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Characterization of the Dynamic Thickness of the Aerobic Layer during Pig Manure Aerobic Composting by Fourier Transform Infrared Microspectroscopy Jinyi Ge, Guangqun Huang, Zengling Yang, Jing Huang, and Lujia Han* Biomass Resources and Utilization Laboratory, College of Engineering, China Agricultural University, Beijing 100083, People’s Republic of China ABSTRACT: A new method for characterizing the aerobic layer thickness in pig manure based on Fourier transform infrared microspectroscopy (FTIRM) is presented to improve the anaerobic/aerobic co-process mechanism, to ensure adequate oxygen supply and, thus, minimize methane emissions during aerobic composting. Freeze-dried manure particles were microtomed into 10 μm thick sections; the spectral range, spectral resolution, and pixel dimensions in the transmission spectra were 4000−650 cm−1, 16 cm−1, and 6.25 × 6.25 μm, respectively. A mean spectrum of 16 scans was used for the second-derivative analysis with nine smoothing points. This is the first attempt at determining the oxidation profile of composting particles according to the radial variations in second-derivative spectra at 2856 and 1568 cm−1, which are attributed to the reactants and products of the oxidation, respectively. In addition, an intermediate area is detected between the aerobic layer and anaerobic core. The experimental values of the aerobic layer thickness are consistent with the estimates, and an exponential increase is observed, which is influenced by multiple dynamic factors. However, the contribution of each factor to dynamic variations in the aerobic layer thickness should be investigated using available methods.

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between CH4 emissions and oxygen use in composting,12−15 because most other mathematical models assuming completely aerobic conditions could not analyze methane generated from a strictly anaerobic environment.7 The anaerobic/aerobic co-process mechanism assumes that compost piles are composed of numerous composting particles and void spaces. The composting particle is in a solid−liquid phase, containing water, inert matter, insoluble substrate (Si), soluble substrate (Ss), and microorganisms (X); this phase is in contact with the gas phase, forming the liquid/gas interface. Together, they constitute a three-phase unit,11,16−24 which is shown in Figure 1 (modified and integrated from refs 18, 20, and 22). Through the water phase at the liquid/gas interface, the gaseous oxygen converts to dissolved oxygen and diffuses into the particle; the oxygen concentration is finally reduced to an extremely low level because of oxygen diffusion and oxygen consumption by aerobic microorganisms, thus forming an outer

INTRODUCTION According to the latest World Meteorological Organization (WMO) Greenhouse Gas Bulletin, because of increased emissions from anthropogenic sources, the globally averaged mole fraction of methane (CH4) reached a new high of 1819 ± 1 ppb in 2012.1 Managing greenhouse gas sources derived from manure is an important concern, because these sources are responsible for 9% of the total biogenic CH4 emissions2 and exhibit an increasing tendency;3 such emissions during aerobic manure composting have been widely studied as a result of the waste produced by inappropriate aeration strategies.2,4−7 Pel et al.8 have suggested that, despite being well-aerated, compost particles rich in organic material also form an oxic−anoxic interface when the particle size approaches the order of millimeters. Given that excessive ventilation would lower the composting temperature, increase the loss of N-containing compounds, and induce additional electricity demand, in turn, offsetting the advantages of aerobic composting,6,9,10 composting strategies must be based on a trade-off between controlling greenhouse gas emissions and reducing the ventilation cost. To solve this problem, the anaerobic/aerobic co-process mechanism11 was developed as a means of investigating the relationship © 2014 American Chemical Society

Received: Revised: Accepted: Published: 5043

January 6, 2014 March 15, 2014 April 3, 2014 April 3, 2014 dx.doi.org/10.1021/es500070z | Environ. Sci. Technol. 2014, 48, 5043−5050

Environmental Science & Technology

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grains using the CO band at 1717 cm−1 and aromatic C−C band at 1496 cm−1 as the indicator bands, respectively.25 FTIRM can also detect the oxidized part in rubber aged in air by the reduced absorbance of the oxygenated functional groups from the exterior to the interior.26 From FTIRM images of the crosssection of a human hair, the thicknesses of the medulla, cortex, and cuticle could be determined according to the spectral changes caused by the variation in the protein and phospholipid concentrations between the hair center and the exterior.30 FTIRM has also been successfully used to measure H2O diffusion in silicate melts.32 Therefore, the aims of this research were to study the structure of pig manure particles, characterize the aerobic layer thickness based on FTIRM measurements, and analyze the integrated influence on dynamic variations in this parameter. Incorporating the changes in the aerobic layer thickness to the anaerobic/ aerobic co-process mechanism helps in developing mathematical models at the microscale and, thus, provides theoretical guidance for operation optimization and emission reduction. For instance, the simulation of oxygen consumption could be useful for designing a feedback controller to obtain an automatic airflow and to maximize the biological activity,15 and an in-depth knowledge of the aerobic layer in composting particles would be beneficial for mitigating CH4 emissions during aerobic composting.12−14

Figure 1. Schematic of the anaerobic/aerobic co-process mechanism in the three-phase unit. Si is the insoluble substrate; Ss is the soluble substrate; X is the microorganisms; and Lp is the aerobic layer thickness.

layer, where aerobic reactions are predominant; the thickness of this aerobic layer is denoted as Lp.18 The study of this layer is important to identify the actual degree of fermentation of the composting particles.11,16−19,21,23 In the anaerobic core, the soluble substrate is derived from the insoluble substrate by hydrolysis, which subsequently diffuses to the aerobic layer and is oxidized into carbon dioxide (CO2), water, heat, and new microorganisms by aerobic reactions; the gas and heat are released through the liquid/gas interface. As the essential parameter in the numerical simulation of the anaerobic/aerobic co-process, Hamelers18 hypothesized that Lp(t) is related to X(t), as shown in eq 1, and is of the order of the magnitude of 50 μm, while other parameters in the equation are assumed to be constant L p (t ) =

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MATERIALS AND METHODS Aerobic Composting Experiments. Pig manure was collected from the livestock and poultry test site of the Chinese Academy of Agricultural Sciences (Changping, Beijing, China). Wheat straw collected from suburban areas of Beijing and cut into 3−5 cm lengths was used as a bulking agent. Pig manure and wheat straw were mixed in a mass ratio of 7:1 to control the moisture content at around 65%, and the C/N ratio was in the range of 15−20, which are the appropriate conditions for aerobic composting.33,34 Figure 2 shows a schematic representation of

2DO2,eff O2,iYO2 μX(t )

DO2,eff = MC 2DO2

(1) (2)

where DO2,eff is the effective diffusion coefficient of oxygen, O2,i is the dissolved oxygen content at the liquid/gas interface, YO2 is the biomass yield on oxygen, μ is the maximal growth rate constant, MC is the compost moisture content, and DO2 is the oxygen diffusion coefficient in pure water. Tseng et al.16 determined that Lp was proportional to the oxygen concentration and inversely proportional to the composting temperature in a certain range, possibly because both of them insignificantly influenced DO2,eff and O2,i in eq 1. Other investigations have suggested that Lp is affected by the compost moisture content and microbial variety.23,24 However, existing studies are still in the stage of theoretical hypothesis, and experimental representation of the aerobic layer in composting particles has not been attempted because of the limited analysis conditions; this is one of the main obstacles for developing the anaerobic/aerobic co-process mechanism.13,16 To solve this problem, we sought a sensitive technique that allows for the interrogation of chemical composition through solid materials; to this end, Fourier transform infrared microspectroscopy (FTIRM) has been widely reported as an effective micro-area analysis method for detecting the distribution of chemical compositions and determining the thickness or penetration depth of multilayer materials.25−32 For instance, FTIRM has been used to quantitate the penetration depth of methyl centralite and dibutyl phthalate in propellant

Figure 2. Schematic of the composting system: (A) composting reactor, (B) ventilation control system, (C) compost material, (D) insulation case, (E) temperature acquisition system, and (F) oxygen measurement device.

the composting system.35 A laboratory 15 L cylindrical reactor (0.40 m height × 0.25 m internal diameter) made of stainless steel was filled with 5.6 kg of raw material and isolated with a layer 5044

dx.doi.org/10.1021/es500070z | Environ. Sci. Technol. 2014, 48, 5043−5050


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of 10 cm polystyrene foam. Air blown at a hourly interval (flow velocity of 0.3 L/min) through the pipe at the bottom of the reactor diffused through the composting material to maintain aerobic conditions. The composting temperature was measured at the interval of 15 min by a Pt100 temperature probe located in the middle of the material, and the oxygen concentration (volume fraction) was monitored 5 times per day by an oxygen sensor (O2S-FR-T2-18X, Apollo Electronics Co., Ltd., China); the mean values of the temperature and oxygen concentration were calculated every day. The experiments lasted 35 days, and the mixing and sampling were performed on days 0, 7, 14, 21, 28, and 35. Samples were stored below −4 °C before use. The moisture content (MC) and organic matter content (OM) of the raw materials and compost mixtures were determined by standard “Test Methods for the Examination of Composting and Compost (TMECC)”.36 Total amounts of carbon (CT) and nitrogen (NT) were tested with an elemental analyzer (Vario EL CHNOS, Elementar Analysensysteme GmbH, Germany) to calculate the CT/NT ratio. Sample Pretreatment. Given that the bulking agent possesses an inferior biodegradability over a limited time period,37−42 pig manure was considered as the main reactant; pig manure particles were regarded as substrates to analyze aerobic layer thickness, which was closely associated with the biochemical reactions. A frozen section technique was adopted in this study to acquire cross-sections of the manure particles, to obtain their chemical compound distribution. The first part of the pretreatment was to obtain the maximum manure particle size to clearly define the separation threshold between manure particles and elongated bulking agent. Given the aggregates being generated from molecular interactions (e.g., van der Waals forces, electrostatic forces, and liquid bridges), deionized water was added to a fresh manure sample in a 1:4 mass ratio and shaken for 10 min.43 The maximum manure particle size was then determined using a laser particle size analysis meter (Mastersizer 3000, Malvern Instruments, Ltd., U.K.) following the ISO 13320-1 method.44 Lyophilization was carried out to avoid water interference during spectral collection and analysis. The mixed sample was frozen at −80 °C for 8 h, dehydrated using a freeze-dryer (ALPHA 1-2 plus, Christ, Osterode, Germany) at −42 °C and 10 Pa for 24 h, and sieved with a specific mesh number according to the maximum manure particle size (e.g., if the maximum manure particle size is 1.34 mm, then

Figure 4. (a) Typical FTIRM image of pig manure particle, indicating the direction of measurement. (b) Original spectra along the oxygen diffusion path. (c) Second-derivative spectra along the oxygen diffusion path.

the mesh number will be 1.5 mm). Dried particles of each sample were embedded in an optimal cutting temperature (OCT)

Figure 3. Temperature and oxygen concentration changes during aerobic composting. 5045



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Figure 5. Typical second-derivative microscopic images at 2856 cm−1 during the composting process at (a) 7 days, (b) 14 days, (c) 21 days, (d) 28 days, and (e) 35 days.

Table 1. Initial Composition of Composting Materials

a

materials

MC (%)a

OM (%)b

CT (%)b

NT (%)b

CT/NTb

pig manure wheat straw compost mixture

71.17 ± 0.78 4.33 ± 0.32 64.16 ± 0.55

84.96 ± 0.04 95.10 ± 0.01 85.98 ± 0.01

42.30 ± 0.15 44.78 ± 0.32 44.17 ± 0.26

4.23 ± 0.02 0.56 ± 0.01 3.08 ± 0.27

9.99 ± 0.01 79.93 ± 2.15 14.66 ± 0.34

On a wet weight basis. bOn a dry weight basis.

Measurement of Aerobic Layer Thickness. In the radial second-derivative spectra within 4000−650 cm−1, two wavelengths that exhibited different oxidation trends were selected as characteristic wavelengths.45−49 The second-derivative microscopic image at the characteristic wavelength was obtained; the values of radial second-derivative spectra at the characteristic wavelength were extracted to measure the aerobic layer thickness.

compound (Sakura Finetek, Torrance, CA) and then sectioned into 10 μm slices with a CM3050-S cryostat (Leica Microsystems GmbH, Wetzlar, Germany). The section thickness was determined via a combination of previous studies and evaluation of a series of FTIRM images to avoid saturation of the detector.25−27 Collection of Spectra. Frozen sections were placed on a ZnS window; the collection of transmission spectra26 was performed using a Fourier transform infrared microscope (PerkinElmer Spotlight 400, Waltham, MA). The spectral range, spectral resolution, and pixel dimension were 4000−650 cm−1, 16 cm−1, and 6.25 × 6.25 μm, respectively. A mean spectrum of 16 scans (determined by a single-factor experiment to maintain an acceptable signal-to-noise ratio) was used to obtain the second derivative with nine smoothing points; spectra were extracted at a 6.25 μm interval inward from the particle edge along the radial direction, the oxygen diffusion path,23 using PerkinElmer SpectrumIMAGE software. No less than three particles of each sample were tested, and for each particle, four sets of radial spectra were extracted both vertically and laterally.

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RESULTS AND DISCUSSION Composting Process and Chemical Analysis. The initial composting compositions are presented in Table 1. The composting temperature, as shown in Figure 3, followed the classic three-phase pattern (mesophilic, thermophilic, and cooling). The temperature rose in the early stage of composting mainly because of the heat released from the active microbial communities.33 The highest temperature (≥50 °C) was maintained for more than 5 days, which met the Chinese National Standard (GB7959-87);50 the compost matrix was maintained above 55 °C for 2 days, and this temperature was sufficient to destroy all pathogenic microbes.33 During the 5046



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Figure 6. Typical second-derivative microscopic images at 1568 cm−1 during the composting process at (a) 7 days, (b) 14 days, (c) 21 days, (d) 28 days, and (e) 35 days.

aromaticity caused by oxidation reactions have been widely reported,45−49 the aliphatic compounds as represented by the aliphatic methylene C−H were oxidized in the aerobic layer, because the absorbance at points 0, 4, and 8 was not detected at 2856 cm−1 in Figure 4c.45−48 Conversely, aromatic compounds were generated and increased in intensity at the same time; therefore, the second-derivative spectra at points 0, 4, and 8 were distinct at 1568 cm−1, representing aromatic CO and CC moieties.45,46,48,49 Therefore, 2856 and 1568 cm−1, characteristic wavelengths assigned to the reactants and products in the aerobic reactions, respectively, were selected to analyze the aerobic layer thickness. Characterization of the Aerobic Layer. The color bars in Figures 5 and 6 indicate the second-derivative values. The yellow−red contours in Figure 5 indicate that the aliphatic C−H band at 2856 cm−1 could not be detected in the outer layer, while the blue contours in Figure 6 indicate the condensed aromatics in this region. The two kinds of contours implied the concentration gradient of the aliphatic compounds and aromatic compounds along the measurement direction, respectively. Both showed dynamic variation during aerobic composting, as presented in panels a−e of Figures 5 and 6. Plots of second-derivative values along the particle radius (panels a and b of Figure 7) can be used to numerically illustrate the concentration gradient and provide a depth profile of degradation-related changes in the manure particle. It can be seen from Figure 7a that the aliphatic compounds were more dilute at the external edge, because the second-derivative value at 2856 cm−1 in this region was zero or positive. Such a concentration gradient is a result of multiple

mesophilic and thermophilic phases, the standard deviations were generally larger than those observed later, as a result of the higher activity of the microorganisms, and the temperature oscillations were mainly derived from the population succession of mesophilic−thermophilic microorganisms.20,22,33,51 The high temperature made the microbes less active, and thus, the reaction heat was reduced, which, in turn, caused a temperature drop. The oxygen concentration presented in Figure 3 was always greater than 10% to provide an aerobic environment. This was almost a “mirror image” of the temperature curve,52 possibly because the exothermic biological reactions that led to an increase in temperature simultaneously consumed more dissolved oxygen. Besides, the maximum manure particle size was 2.71 mm, approximating the value of 2.5 mm obtained by Barrington et al.;53 the higher value could be attributed to the lower moisture content in this study. Characteristic Wavelengths. Figure 4a shows an example of the FTIRM images of pig manure particles; the color of each pixel represents the total absorbance from 4000 to 650 cm−1, although the aerobic layer cannot be discriminated directly from these results. The original and second-derivative spectra along the oxygen diffusion path at points 0, 4, 8, 12, and 16 (corresponding to distances from the particle edge of 0, 25, 50, 75, and 100 μm) are presented in panels b and c of Figure 4. It can be seen that second-derivative spectra can effectively correct the baseline shift and make the radial spectral variation at specific wavelengths much clearer, meaning the heterogeneous distribution of components in the composting particle. Given that a decrease in the aliphatic component content and an increase in 5047



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factors, such as oxygen diffusion and different water contents and microbial activities along the diffusion path, which can be explained in detail as follows. In the outer layer of the composting particle, there exist more micropores containing dissolved oxygen and water for aerobic microbial growth;16,54 although oxygen can penetrate much deeper, the dissolved oxygen was continuously consumed by the aerobic microbes along its diffusion path and, thus, was finally almost depleted. This caused a shift from aerobic to anaerobic metabolism.16 It is possible that oxidation of the aliphatic compounds by aerobic microorganisms was faster than the hydrolysis occurring in the anaerobic area, leading to a greater decomposition of the aliphatics under aerobic conditions.47 In the anaerobic core, the aliphatic compounds were barely decomposed, whereupon the second-derivative values became negative. As a result, the degree of degradation was gradually decreased from the outer aerobic layer to the interior. Conversely, Figure 7b shows that the initial negative second-derivative values at 1568 cm−1 imply the generation of aromatics in the outer layer, which gradually increased to zero or positive along the oxygen diffusion path, because the synthesis was suppressed under anaerobic conditions.49 To facilitate the discrimination of the aerobic layer, the second-derivative value at 1568 cm−1 in each spectrum was subtracted from that at 2856 cm−1.26 As shown in Figure 7c, the difference curve was considered as a measure of the aerobic layer thickness. The start point of the measurement was noted as the start of the aerobic layer; the point where the value became zero or negative indicated the end point. The measurement result in Figure 7c is less than 60 μm, which is in accordance with the estimated value of 50 μm,18 and its variation during aerobic composting would be described in detail in the next section. The degradation profile in the composting particle (Figure 7c) was initially characterized, wherein a 20 μm thick intermediate area adjacent to the anaerobic core was also detected. This transition is better correlated with the actual composting conditions, as opposed to the case in which the particle was split into two parts. The curves and transition regions presented in Figure 7 are consistent with FTIRM analyses for other materials, such as penetration depths of deterrents in propellant grains,25 degradation profiles for aged polymer,26 and H2O diffusion profiles in a haploandesitic melt,32 which demonstrated the effectiveness of using FTIRM for the characterization of the aerobic layer thickness. The outliers were most likely derived from the cracks in the sample particle.32 Dynamic Variation in Aerobic Layer Thickness. In Figure 8a, the experimental aerobic layer thickness (Lp) fluctuated within 0−60 μm, which is consistent with the hypothesized and calculated values in previous studies.16,18,19 The large standard deviation is similar to the early study concerning FTIRM, which attributed this to the non-uniform particles.25 The variation in the aerobic layer thickness can be described by an exponential fitting function, as shown in eq 3 Lp(t ) = 48.1351(1 − e−0.0036t )

(3)

where Lp(t) is the variation in the aerobic layer thickness (μm), t is the time of operation (h), and the applicable range of t is 0−850 h. The changes of O2,i and DO2 presented in Figure 8b were calculated from the oxygen concentration and composting temperature, respectively,55,56 and the combined effects on the dynamic Lp were analyzed as follows. During the initial composting stage, microbial activity was strong and the oxygen uptake rate was enhanced, which led to a decrease in the oxygen concentration, i.e., a decrease in O2,i. Simultaneously, DO2 was

Figure 7. Typical second-derivative spectral variation along the measurement path at (a) 2856 cm−1 and (b) 1568 cm−1. (c) Difference values between the second-derivative spectrum of 2856 and 1568 cm−1 along the measurement path.

increased because of the self-heating process, which immediately supplied dissolved oxygen to the particles and, thus, slowly 5048



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AUTHOR INFORMATION

Corresponding Author

*Telephone: 86-10-6273-6313. Fax: 86-10-6273-6778. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (31201684), the National 12th Five-Year Science and Technology Project (2012BAD47B01), the Program for New Century Excellent Talents in University (NCET-12-0524), and the Beijing Higher Education Young Elite Teacher Project (YETP0319).

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Figure 8. (a) Aerobic layer thickness changes during composting. (b) Factors influencing the aerobic layer thickness. O2,i is the dissolved oxygen content at the liquid/gas interface, and DO2 is the oxygen diffusion coefficient in pure water.

extended Lp. From 7 to 14 days, the oxygen demand of the microorganisms was impaired, and this led to an increase in O2,i. However, the drop in the temperature made DO2 decrease and further impeded the recovery of dissolved oxygen. Thus, the offset between the two aspects left Lp mostly unchanged. Between 14 and 28 days, the microbial metabolism was low and O2,i increased to a peak value, which caused Lp to continue increasing. After 28 days, the compost reached a steady state, as did Lp. Given the above observations, Lp showed dynamic variations caused by the combined effects of the oxygen concentration, temperature, and microbial activity. In conclusion, this study demonstrated that FTIRM is a viable method for characterizing the oxidation profile in pig manure particles and quantifying variations in the aerobic layer thickness, which are conducive to simulate the oxygen uptake rate and methane emissions of the aerobic composting on the basis of the anaerobic/aerobic co-process mechanism. However, to increase the accuracy of the results, microbial activity as the major factor influencing the aerobic layer thickness should be further explored by the microbiological experiments and the contribution of each factor to its dynamic variation should be investigated using available methods. 5049



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