Composting of animal manures and chemical criteria for compost maturity assessment. A review

Bioresource Technology 100 (2009) 5444–5453

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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 b

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 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 2008 Received in revised form 7 November 2008 Accepted 19 November 2008 Available online 31 December 2008 Keywords: Animal manure Composting Compost quality Maturity indices Microbial stability

a b s t r a c t New livestock production systems, based on intensification in large farms, produce huge amount of manures and slurries without enough agricultural land for their direct application as fertilisers. Composting is increasingly considered a good way for recycling the surplus of manure as a stabilised and sanitised endproduct for agriculture, and much research work has been carried out in the last decade. However, high 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 first part of this paper explains the basic concepts of the composting process and how manure characteristics can influence its performance. Then, a summary of those factors such as nitrogen losses (which directly reduce the nutrient content), organic matter humification and compost maturity which affect the quality of composts produced by manure composting is presented. Special attention has been paid to the relevance of using an adequate bulking agent for reducing N-losses and the necessity of standardising the maturity indices due to their great importance amongst compost quality criteria. Ó 2008 Elsevier Ltd. All rights reserved.

1. Introduction Composting of organic wastes is a biooxidative process involving the mineralisation and partial humification of the organic matter, leading to a stabilised final product, free of phytotoxicity and pathogens and with certain humic properties (Zucconi and de Bertoldi, 1987). During the first phase of the process the simple organic carbon compounds are easily mineralised and metabolised by the microorganisms, producing CO2, NH3, H2O, organic acids and heat. The accumulation of this heat raises the temperature of the pile. Composting is a spontaneous biological decomposition process of organic materials in a predominantly aerobic environment. During the process bacteria, fungi and other microorganisms, including microarthropods, break down organic materials to stable, usable organic substances called compost. The composting also implies the volume reduction of the wastes, the destruction of weed seeds and of pathogenic microorganisms. The intensity and concentrated activity of the livestock industry generate vast amounts of biodegradable wastes, which must be managed under appropriate disposal practices to avoid a negative impact on the environment (odour and gaseous emissions, soil and water pollution, etc.; Burton and Turner, 2003). Composting cannot be considered a new technology, but amongst the waste manage* Corresponding author. Tel.: +34 968 396200; fax: +34 968 396213. E-mail address: [email protected] (M.P. Bernal). 0960-8524/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2008.11.027

ment strategies it is gaining interest as a suitable option for manures with economic and environmental profits, since this process eliminates or reduces the risk of spreading of pathogens, parasites and weed seeds associated with direct land application of manure and leads to a final stabilised product which can be used to improve and maintain soil quality and fertility (Larney and Hao, 2007). Composting of animal manures has been traditionally carried out by the farmers after manure collection for better handling, transport and management. Frequently the wastes were heaped up with little regard to control of the process conditions (aeration, temperature, ammonia loss, etc.) and with rudimentary methodology. However, as the fertiliser value of animal manures has been always recognised, nowadays their composting is seen as an alternative way of recycling the manures in farms without enough agricultural land for their direct use as a fertiliser. But, the cost of composting of animal manures can be considerably higher than the direct utilisation of raw manures. Therefore, composting is justified for manures that need to be partially sterilised (Parkinson et al., 2004), and also when compost of high quality is produced, to offset the production costs. The present paper reviews the factors affecting the composting of animal manures for production of high quality compost with added agricultural value, focusing on the nutrient content, organic matter (OM) humification and maturity degree. Complementary information on safety and environmental aspects related to manure composting is reviewed by Moral et al. (2009) in this OECD

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special issue, including the suppressive effect against phytopathogens of compost and recent techniques to determine the OM humification process during composting.

2. The basic concepts of the composting process While composting occurs naturally, efficient composting requires the control of several factors to avoid nuisance problems such as odours and dust, and also for obtaining a quality agricultural product. The controlled conditions are basic for a composting procedure, distinguishing it from aerobic fermentation. Over the last decades, research has been focused on the study of the complex interaction amongst physical, chemical and biological factors that occurs during composting. Therefore, the control of parameters such as bulk density, porosity, particle size, nutrient content, C/N ratio, temperature, pH, moisture and oxygen supply have demonstrated to be key for composting optimisation since they determine the optimal conditions for microbial development and OM degradation (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 adequate initial substrate conditions that must be controlled and maintained as composting progresses. Although it is difficult to generalise for all type of substrates and management conditions, the basic and applied aspects of composting have been summarised in this section. For a particular composting formulation, specific references can be found. The factors affecting the composting process can be divided into two groups: those depending on the formulation of the composting mix, such as nutrient balance, pH, particle size, porosity and moisture; and those dependent on the process management, such as O2 concentration, temperature and water content. Nutritional balance is mainly defined by the C/N ratio. Microorganisms require an energy source (degradable organic-C) and N for their development and activity. The adequate C/N ratio for composting is in the range 25–35, because it is considered that the microorganisms require 30 parts of C per unit of N (Bishop and Godfrey, 1983). High C/N ratios make the process very slow as there is an excess of degradable substrate for the microorganisms. But with a low C/N ratio there is an excess of N per degradable C and inorganic N is produced in excess and can be lost by ammonia volatilisation or by leaching from the composting mass. Then, low C/N ratios can be corrected by adding a bulking agent to provide degradable organic-C. pH: A pH of 6.7–9.0 supports good microbial activity during composting. Optimum values are between 5.5 and 8.0 (de Bertoldi et al., 1983; Miller, 1992). Usually pH is not a key factor for composting since most materials are within this pH range. However, this factor is very relevant for controlling N-losses by ammonia volatilisation, which can be particularly high at pH >7.5. Elemental sulphur (So) has been used as an amendment for avoiding excessively high pH values during composting (Mari et al., 2005). Microorganisms: OM decomposition is carried out by many different groups of microbial populations (Ryckeboer et al., 2003). The microorganisms involved in composting develop according to the temperature of the mass, which defines the different steps of the process (Keener et al., 2000). Bacteria predominate early in composting, fungi are present during all the process but predominate at water levels below 35% and are not active at temperatures >60 °C. Actinomycetes predominate during stabilisation and curing, and together with fungi are able to degrade resistant polymers. Particle size and distribution are critical for balancing the surface area for growth of microorganisms and the maintenance of adequate porosity for aeration. The larger the particle size, the lower the surface area to mass ratio. So compost with large particles does not decompose adequately because the interior of the parti-

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cles has difficult accessibility for the microorganisms, as during decomposition particles may coat the surface with an impenetrable 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, packing and moisture content control the porosity of the composting mass. Porosity: Substrate porosity exerts a great influence on composting performance since appropriate conditions of the physical environment for air distribution must be maintained during the process. Porosity greater than 50% causes the pile to remain at a low temperature because energy lost exceeds heat produced. Too little porosity leads to anaerobic conditions and odour generation. The percentage air-filled pore space of composting piles should be in the range of 35–50%. Aeration: Aeration is a key factor for composting. Proper aeration controls the temperature, removes excess moisture and CO2 and provides O2 for the biological processes. The optimum O2 concentration is between 15% and 20% (Miller, 1992). Controlled aeration should maintain temperatures below 60–65 °C, which ensures enough O2 is supplied (Finstein and Miller, 1985). Moisture: The optimum water content for composting varies with the waste to be composted, but generally the mixture should be at 50–60% (Gajalakshmi and Abbasi, 2008). When the moisture content exceeds 60% O2 movement is inhibited and the process tends to become anaerobic (Das and Keener, 1997). During composting a large quantity of water can evaporate, to control temperature, and as water content diminishes the rate of decomposition decreases, then rewetting should be required in order to maintain the optimum moisture content for the microbial activity. Temperature: The temperature pattern shows the microbial activity and the occurrence of the composting process. The optimum temperature range for composting is 40–65 °C (de Bertoldi et al., 1983), temperatures above 55 °C are required to kill pathogenic microorganisms. But if the temperature achieved exceeds the tolerance range of the thermophilic decomposers, the effect is damaging for composting. At temperatures above 63 °C, microbial activity declines rapidly as the optimum for various thermophiles is surpassed, with activity approaching low values at 72 °C. The range of 52–60 °C is the most favourable for decomposition (Miller, 1992). The regulation of the temperature is required for controlled composting. Excess heat removal can be achieved through several strategies (Miller, 1992): control the size and shape of the composting mass; improve cooling and favourable temperature redistribution by turning operations, which means heat removal through evaporation cooling; and achieve superior temperature control in systems that actively remove heat through temperature feedback-controlled ventilation (Rutgers strategy). The development of the temperature profile indicates the different phases of the process. In general, the composting process can be divided into two main phases: the biooxidative phase and the maturing phase also called the curing phase (Bernal et al., 1996; Chen and Inbar, 1993). The biooxidative phase is developed in three steps (Keener et al., 2000): (i) an initial mesophilic phase lasting 1–3 days, where mesophilic bacteria and fungi degrade simple compounds such as sugars, amino acids, proteins, etc., increasing quickly the temperature; (ii) thermophilic phase, where thermophilic microorganisms degrade fats, cellulose, hemicellulose and some lignin, during this phase the maximum degradation of the OM occurs together with the destruction of pathogens; (iii) cooling phase, characterised by a decrease of the temperature due to the reduction of the microbial activity associated with the depletion of degradable organic substrates, the composting mass is recolonised by mesophilic microorganisms which are able to degrade the remaining sugars, cellulose and hemicellulose. During the different steps of the biodegradation phase, the organic compounds

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are degraded to CO2 and NH3, with the consumption of O2. However, during the maturation phase stabilisation and humification of the OM occur, producing a mature compost with humic characteristics in its OM. Thus, compost can be defined as the stabilised and sanitised product of composting, which has undergone an initial, rapid stage of decomposition, is beneficial to plant growth and has certain humic characteristics, making the composting of waste a key issue for sustainable agriculture and resource management (Gajalakshmi and Abbasi, 2008; Haug, 1993; Jakobsen, 1995; Zucconi and de Bertoldi, 1987). 3. Characteristics of the animal manures for composting Controlled composting allows the safe storage and transport of the final product, adds value to the product because compost is a more concentrated and uniform product than the manure, permits easy spreading and thus uniform distribution in the soil and results 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. The advantages of composting animal manures compared with direct 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 technology which adds value, producing a high quality product for multiple agricultural uses. Certain chemical characteristics of the animal manures are not adequate for composting and could limit the efficiency of the process: excess of moisture, low porosity, high N concentration for the organic-C, which gives a low C/N ratio, and in some cases high pH values (Table 1). Thus, adequate composting management of the manure is required in order to obtain a quality compost. Therefore, different aeration strategies, substrate conditioning-feedstock formulation, bulking agents and process control options have been used in manure composting in order to reduce composting time and costs and enhance the quality of the end-products (Lau et al., 1992; Michel et al., 2004; Solano et al., 2001).

Table 1 Average 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 Liquid manure/slurry Cattle 15–123 Pig 4.9–152 Poultry 10–367 Solid manure Cattle 140–300 Pig 150–330 Poultry 220–700 a b

Organic-C

Total-N

NH4-N

pH

3.8–36 1.0–65 11–112

2.0–7.0 0.6–7.8 2–21

1.0–4.9 0.3–6.6 1.9–9.4

7.1–8.4 6.7–8.9 7.9–8.8

65–126a 42–132a 103–597a

4.2–8.1 3.5–11 10–58

0.3–2.0 0.5–6.0 2.4–18

8.6b 8.1b 7.6b

Bernal, personal communication. Average values.

The addition of a bulking agent for manure composting optimises substrate properties such as air space, moisture content, C/ N ratio, particle density, pH and mechanical structure, affecting positively the decomposition rate. In this sense, lignocellulosic agricultural and forestry by-products are commonly used as bulking agents in co-composting of nitrogen-rich wastes, such as animal 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 byproducts such as pine shavings, chestnut burr and leaves and sawdust (Ahn et al., 2007; Barrington et al., 2002; Guerra-Rodríguez et al., 2001; Huang et al., 2004; Tiquia and Tam, 2002; Wang et al., 2004). All have low moisture and high organic-C contents and high C/N ratios (an average of 50 for cereal straw and >80 for wood by-products), which can compensate for the low values of the animal manures. 4. Strategies for producing high quality compost: nutrient content and OM humification The effectiveness of compost with regard to beneficial effects on soil physical, chemical and biological properties, as well as constituting a nutrient source, depends on the quality of the compost. The quality criteria for compost are established in terms of: nutrient content, humified and stabilised OM, the maturity degree, the hygienisation and the presence of certain toxic compounds such as heavy metals, soluble salts and xenobiotics. The first three factors are reviewed in the present paper, while those related to safety and environmental aspects are reviewed by Moral et al. (2009) in this OECD special issue. The production of compost with a high nutrient content requires the control and reduction of nutrient losses during the process, whilst to ensure a high degree of OM humification enough time should be allowed for the maturation phase. Finally, a high degree of compost maturity requires the establishment of adequate maturity indices. 4.1. Organic matter degradation and nitrogen losses During the active phase of the composting process the organicC decreases in the material due to decomposition of the OM by the microorganisms. This loss of OM reduces the weight of the pile and decreases the C/N ratio. The degradation rate of the OM decreases gradually as composting progresses because of the reduction in available carbon sources, and synthesis reactions of new complex and polymerised organic compounds (humification) prevail over mineralisation during the maturation phase. This process leads to stabilised end-products which act as slow-release fertilisers for agricultural purposes. However, the major concern of manure composting is to control C and N-losses since they reduce the agronomic value of compost and contribute to greenhouse gas emissions (Hao et al., 2004). The degradation of the OM during composting can be estimated 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 parameter used, it should be calculated as a mass balance, taking into account the dry weight reduction of the pile, instead of only the difference in concentration of OM or organic-C in the composting mass. During the composting process, substrate transformation is conditioned by the nature of the OM according to its degradability (Haug, 1993), this property affecting decomposition rate, gas emissions, duration and extent of the process and oxygen requirements. Labile organic compounds, such as simple carbohydrates, fats and amino acids, are degraded quickly in the first stage of composting;

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M.P. Bernal et al. / Bioresource Technology 100 (2009) 5444–5453 Table 2 Organic matter and organic-C losses by mineralisation and N-losses during composting of animal manures. Manure type

Bulking agent

Composting process

OM loss by mineralisation (% of initial OM)

N-loss (% of initial total-N)

Reference

Beef manure

–

Organic-C: 45–62

19–43

Beef manure

Fresh straw-bedded Woodchip-bedded –

Turned windrow Turned windrow Turned windrow Turned windrow Turned windrow In-vessel system Rutgers static pile Forcedventilation Rutgers static pile Turned windrow Unturned windrow Turned windrow

Organic-C: 53 Organic-C: 35 Organic-C: 67

42 12 46

Eghball et al. (1997) Hao et al. (2004)

Beef manure Dairy manure

Poultry manure

Sawdust and wood shavings Wheat straw Hardwood sawdust Wheat straw Wheat straw additives: molasses, office paper, and buffer solutions Cotton gin waste

Poultry litter

–

Pig slurry + Poultry manure Pig manure

Sweet sorghum bagasse

Dairy manure Dairy manure

Pig manure

(partially decomposed with cornstalk)

Shredded wood pallets and sawdust

OM: OM: OM: OM: OM:

67 Organic-C: 63a 67 Organic-C: 64ª 46–76 58–81 29–55a

5a Absenta 7–26 15–43 12–25

OM: 53 Organic-C: 52

26

OM: 9

58

OM: 62

<40

Organic-C: 50–72

3–59

Organic-C: 30–54 OM: 55 Organic-C: 52

Larney et al. (2006) Changa et al. (2003) Michel et al. (2004) Liang et al. (2006) Paredes et al. (1996) Tiquia and Tam (2002) Bernal et al. (1996) Tiquia et al. (2000)

8–60 a

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(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, hemicellulose and lignin are partially degraded and transformed at a lower rate. Therefore, composting involves a partial mineralisation of the organic substrate, leading to carbon losses throughout the process; this is compensated by the higher stabilisation degree of the remaining organic compounds. During composting of animal manures organic-C losses can reach 67% in cattle manure, 52% in poultry manure and 72% in pig manure (Table 2). The composting system and conditions, characteristics of both the bedding material and the bulking agent added for composting and even the environmental conditions of the season (winter or summer; Parkinson et al., 2004) have a great influence on the mineralisation of the OM during composting (Table 2). For instance, the use of woodchips instead of cereal straw as bedding material in beef manure reduced the organic-C loss during composting (Hao et al., 2004) due to the combination of larger particle size, higher C/N ratio and the recalcitrant nature of the woodchips. Similar results were shown by Hansen et al. (1989) and Michel et al. (2004) in composting of poultry manure and cow manure, respectively; they obtained a lower decomposition of the composting substrate when employing amendment materials with recalcitrant OM such as lignin. As a result of the dry weight loss of the material during composting, the concentration of mineral elements increases, if leaching does not occur or is controlled to a minimum. Generally the total N concentration increases during composting due to the concentration effect (Bernal et al., 1996; Paredes et al., 1996). The evolution of N forms shows the mineralisation of the organic compounds during the active phase of composting with the formation of NH4-N. Thus, the highest NH4-N concentration occurs during the thermophilic phase, but the concentration quickly declines as the process progresses. In the thermophilic phase, OM degradation (NH4-N production) and aeration demand are at their maxima, pH is usually >7.5 and nitrification hardly occurs because the high temperatures inhibit the action of the microorganisms responsible for the process (de Bertoldi et al., 1983; Tiquia, 2002). All these conditions favour NH3-volatilisation (Tiquia, 2002; Witter and

López-Real, 1988). Nitrification, detected by the formation of NO3-N, occurs when the temperature falls below thermophilic values (40 °C), the intensity of the process depending on the amount of NH4-N available to the nitrifying bacteria (Tiquia, 2002). Most of the 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 composting process, by decreasing nutrient concentration and hence compost quality, and generate health and environmental problems. Nitrogen losses through composting can occur by NH3-volatilisation, leaching and denitrification. Denitrification can occur as a result of the development of anaerobic microsites within the material. Thus, the aerobic conditions of the compost should be ensured throughout the process. Parkinson et al. (2004) indicated that emission rates of N2O–N were very much lower (about 10 times) than those of NH3–N during composting of cattle manure with wheat straw. Similar results were found by Martins and Dewes (1992) during composting of animal slurries with straw in a composter, with NOx <5%. Losses by leaching can be reduced easily by controlling the moisture content of the pile and by an adequate composting system, designing the installation with an adequate cover from the rain and a system for leachate collection and recirculation within the same compost. The losses as NH4-N can be particularly relevant at the beginning of the process (Martins and Dewes, 1992) and as NO3-N in the last phase of composting, when the nitrification occurs (Parkinson et al., 2004), since nitrate is a very mobile anion, highly soluble. The lack of leachate collection can imply a risk of nitrate contamination of the groundwater. Therefore, most N-losses during composting of animal manures have been found to be due to ammonia volatilisation (Eghball et al., 1997; Martins and Dewes, 1992; Paillat et al., 2005; Parkinson et al., 2004). High N-losses occur in manure composting due to the high initial NH4-N concentration and the presence of easily mineralisable compounds, such as uric acid in poultry manure and slurry. Martins and Dewes (1992) found that during composting of animal slurry with straw NH3-emissions decreased in the order: 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 those implicated in the reactions involved in the following processes: formation of NHþ 4 in the compost, its deprotonation for NH3 formation, conversion of ammonia in solution in the compost into ammonia gas and transfer of ammonia in the gas phase of the compost to the atmosphere

NHþ4 ðcompostÞ $ NH3

ðcompostÞ

þ Hþ $ NH3ðgasÞ $ NH3

ðatmosphereÞ

Therefore, the main factors controlling NH3-losses are the composition of the initial mixture, such as total-N, C/N ratio, degradable 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 cattle manure composting with ammonia volatilisation (>92%), this being conditioned by the C/N ratio, turning frequency and particle size of the bulking agent. Also, Barrington et al. (2002) noted the importance of particle size as a factor affecting carbon availability and hence N immobilisation by microorganisms during composting. Martins and Dewes (1992) identified initial nitrogen content, temperature, high pH (>8) and turning as the main factors which affected gaseous emissions during composting of slurries. As the oxygen supply into the composting mass controls important processes such as biodegradation, ammonification and nitrification, then the aeration rate exerts an important influence on nitrogen dynamics (Guardia et al., 2008). The addition of carbon sources to wastes rich in inorganic-N can result in its partial incorporation into the organic fractions or its immobilisation to form such fractions. During composting of pig slurry and wheat straw initial immobilisation of NH4-N was found by Bernal et al. (1993). The impact of N immobilisation by the microbial biomass on NH3-volatilisation was highlighted by Paillat et al. (2005) in composting experiments with pig manure and slurry. They noted that nitrogen immobilisation by the microbial biomass depends on carbon biodegradability and hence factors such as oxygen (free air space), moisture and C and N biodegradability affect gaseous emissions. They concluded that reduced NH3 emission implies active immobilisation of the NH4-N by the microbial biomass and that the presence of the less biodegradable organicC in sawdust increased NH3 emission, which was decreased by increasing the ratio of wheat straw in manure composting. During composting of dairy manure and wheat straw, the addition of a readily available carbon source such as molasses greatly reduced ammonia losses, while no significant reduction occurred when carbon was hardly degradable, for example when supplied as office paper (Liang et al., 2006). Therefore, amending materials rich in available carbon can reduce nitrogen losses during the composting of organic wastes with a high nitrogen concentration. So, for effective composting to obtain a high quality compost, the selection of the bulking agent is essential. Paredes et al. (1996) found that changing the bulking agent from cotton waste to maize straw decreased OM degradation, organic-N mineralisation and therefore NH3-losses in sewage sludge composting. Mahimairaja et al. (1994) found a N-loss of only 11.2% during 12 weeks of composting of poultry manure and maize straw, while the losses accounted for 25.5% 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 diffusion of NH3 through the pile into the atmosphere, and frequent turning of the pile facilitates this NH3-volatilisation (de Bertoldi et al., 1982). Solano et al. (2001) found that during composting of sheep manure and barley straw, total-N losses were higher than 25% 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 turns from 1 to 3 increased the ammonia-N losses during composting of cattle manure, these being 11% and 18% of initial total-N, respectively. The system used for turning operations also had a high influence on ammonia losses. Turning by a rear-discharge manure spreader instead of with a front-end loader increased N-losses to 17% and 51% of initial total-N for the 1- and 3-turning-time treatments, respectively. The Rutgers static pile composting system maintains a temperature ceiling in the pile, providing a high decomposition rate through the on-demand removal of heat by ventilation, since high temperatures inhibit and slow down decomposition due to a reduction of microbial activity (Finstein et al., 1985). This system has been shown to be a good method for lowering N-losses through NH3-volatilisation and hence for producing a N-rich compost with high concentrations of NO3-N and total-N (Sánchez-Monedero et al., 1996). As composting progresses, stable N compounds are formed, which are less susceptible to volatilisation, denitrification and leaching. Therefore, stabilised materials such as composts seem to constitute a better source of OM and nitrogen for the soil, from an agricultural point of view (Pare et al., 1998). When a comparison among manure management options is established, composting leads to higher C and N-losses compared to 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 fresh manure and compost will increase the soil OM to a greater extent than untransformed wastes (Bernal et al., 1998b). Therefore, for Cconservation, the losses occurring during composting and those occurring after soil application should be considered. According to the results of Bernal et al. (1998b) the addition of mature compost to soil is more favourable from the viewpoint of C-conservation in the system, reducing C-losses in comparison with the use of fresh wastes. In addition, nutrients in composted materials are less susceptible to losses by leaching and volatilisation, and composting also avoids the spreading of pathogens. 4.2. Humification process The humified fraction of the soil OM is the most important one responsible for organic fertility functions in the soil as it is the fraction most resistant to microbial degradation. So the evaluation of the humification degree of the OM during composting is an agronomic criterion for compost quality. The agricultural value of a compost increases when the OM reaches a high level of humification. The humification of the OM during composting is revealed by the formation of humic acids with increasing molecular weight, aromatic characteristics, oxygen and nitrogen concentrations and functional groups, in agreement with the generally accepted humification theories of soil OM (Senesi, 1989). During composting, humic substances (alkali-extractable organic-C, CEX) are produced and humic acid-like organic-C (CHA) increases, while fulvic acidlike organic-C (CFA) and water-extractable organic-C decrease due to microbial degradation. Some indices used for evaluation of the humification 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 indicative of the humification of the OM. Roletto et al. (1985) used these parameters to establish the humification level of the OM of com-

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posts from different origins, including farmyard manure. The limit established were: HR P 7.0; HI P 3.5; PHA P 50; and PI P 1.0. A new humification index was developed by Sequi et al. (1986) based on the assumption that non-humic compounds can be co-extracted with the humic substances during the alkaline extraction procedure. Thus, the new humification index was defined as the ratio of 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 of the humic character and behaviour of the compost is based on the identification of the chemical and structural composition and functional properties, also in comparison with those of humic substances from native soil. Numerous chemical, physico-chemical and spectroscopic methods have been used, such as (Senesi, 1989): elemental and functional group composition, ratio of absorbances measured at 465 and 665 nm (E4/E6), molecular weight distribution, electrophoresis and electrofocusing, pyrolysis-gas chromatography–mass spectrometry (GC–MS), infrared and Fourier transformed-infrared (FT-IR) spectroscopy, electron spin resonance (ESR) spectroscopy and fluorescence spectroscopy (Moral et al., 2009, in this special issue). Amongst these methods, advanced techniques such as NMR, FT-IR and pyrolysis have been employed to achieve a better understanding of the structural changes of the OM during composting and hence to evaluate composting efficiency and compost maturity; this was reviewed thoroughly by Chen (2003). Functional group analysis is the most sensitive method for studying the changes produced in the humic acid structure, compared to other methods such as elemental analysis, gel permeation chromatography and infrared spectroscopy. The composting process yields humic acids with chemical and structural characteristics where similar to those of the more humified 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 used in soil is a high degree of stability or maturity, which implies a stable OM content and the absence of phytotoxic compounds and plant or animal pathogens. Maturity is associated with plantgrowth potential or phytotoxicity (Iannotti et al., 1993), whereas stability is often related to the compost’s microbial activity. However, both stability and maturity usually go hand in hand, since phytotoxic compounds are produced by the microorganisms in unstable composts (Zucconi et al., 1985). Compost maturity and stability are often used interchangeably. However, they each refer to specific properties of these materials.

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Stability refers to a specific stage or decomposition or state of OM during composting, which is related to the types of organic compounds remaining and the resultant biological activity in the material (California Compost Quality Council, 2001). Several definitions for compost stability have been used: Bernal et al. (1998a) related stability to compost microbial activity; The UK Composting Association (2001) defined stability as ‘the degree of biological decomposition that composting feedstocks have achieved’; Hue and Liu (1995) related stability to microbial activity and hence the potential for unpleasant odour generation. Maturity is the degree or level of completeness of composting and 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 of composting’, and the UK Composting Association (2001) defined maturity simply as ‘the degree to which a compost has matured’, and mature compost as ‘compost that does not have a negative affect on seed germination or plant growth’. Bernal et al. (1998a) described maturity as implying ‘a stable OM content and the absence of phytotoxic compounds and plant or animal pathogens’. Similar definitions were used by Chen and Inbar (1993), Iannotti et al. (1993) and Hue and Liu (1995). Immature and poorly stabilised composts may pose a number of problems during storage, marketing and use. During storage these materials may develop anaerobic ‘‘pockets” which can lead to odours and the development of toxic compounds. Continued active decomposition when these materials are added to soil or growth media may have negative impacts on plant growth due to a decreased supply of oxygen and/or available nitrogen or the presence of phytotoxic compounds. Maturity is not described by a single property and therefore maturity is best assessed by measuring two or more parameters of compost. Maturity is, in part, affected by the relative stability of the material but also describes the impact of other compost chemical properties on plant development. Some immature composts may contain high amounts of free ammonia, certain organic acids or other water-soluble compounds which can limit seed germination and root development. All uses of compost require a mature product free of these potentially phytotoxic components. A number of criteria and parameters have been proposed for testing compost maturity, although most of them refer to composts made from city refuse. Maturity parameters are based on different properties: physical, chemical and biological, including microbial activity (Table 3). Physical characteristics such as colour, odour and temperature give a general idea of the decomposition stage reached, but give little information as regards the degree of maturation. Chemical

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

Biological:

Odour, colour, temperature, particle size and inert materials 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. Microbial activity – Respiration (O2 uptake/consumption, CO2 production, self-heating test, biodegradable constituents) – Enzyme activity (phosphatases, dehydrogenases, proteases, etc.) indicators: – ATP content – Nitrogen mineralisation–immobilisation potential, nitrification, etc. – Microbial biomass Phytotoxicity: – Germination and plant growth tests Others: – Viable weed seed, pathogen and ecotoxicity tests

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methods are widely used, including measurement of the C/N ratio in the solid phase (Bernal et al., 1998a; Iglesias-Jimenez and PerezGarcia, 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 water soluble organic-C/total organic-N ratio (Bernal et al., 1998a; Hue and Liu, 1995), volatile organic acids (Iannotti et al., 1994; Manios et al., 1989), nitrification (NH4-N concentration and NH4-N/NO3-N ratio; Bernal et al., 1998a; Finstein and Miller, 1985; Zucconi and de Bertoldi, 1987), cation exchange capacity (CEC) (Harada and Inoko, 1980) and the degree of OM humification (de Nobili and Petrussi, 1988; Iglesias-Jimenez and Perez-Garcia, 1992). Also, the presence of phytotoxic substances such as phenolic acids and volatile fatty acids (Kirchmann and Widen, 1994) may indicate immature composts. Composting is a biochemical transformation of OM by microorganisms whose metabolism occurs in the water-soluble phase. Therefore, a study of the changes occurring in the soluble OM can be useful for assessing compost maturity. A water soluble organic-C/organic-N ratio of 5–6 was established by Chanyasak and Kubota (1981) as an essential indicator of compost maturity (Table 4). However, this ratio is sometimes difficult to evaluate since the concentration of organic-N in the water extract of mature samples is usually very low. For this reason, Hue and Liu (1995) and Bernal et al. (1998a) suggested using the water soluble organic-C/total organic-N ratio as a parameter for assessing compost maturity. Dissolved organic carbon is the most active fraction of carbon and is indicative of compost stability (Wu et al., 2000). Bernal et al. (1998a) established a limit of water-soluble organic-C <1.7% to describe mature composts produced from a wide range of wastes, including animal manures, while 1.0 and 0.4% were set by Hue and 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 in the composting material it is considered ready to be used as a compost (Finstein and Miller, 1985). A high level of NH4-N indicates 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 by Bernal et al. (1998a) as a maturity index for composts of all origins (Table 4). Since maturation also implies the formation of some humic-like substances, the degree of OM humification is generally accepted as a criterion of maturity. Studies in this respect refer to the humifi-

cation ratio, humification index, percent of humic acid, humic acid to fulvic acid ratio and the chemical, physico-chemical and spectroscopic characterisation of humic-like substances. Iglesias-Jimenez and Perez-Garcia (1992) established maturity indices based on the humification level of the OM for city refuse compost. Hue and Liu (1995) proposed a CFA content of 612.5 g/kg, a CEX 660 g/kg and a CEX/water-soluble organic-C ratio P6.0, for mature composts of different origin (Table 4). However, these humification parameters are not useful for indicating maturity in all kinds of compost (Bernal et al., 1998a; Paredes et al., 2000), since the final values of the humic acid content, humic to fulvic acid ratio and humification index depend on the origin of the waste used for composting. Their evolution during composting reveals the humification process of the OM but a limit value cannot be fixed for expressing compost maturity. The humification process produces functional groups, and so increased oxidation of the OM leads to a rise in CEC, for which reason this parameter has been used to evaluate the maturity of city refuse compost (>60 meq/100 g, Harada and Inoko, 1980; 67 meq/100 g, Iglesias-Jimenez and Perez-Garcia, 1992). However, these values cannot be used in compost from wastes such as animal manures, since the limit can be reached in the 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 stability, by determining microbial activity factors such as the microbial biomass count and its metabolic activity, and by the concentration of easily biodegradable constituents. The aerobic respiration rate was previously selected as the most suitable parameter to assess aerobic biological activity and hence stability. In aerobic conditions, one carbon atom derived from catabolism is attached to two oxygen atoms to form carbon dioxide, releasing energy, including heat, in the process. Therefore, respiration can be measured in several ways: carbon dioxide evolution, oxygen consumption and self-heating, which are indicative of the amount of degradable OM still present and which are related inversely to stabilisation (Zucconi and de Bertoldi, 1987). Self-heating uses the Dewar flask method and actually measures temperature rises due to all exothermic biological and chemical activity, so it is not strictly a true measure of respiration, because many biological and chemical reactions not connected to respiration are exothermic. An insufficiently mature compost has a strong demand for O2 and high CO2 production rates, due to intense development of microorganisms as a consequence of the abundance of easily biodegradable 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) Germination index NH4-N C/N CO2 production rate Water soluble organic-C Water soluble (C/N) Water soluble organic-C/Total organic-N CEX CFA CEX/Water soluble organic-C C/N Water soluble organic-C Water soluble organic-C/Total organic-N NH4-N/NO3-N NH4-N Mineralisable-C in 70 days NO3-N/CO2–C ratio (per day) Water soluble organic-C

5–6 >50% <0.4 g/kg <20, preferable <10 6120 mg CO2/kg/h 610 g/kg 616 60.70 660 g/kg 612.5 g/kg P6.0 <12 <17 g/kg <0.55 <0.16 <0.4 g/kg <30% >8 64 g/kg

Chanyasak and Kubota (1981) Zucconi et al. (1981) Zucconi and de Bertoldi (1987) Mathur et al. (1993) Hue and Liu (1995)

Bernal et al. (1998a)

Cooperband et al. (2003) Zmora-Nahum et al. (2005)

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consumption and CO2 production are indicative of compost stability and maturity (Hue and Liu, 1995). Oxygen uptake and CO2 evolution are more direct and have been described as being opposite sides of the same equation under aerobic conditions (BarrenaGómez 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 respiration and hence aerobic biological activity (CCQC, 2001; Hue and Liu, 1995). Hue and Liu (1995) set the limit of the CO2 production rate for compost maturity at 6120 mg CO2 kg1 h1 (Table 4). Wang et al. (2004) used a respiration rate of <1 mg CO2–C g1 dw d-1 to define a highly stabilised compost from cattle and pig manures. Cooperband et al. (2003) suggested a NO3-N/CO2–C ratio > 8 per day as an index of compost maturity (Table 4). Respirometric studies have been carried out in soils amended with compost, in a proportion compatible with agricultural use; these indicate the mineralisation of the compost’s OM (Bernal et al., 1998b; Morel et al., 1979). Mature compost was defined as having mineralisable-C <30% of total organic-C in 70 days, with a rapidly mineralisable-C <7.2% of total organic-C and a slow mineralisation rate <0.35% of total organic-C d1 (Bernal et al., 1998a). Biological methods for estimating the degree of maturity are also based on tests for phytotoxicity. Plant tests used in research and 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 topgrowth and sometimes root mass), combinations of germination and growth, and other biological methods such as enzyme activities (Herrmann and Shann, 1993). According to Zucconi et al. (1981) a germination index below 50% characterises an immature compost (Table 4). Zucconi and de Bertoldi (1987) discussed the differences between germination and growth tests. Germination tests provide an instant picture of phytotoxicity, whereas growing tests will be affected by continuing changes in the stability or maturity of the compost tested: there may be damaging effects on growth in the earlier stages, but beneficial effects later on, with different conclusions depending on the time of assessment. GarcíaGómez et al. (2001) also looked at both germination index and pot trials, the yield of ryegrass showing phytotoxic effects from immature compost even when the germination index was above 87%. The relationship between the CO2 respiration and phytotoxicity of immature compost was studied by García-Gómez et al. (2003), using the CO2–C production by OM mineralisation, N-mineralisa-

tion and plant growth. The CO2–C evolved correlated with plant growth, and immature compost caused N-immobilisation in the soil, leading to plant N-deficiency. Those chemical and biological parameters already discussed have 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 authors identified decreases in water-soluble organic-C, NH4-N, phytotoxic effects and microbial activity and increases in the humification of the OM as indicators of the progressive stabilisation of the composting materials, leading to an acceptable degree of maturity based on the established indices in the literature for composts of different origin. Also, Michel et al. (2004) and Wang et al. (2004) used the criterion of CO2 evolution rate <0.5 mg CO2–C g1 OM d1 or <1 mg CO2–C g1 dw d1, respectively, to consider composts derived from manure as stable materials. Changa et al. (2003) concluded that CO2 and the NH3 SolvitaÒ test can be employed to characterise the maturity/stability stage for quality control of composted manures. Mathur et al. (1990), Guerra-Rodríguez et al. (2001, 2003) assessed phytotoxicity in germination tests, as an indicator of the maturity of manure compost. Tiquia (2005) proposed that values <35 lg TPF (triphenyl formazan) g1 for dehydrogenase activity can be used as a maturity indicator for manures. Ko et al. (2008) proposed the following maturity indices for 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 assess compost quality is widely recognised by researchers. But integration of the most reliable indices seems to be the sole option for evaluation 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 assessment process (CCQC, 2001; TMECC, 2002), which considered first that a compost 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 maturity assessment matrix is applied to classify the material as very mature, mature or immature. According to the maturity classification of the compost, the CCQC gives general guidelines for compost best uses: ‘‘very mature” can be used for soil and peat-based container plant mixes, alternative topsoil blends and turf top-dressing; ‘‘mature” compost for general field use (pastures), vineyards, row 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 CO2 evolution rate Dewar self-heating test Headspace CO2 (SolvitaÒ) Biologically available C

mg O2/g OM/d mg CO2–C/g OM/d Dewar index Colour code mg CO2–C/g C/d

<3 <2 V 7–8 <2

3–10 2–4 V 5–6 2–4

>10 >4 4

Method

units

Very mature

Mature

Immature

NH4-N NH4-N/NO3-N Seedling emergence Seedling vigour In-vitro germination index Earthworm bioassay NH3 (SolvitaÒ) Volatile fatty acids

mg/kg dw – % of control % of control % of control % Weight gain Colour code mmol/g dw

<75 <0.5 >90 >95 >90 <20 5 <200

75–500 0.5–3.0 80–90 85–95 80–90 20–40 4 200–1000

>500 >3.0 < 80 <85 <80 >40 3–1 >1000

Maturity Thresholds (group B)

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cases; ‘‘immature” compost should be used for land application to fallow soil and as a feedstock for compost. However, other quality criteria apart from maturity determine the compost quality, such as the nutrient content, ammonia, pH and soluble salts, and they should be also taken into account to define the compost use. Therefore, the development of a market for compost materials which supports or promotes a waste composting strategy greatly depends on the definition and adoption of quality standards (Brinton, 2000; Hogg et al., 2002). However, there are several compost quality 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 properties such as foreign matter (inert contamination), potentially toxic elements (organic contaminants and heavy metals), sanitisation (pathogens and phytopathogens), maturity and stability, weed seeds, water, OM and nutrient content. Currently, there is a need for harmonisation of such criteria at the international level. 6. Conclusions The composting of animal manures has been demonstrated to be an effective method for producing end-products which are stabilised and sanitised, ensuring their maximum benefit for agriculture. However, the compost should be of high quality in order to guarantee its marketability. Amongst the controllable factors which influence manure composting, the selection of appropriate bulking agents plays an essential role in controlling the decomposition rate and favouring N retention within the compost. In this sense, strategies such as addition of a bulking agent with degradable organic-C, to enhance initial N immobilisation, and process control (moisture, temperature, aeration/turning and particle size) have been shown to reduce ammonia volatilisation and hence nitrogen losses, these being a major concern in manure composting from an environmental point of view. The agricultural value of a compost increases when the OM reaches a high level of stability and maturity, which cannot be established by a single parameter. Several indices based on chemical and stability parameters have been used for manure compost by different authors. However, it is necessary to standardise the criteria used by official institutions from different countries. Acknowledgements The authors thank the Organisation for Economic Co-operation and Development, Co-operative Research Programme: Biological Resource Management for Sustainable Agricultural Systems, for inviting Dr. Bernal to participate in the workshop ‘‘Livestock Waste Treatment Systems of the Future: a challenge to environmental quality, food safety, and sustainability”, where this paper was presented. References Agnew, J.M., Leonard, J.J., 2003. The physical properties of compost. Compost Sci. Util. 1, 238–264. Ahn, H.K., Richard, T.L., Choi, H.L., 2007. Mass and thermal balance during composting of a poultry manure–wood shavings mixture at different aeration rates. Process Biochem. 42, 215–223. Amon, B., Kryvoruchko, V., Amon, T., Zechmeister-Boltenstern, S., 2006. Methane, nitrous oxide and ammonia emissions during storage and after application of dairy cattle slurry and influence of slurry treatment. Agr. Ecosyst. Environ. 112, 153–162. Barrena-Gómez, R., Vázquez Lima, F., Sánchez Ferrer, A., 2006. The use of respiration indices in the composting process: a review. Waste Manage. Res. 24, 37–47. Barrington, S., Choinière, D., Trigui, M., Knight, W., 2002. Effect of carbon source on compost nitrogen and carbon losses. Bioresour. Technol. 83, 189–194. Bernal, M.P., 1990. Utilización de purines de cerdo en la fertilización de suelos calizos en condiciones de regadío. CEBAS-CSIC, Murcia, Spain.

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