You are on page 1of 10

Bioresource Technology 100 (2009) 5444–5453

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Composting of animal manures and chemical criteria for compost maturity


assessment. A review
M.P. Bernal a,*, J.A. Alburquerque a, R. Moral b
a
Department of Soil and Water Conservation and Organic Waste Management, Centro de Edafología y Biología Aplicada del Segura, CSIC, P.O. Box 164, 30100 Murcia, Spain
b
Department of Agrochemistry and Environment, Universidad Miguel Hernández de Elche, EPS-Orihuela, ctra, Beniel Km 3.2, 03312 Orihuela, Alicante, Spain

a r t i c l e i n f o a b s t r a c t

Article history: New livestock production systems, based on intensification in large farms, produce huge amount of man-
Received 10 June 2008 ures and slurries without enough agricultural land for their direct application as fertilisers. Composting is
Received in revised form 7 November 2008 increasingly considered a good way for recycling the surplus of manure as a stabilised and sanitised end-
Accepted 19 November 2008
product for agriculture, and much research work has been carried out in the last decade. However, high
Available online 31 December 2008
quality compost should be produced to overcome the cost of composting.
In order to provide and review the information found in the literature about manure composting, the
Keywords:
first part of this paper explains the basic concepts of the composting process and how manure character-
Animal manure
Composting
istics can influence its performance. Then, a summary of those factors such as nitrogen losses (which
Compost quality directly reduce the nutrient content), organic matter humification and compost maturity which affect
Maturity indices the quality of composts produced by manure composting is presented. Special attention has been paid
Microbial stability to the relevance of using an adequate bulking agent for reducing N-losses and the necessity of standar-
dising the maturity indices due to their great importance amongst compost quality criteria.
Ó 2008 Elsevier Ltd. All rights reserved.

1. Introduction ment strategies it is gaining interest as a suitable option for man-


ures with economic and environmental profits, since this process
Composting of organic wastes is a biooxidative process involv- eliminates or reduces the risk of spreading of pathogens, parasites
ing the mineralisation and partial humification of the organic mat- and weed seeds associated with direct land application of manure
ter, leading to a stabilised final product, free of phytotoxicity and and leads to a final stabilised product which can be used to im-
pathogens and with certain humic properties (Zucconi and de prove and maintain soil quality and fertility (Larney and Hao,
Bertoldi, 1987). During the first phase of the process the simple 2007). Composting of animal manures has been traditionally car-
organic carbon compounds are easily mineralised and metabolised ried out by the farmers after manure collection for better handling,
by the microorganisms, producing CO2, NH3, H2O, organic acids transport and management. Frequently the wastes were heaped up
and heat. The accumulation of this heat raises the temperature of with little regard to control of the process conditions (aeration,
the pile. Composting is a spontaneous biological decomposition temperature, ammonia loss, etc.) and with rudimentary methodol-
process of organic materials in a predominantly aerobic environment. ogy. However, as the fertiliser value of animal manures has been
During the process bacteria, fungi and other microorganisms, always recognised, nowadays their composting is seen as an alter-
including microarthropods, break down organic materials to sta- native way of recycling the manures in farms without enough agri-
ble, usable organic substances called compost. The composting also cultural land for their direct use as a fertiliser. But, the cost of
implies the volume reduction of the wastes, the destruction of composting of animal manures can be considerably higher than
weed seeds and of pathogenic microorganisms. the direct utilisation of raw manures. Therefore, composting is jus-
The intensity and concentrated activity of the livestock industry tified for manures that need to be partially sterilised (Parkinson
generate vast amounts of biodegradable wastes, which must be et al., 2004), and also when compost of high quality is produced,
managed under appropriate disposal practices to avoid a negative to offset the production costs.
impact on the environment (odour and gaseous emissions, soil and The present paper reviews the factors affecting the composting
water pollution, etc.; Burton and Turner, 2003). Composting cannot of animal manures for production of high quality compost with
be considered a new technology, but amongst the waste manage- added agricultural value, focusing on the nutrient content, organic
matter (OM) humification and maturity degree. Complementary
* Corresponding author. Tel.: +34 968 396200; fax: +34 968 396213.
information on safety and environmental aspects related to man-
E-mail address: pbernal@cebas.csic.es (M.P. Bernal). ure composting is reviewed by Moral et al. (2009) in this OECD

0960-8524/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2008.11.027
M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453 5445

special issue, including the suppressive effect against phytopatho- cles has difficult accessibility for the microorganisms, as during
gens of compost and recent techniques to determine the OM humi- decomposition particles may coat the surface with an impenetra-
fication process during composting. ble humified layer (Bernal et al., 1993). However, particles which
are too small can compact the mass, reducing the porosity. These
factors are material specific: particle size and distribution, shape,
2. The basic concepts of the composting process packing and moisture content control the porosity of the compost-
ing mass.
While composting occurs naturally, efficient composting re- Porosity: Substrate porosity exerts a great influence on com-
quires the control of several factors to avoid nuisance problems posting performance since appropriate conditions of the physical
such as odours and dust, and also for obtaining a quality agricul- environment for air distribution must be maintained during the
tural product. The controlled conditions are basic for a composting process. Porosity greater than 50% causes the pile to remain at a
procedure, distinguishing it from aerobic fermentation. Over the low temperature because energy lost exceeds heat produced. Too
last decades, research has been focused on the study of the com- little porosity leads to anaerobic conditions and odour generation.
plex interaction amongst physical, chemical and biological factors The percentage air-filled pore space of composting piles should be
that occurs during composting. Therefore, the control of parame- in the range of 35–50%.
ters such as bulk density, porosity, particle size, nutrient content, Aeration: Aeration is a key factor for composting. Proper aera-
C/N ratio, temperature, pH, moisture and oxygen supply have dem- tion controls the temperature, removes excess moisture and CO2
onstrated to be key for composting optimisation since they deter- and provides O2 for the biological processes. The optimum O2 con-
mine the optimal conditions for microbial development and OM centration is between 15% and 20% (Miller, 1992). Controlled aer-
degradation (Agnew and Leonard, 2003; Das and Keener, 1997; ation should maintain temperatures below 60–65 °C, which
de Bertoldi et al., 1983; Haug, 1993; Miller, 1992; Richard et al., ensures enough O2 is supplied (Finstein and Miller, 1985).
2002). Composting optimisation involves the definition of ade- Moisture: The optimum water content for composting varies
quate initial substrate conditions that must be controlled and with the waste to be composted, but generally the mixture should
maintained as composting progresses. Although it is difficult to be at 50–60% (Gajalakshmi and Abbasi, 2008). When the moisture
generalise for all type of substrates and management conditions, content exceeds 60% O2 movement is inhibited and the process
the basic and applied aspects of composting have been summa- tends to become anaerobic (Das and Keener, 1997). During com-
rised in this section. For a particular composting formulation, spe- posting a large quantity of water can evaporate, to control temper-
cific references can be found. ature, and as water content diminishes the rate of decomposition
The factors affecting the composting process can be divided into decreases, then rewetting should be required in order to maintain
two groups: those depending on the formulation of the composting the optimum moisture content for the microbial activity.
mix, such as nutrient balance, pH, particle size, porosity and mois- Temperature: The temperature pattern shows the microbial
ture; and those dependent on the process management, such as O2 activity and the occurrence of the composting process. The opti-
concentration, temperature and water content. Nutritional balance mum temperature range for composting is 40–65 °C (de Bertoldi
is mainly defined by the C/N ratio. Microorganisms require an en- et al., 1983), temperatures above 55 °C are required to kill patho-
ergy source (degradable organic-C) and N for their development genic microorganisms. But if the temperature achieved exceeds
and activity. The adequate C/N ratio for composting is in the range the tolerance range of the thermophilic decomposers, the effect
25–35, because it is considered that the microorganisms require 30 is damaging for composting. At temperatures above 63 °C, micro-
parts of C per unit of N (Bishop and Godfrey, 1983). High C/N ratios bial activity declines rapidly as the optimum for various thermo-
make the process very slow as there is an excess of degradable sub- philes is surpassed, with activity approaching low values at
strate for the microorganisms. But with a low C/N ratio there is an 72 °C. The range of 52–60 °C is the most favourable for decomposi-
excess of N per degradable C and inorganic N is produced in excess tion (Miller, 1992). The regulation of the temperature is required
and can be lost by ammonia volatilisation or by leaching from the for controlled composting. Excess heat removal can be achieved
composting mass. Then, low C/N ratios can be corrected by adding through several strategies (Miller, 1992): control the size and
a bulking agent to provide degradable organic-C. shape of the composting mass; improve cooling and favourable
pH: A pH of 6.7–9.0 supports good microbial activity during temperature redistribution by turning operations, which means
composting. Optimum values are between 5.5 and 8.0 (de Bertoldi heat removal through evaporation cooling; and achieve superior
et al., 1983; Miller, 1992). Usually pH is not a key factor for com- temperature control in systems that actively remove heat through
posting since most materials are within this pH range. However, temperature feedback-controlled ventilation (Rutgers strategy).
this factor is very relevant for controlling N-losses by ammonia The development of the temperature profile indicates the differ-
volatilisation, which can be particularly high at pH >7.5. Elemental ent phases of the process. In general, the composting process can
sulphur (So) has been used as an amendment for avoiding exces- be divided into two main phases: the biooxidative phase and the
sively high pH values during composting (Mari et al., 2005). maturing phase also called the curing phase (Bernal et al., 1996;
Microorganisms: OM decomposition is carried out by many dif- Chen and Inbar, 1993). The biooxidative phase is developed in
ferent groups of microbial populations (Ryckeboer et al., 2003). The three steps (Keener et al., 2000): (i) an initial mesophilic phase
microorganisms involved in composting develop according to the lasting 1–3 days, where mesophilic bacteria and fungi degrade
temperature of the mass, which defines the different steps of the simple compounds such as sugars, amino acids, proteins, etc.,
process (Keener et al., 2000). Bacteria predominate early in com- increasing quickly the temperature; (ii) thermophilic phase, where
posting, fungi are present during all the process but predominate thermophilic microorganisms degrade fats, cellulose, hemicellu-
at water levels below 35% and are not active at temperatures lose and some lignin, during this phase the maximum degradation
>60 °C. Actinomycetes predominate during stabilisation and cur- of the OM occurs together with the destruction of pathogens; (iii)
ing, and together with fungi are able to degrade resistant polymers. cooling phase, characterised by a decrease of the temperature due
Particle size and distribution are critical for balancing the sur- to the reduction of the microbial activity associated with the deple-
face area for growth of microorganisms and the maintenance of tion of degradable organic substrates, the composting mass is re-
adequate porosity for aeration. The larger the particle size, the low- colonised by mesophilic microorganisms which are able to degrade
er the surface area to mass ratio. So compost with large particles the remaining sugars, cellulose and hemicellulose. During the dif-
does not decompose adequately because the interior of the parti- ferent steps of the biodegradation phase, the organic compounds
5446 M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453

are degraded to CO2 and NH3, with the consumption of O2. How- The addition of a bulking agent for manure composting opti-
ever, during the maturation phase stabilisation and humification mises substrate properties such as air space, moisture content, C/
of the OM occur, producing a mature compost with humic charac- N ratio, particle density, pH and mechanical structure, affecting
teristics in its OM. Thus, compost can be defined as the stabilised positively the decomposition rate. In this sense, lignocellulosic
and sanitised product of composting, which has undergone an ini- agricultural and forestry by-products are commonly used as bul-
tial, rapid stage of decomposition, is beneficial to plant growth and king agents in co-composting of nitrogen-rich wastes, such as ani-
has certain humic characteristics, making the composting of waste mal manures. The most generally used materials are cereal straw
a key issue for sustainable agriculture and resource management (Barrington et al., 2002; Bernal et al., 1993; Martins and Dewes,
(Gajalakshmi and Abbasi, 2008; Haug, 1993; Jakobsen, 1995; Zuc- 1992; Petric and Selimbasić, 2008; Wang et al., 2004), cotton waste
coni and de Bertoldi, 1987). (Paredes et al., 1996), hay (Barrington et al., 2002) and wood by-
products such as pine shavings, chestnut burr and leaves and saw-
3. Characteristics of the animal manures for composting dust (Ahn et al., 2007; Barrington et al., 2002; Guerra-Rodríguez
et al., 2001; Huang et al., 2004; Tiquia and Tam, 2002; Wang
Controlled composting allows the safe storage and transport of et al., 2004). All have low moisture and high organic-C contents
the final product, adds value to the product because compost is a and high C/N ratios (an average of 50 for cereal straw and >80
more concentrated and uniform product than the manure, permits for wood by-products), which can compensate for the low values
easy spreading and thus uniform distribution in the soil and results of the animal manures.
in an absence of pathogens and weed seeds. The compost also can
be used as a fertiliser for pots and as a basis for soil-less substrates.
4. Strategies for producing high quality compost: nutrient
The advantages of composting animal manures compared with di-
content and OM humification
rect application can be summarised in:
The effectiveness of compost with regard to beneficial effects on
– Elimination of pathogens and weeds.
soil physical, chemical and biological properties, as well as consti-
– Microbial stabilisation.
tuting a nutrient source, depends on the quality of the compost.
– Reduction of volume and moisture.
The quality criteria for compost are established in terms of: nutri-
– Removal and control of odours.
ent content, humified and stabilised OM, the maturity degree, the
– Ease of storage, transport and use.
hygienisation and the presence of certain toxic compounds such as
– Production of good quality fertiliser or substrate.
heavy metals, soluble salts and xenobiotics. The first three factors
are reviewed in the present paper, while those related to safety and
However the disadvantages are derived from:
environmental aspects are reviewed by Moral et al. (2009) in this
OECD special issue. The production of compost with a high nutrient
– Cost of installation and management.
content requires the control and reduction of nutrient losses dur-
– Requirement for a bulking agent.
ing the process, whilst to ensure a high degree of OM humification
– Requirement for large areas for storage and operation.
enough time should be allowed for the maturation phase. Finally, a
high degree of compost maturity requires the establishment of
Then, composting of animal manures should be seen as a tech-
adequate maturity indices.
nology which adds value, producing a high quality product for
multiple agricultural uses.
Certain chemical characteristics of the animal manures are not 4.1. Organic matter degradation and nitrogen losses
adequate for composting and could limit the efficiency of the pro-
cess: excess of moisture, low porosity, high N concentration for the During the active phase of the composting process the organic-
organic-C, which gives a low C/N ratio, and in some cases high pH C decreases in the material due to decomposition of the OM by the
values (Table 1). Thus, adequate composting management of the microorganisms. This loss of OM reduces the weight of the pile and
manure is required in order to obtain a quality compost. Therefore, decreases the C/N ratio. The degradation rate of the OM decreases
different aeration strategies, substrate conditioning-feedstock for- gradually as composting progresses because of the reduction in
mulation, bulking agents and process control options have been available carbon sources, and synthesis reactions of new complex
used in manure composting in order to reduce composting time and polymerised organic compounds (humification) prevail over
and costs and enhance the quality of the end-products (Lau et al., mineralisation during the maturation phase. This process leads to
1992; Michel et al., 2004; Solano et al., 2001). stabilised end-products which act as slow-release fertilisers for
agricultural purposes. However, the major concern of manure com-
posting is to control C and N-losses since they reduce the agro-
nomic value of compost and contribute to greenhouse gas
Table 1 emissions (Hao et al., 2004).
Average composition of animal slurry and manure (g/kg fresh weight; Amon et al.,
The degradation of the OM during composting can be estimated
2006; Bernal, 1990; Burton and Turner, 2003; Huang et al., 2004; Mathur et al., 1990;
Menoyo, 1995). as a dry matter loss (Garrison et al., 2001; Parkinson et al., 2004), as
an OM loss, or as an organic-C loss (Table 2). Whatever the param-
Dry matter Organic-C Total-N NH4-N pH
eter used, it should be calculated as a mass balance, taking into ac-
Liquid manure/slurry count the dry weight reduction of the pile, instead of only the
Cattle 15–123 3.8–36 2.0–7.0 1.0–4.9 7.1–8.4
difference in concentration of OM or organic-C in the composting
Pig 4.9–152 1.0–65 0.6–7.8 0.3–6.6 6.7–8.9
Poultry 10–367 11–112 2–21 1.9–9.4 7.9–8.8
mass.
Solid manure During the composting process, substrate transformation is
Cattle 140–300 65–126a 4.2–8.1 0.3–2.0 8.6b conditioned by the nature of the OM according to its degradability
Pig 150–330 42–132a 3.5–11 0.5–6.0 8.1b (Haug, 1993), this property affecting decomposition rate, gas emis-
Poultry 220–700 103–597a 10–58 2.4–18 7.6b
sions, duration and extent of the process and oxygen requirements.
a
Bernal, personal communication. Labile organic compounds, such as simple carbohydrates, fats and
b
Average values. amino acids, are degraded quickly in the first stage of composting;
M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453 5447

Table 2
Organic matter and organic-C losses by mineralisation and N-losses during composting of animal manures.

Manure type Bulking agent Composting OM loss by mineralisation (% of N-loss (% of initial Reference
process initial OM) total-N)
Beef manure – Turned Organic-C: 45–62 19–43 Eghball et al.
windrow (1997)
Beef manure Fresh straw-bedded Turned Organic-C: 53 42 Hao et al. (2004)
Woodchip-bedded windrow Organic-C: 35 12
Beef manure – Turned Organic-C: 67 46 Larney et al.
windrow (2006)
Dairy manure Sawdust and wood shavings Turned OM: 67 Organic-C: 63a 5a Changa et al.
Wheat straw windrow OM: 67 Organic-C: 64ª Absenta (2003)
Dairy manure Hardwood sawdust Turned OM: 46–76 7–26 Michel et al.
Wheat straw windrow OM: 58–81 15–43 (2004)
Dairy manure Wheat straw additives: molasses, office paper, In-vessel OM: 29–55a 12–25 Liang et al. (2006)
and buffer solutions system
Poultry manure Cotton gin waste Rutgers static OM: 53 Organic-C: 52 26 Paredes et al.
pile (1996)
Poultry litter – Forced- OM: 9 58 Tiquia and Tam
ventilation (2002)
Pig slurry + Poultry Sweet sorghum bagasse Rutgers static OM: 62 <40 Bernal et al.
manure pile (1996)
Pig manure (partially decomposed with cornstalk) Turned Organic-C: 50–72 3–59 Tiquia et al.
windrow (2000)
Unturned Organic-C: 30–54 8–60
windrow
a
Pig manure Shredded wood pallets and sawdust Turned OM: 55 Organic-C: 52 43a Changa et al.
windrow (2003)
a
OM, organic-C and/or N-losses were calculated from initial (X1) and final (X2) ash contents according to the equations (Paredes et al., 1996): OM loss
(%) = 100  100[X1(100X2)]/[X2(100X1)] and organic-C or N-loss (%) = 100100[(X1Y2)/(X2Y1)], where Y1 and Y2 are the initial and the final total organic-C or total-N
concentrations, respectively.

other, more resistant organic substrates such as cellulose, hemicel- López-Real, 1988). Nitrification, detected by the formation of
lulose and lignin are partially degraded and transformed at a lower NO3-N, occurs when the temperature falls below thermophilic val-
rate. Therefore, composting involves a partial mineralisation of the ues (40 °C), the intensity of the process depending on the amount
organic substrate, leading to carbon losses throughout the process; of NH4-N available to the nitrifying bacteria (Tiquia, 2002). Most of
this is compensated by the higher stabilisation degree of the the nitrification occurs during maturation, leading to a low NH4-N/
remaining organic compounds. NO3-N ratio in mature compost (Bernal et al., 1998a).
During composting of animal manures organic-C losses can Nitrogen losses impact negatively on the manure composting
reach 67% in cattle manure, 52% in poultry manure and 72% in process, by decreasing nutrient concentration and hence compost
pig manure (Table 2). The composting system and conditions, char- quality, and generate health and environmental problems. Nitro-
acteristics of both the bedding material and the bulking agent gen losses through composting can occur by NH3-volatilisation,
added for composting and even the environmental conditions of leaching and denitrification. Denitrification can occur as a result
the season (winter or summer; Parkinson et al., 2004) have a great of the development of anaerobic microsites within the material.
influence on the mineralisation of the OM during composting (Ta- Thus, the aerobic conditions of the compost should be ensured
ble 2). For instance, the use of woodchips instead of cereal straw as throughout the process. Parkinson et al. (2004) indicated that
bedding material in beef manure reduced the organic-C loss during emission rates of N2O–N were very much lower (about 10 times)
composting (Hao et al., 2004) due to the combination of larger par- than those of NH3–N during composting of cattle manure with
ticle size, higher C/N ratio and the recalcitrant nature of the wood- wheat straw. Similar results were found by Martins and Dewes
chips. Similar results were shown by Hansen et al. (1989) and (1992) during composting of animal slurries with straw in a com-
Michel et al. (2004) in composting of poultry manure and cow poster, with NOx <5%. Losses by leaching can be reduced easily by
manure, respectively; they obtained a lower decomposition of controlling the moisture content of the pile and by an adequate
the composting substrate when employing amendment materials composting system, designing the installation with an adequate
with recalcitrant OM such as lignin. cover from the rain and a system for leachate collection and recir-
As a result of the dry weight loss of the material during com- culation within the same compost. The losses as NH4-N can be par-
posting, the concentration of mineral elements increases, if leach- ticularly relevant at the beginning of the process (Martins and
ing does not occur or is controlled to a minimum. Generally the Dewes, 1992) and as NO3-N in the last phase of composting, when
total N concentration increases during composting due to the con- the nitrification occurs (Parkinson et al., 2004), since nitrate is a
centration effect (Bernal et al., 1996; Paredes et al., 1996). The evo- very mobile anion, highly soluble. The lack of leachate collection
lution of N forms shows the mineralisation of the organic can imply a risk of nitrate contamination of the groundwater.
compounds during the active phase of composting with the forma- Therefore, most N-losses during composting of animal manures
tion of NH4-N. Thus, the highest NH4-N concentration occurs dur- have been found to be due to ammonia volatilisation (Eghball et al.,
ing the thermophilic phase, but the concentration quickly declines 1997; Martins and Dewes, 1992; Paillat et al., 2005; Parkinson
as the process progresses. In the thermophilic phase, OM degrada- et al., 2004). High N-losses occur in manure composting due to
tion (NH4-N production) and aeration demand are at their maxima, the high initial NH4-N concentration and the presence of easily
pH is usually >7.5 and nitrification hardly occurs because the high mineralisable compounds, such as uric acid in poultry manure
temperatures inhibit the action of the microorganisms responsible and slurry. Martins and Dewes (1992) found that during compost-
for the process (de Bertoldi et al., 1983; Tiquia, 2002). All these ing of animal slurry with straw NH3-emissions decreased in the or-
conditions favour NH3-volatilisation (Tiquia, 2002; Witter and der: poultry (77%) > pig (54%) > cattle (47%). As shown in Table 2,
5448 M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453

nitrogen losses can reach 60% of initial N for pig manure, up to 58% and losses of 4.5% with passive and forced aeration, respectively.
for poultry manure and up to 46% for cattle manure. Parkinson et al. (2004) found that increasing the number of turns
The main factors conditioning NH3-volatilisation are those from 1 to 3 increased the ammonia-N losses during composting
implicated in the reactions involved in the following processes: of cattle manure, these being 11% and 18% of initial total-N, respec-
formation of NHþ 4 in the compost, its deprotonation for NH3 forma- tively. The system used for turning operations also had a high
tion, conversion of ammonia in solution in the compost into influence on ammonia losses. Turning by a rear-discharge manure
ammonia gas and transfer of ammonia in the gas phase of the com- spreader instead of with a front-end loader increased N-losses to
post to the atmosphere 17% and 51% of initial total-N for the 1- and 3-turning-time treat-
ments, respectively. The Rutgers static pile composting system
NHþ4 ðcompostÞ $ NH3 ðcompostÞ þ Hþ $ NH3ðgasÞ $ NH3 ðatmosphereÞ maintains a temperature ceiling in the pile, providing a high
decomposition rate through the on-demand removal of heat by
Therefore, the main factors controlling NH3-losses are the com- ventilation, since high temperatures inhibit and slow down
position of the initial mixture, such as total-N, C/N ratio, degrad- decomposition due to a reduction of microbial activity (Finstein
able organic-C and particle size, and the composting conditions, et al., 1985). This system has been shown to be a good method
such as temperature and turning frequency (composting system). for lowering N-losses through NH3-volatilisation and hence for
These are reviewed in the following paragraphs. producing a N-rich compost with high concentrations of NO3-N
Eghball et al. (1997) associated most of the N-losses during cat- and total-N (Sánchez-Monedero et al., 1996).
tle manure composting with ammonia volatilisation (>92%), this As composting progresses, stable N compounds are formed,
being conditioned by the C/N ratio, turning frequency and particle which are less susceptible to volatilisation, denitrification and
size of the bulking agent. Also, Barrington et al. (2002) noted the leaching. Therefore, stabilised materials such as composts seem
importance of particle size as a factor affecting carbon availability to constitute a better source of OM and nitrogen for the soil, from
and hence N immobilisation by microorganisms during compost- an agricultural point of view (Pare et al., 1998).
ing. Martins and Dewes (1992) identified initial nitrogen content, When a comparison among manure management options is
temperature, high pH (>8) and turning as the main factors which established, composting leads to higher C and N-losses compared
affected gaseous emissions during composting of slurries. As the to stockpiling or a direct application to soil (Larney et al., 2006).
oxygen supply into the composting mass controls important pro- However, composting also transforms the OM into a more stable,
cesses such as biodegradation, ammonification and nitrification, sanitised and partially humified end-product compared to fresh
then the aeration rate exerts an important influence on nitrogen manure and compost will increase the soil OM to a greater extent
dynamics (Guardia et al., 2008). than untransformed wastes (Bernal et al., 1998b). Therefore, for C-
The addition of carbon sources to wastes rich in inorganic-N can conservation, the losses occurring during composting and those
result in its partial incorporation into the organic fractions or its occurring after soil application should be considered. According
immobilisation to form such fractions. During composting of pig to the results of Bernal et al. (1998b) the addition of mature com-
slurry and wheat straw initial immobilisation of NH4-N was found post to soil is more favourable from the viewpoint of C-conserva-
by Bernal et al. (1993). The impact of N immobilisation by the tion in the system, reducing C-losses in comparison with the use
microbial biomass on NH3-volatilisation was highlighted by Paillat of fresh wastes. In addition, nutrients in composted materials are
et al. (2005) in composting experiments with pig manure and slur- less susceptible to losses by leaching and volatilisation, and com-
ry. They noted that nitrogen immobilisation by the microbial bio- posting also avoids the spreading of pathogens.
mass depends on carbon biodegradability and hence factors such
as oxygen (free air space), moisture and C and N biodegradability 4.2. Humification process
affect gaseous emissions. They concluded that reduced NH3 emis-
sion implies active immobilisation of the NH4-N by the microbial The humified fraction of the soil OM is the most important one
biomass and that the presence of the less biodegradable organic- responsible for organic fertility functions in the soil as it is the frac-
C in sawdust increased NH3 emission, which was decreased by tion most resistant to microbial degradation. So the evaluation of
increasing the ratio of wheat straw in manure composting. During the humification degree of the OM during composting is an agro-
composting of dairy manure and wheat straw, the addition of a nomic criterion for compost quality. The agricultural value of a
readily available carbon source such as molasses greatly reduced compost increases when the OM reaches a high level of humifica-
ammonia losses, while no significant reduction occurred when car- tion. The humification of the OM during composting is revealed by
bon was hardly degradable, for example when supplied as office the formation of humic acids with increasing molecular weight,
paper (Liang et al., 2006). Therefore, amending materials rich in aromatic characteristics, oxygen and nitrogen concentrations and
available carbon can reduce nitrogen losses during the composting functional groups, in agreement with the generally accepted humi-
of organic wastes with a high nitrogen concentration. So, for effec- fication theories of soil OM (Senesi, 1989). During composting, hu-
tive composting to obtain a high quality compost, the selection of mic substances (alkali-extractable organic-C, CEX) are produced
the bulking agent is essential. Paredes et al. (1996) found that and humic acid-like organic-C (CHA) increases, while fulvic acid-
changing the bulking agent from cotton waste to maize straw de- like organic-C (CFA) and water-extractable organic-C decrease due
creased OM degradation, organic-N mineralisation and therefore to microbial degradation. Some indices used for evaluation of the
NH3-losses in sewage sludge composting. Mahimairaja et al. humification level in the material during composting include
(1994) found a N-loss of only 11.2% during 12 weeks of composting (Roletto et al., 1985; Senesi, 1989):
of poultry manure and maize straw, while the losses accounted for
25.5% of total-N in composting of poultry manure and cotton waste – Humification ratio (HR): CEX/Corg  100;
(Paredes et al., 1996). – Humification index (HI): CHA/Corg  100;
The loss of nitrogen from compost piles also depends on the dif- – Percent of humic acids (PHA): CHA/CEX  100;
fusion of NH3 through the pile into the atmosphere, and frequent – Polymerisation index (PI): CHA/CFA.
turning of the pile facilitates this NH3-volatilisation (de Bertoldi
et al., 1982). Solano et al. (2001) found that during composting of The increase of such parameters during composting is indica-
sheep manure and barley straw, total-N losses were higher than tive of the humification of the OM. Roletto et al. (1985) used these
25% in a pile managed with turning in comparison with no losses parameters to establish the humification level of the OM of com-
M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453 5449

posts from different origins, including farmyard manure. The limit Stability refers to a specific stage or decomposition or state of
established were: HR P 7.0; HI P 3.5; PHA P 50; and PI P 1.0. A OM during composting, which is related to the types of organic
new humification index was developed by Sequi et al. (1986) based compounds remaining and the resultant biological activity in the
on the assumption that non-humic compounds can be co-extracted material (California Compost Quality Council, 2001). Several defi-
with the humic substances during the alkaline extraction proce- nitions for compost stability have been used: Bernal et al.
dure. Thus, the new humification index was defined as the ratio (1998a) related stability to compost microbial activity; The UK
of non-humic substances to humic substances: CNH/(CHA + CFA) Composting Association (2001) defined stability as ‘the degree of
<1.0, for a good degree of humification. biological decomposition that composting feedstocks have
The most appropriate and reliable approach to the evaluation of achieved’; Hue and Liu (1995) related stability to microbial activity
the humic character and behaviour of the compost is based on the and hence the potential for unpleasant odour generation.
identification of the chemical and structural composition and func- Maturity is the degree or level of completeness of composting
tional properties, also in comparison with those of humic sub- and implies improved qualities resulting from ‘ageing’ or ‘curing’
stances from native soil. Numerous chemical, physico-chemical of a product. The California Compost Quality Council (CCQC,
and spectroscopic methods have been used, such as (Senesi, 2001) defined maturity as ‘the degree or level of completeness of
1989): elemental and functional group composition, ratio of absor- composting’, and the UK Composting Association (2001) defined
bances measured at 465 and 665 nm (E4/E6), molecular weight dis- maturity simply as ‘the degree to which a compost has matured’,
tribution, electrophoresis and electrofocusing, pyrolysis-gas and mature compost as ‘compost that does not have a negative af-
chromatography–mass spectrometry (GC–MS), infrared and Fou- fect on seed germination or plant growth’. Bernal et al. (1998a) de-
rier transformed-infrared (FT-IR) spectroscopy, electron spin reso- scribed maturity as implying ‘a stable OM content and the absence
nance (ESR) spectroscopy and fluorescence spectroscopy (Moral of phytotoxic compounds and plant or animal pathogens’. Similar
et al., 2009, in this special issue). Amongst these methods, ad- definitions were used by Chen and Inbar (1993), Iannotti et al.
vanced techniques such as NMR, FT-IR and pyrolysis have been (1993) and Hue and Liu (1995). Immature and poorly stabilised
employed to achieve a better understanding of the structural composts may pose a number of problems during storage, market-
changes of the OM during composting and hence to evaluate com- ing and use. During storage these materials may develop anaerobic
posting efficiency and compost maturity; this was reviewed thor- ‘‘pockets” which can lead to odours and the development of toxic
oughly by Chen (2003). Functional group analysis is the most compounds. Continued active decomposition when these materials
sensitive method for studying the changes produced in the humic are added to soil or growth media may have negative impacts on
acid structure, compared to other methods such as elemental anal- plant growth due to a decreased supply of oxygen and/or available
ysis, gel permeation chromatography and infrared spectroscopy. nitrogen or the presence of phytotoxic compounds.
The composting process yields humic acids with chemical and Maturity is not described by a single property and therefore
structural characteristics where similar to those of the more humi- maturity is best assessed by measuring two or more parameters
fied soil humic acids (Sánchez-Monedero et al., 2002). of compost. Maturity is, in part, affected by the relative stability
of the material but also describes the impact of other compost
5. Maturity assessment for quality compost chemical properties on plant development. Some immature com-
posts may contain high amounts of free ammonia, certain organic
The principal requirement of a compost for it to be safely used acids or other water-soluble compounds which can limit seed ger-
in soil is a high degree of stability or maturity, which implies a sta- mination and root development. All uses of compost require a ma-
ble OM content and the absence of phytotoxic compounds and ture product free of these potentially phytotoxic components. A
plant or animal pathogens. Maturity is associated with plant- number of criteria and parameters have been proposed for testing
growth potential or phytotoxicity (Iannotti et al., 1993), whereas compost maturity, although most of them refer to composts made
stability is often related to the compost’s microbial activity. How- from city refuse. Maturity parameters are based on different prop-
ever, both stability and maturity usually go hand in hand, since erties: physical, chemical and biological, including microbial activ-
phytotoxic compounds are produced by the microorganisms in ity (Table 3).
unstable composts (Zucconi et al., 1985). Physical characteristics such as colour, odour and temperature
Compost maturity and stability are often used interchangeably. give a general idea of the decomposition stage reached, but give lit-
However, they each refer to specific properties of these materials. tle information as regards the degree of maturation. Chemical

Table 3
Current criteria evaluated in the literature to characterise compost quality.

Physical: Odour, colour, temperature, particle size and inert materials


Chemical: Carbon and nitrogen – C/N ratio in solid and water extract
analyses
Cation exchange – CEC, CEC/total organic-C ratio, etc.
capacity
Water-soluble extract – pH, EC, organic-C, ions, etc.
Mineral nitrogen – NH4-N content, NH4-N/NO3-N ratio
Pollutants – Heavy metals and organics.
Organic matter quality, – Organic composition: lignin, complex carbohydrates, lipids, sugars, etc.
humification – Humification indices and humic-like substances characterisation: elemental and functional group analyses, molecular
weight distribution, E4/E6 ratio, pyrolysis GC-MS, spectroscopic analyses (NMR and FTIR, Fluorescence, etc.), etc.
Biological: Microbial activity – Respiration (O2 uptake/consumption, CO2 production, self-heating test, biodegradable constituents)
indicators: – Enzyme activity (phosphatases, dehydrogenases, proteases, etc.)
– ATP content
– Nitrogen mineralisation–immobilisation potential, nitrification, etc.
– Microbial biomass
Phytotoxicity: – Germination and plant growth tests
Others: – Viable weed seed, pathogen and ecotoxicity tests
5450 M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453

methods are widely used, including measurement of the C/N ratio cation ratio, humification index, percent of humic acid, humic acid
in the solid phase (Bernal et al., 1998a; Iglesias-Jimenez and Perez- to fulvic acid ratio and the chemical, physico-chemical and spec-
Garcia, 1992) and in the water extract (Chanyasak and Kubota, troscopic characterisation of humic-like substances. Iglesias-Jime-
1981; Hue and Liu, 1995), water soluble organic-C (Bernal et al., nez and Perez-Garcia (1992) established maturity indices based
1998a; Hue and Liu, 1995; Zmora-Nahum et al., 2005), the water on the humification level of the OM for city refuse compost. Hue
soluble organic-C/total organic-N ratio (Bernal et al., 1998a; Hue and Liu (1995) proposed a CFA content of 612.5 g/kg, a
and Liu, 1995), volatile organic acids (Iannotti et al., 1994; Manios CEX 660 g/kg and a CEX/water-soluble organic-C ratio P6.0, for ma-
et al., 1989), nitrification (NH4-N concentration and NH4-N/NO3-N ture composts of different origin (Table 4). However, these humifi-
ratio; Bernal et al., 1998a; Finstein and Miller, 1985; Zucconi and cation parameters are not useful for indicating maturity in all kinds
de Bertoldi, 1987), cation exchange capacity (CEC) (Harada and of compost (Bernal et al., 1998a; Paredes et al., 2000), since the fi-
Inoko, 1980) and the degree of OM humification (de Nobili and Pet- nal values of the humic acid content, humic to fulvic acid ratio and
russi, 1988; Iglesias-Jimenez and Perez-Garcia, 1992). Also, the humification index depend on the origin of the waste used for
presence of phytotoxic substances such as phenolic acids and vol- composting. Their evolution during composting reveals the humi-
atile fatty acids (Kirchmann and Widen, 1994) may indicate imma- fication process of the OM but a limit value cannot be fixed for
ture composts. expressing compost maturity. The humification process produces
Composting is a biochemical transformation of OM by microor- functional groups, and so increased oxidation of the OM leads to
ganisms whose metabolism occurs in the water-soluble phase. a rise in CEC, for which reason this parameter has been used to
Therefore, a study of the changes occurring in the soluble OM evaluate the maturity of city refuse compost (>60 meq/100 g, Hara-
can be useful for assessing compost maturity. A water soluble or- da and Inoko, 1980; 67 meq/100 g, Iglesias-Jimenez and Perez-Gar-
ganic-C/organic-N ratio of 5–6 was established by Chanyasak and cia, 1992). However, these values cannot be used in compost from
Kubota (1981) as an essential indicator of compost maturity (Table wastes such as animal manures, since the limit can be reached in
4). However, this ratio is sometimes difficult to evaluate since the the wastes before composting (Bernal et al., 1996; Bernal et al.,
concentration of organic-N in the water extract of mature samples 1998a; Paredes et al., 2000).
is usually very low. For this reason, Hue and Liu (1995) and Bernal The maturity of a compost can be assessed by its microbial sta-
et al. (1998a) suggested using the water soluble organic-C/total or- bility, by determining microbial activity factors such as the micro-
ganic-N ratio as a parameter for assessing compost maturity. Dis- bial biomass count and its metabolic activity, and by the
solved organic carbon is the most active fraction of carbon and is concentration of easily biodegradable constituents. The aerobic
indicative of compost stability (Wu et al., 2000). Bernal et al. respiration rate was previously selected as the most suitable
(1998a) established a limit of water-soluble organic-C <1.7% to de- parameter to assess aerobic biological activity and hence stability.
scribe mature composts produced from a wide range of wastes, In aerobic conditions, one carbon atom derived from catabolism is
including animal manures, while 1.0 and 0.4% were set by Hue attached to two oxygen atoms to form carbon dioxide, releasing
and Liu (1995) and Zmora-Nahum et al. (2005), respectively. energy, including heat, in the process. Therefore, respiration can
Compost maturity can also be defined in terms of nitrification. be measured in several ways: carbon dioxide evolution, oxygen
When the NH4-N concentration decreases and NO3-N appears in consumption and self-heating, which are indicative of the amount
the composting material it is considered ready to be used as a of degradable OM still present and which are related inversely to
compost (Finstein and Miller, 1985). A high level of NH4-N stabilisation (Zucconi and de Bertoldi, 1987). Self-heating uses
indicates unstabilised material, leading Zucconi and de Bertoldi the Dewar flask method and actually measures temperature rises
(1987) to establish a limit of 0.04% for mature city refuse compost. due to all exothermic biological and chemical activity, so it is not
An NH4-N/NO3-N ratio lower than 0.16 was established by strictly a true measure of respiration, because many biological
Bernal et al. (1998a) as a maturity index for composts of all origins and chemical reactions not connected to respiration are exother-
(Table 4). mic. An insufficiently mature compost has a strong demand for
Since maturation also implies the formation of some humic-like O2 and high CO2 production rates, due to intense development of
substances, the degree of OM humification is generally accepted as microorganisms as a consequence of the abundance of easily bio-
a criterion of maturity. Studies in this respect refer to the humifi- degradable compounds in the raw material. For this reason, O2

Table 4
Maturity indices established for composts of different sources.

Parameter Value Reference


Water soluble (C/N) 5–6 Chanyasak and Kubota (1981)
Germination index >50% Zucconi et al. (1981)
NH4-N <0.4 g/kg Zucconi and de Bertoldi (1987)
C/N <20, preferable <10 Mathur et al. (1993)
CO2 production rate 6120 mg CO2/kg/h Hue and Liu (1995)
Water soluble organic-C 610 g/kg
Water soluble (C/N) 616
Water soluble organic-C/Total organic-N 60.70
CEX 660 g/kg
CFA 612.5 g/kg
CEX/Water soluble organic-C P6.0
C/N <12 Bernal et al. (1998a)
Water soluble organic-C <17 g/kg
Water soluble organic-C/Total organic-N <0.55
NH4-N/NO3-N <0.16
NH4-N <0.4 g/kg
Mineralisable-C in 70 days <30%
NO3-N/CO2–C ratio (per day) >8 Cooperband et al. (2003)
Water soluble organic-C 64 g/kg Zmora-Nahum et al. (2005)
M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453 5451

consumption and CO2 production are indicative of compost stabil- tion and plant growth. The CO2–C evolved correlated with plant
ity and maturity (Hue and Liu, 1995). Oxygen uptake and CO2 evo- growth, and immature compost caused N-immobilisation in the
lution are more direct and have been described as being opposite soil, leading to plant N-deficiency.
sides of the same equation under aerobic conditions (Barrena- Those chemical and biological parameters already discussed
Gómez et al., 2006; Iannotti et al., 1993, 1994). have been used to evaluate maturity in manure compost
CO2 evolution correlates directly with aerobic respiration and, (Gómez-Brandón et al., 2008; Goyal et al., 2005; Huang et al.,
of the three techniques considered, is the truest measure of respi- 2006; Solano et al., 2001; Tiquia and Tam, 1998). These authors
ration and hence aerobic biological activity (CCQC, 2001; Hue and identified decreases in water-soluble organic-C, NH4-N, phytotoxic
Liu, 1995). Hue and Liu (1995) set the limit of the CO2 production effects and microbial activity and increases in the humification of
rate for compost maturity at 6120 mg CO2 kg1 h1 (Table 4). the OM as indicators of the progressive stabilisation of the com-
Wang et al. (2004) used a respiration rate of <1 mg CO2–C g1 posting materials, leading to an acceptable degree of maturity
dw d-1 to define a highly stabilised compost from cattle and pig based on the established indices in the literature for composts of
manures. Cooperband et al. (2003) suggested a NO3-N/CO2–C ra- different origin. Also, Michel et al. (2004) and Wang et al. (2004)
tio > 8 per day as an index of compost maturity (Table 4). Respiro- used the criterion of CO2 evolution rate <0.5 mg CO2–C g1 OM
metric studies have been carried out in soils amended with d1 or <1 mg CO2–C g1 dw d1, respectively, to consider composts
compost, in a proportion compatible with agricultural use; these derived from manure as stable materials. Changa et al. (2003) con-
indicate the mineralisation of the compost’s OM (Bernal et al., cluded that CO2 and the NH3 SolvitaÒ test can be employed to char-
1998b; Morel et al., 1979). Mature compost was defined as having acterise the maturity/stability stage for quality control of
mineralisable-C <30% of total organic-C in 70 days, with a rapidly composted manures. Mathur et al. (1990), Guerra-Rodríguez
mineralisable-C <7.2% of total organic-C and a slow mineralisation et al. (2001, 2003) assessed phytotoxicity in germination tests, as
rate <0.35% of total organic-C d1 (Bernal et al., 1998a). an indicator of the maturity of manure compost. Tiquia (2005) pro-
Biological methods for estimating the degree of maturity are posed that values <35 lg TPF (triphenyl formazan) g1 for dehy-
also based on tests for phytotoxicity. Plant tests used in research drogenase activity can be used as a maturity indicator for
and in quality standards can be divided into four broad categories: manures. Ko et al. (2008) proposed the following maturity indices
germination tests (including root assessments) (Zucconi et al., for manure and sawdust compost: NH4/NO3 <1.0, NH3-emission
1981 and Zucconi et al., 1985), growth tests (assessment of top- <20 ppm, CHA/CFA >2.5 and germination index >110.
growth and sometimes root mass), combinations of germination The relevance of maturity and stability parameters to assess
and growth, and other biological methods such as enzyme activi- compost quality is widely recognised by researchers. But integra-
ties (Herrmann and Shann, 1993). According to Zucconi et al. tion of the most reliable indices seems to be the sole option for
(1981) a germination index below 50% characterises an immature evaluation of the maturity/stability stage of composted materials
compost (Table 4). Zucconi and de Bertoldi (1987) discussed the (Eggen and Vethe, 2001; Mathur et al., 1993; Riffaldi et al.,
differences between germination and growth tests. Germination 1986). A clear example of this is the CCQC maturity assessment
tests provide an instant picture of phytotoxicity, whereas growing process (CCQC, 2001; TMECC, 2002), which considered first that a
tests will be affected by continuing changes in the stability or compost with a C/N ratio >25 is immature. When the C/N is 625,
maturity of the compost tested: there may be damaging effects at least one test of group A (stability) and another of group B
on growth in the earlier stages, but beneficial effects later on, with (maturity) must be determined (Table 5). Then, the maturity
different conclusions depending on the time of assessment. García- assessment matrix is applied to classify the material as very ma-
Gómez et al. (2001) also looked at both germination index and pot ture, mature or immature. According to the maturity classification
trials, the yield of ryegrass showing phytotoxic effects from imma- of the compost, the CCQC gives general guidelines for compost best
ture compost even when the germination index was above 87%. uses: ‘‘very mature” can be used for soil and peat-based container
The relationship between the CO2 respiration and phytotoxicity plant mixes, alternative topsoil blends and turf top-dressing;
of immature compost was studied by García-Gómez et al. (2003), ‘‘mature” compost for general field use (pastures), vineyards, row
using the CO2–C production by OM mineralisation, N-mineralisa- crops and as a substitute for low analysis organic fertilisers in some

Table 5
Maturity assessment according to CCQC maturity index (TMECC, 2002).

C/N ratio 625


Stability Thresholds (group A)
Method Units Very stable Stable Unstable
Specific oxygen uptake rate mg O2/g OM/d <3 3–10 >10
CO2 evolution rate mg CO2–C/g OM/d <2 2–4 >4
Dewar self-heating test Dewar index V V <V
Headspace CO2 (SolvitaÒ) Colour code 7–8 5–6 1–4
Biologically available C mg CO2–C/g C/d <2 2–4 >4
Maturity Thresholds (group B)
Method units Very mature Mature Immature
NH4-N mg/kg dw <75 75–500 >500
NH4-N/NO3-N – <0.5 0.5–3.0 >3.0
Seedling emergence % of control >90 80–90 < 80
Seedling vigour % of control >95 85–95 <85
In-vitro germination index % of control >90 80–90 <80
Earthworm bioassay % Weight gain <20 20–40 >40
NH3 (SolvitaÒ) Colour code 5 4 3–1
Volatile fatty acids mmol/g dw <200 200–1000 >1000
5452 M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453

cases; ‘‘immature” compost should be used for land application to Bernal, M.P., Lopez-Real, J.M., Scott, K.M., 1993. Application of natural zeolites for
the reduction of ammonia emissions during the composting of organic wastes
fallow soil and as a feedstock for compost. However, other quality
in a composting simulator. Bioresour. Technol. 43, 35–39.
criteria apart from maturity determine the compost quality, such Bernal, M.P., Navarro, A.F., Roig, A., Cegarra, J., García, D., 1996. Carbon and nitrogen
as the nutrient content, ammonia, pH and soluble salts, and they transformation during composting of sweet sorghum bagasse. Biol. Fert. Soils
should be also taken into account to define the compost use. 22, 141–148.
Bernal, M.P., Paredes, C., Sánchez-Monedero, M.A., Cegarra, J., 1998a. Maturity and
Therefore, the development of a market for compost materials stability parameters of composts prepared with a wide range of organic wastes.
which supports or promotes a waste composting strategy greatly Bioresour. Technol. 63, 91–99.
depends on the definition and adoption of quality standards (Brin- Bernal, M.P., Sánchez-Monedero, M.A., Paredes, C., Roig, A., 1998b. Carbon
mineralization from organic wastes at different composting stages during
ton, 2000; Hogg et al., 2002). However, there are several compost their incubation with soil. Agr. Ecosyst. Environ. 69, 175–189.
quality standards proposed by official and private organisations Bishop, P.L., Godfrey, C., 1983. Nitrogen transformation during sewage composting.
(BOE, 2005; BSI, 2005; European Commission, 2001; Ge et al., Biocycle 24, 34–39.
BOE, 2005. Real Decreto 824/2005, de 8 de julio, sobre productos fertilizantes.
2006; TMECC, 2002), which take into account compost properties Boletín Oficial del Estado 171, 25592–25669.
such as foreign matter (inert contamination), potentially toxic ele- Brinton, W., 2000. Compost Quality Standards and Guidelines. Final Report by
ments (organic contaminants and heavy metals), sanitisation Woods End Research Laboratories for the New York State Association of
Recyclers.
(pathogens and phytopathogens), maturity and stability, weed BSI, 2005. PAS 100:2005, Specification for Composted Materials. British Standard
seeds, water, OM and nutrient content. Currently, there is a need Institution, London.
for harmonisation of such criteria at the international level. Burton, H., Turner, C., 2003. Manure management, second ed.. Treatment Strategies
for Sustainable Agriculture Silsoe Research Institute, Lister and Durling Printers,
Flitwick, Bedford, UK.
6. Conclusions California Compost Quality Council (CCQC), 2001. Compost Maturity Index,
Technical Report.
Changa, C.M., Wang, P., Watson, M.E., Hoitink, H.A.J., Michel Jr., F.C., 2003.
The composting of animal manures has been demonstrated to Assessment of the reliability of a commercial maturity test kit for composted
be an effective method for producing end-products which are sta- manures. Compost Sci. Util. 11, 125–143.
bilised and sanitised, ensuring their maximum benefit for agricul- Chanyasak, V., Kubota, H., 1981. Carbon/organic nitrogen ratio in water extract as
measure of compost degradation. J. Ferment. Technol. 59, 215–219.
ture. However, the compost should be of high quality in order to Chen, Y., Inbar, Y., 1993. Chemical and spectroscopical analyses of organic matter
guarantee its marketability. transformation during composting in relation to compost maturity. In: Hoitink,
Amongst the controllable factors which influence manure com- H.A.J., Keener, H.M. (Eds.), Science and Engineering of Composting: Design,
Environmental, Microbiological and Utilization Aspects. Renaissance
posting, the selection of appropriate bulking agents plays an essen-
Publications, Ohio, pp. 551–600.
tial role in controlling the decomposition rate and favouring N Chen, Y., 2003. Nuclear magnetic resonance, infra-red and pyrolysis: application of
retention within the compost. In this sense, strategies such as addi- spectroscopic methodologies to maturity determination of composts. Compost
Sci. Util. 11, 152–168.
tion of a bulking agent with degradable organic-C, to enhance ini-
Cooperband, L.R., Stone, A.G., Fryda, M.R., Ravet, J.L., 2003. Relating compost
tial N immobilisation, and process control (moisture, temperature, measures of stability and maturity to plant growth. Compost Sci. Util. 11, 113–
aeration/turning and particle size) have been shown to reduce 124.
ammonia volatilisation and hence nitrogen losses, these being a Das, K., Keener, H.M., 1997. Moisture effect on compaction and permeability in
composts. J. Environ. Eng. 123, 275–281.
major concern in manure composting from an environmental point de Bertoldi, M., Vallini, G., Pera, A., Zucconi, F., 1982. Comparison of three windrow
of view. compost systems. Biocycle 23, 45–50.
The agricultural value of a compost increases when the OM de Bertoldi, M., Vallini, G., Pera, A., 1983. The biology of composting: a review.
Waste Manage. Res. 1, 157–176.
reaches a high level of stability and maturity, which cannot be de Nobili, M., Petrussi, F., 1988. Humification index (HI) as evaluation of the
established by a single parameter. Several indices based on chem- stabilization degree during composting. J. Ferment. Technol. 66, 577–583.
ical and stability parameters have been used for manure compost Eggen, T., Vethe, O., 2001. Stability indices for different composts. Compost Sci. Util.
9, 19–26.
by different authors. However, it is necessary to standardise the Eghball, B., Power, J.F., Gilley, J.E., Doran, J.W., 1997. Nutrient, carbon, and
criteria used by official institutions from different countries. mass loss of beef cattle feedlot manure during composting. J. Environ.
Qual. 26, 189–193.
European Commission, 2001. Working document: biological treatment of biowaste,
Acknowledgements
2nd draft, p. 22.
Finstein, M.S., Miller, F.C., 1985. Principles of composting leading to maximization
The authors thank the Organisation for Economic Co-operation of decomposition rate, odor control, and cost effectiveness. In: Gasser, J.K.R.
(Ed.), Composting of Agricultural and Other Wastes. Elsevier Applied Science
and Development, Co-operative Research Programme: Biological
Publications, Barking, Essex, pp. 13–26.
Resource Management for Sustainable Agricultural Systems, for Finstein, M.S., Miller, F.C., MacGregor, S.T., Psarianos, K.M., 1985. The Rutgers
inviting Dr. Bernal to participate in the workshop ‘‘Livestock Waste strategy for composting: process design and control. EPA Project Summary, EPA
Treatment Systems of the Future: a challenge to environmental 600/S2-85/059, Cincinnati, Ohio.
Gajalakshmi, S., Abbasi, S.A., 2008. Solid waste management by composting: state of
quality, food safety, and sustainability”, where this paper was the art. Crit. Rev. Environ. Sci. Technol. 38, 311–400.
presented. García-Gómez, A., Bernal, M.P., Cegarra, J., Roig, A., 2001. Plant response to the latent
phytotoxicity in agroindustrial wastes in different stages of the composting
process. In: Proceedings of the International Conference ORBIT 2001 on
References Biological Processing of Waste: A Product-oriented Perspective, Sevilla, Spain,
pp. 321–325.
Agnew, J.M., Leonard, J.J., 2003. The physical properties of compost. Compost Sci. García-Gómez, A., Bernal, M.P., Roig, A., 2003. Carbon mineralisation and plant
Util. 1, 238–264. growth in soil amended with compost samples at different degrees of maturity.
Ahn, H.K., Richard, T.L., Choi, H.L., 2007. Mass and thermal balance during Waste Manage. Res. 21, 161–171.
composting of a poultry manure–wood shavings mixture at different aeration Garrison, M.V., Richard, T.L., Tiquia, S.M., Honeyman, M.S., 2001. Nutrient losses
rates. Process Biochem. 42, 215–223. from unlined bedded swine hoop structure and an associated windrow
Amon, B., Kryvoruchko, V., Amon, T., Zechmeister-Boltenstern, S., 2006. Methane, composting site. Paper 01-2238. ASAE Annual International Meeting,
nitrous oxide and ammonia emissions during storage and after application of Sacramento, CA, 30 July–1, August 2002. ASAE, St. Joseph, MI.
dairy cattle slurry and influence of slurry treatment. Agr. Ecosyst. Environ. 112, Ge, B., McCartney, D., Zeb, J., 2006. Compost environmental protection standards in
153–162. Canada. J. Environ. Eng. Sci. 5, 221–234.
Barrena-Gómez, R., Vázquez Lima, F., Sánchez Ferrer, A., 2006. The use of respiration Gómez-Brandón, M., Lazcano, C., Domínguez, J., 2008. The evaluation of stability
indices in the composting process: a review. Waste Manage. Res. 24, 37–47. and maturity during the composting of cattle manure. Chemosphere 70, 436–
Barrington, S., Choinière, D., Trigui, M., Knight, W., 2002. Effect of carbon source on 444.
compost nitrogen and carbon losses. Bioresour. Technol. 83, 189–194. Goyal, S., Dhull, S.K., Kapoor, K.K., 2005. Chemical and biological changes during
Bernal, M.P., 1990. Utilización de purines de cerdo en la fertilización de suelos composting of different organic wastes and assessment of compost maturity.
calizos en condiciones de regadío. CEBAS-CSIC, Murcia, Spain. Bioresour. Technol. 96, 1584–1591.
M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453 5453

Guardia, A., Petiot, C., Rogeau, D., Druilhe, C., 2008. Influence of aeration rate on Morel, J.L., Guckert, A., Nicolardot, B., Benistant, D., Catroux, G., Germon, J.C., 1979.
nitrogen dynamics during composting. Waste Manage. 28, 575–587. Etude de I’évolution des caractéristiques physico-chimiques et de la stabilité
Guerra-Rodríguez, E., Díaz-Ravina, M., Vázquez, M., 2001. Co-composting of biologique des ordures ménagères au tours du compostege. Agronomie 6, 693–
chestnut burr and leaf litter with solid poultry manure. Bioresour. Technol. 701.
78, 107–109. Paillat, J.M., Robin, P., Hassouna, M., Leterme, P., 2005. Predicting ammonia and
Guerra-Rodríguez, E., Vázquez, M., Díaz-Ravina, M., 2003. Dynamics of the co- carbon dioxide emissions from carbon and nitrogen biodegradability during
composting of barley waste with liquid poultry manure. J. Sci. Food Agric. 83, animal waste composting. Atmos. Environ. 39, 6833–6842.
166–172. Pare, T., Dinel, H., Schnitzer, M., Dumontet, S., 1998. Transformations of carbon and
Hansen, R.C., Keener, H.M., Hoitink, H.A.J., 1989. Poultry manure composting. An nitrogen during composting of animal manure and shredded paper. Biol. Fert.
exploratory study. Trans. ASAE 32, 2151–2158. Soils 26, 173–178.
Hao, X., Chang, C., Larney, F.J., 2004. Carbon, nitrogen balances and greenhouse gas Paredes, C., Bernal, M.P., Cegarra, J., Roig, A., Navarro, A.F., 1996. Nitrogen
emission during cattle feedlot manure composting. J. Environ. Qual. 33, 37–44. transformation during the composting of different organic wastes. In: Van
Harada, Y., Inoko, A., 1980. Relationship between cation-exchange capacity and Cleemput, O., Vermoesen, G., Hofman, A. (Eds.), Progress in Nitrogen Cycling
degree of maturity of city refuse composts. Soil Sci. Plant Nutr. 26, 353–362. Studies. Kluwer Academic Publishers, Dordrecht, pp. 121–125.
Haug, R.T., 1993. The Practical Handbook of Compost Engineering. Lewis Publishers, Paredes, C., Roig, A., Bernal, M.P., Sánchez-Monedero, M.A., Cegarra, J., 2000.
Boca Raton, FL. Evolution of organic matter and nitrogen during co-composting of olive mill
Herrmann, R.F., Shann, J.R., 1993. Enzyme activities as indicators of municipal solid wastewater with solid organic wastes. Biol. Fert. Soils 32, 222–227.
waste compost maturity. Compost Sci. Util. 1, 54–63. Parkinson, R., Gibbs, P., Burchett, S., Misselbrook, T., 2004. Effect of turning regime
Hogg, D., Barth, J., Faviono, E., Centemero, M., Caimi, V., Amlinger, F., Devliegher, W., and seasonal weather conditions on nitrogen and phosphorus losses during
Brinton, W., Antler, S., 2002. Comparison of compost standards within the EU, aerobic composting of cattle manure. Bioresour. Technol. 91, 171–178.
North America, and Australasia. Main report, The Waste and Resources Action Petric, I., Selimbasić, V., 2008. Composting of poultry manure and wheat straw in a
Programme, Banbury, Oxon, UK. closed reactor: optimum mixture ratio and evolution of parameters.
Huang, G.F., Wong, J.W.C., Wu, Q.T., Nagar, B.B., 2004. Effect of C/N on composting of Biodegradation 19, 53–63.
pig manure with sawdust. Waste Manage. 24, 805–813. Richard, T.L., Hamelers, H.V.M., Veeken, A.H.M., Silva, T., 2002. Moisture
Huang, G.F., Wu, Q.T., Wong, J.W.C., Nagar, B.B., 2006. Transformation of organic relationships in composting processes. Compost Sci. Util. 10, 286–302.
matter during co-composting of pig manure with sawdust. Bioresour. Technol. Riffaldi, R., Levi-Minzi, R., Pera, A., de Bertoldi, M., 1986. Evaluation of compost
97, 1834–1842. maturity by means of chemical and microbial analyses. Waste Manage. Res. 4,
Hue, N.V., Liu, J., 1995. Predicting compost stability. Compost Sci. Util. 3, 8–15. 387–396.
Iannotti, D.A., Pang, T., Toth, B.L., Elwell, D.L., Keener, H.M., Hoitink, H.A.J., 1993. A Roletto, E., Barberis, R., Consiglio, M., Jodice, R., 1985. Chemical parameters for
quantitative respirometric method for monitoring compost stability. Compost evaluating compost maturity. Biocycle (March), 46–48.
Sci. Util. 1, 52–65. Ryckeboer, J., Mergaert, J., Vaes, K., Klammer, S., De Clercq, D., Coosemans, J., Insam,
Iannotti, D.A., Grebus, M.E., Toth, B.L., Madden, L.V., Hoitink, H.A.J., 1994. Oxygen H., Swings, J., 2003. A survey of bacteria and fungi occurring during composting
respirometry to assess stability and maturity of composted municipal solid and self-heating processes. Ann. Microbiol. 53, 349–410.
waste. J. Environ. Qual. 23, 1177–1183. Sánchez-Monedero, M.A., Bernal, M.P., Roig, A., Cegarra, J., García, D., 1996. The
Iglesias-Jimenez, E., Perez-Garcia, V., 1992. Determination of maturity indices for effectiveness of the Rutgers system and the addition of bulking agent in
city refuse composts. Agr. Ecosyst. Environ. 38, 331–343. reducing N-losses during composting. In: Van Cleemput, O., Hofman, G.,
Jakobsen, S.T., 1995. Aerobic decomposition of organic wastes 2. Value of compost Vermoesen, A. (Eds.), Progress in Nitrogen Cycling Studies. Kluwer Academic
as a fertilizer. Resour. Conserv. Recy. 13, 57–71. Publishers, Dordrecht, pp. 133–139.
Keener, H.M., Dick, W.A., Hoitink, H.A.J., 2000. Composting and beneficial utilization Sánchez-Monedero, M.A., Cegarra, J., García, D., Roig, A., 2002. Chemical and
of composted by-product materials. In: Dick, W.A. (Ed.), Land Application of structural evolution of humic acids during composting. Biodegradation 13, 361–
Agricultural, Industrial, and Municipal By-Products. Soil Science Society of 371.
America, Inc., Madison, pp. 315–341. Senesi, N., 1989. Composted materials as organic fertilisers. Sci. Total Environ. (81/
Kirchmann, H., Widen, P., 1994. Separately collected organic household wastes. 82), 521–542.
Swedish J. Agric. Res. 24, 3–12. Sequi, P., de Nobili, M., Leita, L., Cercignani, G., 1986. A new index of humification.
Ko, H.J., Kim, K.Y., Kim, H.T., Kim, C.N., Umeda, M., 2008. Evaluation of maturity Agrochimica 30, 175–179.
parameters and heavy metal contents in composts made from animal manure. Solano, M.L., Iriarte, F., Ciria, P., Negro, M.J., 2001. Performance characteristics of
Waste Manage. 28, 813–820. three aeration systems in the composting of sheep manure and straw. J. Agric.
Larney, F.J., Buckley, K.E., Hao, X., McCaughey, W.P., 2006. Fresh, stockpiled, and Eng. Res. 79, 317–329.
composted beef cattle feedlot manure: Nutrient levels and mass balance Tiquia, S.M., Tam, N.F.Y., 1998. Composting of spent pig litter in turned and forced-
estimates in Alberta and Manitoba. J. Environ. Qual. 35, 1844–1854. aerated piles. Environ. Pollut. 99, 329–337.
Larney, F.J., Hao, X., 2007. A review of composting as a management alternative for Tiquia, S.M., Richard, T.L., Honeyman, M.S., 2000. Effect of windrow turning and
beef cattle feedlot manure in southern Alberta, Canada. Bioresour. Technol. 98, seasonal temperatures on composting of hog manure from hoop structures.
3221–3227. Environ. Technol. 21, 1037–1046.
Lau, A.K., Lo, K.V., Liao, R.H., Yu, J.C., 1992. Aeration experiments for swine waste Tiquia, S.M., 2002. Microbial transformation of nitrogen during composting. In:
composting. Bioresour. Technol. 41, 145–152. Insam, H., Riddech, N., Klammer, S. (Eds.), Microbiology of Composting and
Liang, Y., Leonard, J.J., Feddes, J.J.R., McGill, W.B., 2006. Influence of carbon and Other Biodegradation Processes. Springer-Verlag, Berlin, Heidelberg, pp. 237–
buffer amendment on ammonia volatilization in composting. Bioresour. 245.
Technol. 97, 748–761. Tiquia, S., Tam, N., 2002. Characterization and composting of poultry litter in forced-
Mahimairaja, S., Bolan, N.S., Hedley, M.J., Macgregor, A.N., 1994. Losses and aeration piles. Process Biochem. 37, 869–880.
transformation of nitrogen during composting of poultry manure with Tiquia, S.M., 2005. Microbiological parameters as indicators of compost maturity. J.
different amendments: an incubation experiment. Bioresour. Technol. 47, Appl. Microbiol. 99, 816–828.
265–273. TMECC, 2002. Test Methods for the Examination of Composting and Compost. US
Manios, V.I., Tsikalas, P.E., Siminis, H.I., 1989. Phytotoxicity of olive tree compost in Composting Council, Bethesda, MD.
relation to organic acid concentration. Biol. Wastes 27, 307–317. UK Composting Association, 2001. Large-Scale Composting. A Practical Manual for
Mari, I., Ehaliotis, C., Kotsou, M., Chatzipavlidis, I., Georgakakis, D., 2005. Use of the UK.
sulfur to control pH in composts derived from olive processing by-products. Wang, P., Changa, C.M., Watson, M.E., Dick, W.A., Chen, Y., Hoitink, H.A.J., 2004.
Compost Sci. Util. 13, 281–287. Maturity indices for composted dairy and pig manures. Soil Biol. Biochem. 36,
Martins, O., Dewes, T., 1992. Loss of nitrogenous compounds during composting of 767–776.
animal wastes. Bioresour. Technol. 42, 103–111. Witter, E., López-Real, J., 1988. Nitrogen losses during the composting of sewage
Mathur, S.P., Patni, N.K., Levesque, M.P., 1990. Static pile, passive aeration sludge, and the effectiveness of clay soil, zeolite, and compost in adsorbing the
composting of manure slurries using peat as a bulking agent. Biol. Wastes 34, volatilized ammonia. Biol. Wastes 23, 279–294.
323–333. Wu, L., Ma, L.Q., Martinez, G.A., 2000. Comparison of methods for evaluating
Mathur, S.P., Owen, G., Dinel, H., Schnitzer, M., 1993. Determination of compost stability and maturity of biosolids compost. J. Environ. Qual. 29, 424–429.
biomaturity. Literature review. Biol. Agric. Hortic. 10, 65–85. Zmora-Nahum, S., Markovitch, O., Tarchitzky, J., Chen, Y., 2005. Dissolved organic
Menoyo, A., 1995. Valoración agronómica de la gallinaza: Compostaje. Ph.D. Thesis, carbon (DOC) as a parameter of compost maturity. Soil Biol. Biochem. 37, 2109–
University Pais Vasco, Bilbao. 2116.
Michel Jr., F.C., Pecchia, J.A., Rigot, J., Keener, H.M., 2004. Mass and nutrient losses Zucconi, F., Pera, A., Forte, M., de Bertoldi, M., 1981. Evaluating toxicity of immature
during the composting of dairy manure amended with sawdust or straw. compost. Biocycle 22, 54–57.
Compost Sci. Util. 12, 323–334. Zucconi, F., Monaco, A., Forte, M., de Bertoldi, M., 1985. Phytotoxins during the
Miller, F.C., 1992. Composting as a process based on the control of ecologically stabilization of organic matter. In: Gasser, J.K.R. (Ed.), Composting of
selective factors. In: Metting, F.B., Jr. (Ed.), Soil Microbial Ecology, Applications Agricultural and Other Wastes. Elsevier Applied Science Publishers, Barking,
in Agricultural and Environmental Management. Marcel Dekker, Inc., New York, pp. 73–85.
pp. 515–544. Zucconi, F., de Bertoldi, M., 1987. Compost specifications for the production and
Moral, R., Paredes, C., Bustamente, M.A., Marhuenda-Egea, F., Bernal, M.P., 2009. characterization of compost from municipal solid waste. In: de Bertoldi, M.,
Utilisation of manure composts by high-value crops: safety and environmental Ferranti, M.P., L’Hermite, P., Zucconi, F. (Eds.), Compost: Production, Quality and
challenges. Bioresour. Technol. 100, 5454–5460. Use. Elsevier, Barking, pp. 30–50.

You might also like