Bioresource Technology 100 (2009) 5444–5453

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Bioresource Technology

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Composting of animal manures and chemical criteria for compost maturityassessment. 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, Spainb 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

Article history:Received 10 June 2008Received in revised form 7 November 2008Accepted 19 November 2008Available online 31 December 2008

Keywords:Animal manureCompostingCompost qualityMaturity indicesMicrobial stability

0960-8524/$ - see front matter � 2008 Elsevier Ltd. Adoi:10.1016/j.biortech.2008.11.027

* Corresponding author. Tel.: +34 968 396200; fax:E-mail address: pbernal@cebas.csic.es (M.P. Berna

a b s t r a c t

New livestock production systems, based on intensification in large farms, produce huge amount of man-ures and slurries without enough agricultural land for their direct application as fertilisers. Composting isincreasingly considered a good way for recycling the surplus of manure as a stabilised and sanitised end-product for agriculture, and much research work has been carried out in the last decade. However, highquality 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, thefirst part of this paper explains the basic concepts of the composting process and how manure character-istics can influence its performance. Then, a summary of those factors such as nitrogen losses (whichdirectly reduce the nutrient content), organic matter humification and compost maturity which affectthe quality of composts produced by manure composting is presented. Special attention has been paidto 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.

� 2008 Elsevier Ltd. All rights reserved.

1. Introduction

Composting of organic wastes is a biooxidative process involv-ing the mineralisation and partial humification of the organic mat-ter, leading to a stabilised final product, free of phytotoxicity andpathogens and with certain humic properties (Zucconi and deBertoldi, 1987). During the first phase of the process the simpleorganic carbon compounds are easily mineralised and metabolisedby the microorganisms, producing CO2, NH3, H2O, organic acidsand heat. The accumulation of this heat raises the temperature ofthe pile. Composting is a spontaneous biological decompositionprocess of organic materials in a predominantly aerobic environment.During the process bacteria, fungi and other microorganisms,including microarthropods, break down organic materials to sta-ble, usable organic substances called compost. The composting alsoimplies the volume reduction of the wastes, the destruction ofweed seeds and of pathogenic microorganisms.

The intensity and concentrated activity of the livestock industrygenerate vast amounts of biodegradable wastes, which must bemanaged under appropriate disposal practices to avoid a negativeimpact on the environment (odour and gaseous emissions, soil andwater pollution, etc.; Burton and Turner, 2003). Composting cannotbe considered a new technology, but amongst the waste manage-

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ment strategies it is gaining interest as a suitable option for man-ures with economic and environmental profits, since this processeliminates or reduces the risk of spreading of pathogens, parasitesand weed seeds associated with direct land application of manureand leads to a final stabilised product which can be used to im-prove and maintain soil quality and fertility (Larney and Hao,2007). Composting of animal manures has been traditionally car-ried out by the farmers after manure collection for better handling,transport and management. Frequently the wastes were heaped upwith little regard to control of the process conditions (aeration,temperature, ammonia loss, etc.) and with rudimentary methodol-ogy. However, as the fertiliser value of animal manures has beenalways recognised, nowadays their composting is seen as an alter-native way of recycling the manures in farms without enough agri-cultural land for their direct use as a fertiliser. But, the cost ofcomposting of animal manures can be considerably higher thanthe direct utilisation of raw manures. Therefore, composting is jus-tified for manures that need to be partially sterilised (Parkinsonet al., 2004), and also when compost of high quality is produced,to offset the production costs.

The present paper reviews the factors affecting the compostingof animal manures for production of high quality compost withadded agricultural value, focusing on the nutrient content, organicmatter (OM) humification and maturity degree. Complementaryinformation on safety and environmental aspects related to man-ure composting is reviewed by Moral et al. (2009) in this OECD

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special issue, including the suppressive effect against phytopatho-gens of compost and recent techniques to determine the OM humi-fication process during composting.

2. The basic concepts of the composting process

While composting occurs naturally, efficient composting re-quires the control of several factors to avoid nuisance problemssuch as odours and dust, and also for obtaining a quality agricul-tural product. The controlled conditions are basic for a compostingprocedure, distinguishing it from aerobic fermentation. Over thelast decades, research has been focused on the study of the com-plex interaction amongst physical, chemical and biological factorsthat occurs during composting. Therefore, the control of parame-ters such as bulk density, porosity, particle size, nutrient content,C/N ratio, temperature, pH, moisture and oxygen supply have dem-onstrated to be key for composting optimisation since they deter-mine the optimal conditions for microbial development and OMdegradation (Agnew and Leonard, 2003; Das and Keener, 1997;de Bertoldi et al., 1983; Haug, 1993; Miller, 1992; Richard et al.,2002). Composting optimisation involves the definition of ade-quate initial substrate conditions that must be controlled andmaintained as composting progresses. Although it is difficult togeneralise for all type of substrates and management conditions,the basic and applied aspects of composting have been summa-rised in this section. For a particular composting formulation, spe-cific references can be found.

The factors affecting the composting process can be divided intotwo groups: those depending on the formulation of the compostingmix, such as nutrient balance, pH, particle size, porosity and mois-ture; and those dependent on the process management, such as O2

concentration, temperature and water content. Nutritional balanceis mainly defined by the C/N ratio. Microorganisms require an en-ergy source (degradable organic-C) and N for their developmentand activity. The adequate C/N ratio for composting is in the range25–35, because it is considered that the microorganisms require 30parts of C per unit of N (Bishop and Godfrey, 1983). High C/N ratiosmake the process very slow as there is an excess of degradable sub-strate for the microorganisms. But with a low C/N ratio there is anexcess of N per degradable C and inorganic N is produced in excessand can be lost by ammonia volatilisation or by leaching from thecomposting mass. Then, low C/N ratios can be corrected by addinga bulking agent to provide degradable organic-C.

pH: A pH of 6.7–9.0 supports good microbial activity duringcomposting. Optimum values are between 5.5 and 8.0 (de Bertoldiet al., 1983; Miller, 1992). Usually pH is not a key factor for com-posting since most materials are within this pH range. However,this factor is very relevant for controlling N-losses by ammoniavolatilisation, which can be particularly high at pH >7.5. Elementalsulphur (So) has been used as an amendment for avoiding exces-sively high pH values during composting (Mari et al., 2005).

Microorganisms: OM decomposition is carried out by many dif-ferent groups of microbial populations (Ryckeboer et al., 2003). Themicroorganisms involved in composting develop according to thetemperature of the mass, which defines the different steps of theprocess (Keener et al., 2000). Bacteria predominate early in com-posting, fungi are present during all the process but predominateat water levels below 35% and are not active at temperatures>60 �C. Actinomycetes predominate during stabilisation and cur-ing, and together with fungi are able to degrade resistant polymers.

Particle size and distribution are critical for balancing the sur-face area for growth of microorganisms and the maintenance ofadequate porosity for aeration. The larger the particle size, the low-er the surface area to mass ratio. So compost with large particlesdoes not decompose adequately because the interior of the parti-

cles has difficult accessibility for the microorganisms, as duringdecomposition particles may coat the surface with an impenetra-ble humified layer (Bernal et al., 1993). However, particles whichare too small can compact the mass, reducing the porosity. Thesefactors are material specific: particle size and distribution, shape,packing and moisture content control the porosity of the compost-ing mass.

Porosity: Substrate porosity exerts a great influence on com-posting performance since appropriate conditions of the physicalenvironment for air distribution must be maintained during theprocess. Porosity greater than 50% causes the pile to remain at alow temperature because energy lost exceeds heat produced. Toolittle porosity leads to anaerobic conditions and odour generation.The percentage air-filled pore space of composting piles should bein the range of 35–50%.

Aeration: Aeration is a key factor for composting. Proper aera-tion controls the temperature, removes excess moisture and CO2

and provides O2 for the biological processes. The optimum O2 con-centration is between 15% and 20% (Miller, 1992). Controlled aer-ation should maintain temperatures below 60–65 �C, whichensures enough O2 is supplied (Finstein and Miller, 1985).

Moisture: The optimum water content for composting varieswith the waste to be composted, but generally the mixture shouldbe at 50–60% (Gajalakshmi and Abbasi, 2008). When the moisturecontent exceeds 60% O2 movement is inhibited and the processtends to become anaerobic (Das and Keener, 1997). During com-posting a large quantity of water can evaporate, to control temper-ature, and as water content diminishes the rate of decompositiondecreases, then rewetting should be required in order to maintainthe optimum moisture content for the microbial activity.

Temperature: The temperature pattern shows the microbialactivity and the occurrence of the composting process. The opti-mum temperature range for composting is 40–65 �C (de Bertoldiet al., 1983), temperatures above 55 �C are required to kill patho-genic microorganisms. But if the temperature achieved exceedsthe tolerance range of the thermophilic decomposers, the effectis damaging for composting. At temperatures above 63 �C, micro-bial activity declines rapidly as the optimum for various thermo-philes is surpassed, with activity approaching low values at72 �C. The range of 52–60 �C is the most favourable for decomposi-tion (Miller, 1992). The regulation of the temperature is requiredfor controlled composting. Excess heat removal can be achievedthrough several strategies (Miller, 1992): control the size andshape of the composting mass; improve cooling and favourabletemperature redistribution by turning operations, which meansheat removal through evaporation cooling; and achieve superiortemperature control in systems that actively remove heat throughtemperature feedback-controlled ventilation (Rutgers strategy).

The development of the temperature profile indicates the differ-ent phases of the process. In general, the composting process canbe divided into two main phases: the biooxidative phase and thematuring phase also called the curing phase (Bernal et al., 1996;Chen and Inbar, 1993). The biooxidative phase is developed inthree steps (Keener et al., 2000): (i) an initial mesophilic phaselasting 1–3 days, where mesophilic bacteria and fungi degradesimple compounds such as sugars, amino acids, proteins, etc.,increasing quickly the temperature; (ii) thermophilic phase, wherethermophilic microorganisms degrade fats, cellulose, hemicellu-lose and some lignin, during this phase the maximum degradationof the OM occurs together with the destruction of pathogens; (iii)cooling phase, characterised by a decrease of the temperature dueto the reduction of the microbial activity associated with the deple-tion of degradable organic substrates, the composting mass is re-colonised by mesophilic microorganisms which are able to degradethe remaining sugars, cellulose and hemicellulose. During the dif-ferent steps of the biodegradation phase, the organic compounds

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are degraded to CO2 and NH3, with the consumption of O2. How-ever, during the maturation phase stabilisation and humificationof the OM occur, producing a mature compost with humic charac-teristics in its OM. Thus, compost can be defined as the stabilisedand sanitised product of composting, which has undergone an ini-tial, rapid stage of decomposition, is beneficial to plant growth andhas certain humic characteristics, making the composting of wastea key issue for sustainable agriculture and resource management(Gajalakshmi and Abbasi, 2008; Haug, 1993; Jakobsen, 1995; Zuc-coni and de Bertoldi, 1987).

3. Characteristics of the animal manures for composting

Controlled composting allows the safe storage and transport ofthe final product, adds value to the product because compost is amore concentrated and uniform product than the manure, permitseasy spreading and thus uniform distribution in the soil and resultsin an absence of pathogens and weed seeds. The compost also canbe used as a fertiliser for pots and as a basis for soil-less substrates.The advantages of composting animal manures compared with di-rect application can be summarised in:

– Elimination of pathogens and weeds.– Microbial stabilisation.– Reduction of volume and moisture.– Removal and control of odours.– Ease of storage, transport and use.– Production of good quality fertiliser or substrate.

However the disadvantages are derived from:

– Cost of installation and management.– Requirement for a bulking agent.– Requirement for large areas for storage and operation.

Then, composting of animal manures should be seen as a tech-nology which adds value, producing a high quality product formultiple agricultural uses.

Certain chemical characteristics of the animal manures are notadequate for composting and could limit the efficiency of the pro-cess: excess of moisture, low porosity, high N concentration for theorganic-C, which gives a low C/N ratio, and in some cases high pHvalues (Table 1). Thus, adequate composting management of themanure is required in order to obtain a quality compost. Therefore,different aeration strategies, substrate conditioning-feedstock for-mulation, bulking agents and process control options have beenused in manure composting in order to reduce composting timeand costs and enhance the quality of the end-products (Lau et al.,1992; Michel et al., 2004; Solano et al., 2001).

Table 1Average composition of animal slurry and manure (g/kg fresh weight; Amon et al.,2006; Bernal, 1990; Burton and Turner, 2003; Huang et al., 2004; Mathur et al., 1990;Menoyo, 1995).

Dry matter Organic-C Total-N NH4-N pH

Liquid manure/slurryCattle 15–123 3.8–36 2.0–7.0 1.0–4.9 7.1–8.4Pig 4.9–152 1.0–65 0.6–7.8 0.3–6.6 6.7–8.9Poultry 10–367 11–112 2–21 1.9–9.4 7.9–8.8Solid manureCattle 140–300 65–126a 4.2–8.1 0.3–2.0 8.6b

Pig 150–330 42–132a 3.5–11 0.5–6.0 8.1b

Poultry 220–700 103–597a 10–58 2.4–18 7.6b

a Bernal, personal communication.b Average values.

The addition of a bulking agent for manure composting opti-mises substrate properties such as air space, moisture content, C/N ratio, particle density, pH and mechanical structure, affectingpositively the decomposition rate. In this sense, lignocellulosicagricultural and forestry by-products are commonly used as bul-king agents in co-composting of nitrogen-rich wastes, such as ani-mal manures. The most generally used materials are cereal straw(Barrington et al., 2002; Bernal et al., 1993; Martins and Dewes,1992; Petric and Selimbasic, 2008; Wang et al., 2004), cotton waste(Paredes et al., 1996), hay (Barrington et al., 2002) and wood by-products such as pine shavings, chestnut burr and leaves and saw-dust (Ahn et al., 2007; Barrington et al., 2002; Guerra-Rodríguezet al., 2001; Huang et al., 2004; Tiquia and Tam, 2002; Wanget al., 2004). All have low moisture and high organic-C contentsand high C/N ratios (an average of 50 for cereal straw and >80for wood by-products), which can compensate for the low valuesof the animal manures.

4. Strategies for producing high quality compost: nutrientcontent and OM humification

The effectiveness of compost with regard to beneficial effects onsoil physical, chemical and biological properties, as well as consti-tuting a nutrient source, depends on the quality of the compost.The quality criteria for compost are established in terms of: nutri-ent content, humified and stabilised OM, the maturity degree, thehygienisation and the presence of certain toxic compounds such asheavy metals, soluble salts and xenobiotics. The first three factorsare reviewed in the present paper, while those related to safety andenvironmental aspects are reviewed by Moral et al. (2009) in thisOECD special issue. The production of compost with a high nutrientcontent requires the control and reduction of nutrient losses dur-ing the process, whilst to ensure a high degree of OM humificationenough time should be allowed for the maturation phase. Finally, ahigh degree of compost maturity requires the establishment ofadequate maturity indices.

4.1. Organic matter degradation and nitrogen losses

During the active phase of the composting process the organic-C decreases in the material due to decomposition of the OM by themicroorganisms. This loss of OM reduces the weight of the pile anddecreases the C/N ratio. The degradation rate of the OM decreasesgradually as composting progresses because of the reduction inavailable carbon sources, and synthesis reactions of new complexand polymerised organic compounds (humification) prevail overmineralisation during the maturation phase. This process leads tostabilised end-products which act as slow-release fertilisers foragricultural 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 gasemissions (Hao et al., 2004).

The degradation of the OM during composting can be estimatedas a dry matter loss (Garrison et al., 2001; Parkinson et al., 2004), asan OM loss, or as an organic-C loss (Table 2). Whatever the param-eter used, it should be calculated as a mass balance, taking into ac-count the dry weight reduction of the pile, instead of only thedifference in concentration of OM or organic-C in the compostingmass.

During the composting process, substrate transformation isconditioned by the nature of the OM according to its degradability(Haug, 1993), this property affecting decomposition rate, gas emis-sions, duration and extent of the process and oxygen requirements.Labile organic compounds, such as simple carbohydrates, fats andamino acids, are degraded quickly in the first stage of composting;

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

Manure type Bulking agent Compostingprocess

OM loss by mineralisation (% ofinitial OM)

N-loss (% of initialtotal-N)

Reference

Beef manure – Turnedwindrow

Organic-C: 45–62 19–43 Eghball et al.(1997)

Beef manure Fresh straw-bedded Turnedwindrow

Organic-C: 53 42 Hao et al. (2004)Woodchip-bedded Organic-C: 35 12

Beef manure – Turnedwindrow

Organic-C: 67 46 Larney et al.(2006)

Dairy manure Sawdust and wood shavings Turnedwindrow

OM: 67 Organic-C: 63a 5a Changa et al.(2003)Wheat straw OM: 67 Organic-C: 64ª Absenta

Dairy manure Hardwood sawdust Turnedwindrow

OM: 46–76 7–26 Michel et al.(2004)Wheat straw OM: 58–81 15–43

Dairy manure Wheat straw additives: molasses, office paper,and buffer solutions

In-vesselsystem

OM: 29–55a 12–25 Liang et al. (2006)

Poultry manure Cotton gin waste Rutgers staticpile

OM: 53 Organic-C: 52 26 Paredes et al.(1996)

Poultry litter – Forced-ventilation

OM: 9 58 Tiquia and Tam(2002)

Pig slurry + Poultrymanure

Sweet sorghum bagasse Rutgers staticpile

OM: 62 <40 Bernal et al.(1996)

Pig manure (partially decomposed with cornstalk) Turnedwindrow

Organic-C: 50–72 3–59 Tiquia et al.(2000)

Unturnedwindrow

Organic-C: 30–54 8–60

Pig manure Shredded wood pallets and sawdust Turnedwindrow

OM: 55 Organic-C: 52a 43a Changa et al.(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(100�X2)]/[X2(100�X1)] and organic-C or N-loss (%) = 100�100[(X1Y2)/(X2Y1)], where Y1 and Y2 are the initial and the final total organic-C or total-Nconcentrations, respectively.

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other, more resistant organic substrates such as cellulose, hemicel-lulose and lignin are partially degraded and transformed at a lowerrate. Therefore, composting involves a partial mineralisation of theorganic substrate, leading to carbon losses throughout the process;this is compensated by the higher stabilisation degree of theremaining organic compounds.

During composting of animal manures organic-C losses canreach 67% in cattle manure, 52% in poultry manure and 72% inpig manure (Table 2). The composting system and conditions, char-acteristics of both the bedding material and the bulking agentadded for composting and even the environmental conditions ofthe season (winter or summer; Parkinson et al., 2004) have a greatinfluence on the mineralisation of the OM during composting (Ta-ble 2). For instance, the use of woodchips instead of cereal straw asbedding material in beef manure reduced the organic-C loss duringcomposting (Hao et al., 2004) due to the combination of larger par-ticle size, higher C/N ratio and the recalcitrant nature of the wood-chips. Similar results were shown by Hansen et al. (1989) andMichel et al. (2004) in composting of poultry manure and cowmanure, respectively; they obtained a lower decomposition ofthe composting substrate when employing amendment materialswith recalcitrant OM such as lignin.

As a result of the dry weight loss of the material during com-posting, the concentration of mineral elements increases, if leach-ing does not occur or is controlled to a minimum. Generally thetotal N concentration increases during composting due to the con-centration effect (Bernal et al., 1996; Paredes et al., 1996). The evo-lution of N forms shows the mineralisation of the organiccompounds during the active phase of composting with the forma-tion of NH4-N. Thus, the highest NH4-N concentration occurs dur-ing the thermophilic phase, but the concentration quickly declinesas the process progresses. In the thermophilic phase, OM degrada-tion (NH4-N production) and aeration demand are at their maxima,pH is usually >7.5 and nitrification hardly occurs because the hightemperatures inhibit the action of the microorganisms responsiblefor the process (de Bertoldi et al., 1983; Tiquia, 2002). All theseconditions favour NH3-volatilisation (Tiquia, 2002; Witter and

López-Real, 1988). Nitrification, detected by the formation ofNO3-N, occurs when the temperature falls below thermophilic val-ues (40 �C), the intensity of the process depending on the amountof NH4-N available to the nitrifying bacteria (Tiquia, 2002). Most ofthe nitrification occurs during maturation, leading to a low NH4-N/NO3-N ratio in mature compost (Bernal et al., 1998a).

Nitrogen losses impact negatively on the manure compostingprocess, by decreasing nutrient concentration and hence compostquality, and generate health and environmental problems. Nitro-gen losses through composting can occur by NH3-volatilisation,leaching and denitrification. Denitrification can occur as a resultof the development of anaerobic microsites within the material.Thus, the aerobic conditions of the compost should be ensuredthroughout the process. Parkinson et al. (2004) indicated thatemission rates of N2O–N were very much lower (about 10 times)than those of NH3–N during composting of cattle manure withwheat straw. Similar results were found by Martins and Dewes(1992) during composting of animal slurries with straw in a com-poster, with NOx <5%. Losses by leaching can be reduced easily bycontrolling the moisture content of the pile and by an adequatecomposting system, designing the installation with an adequatecover from the rain and a system for leachate collection and recir-culation within the same compost. The losses as NH4-N can be par-ticularly relevant at the beginning of the process (Martins andDewes, 1992) and as NO3-N in the last phase of composting, whenthe nitrification occurs (Parkinson et al., 2004), since nitrate is avery mobile anion, highly soluble. The lack of leachate collectioncan imply a risk of nitrate contamination of the groundwater.

Therefore, most N-losses during composting of animal manureshave been found to be due to ammonia volatilisation (Eghball et al.,1997; Martins and Dewes, 1992; Paillat et al., 2005; Parkinsonet al., 2004). High N-losses occur in manure composting due tothe high initial NH4-N concentration and the presence of easilymineralisable compounds, such as uric acid in poultry manureand slurry. Martins and Dewes (1992) found that during compost-ing of animal slurry with straw NH3-emissions decreased in the or-der: poultry (77%) > pig (54%) > cattle (47%). As shown in Table 2,

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nitrogen losses can reach 60% of initial N for pig manure, up to 58%for poultry manure and up to 46% for cattle manure.

The main factors conditioning NH3-volatilisation are thoseimplicated in the reactions involved in the following processes:formation of NHþ4 in the compost, its deprotonation for NH3 forma-tion, conversion of ammonia in solution in the compost intoammonia gas and transfer of ammonia in the gas phase of the com-post to the atmosphere

NHþ4 ðcompostÞ $ NH3 ðcompostÞ þHþ $ NH3ðgasÞ $ NH3 ðatmosphereÞ

Therefore, the main factors controlling NH3-losses are the com-position of the initial mixture, such as total-N, C/N ratio, degrad-able organic-C and particle size, and the composting conditions,such as temperature and turning frequency (composting system).These are reviewed in the following paragraphs.

Eghball et al. (1997) associated most of the N-losses during cat-tle manure composting with ammonia volatilisation (>92%), thisbeing conditioned by the C/N ratio, turning frequency and particlesize of the bulking agent. Also, Barrington et al. (2002) noted theimportance of particle size as a factor affecting carbon availabilityand hence N immobilisation by microorganisms during compost-ing. Martins and Dewes (1992) identified initial nitrogen content,temperature, high pH (>8) and turning as the main factors whichaffected gaseous emissions during composting of slurries. As theoxygen supply into the composting mass controls important pro-cesses such as biodegradation, ammonification and nitrification,then the aeration rate exerts an important influence on nitrogendynamics (Guardia et al., 2008).

The addition of carbon sources to wastes rich in inorganic-N canresult in its partial incorporation into the organic fractions or itsimmobilisation to form such fractions. During composting of pigslurry and wheat straw initial immobilisation of NH4-N was foundby Bernal et al. (1993). The impact of N immobilisation by themicrobial biomass on NH3-volatilisation was highlighted by Paillatet al. (2005) in composting experiments with pig manure and slur-ry. They noted that nitrogen immobilisation by the microbial bio-mass depends on carbon biodegradability and hence factors suchas oxygen (free air space), moisture and C and N biodegradabilityaffect gaseous emissions. They concluded that reduced NH3 emis-sion implies active immobilisation of the NH4-N by the microbialbiomass and that the presence of the less biodegradable organic-C in sawdust increased NH3 emission, which was decreased byincreasing the ratio of wheat straw in manure composting. Duringcomposting of dairy manure and wheat straw, the addition of areadily available carbon source such as molasses greatly reducedammonia losses, while no significant reduction occurred when car-bon was hardly degradable, for example when supplied as officepaper (Liang et al., 2006). Therefore, amending materials rich inavailable carbon can reduce nitrogen losses during the compostingof organic wastes with a high nitrogen concentration. So, for effec-tive composting to obtain a high quality compost, the selection ofthe bulking agent is essential. Paredes et al. (1996) found thatchanging the bulking agent from cotton waste to maize straw de-creased OM degradation, organic-N mineralisation and thereforeNH3-losses in sewage sludge composting. Mahimairaja et al.(1994) found a N-loss of only 11.2% during 12 weeks of compostingof poultry manure and maize straw, while the losses accounted for25.5% of total-N in composting of poultry manure and cotton waste(Paredes et al., 1996).

The loss of nitrogen from compost piles also depends on the dif-fusion of NH3 through the pile into the atmosphere, and frequentturning of the pile facilitates this NH3-volatilisation (de Bertoldiet al., 1982). Solano et al. (2001) found that during composting ofsheep manure and barley straw, total-N losses were higher than25% in a pile managed with turning in comparison with no losses

and losses of 4.5% with passive and forced aeration, respectively.Parkinson et al. (2004) found that increasing the number of turnsfrom 1 to 3 increased the ammonia-N losses during compostingof cattle manure, these being 11% and 18% of initial total-N, respec-tively. The system used for turning operations also had a highinfluence on ammonia losses. Turning by a rear-discharge manurespreader instead of with a front-end loader increased N-losses to17% and 51% of initial total-N for the 1- and 3-turning-time treat-ments, respectively. The Rutgers static pile composting systemmaintains a temperature ceiling in the pile, providing a highdecomposition rate through the on-demand removal of heat byventilation, since high temperatures inhibit and slow downdecomposition due to a reduction of microbial activity (Finsteinet al., 1985). This system has been shown to be a good methodfor lowering N-losses through NH3-volatilisation and hence forproducing a N-rich compost with high concentrations of NO3-Nand total-N (Sánchez-Monedero et al., 1996).

As composting progresses, stable N compounds are formed,which are less susceptible to volatilisation, denitrification andleaching. Therefore, stabilised materials such as composts seemto constitute a better source of OM and nitrogen for the soil, froman agricultural point of view (Pare et al., 1998).

When a comparison among manure management options isestablished, composting leads to higher C and N-losses comparedto stockpiling or a direct application to soil (Larney et al., 2006).However, composting also transforms the OM into a more stable,sanitised and partially humified end-product compared to freshmanure and compost will increase the soil OM to a greater extentthan untransformed wastes (Bernal et al., 1998b). Therefore, for C-conservation, the losses occurring during composting and thoseoccurring after soil application should be considered. Accordingto the results of Bernal et al. (1998b) the addition of mature com-post to soil is more favourable from the viewpoint of C-conserva-tion in the system, reducing C-losses in comparison with the useof fresh wastes. In addition, nutrients in composted materials areless susceptible to losses by leaching and volatilisation, and com-posting also avoids the spreading of pathogens.

4.2. Humification process

The humified fraction of the soil OM is the most important oneresponsible for organic fertility functions in the soil as it is the frac-tion most resistant to microbial degradation. So the evaluation ofthe humification degree of the OM during composting is an agro-nomic criterion for compost quality. The agricultural value of acompost increases when the OM reaches a high level of humifica-tion. The humification of the OM during composting is revealed bythe formation of humic acids with increasing molecular weight,aromatic characteristics, oxygen and nitrogen concentrations andfunctional groups, in agreement with the generally accepted humi-fication theories of soil OM (Senesi, 1989). During composting, hu-mic substances (alkali-extractable organic-C, CEX) are producedand humic acid-like organic-C (CHA) increases, while fulvic acid-like organic-C (CFA) and water-extractable organic-C decrease dueto microbial degradation. Some indices used for evaluation of thehumification level in the material during composting include(Roletto et al., 1985; Senesi, 1989):

– Humification ratio (HR): CEX/Corg � 100;– Humification index (HI): CHA/Corg � 100;– Percent of humic acids (PHA): CHA/CEX � 100;– Polymerisation index (PI): CHA/CFA.

The increase of such parameters during composting is indica-tive of the humification of the OM. Roletto et al. (1985) used theseparameters to establish the humification level of the OM of com-

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posts from different origins, including farmyard manure. The limitestablished were: HR P 7.0; HI P 3.5; PHA P 50; and PI P 1.0. Anew humification index was developed by Sequi et al. (1986) basedon the assumption that non-humic compounds can be co-extractedwith the humic substances during the alkaline extraction proce-dure. Thus, the new humification index was defined as the ratioof non-humic substances to humic substances: CNH/(CHA + CFA)<1.0, for a good degree of humification.

The most appropriate and reliable approach to the evaluation ofthe humic character and behaviour of the compost is based on theidentification of the chemical and structural composition and func-tional properties, also in comparison with those of humic sub-stances from native soil. Numerous chemical, physico-chemicaland spectroscopic methods have been used, such as (Senesi,1989): elemental and functional group composition, ratio of absor-bances measured at 465 and 665 nm (E4/E6), molecular weight dis-tribution, electrophoresis and electrofocusing, pyrolysis-gaschromatography–mass spectrometry (GC–MS), infrared and Fou-rier transformed-infrared (FT-IR) spectroscopy, electron spin reso-nance (ESR) spectroscopy and fluorescence spectroscopy (Moralet al., 2009, in this special issue). Amongst these methods, ad-vanced techniques such as NMR, FT-IR and pyrolysis have beenemployed to achieve a better understanding of the structuralchanges of the OM during composting and hence to evaluate com-posting efficiency and compost maturity; this was reviewed thor-oughly by Chen (2003). Functional group analysis is the mostsensitive method for studying the changes produced in the humicacid structure, compared to other methods such as elemental anal-ysis, gel permeation chromatography and infrared spectroscopy.The composting process yields humic acids with chemical andstructural characteristics where similar to those of the more humi-fied soil humic acids (Sánchez-Monedero et al., 2002).

5. Maturity assessment for quality compost

The principal requirement of a compost for it to be safely usedin soil is a high degree of stability or maturity, which implies a sta-ble OM content and the absence of phytotoxic compounds andplant or animal pathogens. Maturity is associated with plant-growth potential or phytotoxicity (Iannotti et al., 1993), whereasstability is often related to the compost’s microbial activity. How-ever, both stability and maturity usually go hand in hand, sincephytotoxic compounds are produced by the microorganisms inunstable composts (Zucconi et al., 1985).

Compost maturity and stability are often used interchangeably.However, they each refer to specific properties of these materials.

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

Physical: Odour, colour, temperature, particle size and inert materialsChemical: Carbon and nitrogen

analyses– C/N ratio in solid and water extract

Cation exchangecapacity

– CEC, CEC/total organic-C ratio, etc.

Water-soluble extract – pH, EC, organic-C, ions, etc.Mineral nitrogen – NH4-N content, NH4-N/NO3-N ratioPollutants – Heavy metals and organics.Organic matter quality,humification

– Organic composition: lignin, complex carb– Humification indices and humic-like sub

weight distribution, E4/E6 ratio, pyrolysisBiological: Microbial activity

indicators:– Respiration (O2 uptake/consumption, CO2

– Enzyme activity (phosphatases, dehydrog– ATP content– Nitrogen mineralisation–immobilisation p– Microbial biomass

Phytotoxicity: – Germination and plant growth testsOthers: – Viable weed seed, pathogen and ecotoxicit

Stability refers to a specific stage or decomposition or state ofOM during composting, which is related to the types of organiccompounds remaining and the resultant biological activity in thematerial (California Compost Quality Council, 2001). Several defi-nitions for compost stability have been used: Bernal et al.(1998a) related stability to compost microbial activity; The UKComposting Association (2001) defined stability as ‘the degree ofbiological decomposition that composting feedstocks haveachieved’; Hue and Liu (1995) related stability to microbial activityand hence the potential for unpleasant odour generation.

Maturity is the degree or level of completeness of compostingand implies improved qualities resulting from ‘ageing’ or ‘curing’of a product. The California Compost Quality Council (CCQC,2001) defined maturity as ‘the degree or level of completeness ofcomposting’, and the UK Composting Association (2001) definedmaturity simply as ‘the degree to which a compost has matured’,and mature compost as ‘compost that does not have a negative af-fect on seed germination or plant growth’. Bernal et al. (1998a) de-scribed maturity as implying ‘a stable OM content and the absenceof phytotoxic compounds and plant or animal pathogens’. Similardefinitions were used by Chen and Inbar (1993), Iannotti et al.(1993) and Hue and Liu (1995). Immature and poorly stabilisedcomposts may pose a number of problems during storage, market-ing and use. During storage these materials may develop anaerobic‘‘pockets” which can lead to odours and the development of toxiccompounds. Continued active decomposition when these materialsare added to soil or growth media may have negative impacts onplant growth due to a decreased supply of oxygen and/or availablenitrogen or the presence of phytotoxic compounds.

Maturity is not described by a single property and thereforematurity is best assessed by measuring two or more parametersof compost. Maturity is, in part, affected by the relative stabilityof the material but also describes the impact of other compostchemical properties on plant development. Some immature com-posts may contain high amounts of free ammonia, certain organicacids or other water-soluble compounds which can limit seed ger-mination and root development. All uses of compost require a ma-ture product free of these potentially phytotoxic components. Anumber of criteria and parameters have been proposed for testingcompost maturity, although most of them refer to composts madefrom city refuse. Maturity parameters are based on different prop-erties: physical, chemical and biological, including microbial activ-ity (Table 3).

Physical characteristics such as colour, odour and temperaturegive a general idea of the decomposition stage reached, but give lit-tle information as regards the degree of maturation. Chemical

ohydrates, lipids, sugars, etc.stances characterisation: elemental and functional group analyses, molecularGC-MS, spectroscopic analyses (NMR and FTIR, Fluorescence, etc.), etc.production, self-heating test, biodegradable constituents)

enases, proteases, etc.)

otential, nitrification, etc.

y tests

5450 M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453

methods are widely used, including measurement of the C/N ratioin the solid phase (Bernal et al., 1998a; Iglesias-Jimenez and Perez-Garcia, 1992) and in the water extract (Chanyasak and Kubota,1981; Hue and Liu, 1995), water soluble organic-C (Bernal et al.,1998a; Hue and Liu, 1995; Zmora-Nahum et al., 2005), the watersoluble organic-C/total organic-N ratio (Bernal et al., 1998a; Hueand Liu, 1995), volatile organic acids (Iannotti et al., 1994; Manioset al., 1989), nitrification (NH4-N concentration and NH4-N/NO3-Nratio; Bernal et al., 1998a; Finstein and Miller, 1985; Zucconi andde Bertoldi, 1987), cation exchange capacity (CEC) (Harada andInoko, 1980) and the degree of OM humification (de Nobili and Pet-russi, 1988; Iglesias-Jimenez and Perez-Garcia, 1992). Also, thepresence of phytotoxic substances such as phenolic acids and vol-atile fatty acids (Kirchmann and Widen, 1994) may indicate imma-ture composts.

Composting is a biochemical transformation of OM by microor-ganisms whose metabolism occurs in the water-soluble phase.Therefore, a study of the changes occurring in the soluble OMcan be useful for assessing compost maturity. A water soluble or-ganic-C/organic-N ratio of 5–6 was established by Chanyasak andKubota (1981) as an essential indicator of compost maturity (Table4). However, this ratio is sometimes difficult to evaluate since theconcentration of organic-N in the water extract of mature samplesis usually very low. For this reason, Hue and Liu (1995) and Bernalet al. (1998a) suggested using the water soluble organic-C/total or-ganic-N ratio as a parameter for assessing compost maturity. Dis-solved organic carbon is the most active fraction of carbon and isindicative of compost stability (Wu et al., 2000). Bernal et al.(1998a) established a limit of water-soluble organic-C <1.7% to de-scribe mature composts produced from a wide range of wastes,including animal manures, while 1.0 and 0.4% were set by Hueand Liu (1995) and Zmora-Nahum et al. (2005), respectively.

Compost maturity can also be defined in terms of nitrification.When the NH4-N concentration decreases and NO3-N appears inthe composting material it is considered ready to be used as acompost (Finstein and Miller, 1985). A high level of NH4-Nindicates unstabilised material, leading Zucconi and de Bertoldi(1987) to establish a limit of 0.04% for mature city refuse compost.An NH4-N/NO3-N ratio lower than 0.16 was established byBernal et al. (1998a) as a maturity index for composts of all origins(Table 4).

Since maturation also implies the formation of some humic-likesubstances, the degree of OM humification is generally accepted asa criterion of maturity. Studies in this respect refer to the humifi-

Table 4Maturity indices established for composts of different sources.

Parameter Value

Water soluble (C/N) 5–6Germination index >50%NH4-N <0.4 g/kC/N <20, preCO2 production rate 6120 mWater soluble organic-C 610 g/kWater soluble (C/N) 616Water soluble organic-C/Total organic-N 60.70CEX 660 g/kCFA 612.5 gCEX/Water soluble organic-C P6.0C/N <12Water soluble organic-C <17 g/kWater soluble organic-C/Total organic-N <0.55NH4-N/NO3-N <0.16NH4-N <0.4 g/kMineralisable-C in 70 days <30%NO3-N/CO2–C ratio (per day) >8Water soluble organic-C 64 g/kg

cation ratio, humification index, percent of humic acid, humic acidto fulvic acid ratio and the chemical, physico-chemical and spec-troscopic characterisation of humic-like substances. Iglesias-Jime-nez and Perez-Garcia (1992) established maturity indices basedon the humification level of the OM for city refuse compost. Hueand Liu (1995) proposed a CFA content of 612.5 g/kg, aCEX 660 g/kg and a CEX/water-soluble organic-C ratio P6.0, for ma-ture composts of different origin (Table 4). However, these humifi-cation parameters are not useful for indicating maturity in all kindsof compost (Bernal et al., 1998a; Paredes et al., 2000), since the fi-nal values of the humic acid content, humic to fulvic acid ratio andhumification index depend on the origin of the waste used forcomposting. Their evolution during composting reveals the humi-fication process of the OM but a limit value cannot be fixed forexpressing compost maturity. The humification process producesfunctional groups, and so increased oxidation of the OM leads toa rise in CEC, for which reason this parameter has been used toevaluate the maturity of city refuse compost (>60 meq/100 g, Hara-da and Inoko, 1980; 67 meq/100 g, Iglesias-Jimenez and Perez-Gar-cia, 1992). However, these values cannot be used in compost fromwastes such as animal manures, since the limit can be reached inthe wastes before composting (Bernal et al., 1996; Bernal et al.,1998a; Paredes et al., 2000).

The maturity of a compost can be assessed by its microbial sta-bility, by determining microbial activity factors such as the micro-bial biomass count and its metabolic activity, and by theconcentration of easily biodegradable constituents. The aerobicrespiration rate was previously selected as the most suitableparameter to assess aerobic biological activity and hence stability.In aerobic conditions, one carbon atom derived from catabolism isattached to two oxygen atoms to form carbon dioxide, releasingenergy, including heat, in the process. Therefore, respiration canbe measured in several ways: carbon dioxide evolution, oxygenconsumption and self-heating, which are indicative of the amountof degradable OM still present and which are related inversely tostabilisation (Zucconi and de Bertoldi, 1987). Self-heating usesthe Dewar flask method and actually measures temperature risesdue to all exothermic biological and chemical activity, so it is notstrictly a true measure of respiration, because many biologicaland chemical reactions not connected to respiration are exother-mic. An insufficiently mature compost has a strong demand forO2 and high CO2 production rates, due to intense development ofmicroorganisms as a consequence of the abundance of easily bio-degradable compounds in the raw material. For this reason, O2

Reference

Chanyasak and Kubota (1981)Zucconi et al. (1981)

g Zucconi and de Bertoldi (1987)ferable <10 Mathur et al. (1993)g CO2/kg/h Hue and Liu (1995)g

g/kg

Bernal et al. (1998a)g

g

Cooperband et al. (2003)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-ity and maturity (Hue and Liu, 1995). Oxygen uptake and CO2 evo-lution are more direct and have been described as being oppositesides of the same equation under aerobic conditions (Barrena-Gómez et al., 2006; Iannotti et al., 1993, 1994).

CO2 evolution correlates directly with aerobic respiration and,of the three techniques considered, is the truest measure of respi-ration and hence aerobic biological activity (CCQC, 2001; Hue andLiu, 1995). Hue and Liu (1995) set the limit of the CO2 productionrate for compost maturity at 6120 mg CO2 kg�1 h�1 (Table 4).Wang et al. (2004) used a respiration rate of <1 mg CO2–C g�1

dw d-1 to define a highly stabilised compost from cattle and pigmanures. Cooperband et al. (2003) suggested a NO3-N/CO2–C ra-tio > 8 per day as an index of compost maturity (Table 4). Respiro-metric studies have been carried out in soils amended withcompost, in a proportion compatible with agricultural use; theseindicate the mineralisation of the compost’s OM (Bernal et al.,1998b; Morel et al., 1979). Mature compost was defined as havingmineralisable-C <30% of total organic-C in 70 days, with a rapidlymineralisable-C <7.2% of total organic-C and a slow mineralisationrate <0.35% of total organic-C d�1 (Bernal et al., 1998a).

Biological methods for estimating the degree of maturity arealso based on tests for phytotoxicity. Plant tests used in researchand in quality standards can be divided into four broad categories:germination tests (including root assessments) (Zucconi et al.,1981 and Zucconi et al., 1985), growth tests (assessment of top-growth and sometimes root mass), combinations of germinationand growth, and other biological methods such as enzyme activi-ties (Herrmann and Shann, 1993). According to Zucconi et al.(1981) a germination index below 50% characterises an immaturecompost (Table 4). Zucconi and de Bertoldi (1987) discussed thedifferences between germination and growth tests. Germinationtests provide an instant picture of phytotoxicity, whereas growingtests will be affected by continuing changes in the stability ormaturity of the compost tested: there may be damaging effectson growth in the earlier stages, but beneficial effects later on, withdifferent conclusions depending on the time of assessment. García-Gómez et al. (2001) also looked at both germination index and pottrials, the yield of ryegrass showing phytotoxic effects from imma-ture compost even when the germination index was above 87%.The relationship between the CO2 respiration and phytotoxicityof immature compost was studied by García-Gómez et al. (2003),using the CO2–C production by OM mineralisation, N-mineralisa-

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

C/N ratio 625

Stability Thresholds (group A)

Method Units

Specific oxygen uptake rate mg O2/g OM/dCO2 evolution rate mg CO2–C/g OM/dDewar self-heating test Dewar indexHeadspace CO2 (Solvita�) Colour codeBiologically available C mg CO2–C/g C/d

Maturity Thresholds (group B)

Method units

NH4-N mg/kg dwNH4-N/NO3-N –Seedling emergence % of controlSeedling vigour % of controlIn-vitro germination index % of controlEarthworm bioassay % Weight gainNH3 (Solvita�) Colour codeVolatile fatty acids mmol/g dw

tion and plant growth. The CO2–C evolved correlated with plantgrowth, and immature compost caused N-immobilisation in thesoil, leading to plant N-deficiency.

Those chemical and biological parameters already discussedhave been used to evaluate maturity in manure compost(Gómez-Brandón et al., 2008; Goyal et al., 2005; Huang et al.,2006; Solano et al., 2001; Tiquia and Tam, 1998). These authorsidentified decreases in water-soluble organic-C, NH4-N, phytotoxiceffects and microbial activity and increases in the humification ofthe OM as indicators of the progressive stabilisation of the com-posting materials, leading to an acceptable degree of maturitybased on the established indices in the literature for composts ofdifferent origin. Also, Michel et al. (2004) and Wang et al. (2004)used the criterion of CO2 evolution rate <0.5 mg CO2–C g�1 OMd�1 or <1 mg CO2–C g�1 dw d�1, respectively, to consider compostsderived from manure as stable materials. Changa et al. (2003) con-cluded that CO2 and the NH3 Solvita� test can be employed to char-acterise the maturity/stability stage for quality control ofcomposted manures. Mathur et al. (1990), Guerra-Rodríguezet al. (2001, 2003) assessed phytotoxicity in germination tests, asan indicator of the maturity of manure compost. Tiquia (2005) pro-posed that values <35 lg TPF (triphenyl formazan) g�1 for dehy-drogenase activity can be used as a maturity indicator formanures. Ko et al. (2008) proposed the following maturity indicesfor manure and sawdust compost: NH4/NO3 <1.0, NH3-emission<20 ppm, CHA/CFA >2.5 and germination index >110.

The relevance of maturity and stability parameters to assesscompost quality is widely recognised by researchers. But integra-tion of the most reliable indices seems to be the sole option forevaluation of the maturity/stability stage of composted materials(Eggen and Vethe, 2001; Mathur et al., 1993; Riffaldi et al.,1986). A clear example of this is the CCQC maturity assessmentprocess (CCQC, 2001; TMECC, 2002), which considered first that acompost with a C/N ratio >25 is immature. When the C/N is 625,at least one test of group A (stability) and another of group B(maturity) must be determined (Table 5). Then, the maturityassessment matrix is applied to classify the material as very ma-ture, mature or immature. According to the maturity classificationof the compost, the CCQC gives general guidelines for compost bestuses: ‘‘very mature” can be used for soil and peat-based containerplant mixes, alternative topsoil blends and turf top-dressing;‘‘mature” compost for general field use (pastures), vineyards, rowcrops and as a substitute for low analysis organic fertilisers in some

Very stable Stable Unstable

<3 3–10 >10<2 2–4 >4V V <V7–8 5–6 1–4<2 2–4 >4

Very mature Mature Immature

<75 75–500 >500<0.5 0.5–3.0 >3.0>90 80–90 < 80>95 85–95 <85>90 80–90 <80<20 20–40 >405 4 3–1<200 200–1000 >1000

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cases; ‘‘immature” compost should be used for land application tofallow soil and as a feedstock for compost. However, other qualitycriteria apart from maturity determine the compost quality, suchas the nutrient content, ammonia, pH and soluble salts, and theyshould be also taken into account to define the compost use.

Therefore, the development of a market for compost materialswhich supports or promotes a waste composting strategy greatlydepends on the definition and adoption of quality standards (Brin-ton, 2000; Hogg et al., 2002). However, there are several compostquality standards proposed by official and private organisations(BOE, 2005; BSI, 2005; European Commission, 2001; Ge et al.,2006; TMECC, 2002), which take into account compost propertiessuch as foreign matter (inert contamination), potentially toxic ele-ments (organic contaminants and heavy metals), sanitisation(pathogens and phytopathogens), maturity and stability, weedseeds, water, OM and nutrient content. Currently, there is a needfor harmonisation of such criteria at the international level.

6. Conclusions

The composting of animal manures has been demonstrated tobe an effective method for producing end-products which are sta-bilised and sanitised, ensuring their maximum benefit for agricul-ture. However, the compost should be of high quality in order toguarantee its marketability.

Amongst the controllable factors which influence manure com-posting, the selection of appropriate bulking agents plays an essen-tial role in controlling the decomposition rate and favouring Nretention within the compost. In this sense, strategies such as addi-tion of a bulking agent with degradable organic-C, to enhance ini-tial N immobilisation, and process control (moisture, temperature,aeration/turning and particle size) have been shown to reduceammonia volatilisation and hence nitrogen losses, these being amajor concern in manure composting from an environmental pointof view.

The agricultural value of a compost increases when the OMreaches a high level of stability and maturity, which cannot beestablished by a single parameter. Several indices based on chem-ical and stability parameters have been used for manure compostby different authors. However, it is necessary to standardise thecriteria used by official institutions from different countries.

Acknowledgements

The authors thank the Organisation for Economic Co-operationand Development, Co-operative Research Programme: BiologicalResource Management for Sustainable Agricultural Systems, forinviting Dr. Bernal to participate in the workshop ‘‘Livestock WasteTreatment Systems of the Future: a challenge to environmentalquality, food safety, and sustainability”, where this paper waspresented.

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