill wastewater

SMO-I 0 0.0 119 86.4 86.4 a 95.2 b

SMO-T 28 47.0 91 34.0 81.0 b 98.8 a

SMO-E 63 54.9 56 16.6 71.5 c 85.8 c

SMO-M 119 65.6 0 0.0 65.6 d 78.7 d

Mixture PPB: pig slurry�poultry manure�sweet sorghum bagasse

PPB-I 0 0.0 112 47.5 47.5 c 63.3 a

PPB-E 56 48.4 56 6.8 55.2 b 60.4 b

PPB-M 112 58.5 0 0.0 58.5 a 64.1 a

Mixture RB: city refuse�sweet sorghum bagasse

RB-I 0 0.0 133 >100 >100 a >100 a

RB-T 35 53.3 98 6.9 60.2 d 63.4 c

RB-E 77 73.8 56 1.7 75.5 b 76.8 b

RB-M 133 74.2 0 0.0 74.2 c 76.7 b

a Calculated from the equation parameters (Table 3) and refered as precentage of initial TOC.b Total decomposition in composting and soil during the same length in all samples from each mixture (total time�in composting�in soil).

Values greater than 100% may indicate priming effect in soil. Values of total C loss followed by the same letter in samples from the same

mixture are not statistically different at P<0.05 according to LSD.

M.P. Bernal et al. / Agriculture, Ecosystems and Environment 69 (1998) 175±189 187

soils the input of organic matter through roots and crop

residues may be an important effect on soil organic

matter. Then the nitrogen supplied should have a

relevant in¯uence on organic C conservation in agri-

culture. The animal manures have been traditionally

used in soils as the fresh material, because of their high

concentration in nitrogen. If composted without a

bulking agent, their carbon stability will be improved,

but their available nitrogen may decreased (Tyson and

Cabrera, 1993) and high amount of N lost through

NH3-volatilization. From the agricultural point of

view, manures can be directly applied to soil and a

maximum bene®t can be obtained from nitrogen, but

sowing should be delayed to allow the soil micro-

organisms to degrade the labile organic matter and to

avoid any negative effect to plants.

In contrast, immature composts have been demon-

strated to cause N-immobilization in soil (Sims, 1990;

Beloso et al., 1993; Bernal et al., 1998a), and matura-

tion improves the fertilizer value of composts (Bernal

et al., 1998a). The initial material for composting, as

those described here, is a mixture of two or more

wastes in order to obtain an adequate C/N ratio for

composting (about 25, De Bertoldi et al., 1983), which

is greater than the values found in animal manures.

Then for the agricultural use of composts it is neces-

sary to ensure a good degree of compost maturity if the

maximum bene®t for C and N recycling have to be

ensured through composting.

4. Conclusions

The lowest degree of C mineralization in soil

occurred in composts which had undergone a matura-

tion phase. Values of C mineralized higher than 25%

of TOC after 70 days of incubation may indicate a low

degree of compost maturity. The composts made from

slowly degradable wastes, such as maize straw, may

show a high degree of C mineralization in soil because

longer composting times may required for a good

degree of maturation and microbial stability to be

achieved.

The organic C of the wastes is constituted by two

fractions of different degrees of biodegradability. The

labile organic compounds mineralize quickly in soil,

following a ®rst-order kinetic function, and are

reduced during composting. However, the resistant

C fraction mineralizes slowly in soil and usually

follows a zero-order kinetic function, regardless of

the length of composting time. More than 88% of TOC

in the mature composts was slowly mineralizable with

a rate constant ranging from 0.0030 to 0.0010 dayÿ1.

There were only small differences in the slowly

mineralizable C and the rate constant (KS) between

samples taken at the end of the active phase and those

taken after maturation, indicating that the stabilized

organic C compounds resulting from both stages of

composting are of similar microbiological degradabil-

ity.

As regards organic C conservation, the composting

of organic wastes before addition to soil is a more

effective way of reducing CO2±C losses than the direct

application of wastes which are either untreated, or

slightly transformed during the thermophilic phase of

composting. To protect the soil and conserve the

organic carbon content, mature composts with a sta-

bilized organic C are preferable to non-transformed

wastes, which may promote degradation of native soil

organic matter.

Acknowledgements

The authors wish to thank Dr. J.L. Gonzalez-Andu-

jar for his statistical advice, and Mr. P. Thomas for the

English revision. Research was carried out in the

framework of EC contract N8 EVWA-CT 92-0006.

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