Article pubs.acs.org/EF
Anaerobic Co-digestion of Agricultural Byproducts with Manure for Enhanced Biogas Production Marie M. Søndergaard,† Ioannis A. Fotidis,*,† Adam Kovalovszki, and Irini Angelidaki Department of Environmental Engineering, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark S Supporting Information *
ABSTRACT: Biogas is extensively promoted as a promising renewable energy. Therefore, the search of appropriate cosubstrates has come into focus. In this study, we examined the potential of using agricultural byproducts as alternative cosubstrates for increased biogas production. The biochemical methane potential (BMP) of six agricultural organic byproducts were tested. Consecutively, the byproduct with the highest BMP was used as a co-digestion substrate with manure, in a continuous stirred tank reactor (CSTR). Meadow grass had the highest BMP value [388 ± 30 NmL of CH4 g−1 of volatile solids (VS)] among all mono-substrates tested. On the basis of BMP, the substrates ranked as follows: meadow grass > spring barley, winter wheat, winter barley, ryegrass > rapeseed > manure. Co-digestion of manure with byproducts resulted in only an additive and not synergistic methane production. Continuous co-digestion of 34 g L−1 raw meadow grass with manure increased the methane production rate of the CSTR reactor by 114% compared to the manure alone.
1. INTRODUCTION The anthropogenic emissions of greenhouse gases to the atmosphere have been proven to lead to a temperature increase and climate changes.1 European Union (EU) member countries have agreed to reduce 40% of the total CO2 emissions by the year 2030 compared to the emissions in 1990,2 with 27% of the energy deriving from renewable energy sources, such as solar, wind, hydro, wave, tidal, geothermal, and bioenergy. Specifically, bioenergy is a key player in this transition process, because of its role as a substitute for fossil fuels, which are widely used for production of diesel, gasoline, natural gas, etc. The growing demand for bioenergy is immediately posing an ethical dilemma, because first-generation biofuels are competing for land and water used for food and fiber production. On the other hand, the second-generation biofuels focus on production from byproducts, which, in turn, imposes other obstacles regarding the often rigid and fibrous quality of these biomasses.3 Anaerobic digestion (AD) is an efficient bioenergy technology that produces renewable energy from animal manures with the additional benefits of solving manure storage, improving fertilizer quality, and preventing eutrophication of local water environments.4 However, the microbially available organic content of manures is often poor in both quantity and quality, and co-digestion with more energy-rich organic material is necessary to increase the methane production rate and ensure an economically sustainable biogas production.5,6 Co-digestion signifies the simultaneous AD of several substrates with different characteristics, supplementing each other and providing a combined broader substrate with a more balanced composition with regard to the microbial needs. Specifically, codigestion (a) adjusts the C/N ratio, moisture content, and pH, (b) increases the buffer capacity and the concentration of the biodegradable matter in the substrate, (c) dilutes potentially inhibitory or toxic compounds, and (d) increases resilience as a result of a wider species range of microorganisms.7 On the © 2015 American Chemical Society
other hand, the disadvantages of co-digestion relate mainly to economics (costs of collection, transport, and pretreatment) and physical process settings (crust formation in the digestion tank and risk of clogging of pipes and pumps as a result of the fibrous nature of the byproducts).8 Because traditional co-substrates, such as organic waste from the food-processing industries, are scarce, and because usage of energy crops should be avoided, alternative co-substrates for manure-based biogas production need to be identified. Furthermore, transportation of substrates could become the major operational cost for biogas plants (especially for distances higher than 20 km);9 thus, the proximity of the co-substrates and the year-round availability are equally significant. In this context, agricultural byproducts in the form of straw and hay are potential co-substrate candidates, because they exist in vast amounts in the European rural areas. Specifically, straw from grain and cereal production as well as hay from meadows and grasslands are often not used or collected from the fields; thus, vast amounts of these lignocellulosic biomasses are available near manure-based biogas plants.10 It has been suggested that these biomasses may be appropriate AD substrates for sustainable bioenergy production.11 Furthermore, a relatively small amount of hay or straw is enough to significantly increase the organic loading rate (OLR) of a continuous AD reactor as a result of their high organic content. Agricultural byproducts as a result of their availability and proximity have been widely investigated as substrates for biogas production as well as for biorefinery applications.12 Many studies have found that pretreatment of agricultural byproducts is important to break the lignocellulosic composite structures and make the sugar polymers bioavailable, to obtain sufficiently high biogas yields.13,14 Simple mechanical pretreatment (millReceived: October 9, 2015 Revised: November 24, 2015 Published: November 24, 2015 8088
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Energy & Fuels ing) of straws and hays has proven to be a very efficient method to improve their enzymatic digestibility.15,16 Milling does not only address the accessibility of the sugars but also the challenge of how to technically add dry fibrous biomass in a continuous digestion process, without causing excessive wear on pumps and macerators, and avoid flotation and crust formation in the digester tank.17 Because efficient pretreatment methods exist, identifying the best co-digestion substrate among the vast amount of available agricultural byproducts would enable a more economically feasible full-scale manurebased AD process. Furthermore, it is still unclear to which degree the OLR increase affects the AD process. Finally, it has not thus far been clarified whether co-digestion of manure with agricultural byproducts results in synergistic or just additive methane production. In this study, six pretreated (milled) agricultural byproducts derived from a typical north European rural area (Kalundborg municipality, Denmark) were tested to identify the best codigestion substrate that can be combined with manure for optimal biogas production in a continuous stirred-tank reactor (CSTR). Therefore, the aim was to investigate if typical fullscale biogas plants can use the available agricultural byproducts that they have in close proximity, as alternative co-substrates, to produce second-generation biogas with high methane production rates. An additional aim was to identify potential effects caused by the biochemical characteristics of the co-digestion biomasses and the operational conditions (e.g., continuous codigestion, OLR, etc.). To fulfill these aims, the biochemical methane potential (BMP) of six agricultural byproducts and a manure was determined. The best performing agricultural byproduct was selected and was continuously co-digested with the manure in a CSTR lab-scale reactor under increasing OLRs, to evaluate the efficiency and different co-digestion strategies. The results of this study could be proven valuable for the biogas plant operators to enhance the efficiency of the AD process and to improve the economy of their biogas plant.
Table 1. Characteristics of the Inocula Used in the BMP Experiments and CSTR Experiment (n = 3; SD) parameter TSa (g L−1) VSb (g L−1) VFAc (g L−1) TKNd (g of N L−1) ammonia (g of NH4+ N L−1) pH a
inoculum I
inoculum II
27.25 ± 15.18 ± 0.1 ± 2.91 ± 2.16 ± 8.6
20.41 ± 12.03 ± 0.1 ± 3.02 ± 2.23 ± 8.3
3.1 1.3 0.0 0.2 0.1
1.3 1.1 0.0 0.1 0.1
inoculum III 38.8 ± 30.4 ± 1.8 ± 2.58 ± 1.91 ± 8.0
1.3 0.4 0.2 0.1 0.3
TS = total solids. bVS = volatile solids. cVFA = volatile fatty acids. TKN = total Kjeldahl nitrogen.
d
which was based on the approximated availability of cow and pig manure in the typical rural area. Total solids (TS), dry matter (DM), and volatile solids (VS) of the initial nine biomasses are shown in Table 2. Total Kjeldahl nitrogen (TKN), ammonia nitrogen, pH, and
Table 2. TS, DM, and VS of the Biomasses (n = 3; SD) sample meadow grass spring barley winter wheat winter barley ryegrass rapeseed pig manure cow manure manure (2 cow/1 pig, v v−1, BMP) manure (2 cow/1 pig, v v−1, CSTR)
TS or DM ± SD (g L−1) 926.48 942.08 936.26 927.83 935.58 883.3 39.28 62.34 56.52
± ± ± ± ± ± ± ± ±
1.2 1.4 0.9 15.2 5.8 8.6 0.4 0.2 0.6
40.04 ± 1.3
VS ± SD (g L−1) 863.97 876.42 846.68 862.93 879.04 776.89 27.33 47.68 42.65
± ± ± ± ± ± ± ± ±
3.3 20.3 16.4 7.3 11.7 1.3 0.4 0.2 1.3
21.42 ± 0.2
volatile fatty acids (VFA) for the manure biomasses and the manure are shown in Table S1 of the Supporting Information, while the sugar, nitrogen, and crude fiber contents of the agricultural byproducts are shown in Table S2 of the Supporting Information. 2.3. BMP Assay I and BMP Assay II Experimental Setup. In both batch assays, 320 mL glass batch reactors (serum vials) with 100 mL working volume were used. A total of 20 mL of substrate and/or water along with 80 mL of inoculum was added in each reactor. Methane production of all mono-substrates was determined in BMP assay I, and co-digestion of the manure with either winter wheat, spring barley, or meadow grass was tested in BMP assay II. For grass and straw substrates in BMP assay I, three different concentrations were tested to avoid any possible organic overloading or other potential inhibition, which might result in underestimation of the methane potential, as described by Angelidaki et al.18 The exact VS concentrations tested in BMP assay I are shown in Table S3 of the Supporting Information. In BMP assay II, winter wheat, spring barley, and meadow grass were mixed with the manure (manure−co-substrate mixtures) in three different ratios, giving a total VS concentration of approximately 63, 83, and 104 g of VS L−1, respectively (the exact concentrations tested are presented in Table S4 of the Supporting Information). Cellulose (Avicel PH-101, Sigma-Aldrich) was used (2 g L−1) as the control substrate to validate the two BMP assays. The BMP value of the control substrate Avicel in BMP assays I and II was not significantly different (p > 0.05) from the theoretical value (415 NmL of CH4 g−1 of VS),19 which supports the validity and accuracy of the BMP assay procedure. Batch reactors with 80 mL of inoculum and 20 mL of water (blanks) were included to determine the residual methane production from the inoculum. The batch reactors were flushed with a N2/CO2 (80:20) gas mixture to ensure anaerobic conditions, closed with butyl rubber stoppers, sealed with aluminum caps, and placed in a 53 ± 1 °C incubator. All assays were conducted in triplicates (n = 3) and run for a minimum of 1 month, and all of the
2. MATERIALS AND METHODS The BMP of the mono- and co-digested substrates were assessed through two thermophilic (53 ± 1 °C) experimental series, denoted “BMP assay I” for mono-substrates and “BMP assay II” for co-digested substrates (i.e., manure co-digested with one of the pretreated herbal biomasses). Subsequently, the best co-digestion mixture was used in a CSTR reactor experimental series, testing different co-digestion strategies. 2.1. Inocula. Thermophilic methanogenic inocula (53 ± 1 °C) with similar characteristics were used in all experiments. For the two BMP assays, inocula were obtained twice (inoculum I and II) from Snertinge centralized biogas plant in Denmark for BMP assay I and BMP assay II, respectively. The inocula for the BMP were allowed to degas for 7 days in an incubator prior to use to minimize the background methane production from the inoculum. For the CSTR experiment, inoculum was derived from a thermophilic lab-scale CSTR reactor (inoculum III) fed with cow manure. The basic characteristics of the inocula used in the BMP and CSTR assays are shown in Table 1. 2.2. Mono- and Co-substrates. The agricultural byproducts tested in the BMP assays were milled straw from “meadow grass”, “spring barley”, “winter wheat”, “winter barley”, “ryegrass”, and “rapeseed”. Straw and grass biomasses were milled on a hammer mill to a particle size of approximately 0.1−0.4 mm. The agricultural byproducts are denoted by the full crop name, but only the stem of the crop was used in the study. Additionally, the BMP of “pig manure”, “cow manure”, and manure mixture named “manure” was determined. The manure consisted of cow and pig manure at a ratio of 2:1 (v v−1), 8089
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Energy & Fuels Table 3. Operational Parameters in the Different Experimental Periods of the CSTR Reactor experimental period (days)
P-I (0−12)
P-II (13−61)
P-III (62−91)
P-IV (92−107)
OLR (g of VS L−1 day−1) meadow grass VS in feedstock (% VS meadow grass in total VS) raw meadow grass (g L−1 meadow grass in feedstock) feedstock TS (g L−1)
2 0 0 40
2.6 23 12 50
3.2 37 23 60
3.8 47 34 70
contrast to meadow grass, the BMP value of rapeseed (258 ± 10 NmL of CH4 g−1 of VS) was significantly lower (p < 0.05) than the BMPs of all of the other agricultural byproducts, and at the same time, statistically similar (p > 0.05) to the BMP values of the manure biomasses. Additionally, the BMP values of spring barley (335 ± 7 NmL of CH4 g−1 of VS), winter barley (322 ± 16 NmL of CH4 g−1 of VS), winter wheat (319 ± 19 NmL of CH4 g−1 of VS), and ryegrass (314 ± 11 NmL of CH4 g−1 of VS), were similar (p > 0.05). The only exception was that the BMP of spring barley was significantly higher (p < 0.05) compared to the BMP of ryegrass. Cow manure had a statistically (p < 0.05) lower BMP (255 ± 17 NmL of CH4 g−1 of VS) compared to the BMP of mixed cow and pig (289 ± 9 NmL of CH4 g−1 of VS) and pig (323 ± 27 NmL of CH4 g−1 of VS) manures. On the basis of the methane production yield per ton of raw material (Figure 1b), the substrates were ranked as follows (p < 0.05): meadow grass > spring barley, winter wheat, winter barley, ryegrass > rapeseed > pig manure, mixed manure > cow manure. Thus, meadow grass was the best co-digestion
methane productions presented were normalized (in NmL) to the standard temperature and pressure (STP; 273.15 K and 1013.25 hPa) conditions. 2.4. CSTR Experimental Setup. The CSTR experimental setup consisted of a lab-scale CSTR reactor with 5 and 3.5 L total and working volumes, respectively. The reactor temperature was kept at 54 ± 1 °C via a build-in water-heating jacket. The content of the reactor was stirred with a build-in metallic stirrer powered by an electric motor every 13 s for 11 s with 70 rpm. Feedstock was kept in an Erlenmeyer flask (1 L) connected to the reactor with a feeding pump. The feedstock was mixed with a magnetic stirrer for 1 h before feeding with approximately 1000 rpm to maintain homogeneity. The biogas production of the reactor was measured with a water-displacement gas counter. The CSTR experiment was divided into four experimental periods, which are presented in Table 3, along with the different operational parameters. The hydraulic retention time (HRT) was 15 days throughout the experimental period. The CSTR reactor was started with the manure as feedstock until a steady-state methane production was achieved (period P-I). At that point, the OLR of the reactor was gradually increased in three consecutive steps (periods P-II−P-IV), with increasing milled meadow grass shares as co-digestion substrate mixed with the manure. Unfortunately, at day 108, we had to terminate the experiment as a result of leakage caused by damage of the interior paddle of the reactor. 2.5. Analytical Methods. TS, DM, VS, TKN, and total ammonia were analyzed according to the procedures of the American Public Health Association (APHA).20 The methane production in the BMP assays was measured by gas chromatography in a Shimatzu gas chromatograph with a flame ionization detector.21 Biogas composition in the headspace of the CSTR reactor was analyzed by gas chromatography on a 82-12 Microlab Århus A/S gas chromatograph.22 VFA were analyzed by gas chromatography on a Shimadzu GC-2010 with a Shimadzu AOI-20i auto injector.23 The pH in all experimental assays was determined with a digital pH meter, FEP20, Mettler Toledo. 2.6. Statistical Analysis and Calculations. The GraphPad Prism program (GraphPad Software, Inc., San Diego, CA) was used for all statistical analysis. Student’s t test and one-way analysis of variance (ANOVA) for statistically significant difference (p < 0.05) were used to compare the BMP values of the substrates and the methane production rates of the CSTR reactor. The BMP values used for the comparison between the different agricultural substrates was the highest one of the three tested organic loadings for each substrate. The maximum expected methane production rate and yield of each experimental period of the CSTR experiment were calculated on the basis of the BMP of the mono-substrates (assay I) and compared to the obtained methane production rate and yield under steady state. In this context, steady state was defined as a period of 10 successive days with less than 10% variation in the methane yield, methane production, and pH.22 Finally, all values were the mean of three independent replicates (n = 3) ± standard deviation (SD).
3. RESULTS AND DISCUSSION 3.1. BMP Assay I. Meadow grass had the highest (p < 0.05) BMP value (388 ± 30 NmL of CH4 g−1 of VS) compared to all of the agricultural byproducts and the manure biomasses tested in the BMP assay I. This BMP value for meadow grass was within the range of previous studies, which was 288−406 NmL of CH4 g−1 of VS for different meadow grass samples.24,25 In
Figure 1. BMP assay I: (a) BMP values and (b) methane production per ton of raw material (n = 3; SD). 8090
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0.05) compared to the two BMP values of spring barley and winter wheat at the same VS concentration. Finally, all BMP values derived from BMP assay II were similar (p > 0.05) to the expected BMP values, calculated as additive contributions of the manure−co-substrates based on the results of BMP assay I (Figure S1 of the Supporting Information). Thus, no synergistic effect, where co-digestion could increase the overall yield beyond a merely additive contribution of the single substrates, was found, which was in contradiction with a previous report.7 Furthermore, it seems that the initial high organic loads (63− 106 g of VS L−1) did not negatively affect the AD process. These results along with the similar methane production rates for both BMP assay I and II indicated that neither synergistic nor antagonistic interactions occurred in the BMP co-digestion experiments. As seen in Figure 2b, the methane production per ton of raw co-digested substrate was significantly (p < 0.05) increased alongside the VS concentration of all of the co-digested agricultural byproducts. The co-digestion batch reactors had 62−221% higher methane production compared to the reactors with manure (Table 4).
agricultural byproduct in terms of both the BMP value and raw substrate methane yield. This could be explained by the fact that meadow grass, among the organic byproducts studied (Table S2 of the Supporting Information), had the lowest crude fiber content (31% of the DM) that has very low biodegradability.26 At the same time, meadow grass had the highest N (1.94% of the DM) content and the second highest sugar content (66.4% of the DM) among the agricultural byproducts. This high content of easily digestible sugars27 combined with the favorable C/N ratio derived from the high N content28 most likely lead to the high BMP values for meadow grass. The negative impact of the crude fibers to the AD process becomes profound with winter barley, where the higher sugar content (72.4% of the DM) compared to all of the byproducts is not enough to compensate for the high crude fiber content (45.2% of the DM). Similar correspondence between BMP values and biochemical composition of the substrates has been previously reported for agricultural products and/or agricultural byproducts.29−31 On the basis of superior BMP values that winter wheat, spring barley, and meadow grass showed compared to the other tested mono-substrates, they were chosen for co-digestion with the manure in the second BMP assay (BMP assay II). 3.2. BMP Assay II. Almost all of the BMP values of the manure−co-substrate mixtures were similar (p > 0.05) and, at the same time, higher (p < 0.05) than the BMP value of the manure, as shown in Figure 2a. An exception was the codigested spring barley BMP value (organic load of 83.9 g of VS L−1) that was similar (p > 0.05) to the BMP of manure. Another exception was that the BMP value of the co-digested meadow grass at 83.8 g of VS L−1 was significantly higher (p
0.05). During period P-III, another steady state was established (days 75−91), with an average methane
production rate of 765 ± 31 NmL of CH4 L−1 day−1 (73% of the expected methane production with 64.0 ± 0.2% CH4 in the biogas), which was 31% higher (p < 0.05) compared to the methane production rate at period P-II. The results derived from P-IV of the experiment indicated a sound process with an increased methane production rate as an effect of the increased OLR. Specifically, the average methane production rate was 1002 ± 56 NmL of CH4 L−1 day−1 (with 65.2 ± 0.8% CH4 in the biogas), corresponding to 78% of the maximum expected one. At the same time, the methane production yield was significantly increased (p < 0.05) compared to the average methane production yields of the previous experimental periods (P-I, P-II, and P-III). According to Lehtomäki et al.,33 the highest specific methane yields in CSTR reactor co-digestion experiments of cow manure with grass or straw were obtained with 70:30% of VS manure/VS crop ratio in the feedstock and, above that ratio, the yield was significantly decreased. In this study, the methane production yield was increased (p < 0.05) at a VS manure/VS crop ratio of 53:47% (Table 2). This result indicates that VS manure/VS co-substrate ratio does not alone define the co-digestion limit between the manure and the agricultural byproducts. A possible explanation is that nitrogen (i.e., C/N ratio) could be the limiting factor affecting the AD 8092
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Energy & Fuels process efficiency.36 Specifically, better C/N ratio levels were provided by the available nitrogen in the substrate (pig and cow manure) used in this experiment (3.64 g of N L−1; Table S1 of the Supporting Information) compared to the 2.1 g of N L−1 (cow manure) of the aforementioned study. Thus, the TKN concentration and the C/N ratio of the co-digestion mixture seem to be key parameters determining the outcome of the AD process. The pH and VFA levels throughout the experiment verified a well-functioning process (Figure 4c). Specifically, the pH remained between 7.6 and 8.3 throughout all four experimental periods, demonstrating a healthy AD process.37 Additionally, the VFA accumulation throughout the experiment remained within the optimum levels (70 g of TS L−1). A total of 72−78% of the expected methane yield was reached when meadow grass and manure were co-digested under continuous conditions. Altogether, many of the agricultural byproducts available in European rural areas could be considered as suitable AD cosubstrates for efficient production of second-generation biogas.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.energyfuels.5b02373. Biomass analytical characteristics (Tables S1 and S2), experimental setup of the batch reactors for the BMP assays I and II (Tables S3 and S4), and comparison of measured and calculated BMP values (Figure S1) (PDF)
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REFERENCES
AUTHOR INFORMATION
Corresponding Author
*Telephone: +45-45251418. Fax: +45-45933850. E-mail:
[email protected]. Author Contributions †
Marie M. Søndergaard and Ioannis A. Fotidis contributed equally to this work. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was partially supported by regional project Bioenergy Zealand, founded by the European Fund for Regional Development, and Growth Forum Zealand. Moreover, the project was supported by ForskEl Project 12197, “Improving Synergy and Robustness of the Manure Codigestion Process”. The authors thank Nils Lass Rasmussen 8093
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