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Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content
Bioresource Technology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Bioresource Technology journal homepage: www.elsevier.com/locate/biortech
Short Communication
Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content Giorgos Markou ⇑ Department of Agricultural Engineering, Institute of Soil and Water Resources, Hellenic Agricultural Organization-Demeter, Leoforos Dimokratias 61, 13561 Athens, Greece Department of Natural Resources Management and Agricultural Engineering, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece
h i g h l i g h t s Poultry litter (PL) were pre-treated in a two phase process. In the first phase ammonia was produced and accumulated. In the second phase ammonia was stripped out. PL with lower N content displayed better bio-methane production.
a r t i c l e
i n f o
Article history: Received 8 June 2015 Received in revised form 19 July 2015 Accepted 20 July 2015 Available online xxxx Keywords: Ammonia inhibition Anaerobic digestion C/N ratio Biogas Poultry litter
a b s t r a c t Poultry litter (PL) was pre-treated in order to reduce its nitrogen content and to increase the C/N ratio. The pre-treatment consisted of a first anaerobiosis phase of about 60 days in order to accumulate ammonia nitrogen, followed by an ammonia stripping phase by heating the substrate at 80 °C for 24 h. The digestion was performed with PL and pre-treated PL (TPL) after ammonia stripping as mono-substrate under four total solids loads, i.e. 5%, 10%, 15% and 20%. The TPL after ammonia stripping displayed lower ammonia (62–73%) and VFA (41–65%) concentrations compared to digesters with raw PL, while bio-methane yield increased about 8–124%. Bio-methane yields in the series with TPL after ammonia stripping were about 193, 196, 215 and 147 LCH4 /kgCOD, based on the COD added, for 5%, 10%, 15% and 20% TS load, respectively. The results indicate that lowering nitrogen content using the suggested process improves bio-methane yields significantly. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Poultry livestock is an important agricultural sector which expands over time. In many cases, poultry are produced under intensive conditions, generating vast amounts of poultry litter (PL). PL are organic solid wastes rich in C, N, P, K and other elements. Therefore, PL is used as fertilizers and soil conditioner mainly after its composting (Kelleher et al., 2002). However, an alternative to composting technology is anaerobic digestion, by which the organic matter is degraded down to biogas. The latter is a combustible mixture, which could be used for energy production. In addition, after anaerobic digestion the effluents, which are stabilized and rich in nutrients, could also be used as fertilizers and soil conditioner as like PL compost (Kelleher et al., 2002). Thus,
⇑ Address: Department of Natural Resources Management and Agricultural Engineering, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece. E-mail addresses: [email protected], [email protected]
anaerobic digestion is advantageous compared to composting due to the additional gain of biogas. PL contains about 60–85% (dry basis) of volatile solids, which are highly digestible and could be used as substrate for the production of biogas through the anaerobic digestion technology (Niu et al., 2013). However, a major limitation of using PL for biogas production is its low C/N ratio, which is around 5–8. Substrates with low C/N ratio during the anaerobic digestion tend to accumulate ammonia, which is toxic to the anaerobic microflora. The main parameters that render ammonia toxic is its concentration in combination with the pH of the liquor, which determines the generated amounts of free ammonia (FA). The latter has been considered as the main toxic ammoniac species (Chen et al., 2008; Rajagopal et al., 2013). For an unhindered anaerobic digestion ammonia concentration should be kept to a level below 3 g/L that do not cause toxicity. To achieve this there are various suggested strategies, such as diluting PL (Bujoczek et al., 2000), adjusting C/N ratio of the digester by co-digesting PL with a carbon rich co-substrate(s) (Abouelenien
http://dx.doi.org/10.1016/j.biortech.2015.07.067 0960-8524/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
G. Markou / Bioresource Technology xxx (2015) xxx–xxx
et al., 2014), addition of phosphorite ore (Krylova et al., 1997), removing ammonia by biogas recycle (Abouelenien et al., 2010) and using multiple ammonia stripping phases during drydigestion of PL (Abouelenien et al., 2009b). Among the above strategies, ammonia stripping has been investigated by several researchers and seems to be a feasible strategy for removing ammonia nitrogen from the substrate (Jiang et al., 2014; Serna-Maza et al., 2014). Ammonia removal by stripping is based on forcing the dissociation equilibrium of NH+4/NH3 to favor FA (NH3) formation. FA is a gaseous molecule that is stripped out from aqueous solutions relative easily. The ratio of FA to total ammonia (TA) is a function depending mainly on pH and temperature and can be calculated by the following equation (Niu et al., 2013):
FA ¼ TA
1þ
10pH
!1
120 FA to TA ratio (%)
2
100 80 pH 7.5 pH 8.5 pH 9.5
60 40 20 0 40
50
60
70
80
90
100
Temperature (oC) Fig. 1. Effect of pH and temperature on the ratio of free ammonia to total ammonia.
2.2. Anaerobic digestion
272:92 T
10ð0:9018þ
To enhance the FA species, the pH of the substrate should be very high (>10) or/and temperature should be raised (Abouelenien et al., 2009b). As can be seen in Fig. 1 the most influencing factor, in the range investigated, is the pH of the substrate, while temperature has lower effect on the FA formation. However, to increase the pH, the addition of alkalis (such as NaOH, CaO, KOH, and Ca(OH)2) is required. The addition of ions in excessive amounts can negatively influence the methanogens lowering the biogas production (Chen et al., 2008). Therefore, in substrates that vast amounts of alkalis are needed, stripping by increasing temperature may be a potential choice, especially when waste thermal energy derived from electrical energy production by combusting biogas is available. However, ammonia nitrogen concentration in raw PL is relative low and the most nitrogen contained is in the organic form of proteins and uric acid. In order to remove nitrogen from PL by ammonia stripping, proteins or uric acid should be first degraded down to ammonia. For this reason, PL could be stored under dry anaerobic conditions for protein and uric acid degradation to convert organic nitrogen to ammonia (Abouelenien et al., 2009b; Kirchmann and Witter, 1989), followed by ammonia stripping to reduce the nitrogen content. Reducing the nitrogen content it is hypothesized that the anaerobic digestion of PL would be enhanced. Since, to the best knowledge of the author, there is no available information about the anaerobic digestion of PL treated by this approach, aim of this study was to investigate the anaerobic digestion performance of PL with low nitrogen content derived by the above mentioned two phase treatment.
2. Methods 2.1. Poultry litter collection and treatment PL was collected from an egg laying poultry farm in Megara, Attiki, Greece. PL was transferred to the lab and stored in a freezer at 26 °C. Some physiochemical characteristics of PL are listed in Table 1. Since the ammoniac nitrogen in PL was about 20% of the TKN, in order to increase the ammoniac nitrogen content, the PL was stored under anaerobic conditions (Kirchmann and Witter, 1989) for a period of about 60 days under room temperature 17–22 °C. The process of anaerobiosis of PL was not monitored and therefore it was not be optimized. At the end of the anaerobiosis the physiochemical characteristics of treated PL (TPL) are listed in Table 1. For the removal of ammonia, the TPL was placed inside an oven and heated at 80 °C and aerated for 24 h. The physiochemical characteristics of TPL after the ammonia stripping are listed in Table 1.
The anaerobic digestion was accomplished in 500 ml poly(ethylene terephthalate) (PET) bottles with working volume of 300 ml. Digesters were placed on a water-bath with constant temperature (35 ± 2 °C) and were intermittently stirred with magnetic stirrers with agitation cycle of 15:15 min on:off. As inoculum, sludge from mesophilic anaerobic digestion of swine manure and corn silage was used with PL substrate in a ratio of 3:1. After about two weeks, the digestion was switched in the semi-continuous mode and the hydraulic retention time (HRT) was set at 30 days. The feeding of the substrate was performed every two days. The digestion was considered as steady after about 2 times the HRT (60 days of operation). Digesters were run in duplicates.
2.3. Analytical methods Total ammonia, total Kjeldahl nitrogen (TKN), total solids, ash and chemical oxygen demand (COD), were determined by standard methods (APHA, 1995). Volatile fatty acids (VFA) were determined on the supernatant of centrifuged (10 min in 5000 rpm) samples according to Montgomery et al. (1962). Organic carbon was measured according to Yeomans and Bremner (1988). The ratio of carbon to nitrogen (C/N) of the samles was calculated as the ratio of the organic carbon to the TKN, which represents the total nitrogen (organic and inorganic) content of the samples. Biogas was trapped inside a vessel contained aqueous solution, which was replaced during biogas production. Solution of 0.1 N H2SO4 was used in order to avoid the dissolution of CO2 into the solution. Bio-methane was measured by passing biogas into a solution 5% NaOH. The NaOH solution absorbed the CO2 of the biogas and the difference between the volume before and after CO2 absorption was considered as the volume of produced bio-methane. The pH values were measured with a pH 209 (Hanna Instruments) pH meter. All analyses were made for two continuously feds in
Table 1 Physicochemical characterization of raw poultry litter, after their anaerobiosis, and after ammonia stripping. Parameter
Raw
After anaerobiosis of 60 days
After ammonia stripping
pH (1:10 H2O) Total solids (%) Ash (% TS) COD (mg-O2/g) TKN (mg-N/g) Ammoniac nitrogen (mg/g) Organic carbon (mg/g) C/N ratio
6.74 23.3 ± 0.55 27.6 ± 1.51 990 ± 55 52.5 ± 0.1 11.2 ± 1.1
8.29 19.71 ± 0.34 30.2 ± 1.90 960 ± 26 51.0 ± 0.5 36.4 ± 1.7
6.63 – 32.6 ± 1.51 860 ± 173 25.3 ± 0.1 1.86 ± 0.31
336 ± 26 6.4
312 ± 12 6.11
296 ± 11 11.7
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
G. Markou / Bioresource Technology xxx (2015) xxx–xxx
triplicates for each run (n = 12), except biogas, which measurement were recorded for three continuously feds once per run (n = 6). 3. Results and discussion In order to be a mono-digestion of PL feasible, a strategy for the lowering ammonia nitrogen concentration in the digestion liquor is required (Abouelenien et al., 2014). In the present study PL was treated on the first stage by storing it under anaerobic conditions for the degradation of organic nitrogen (proteins and uric acid) and the accumulation of ammonia. After 60 days of storing the ammonia nitrogen of TPL was increased considerable, by a factor of three, i.e. from about 11 mg/g to 36 mg/g (Table 1). This increase in ammonia caused an increase of the substrate pH, which reached a value about 8.3. This increase of pH was desired because it would favor the formation of FA and its easier removal by stripping. After the second phase of ammonia stripping, the TPL contained ammonia nitrogen less than 2 mg/g, a fact that indicates that ammonia stripping from substrate through heating was very effective. After the whole process, the C/N ratio was increased from 6.4 to 11.7. This C/N ratio, though is still significantly lower than the desired range of 20–30:1. Due to ammonia stripping the pH of the substrate decreased again reaching almost the value of the raw PL. However, a consequence of the whole process was an around 15% decrease of the COD values of the substrate. This indicates that some organic matter was degraded and lost, probably as methane, CO2 and water during the storage of PL under anaerobic conditions and their heating for 24 h. After ammonia stripping, the TPL with lower nitrogen content were used as mono-substrate for their anaerobic digestion. The anaerobic digestion was performed with four different TS loads (5%, 10%, 15% and 20%). An additional experimental series with the digestion of raw PL with the same four TS loads was used to serve as control runs for comparison purposes. As was mentioned before, during anaerobic digestion the organic matter is degraded by the anaerobic microflora. The methanogenic process is accomplished through four main phases, (i) hydrolytic phase, in which macromolecules, such as proteins, carbohydrates and fats, are broken down to amino acids, sugars and fatty acids, respectively (ii) acidogenic phase, in which sugars, amino acids, and fatty acids are converted to VFA, (iii) acetogenic phase, in which acetate, H2 and CO2, are formed, and (iv) methanogenic phase, in which acetate, H2 and CO2, are used as substrates for the production of biogas. During the acidogenic phase, the nitrogenous organic compounds are also degraded into VFA, CO2, H2 and ammonia. As higher the organic nitrogen content so higher the final ammonia concentration inside the digester. However, the tolerance of the digester to the TA depends on various parameters, such as pH, acclimatization of microflora, temperature etc., and it is hard to define the TA levels as an indicator to the state of an anaerobic process. Nonetheless, for an unhindered anaerobic digestion, TA concentration should not exceed 2.5–3 g/L (Chen et al., 2008; Yenigün and Demirel, 2013). As shown in Fig. 2, as expected, the ammonia concentrations in the digestion liquor of the control digesters were considerable higher compared to the series with TPL after ammonia stripping. In the most of the control digesters (with 10%, 15% and 20% TS loads), TA concentration exceeded 2.5–3 g/L. The general trend was increasing TA concentration as TS loads increased. Such high TA concentrations are typically reported by works dealing with anaerobic digestion of PL (Abouelenien et al., 2009b; Bujoczek et al., 2000). In contrast, in the series with TPL after ammonia stripping, TA concentrations were much lower than 2.5–3 g/L. The treatment of PL applied in the study resulted as expected to the decrease of TA concentration in the digester liquor about 62%,
3
67%, 69% and 73% compared to the corresponding control digesters. The pH values of the digestion liquor was higher in the series with PL than with PLT after ammonia stripping. The pH of the liquor was 7.81 ± 0.01, 7.99 ± 0.04, 8.06 ± 0.03 and 8.00 ± 0.06, for raw PL and 7.55 ± 0.03, 7.70 ± 0.06, 7.73 ± 0.12 and 7.77 ± 0.04 for TPL after ammonia stripping for TS loads of 5%, 10%. 15% and 20%, respectively. A consequence of the accumulation of TA is the inhibition of methanogens, lowering their acetoclastic and hydrogenotrophic methanogenic activity. Inhibited methanogens can not consume the produced VFA during acidogenesis/acetogenesis, while VFA still continue to be produced and accumulated in the digestion liquor. The accumulation of TA along with VFA have a finally negatively synergetic effect on the biogas production (Franke-Whittle et al., 2014; Lü et al., 2013; Yenigün and Demirel, 2013). Nonetheless, as like TA concentration, it is not easy to define which VFA levels effect the state of an anaerobic digestion process, because different systems can tolerate different levels of VFA (Franke-Whittle et al., 2014). In any case, all digesters in the series with raw PL displayed considerable higher VFA concentrations compared to the series with TPL after ammonia stripping (Fig. 2). Especially, as the TS load increased the differences of the accumulated VFA between the experimental series were much higher. Obviously this is a consequence of the higher TA concentrations at higher TS loads that inhibits methanogens in higher degree. VFA in the series of TPL after ammonia stripping were about 41%, 41%, 66% and 51% lower compared to the corresponding control digesters. This indicates that the VFA produced during acidogenesis/acetogenesis were consumed by the methanogens, keeping their concentrations in relative low levels. COD is a parameter to determine the organic load of a substrate. Higher COD values correspond to higher organic loads. Consequently, the higher the removal of COD the higher the removal of organic matter, which could be translated to higher biogas and bio-methane yields. Moreover, higher removal of COD means lower organic load to the effluents, having lower post-treatment requirements for their disposal. As shown in Fig. 2, in the series with raw PL, the COD removal was higher as the TS load decreased, while the residual COD was higher at higher TS loads. In contrast, in the series with TPL after ammonia stripping, the COD removal was increased as TS load increased up to 15% and decreased considerable at 20% TS load. The differences between the two experimental series indicates that lowering the nitrogen content had a significant positive effect on the organic matter degradation, resulting to the improvement of bio-methane yield (Fig. 3) of 9%, 18%, 46% and 124% for TS loads of 5%, 10%, 15% and 20%, respectively. Bio-methane yields in the TPL after ammonia stripping series were about 193, 196, 215 and 147 LCH4 /kgCOD (based on the COD added), for 5%, 10%, 15% and 20% TS loads, respectively. It is reported that the optimum TS load for PL digestion is about 5% (Bujoczek et al., 2000), which explains the low differences in bio-methane yield between raw PL and TPL after ammonia stripping with 5% TS load. However, increasing TS load it is necessary to reduce the PL nitrogen content, in order a mono-digestion to be feasible. The better anaerobic conditions of the series with TPL after ammonia striping resulted also to a higher bio-methane content in biogas (Fig. 3). This probably was due to the affection of the interaction between the buffering sub-systems of carbonate–bicarbonate, ammonium/ammonia and unionized/ionized VFA (Procházka et al., 2012). Other studies investigating the improvement of biogas production by PL report an increase of 93% when PL was co-digested with carbon rich co-substrates (Abouelenien et al., 2014), over than 195% when phosphorite ore at a concentration of 5% was added to the digester (Krylova et al., 1997), while a bio-methane yield
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
4
G. Markou / Bioresource Technology xxx (2015) xxx–xxx
Raw PL
TPL after ammonia stripping
Raw PL
TPL after ammonia stripping
Raw PL
TPL after ammonia stripping
COD removal COD removal
Fig. 2. Concentrations of total ammonia, volatile fatty acids, and residual COD in the liquor of the anaerobic digestion of (a) raw and (b) pre-treated poultry litter after ammonia stripping with four different total solids loads (5%, 10%, 15% and 20%).
Raw PL
TPL after ammonia stripping
CH4 content (%)
CH4 content
CH4 content
Fig. 3. Bio-methane yield and CO2 content in biogas of (a) raw and (b) pre-treated poultry litter after ammonia stripping with four different total solids loads (5%, 10%, 15% and 20%).
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
G. Markou / Bioresource Technology xxx (2015) xxx–xxx
of 195 ml/g of volatile solids was obtained through removing ammonia by biogas recycle in thermophylic digesters (Abouelenien et al., 2010) and a bio-methane yield of 104 ml/g of volatile solids using multiple ammonia stripping phases during thermophylic dry-digestion of PL (Abouelenien et al., 2009a). A significant issue however, related to the present approach is the energy consumption for the pre-treatment of the substrate. It is probably that the energy (direct or indirect) consumption by this approach would be higher compared to other methods for the improvement of biogas production from PL (Abouelenien et al., 2010, 2009b, 2014; Dong and Tollner, 2003; Krylova et al., 1997). Nevertheless, an energy consumption comparison between the methods is not applicable mainly due to the lack of detailed information. In any case, a potential advantage of the present approach is that waste thermal energy derived from the electrical energy production of biogas combustion could be used, minimizing the input of energy for the pre-treatment of PL. It would be of interest to investigate if this approach could be used also for solid or high solid substrates with low C/N, such as livestock manures (from pigs, cows, etc.), slaughterhouse wastes or fish wastes. Also it would be interesting to investigate whether this approach is applicable also to liquid substrates (wastewaters) with low C/N ratio. 4. Conclusions In the present study the effect of lowering of the nitrogen content of PL on the biogas production performance was investigated. PL with low nitrogen content displayed generally lower ammonia (62–73%) and VFA (41–65%) concentrations in the digestion liquor compared to digesters with raw PL, while bio-methane yield increased from 8% up to 124%, depending on TS load of the digesters. Bio-methane yields were about 193, 196, 215 and 147 LCH4 /kgCOD, based on the COD added, for 5%, 10%, 15% and 20% TS loads, respectively. The results indicate that lowering nitrogen content using the suggested process improves bio-methane yields significantly. Acknowledgements This research project is funded under the Action ‘‘Research & Technology Development Innovation projects (AgroETAK)’’, MIS 453350, in the framework of the Operational Program ‘‘Human Resources Development’’. It is co-funded by the European Social Fund and by National Resources through the National Strategic Reference Framework 2007–2013 (NSRF 2007–2013) coordinated by the Hellenic Agricultural Organisation ‘‘DEMETER’’ (Institute of Soil and Water Resources/Scientific supervisor: Dr. Dimitris
5
Oiconomou). Vassilis Kompoulis is kindly acknowledged for providing the poultry litter. References Abouelenien, F., Fujiwara, W., Namba, Y., Kosseva, M., Nishio, N., Nakashimada, Y., 2010. Improved methane fermentation of chicken manure via ammonia removal by biogas recycle. Bioresour. Technol. 101, 6368–6373. Abouelenien, F., Kitamura, Y., Nishio, N., Nakashimada, Y., 2009a. Dry anaerobic ammonia–methane production from chicken manure. Appl. Microbiol. Biotechnol. 82, 757–764. Abouelenien, F., Nakashimada, Y., Nishio, N., 2009b. Dry mesophilic fermentation of chicken manure for production of methane by repeated batch culture. J. Biosci. Bioeng. 107, 293–295. Abouelenien, F., Namba, Y., Kosseva, M.R., Nishio, N., Nakashimada, Y., 2014. Enhancement of methane production from co-digestion of chicken manure with agricultural wastes. Bioresour. Technol. 159, 80–87. APHA, 1995. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC. Bujoczek, G., Oleszkiewicz, J., Sparling, R., Cenkowski, S., 2000. High solid anaerobic digestion of chicken manure. J. Agric. Eng. Res. 76, 51–60. Chen, Y., Cheng, J.J., Creamer, K.S., 2008. Inhibition of anaerobic digestion process: a review. Bioresour. Technol. 99, 4044–4064. Dong, X., Tollner, E.W., 2003. Evaluation of Anammox and denitrification during anaerobic digestion of poultry manure. Bioresour. Technol. 86, 139–145. Franke-Whittle, I.H., Walter, A., Ebner, C., Insam, H., 2014. Investigation into the effect of high concentrations of volatile fatty acids in anaerobic digestion on methanogenic communities. Waste Manage. 34, 2080–2089. Jiang, A., Zhang, T., Zhao, Q.-B., Li, X., Chen, S., Frear, C.S., 2014. Evaluation of an integrated ammonia stripping, recovery, and biogas scrubbing system for use with anaerobically digested dairy manure. Biosyst. Eng. 119, 117–126. Kelleher, B., Leahy, J., Henihan, A., O’dwyer, T., Sutton, D., Leahy, M., 2002. Advances in poultry litter disposal technology–a review. Bioresour. Technol. 83, 27–36. Kirchmann, H., Witter, E., 1989. Ammonia volatilization during aerobic and anaerobic manure decomposition. Plant Soil 115, 35–41. Krylova, N.I., Khabiboulline, R.E., Naumova, R.P., Nagel, M.A., 1997. The influence of ammonium and methods for removal during the anaerobic treatment of poultry manure. J. Chem. Technol. Biotechnol. 70, 99–105. Lü, F., Hao, L., Guan, D., Qi, Y., Shao, L., He, P., 2013. Synergetic stress of acids and ammonium on the shift in the methanogenic pathways during thermophilic anaerobic digestion of organics. Water Res. 47, 2297–2306. Montgomery, H., Dymock, J.F., Thom, N.S., 1962. The rapid colorimetric determination of organic acids and their salts in sewage sludge liquor. The Analyst 87, 947–952. Niu, Q., Qiao, W., Qiang, H., Hojo, T., Li, Y.-Y., 2013. Mesophilic methane fermentation of chicken manure at a wide range of ammonia concentration: stability, inhibition and recovery. Bioresour. Technol. 137, 358–367. Procházka, J., Dolejš, P., Máca, J., Dohányos, M., 2012. Stability and inhibition of anaerobic processes caused by insufficiency or excess of ammonia nitrogen. Appl. Microbiol. Biotechnol. 93, 439–447. Rajagopal, R., Massé, D.I., Singh, G., 2013. A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour. Technol. 143, 632–641. Serna-Maza, A., Heaven, S., Banks, C.J., 2014. Ammonia removal in food waste anaerobic digestion using a side-stream stripping process. Bioresour. Technol. 152, 307–315. Yenigün, O., Demirel, B., 2013. Ammonia inhibition in anaerobic digestion: a review. Process Biochem. 48, 901–911. Yeomans, J., Bremner, J.M., 1988. A rapid and precise method for routine determination of organic carbon in soil 1. Commun. Soil Sci. Plant Anal. 19, 1467–1476.
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
Contents lists available at ScienceDirect
Bioresource Technology journal homepage: www.elsevier.com/locate/biortech
Short Communication
Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content Giorgos Markou ⇑ Department of Agricultural Engineering, Institute of Soil and Water Resources, Hellenic Agricultural Organization-Demeter, Leoforos Dimokratias 61, 13561 Athens, Greece Department of Natural Resources Management and Agricultural Engineering, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece
h i g h l i g h t s Poultry litter (PL) were pre-treated in a two phase process. In the first phase ammonia was produced and accumulated. In the second phase ammonia was stripped out. PL with lower N content displayed better bio-methane production.
a r t i c l e
i n f o
Article history: Received 8 June 2015 Received in revised form 19 July 2015 Accepted 20 July 2015 Available online xxxx Keywords: Ammonia inhibition Anaerobic digestion C/N ratio Biogas Poultry litter
a b s t r a c t Poultry litter (PL) was pre-treated in order to reduce its nitrogen content and to increase the C/N ratio. The pre-treatment consisted of a first anaerobiosis phase of about 60 days in order to accumulate ammonia nitrogen, followed by an ammonia stripping phase by heating the substrate at 80 °C for 24 h. The digestion was performed with PL and pre-treated PL (TPL) after ammonia stripping as mono-substrate under four total solids loads, i.e. 5%, 10%, 15% and 20%. The TPL after ammonia stripping displayed lower ammonia (62–73%) and VFA (41–65%) concentrations compared to digesters with raw PL, while bio-methane yield increased about 8–124%. Bio-methane yields in the series with TPL after ammonia stripping were about 193, 196, 215 and 147 LCH4 /kgCOD, based on the COD added, for 5%, 10%, 15% and 20% TS load, respectively. The results indicate that lowering nitrogen content using the suggested process improves bio-methane yields significantly. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Poultry livestock is an important agricultural sector which expands over time. In many cases, poultry are produced under intensive conditions, generating vast amounts of poultry litter (PL). PL are organic solid wastes rich in C, N, P, K and other elements. Therefore, PL is used as fertilizers and soil conditioner mainly after its composting (Kelleher et al., 2002). However, an alternative to composting technology is anaerobic digestion, by which the organic matter is degraded down to biogas. The latter is a combustible mixture, which could be used for energy production. In addition, after anaerobic digestion the effluents, which are stabilized and rich in nutrients, could also be used as fertilizers and soil conditioner as like PL compost (Kelleher et al., 2002). Thus,
⇑ Address: Department of Natural Resources Management and Agricultural Engineering, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece. E-mail addresses: [email protected], [email protected]
anaerobic digestion is advantageous compared to composting due to the additional gain of biogas. PL contains about 60–85% (dry basis) of volatile solids, which are highly digestible and could be used as substrate for the production of biogas through the anaerobic digestion technology (Niu et al., 2013). However, a major limitation of using PL for biogas production is its low C/N ratio, which is around 5–8. Substrates with low C/N ratio during the anaerobic digestion tend to accumulate ammonia, which is toxic to the anaerobic microflora. The main parameters that render ammonia toxic is its concentration in combination with the pH of the liquor, which determines the generated amounts of free ammonia (FA). The latter has been considered as the main toxic ammoniac species (Chen et al., 2008; Rajagopal et al., 2013). For an unhindered anaerobic digestion ammonia concentration should be kept to a level below 3 g/L that do not cause toxicity. To achieve this there are various suggested strategies, such as diluting PL (Bujoczek et al., 2000), adjusting C/N ratio of the digester by co-digesting PL with a carbon rich co-substrate(s) (Abouelenien
http://dx.doi.org/10.1016/j.biortech.2015.07.067 0960-8524/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
G. Markou / Bioresource Technology xxx (2015) xxx–xxx
et al., 2014), addition of phosphorite ore (Krylova et al., 1997), removing ammonia by biogas recycle (Abouelenien et al., 2010) and using multiple ammonia stripping phases during drydigestion of PL (Abouelenien et al., 2009b). Among the above strategies, ammonia stripping has been investigated by several researchers and seems to be a feasible strategy for removing ammonia nitrogen from the substrate (Jiang et al., 2014; Serna-Maza et al., 2014). Ammonia removal by stripping is based on forcing the dissociation equilibrium of NH+4/NH3 to favor FA (NH3) formation. FA is a gaseous molecule that is stripped out from aqueous solutions relative easily. The ratio of FA to total ammonia (TA) is a function depending mainly on pH and temperature and can be calculated by the following equation (Niu et al., 2013):
FA ¼ TA
1þ
10pH
!1
120 FA to TA ratio (%)
2
100 80 pH 7.5 pH 8.5 pH 9.5
60 40 20 0 40
50
60
70
80
90
100
Temperature (oC) Fig. 1. Effect of pH and temperature on the ratio of free ammonia to total ammonia.
2.2. Anaerobic digestion
272:92 T
10ð0:9018þ
To enhance the FA species, the pH of the substrate should be very high (>10) or/and temperature should be raised (Abouelenien et al., 2009b). As can be seen in Fig. 1 the most influencing factor, in the range investigated, is the pH of the substrate, while temperature has lower effect on the FA formation. However, to increase the pH, the addition of alkalis (such as NaOH, CaO, KOH, and Ca(OH)2) is required. The addition of ions in excessive amounts can negatively influence the methanogens lowering the biogas production (Chen et al., 2008). Therefore, in substrates that vast amounts of alkalis are needed, stripping by increasing temperature may be a potential choice, especially when waste thermal energy derived from electrical energy production by combusting biogas is available. However, ammonia nitrogen concentration in raw PL is relative low and the most nitrogen contained is in the organic form of proteins and uric acid. In order to remove nitrogen from PL by ammonia stripping, proteins or uric acid should be first degraded down to ammonia. For this reason, PL could be stored under dry anaerobic conditions for protein and uric acid degradation to convert organic nitrogen to ammonia (Abouelenien et al., 2009b; Kirchmann and Witter, 1989), followed by ammonia stripping to reduce the nitrogen content. Reducing the nitrogen content it is hypothesized that the anaerobic digestion of PL would be enhanced. Since, to the best knowledge of the author, there is no available information about the anaerobic digestion of PL treated by this approach, aim of this study was to investigate the anaerobic digestion performance of PL with low nitrogen content derived by the above mentioned two phase treatment.
2. Methods 2.1. Poultry litter collection and treatment PL was collected from an egg laying poultry farm in Megara, Attiki, Greece. PL was transferred to the lab and stored in a freezer at 26 °C. Some physiochemical characteristics of PL are listed in Table 1. Since the ammoniac nitrogen in PL was about 20% of the TKN, in order to increase the ammoniac nitrogen content, the PL was stored under anaerobic conditions (Kirchmann and Witter, 1989) for a period of about 60 days under room temperature 17–22 °C. The process of anaerobiosis of PL was not monitored and therefore it was not be optimized. At the end of the anaerobiosis the physiochemical characteristics of treated PL (TPL) are listed in Table 1. For the removal of ammonia, the TPL was placed inside an oven and heated at 80 °C and aerated for 24 h. The physiochemical characteristics of TPL after the ammonia stripping are listed in Table 1.
The anaerobic digestion was accomplished in 500 ml poly(ethylene terephthalate) (PET) bottles with working volume of 300 ml. Digesters were placed on a water-bath with constant temperature (35 ± 2 °C) and were intermittently stirred with magnetic stirrers with agitation cycle of 15:15 min on:off. As inoculum, sludge from mesophilic anaerobic digestion of swine manure and corn silage was used with PL substrate in a ratio of 3:1. After about two weeks, the digestion was switched in the semi-continuous mode and the hydraulic retention time (HRT) was set at 30 days. The feeding of the substrate was performed every two days. The digestion was considered as steady after about 2 times the HRT (60 days of operation). Digesters were run in duplicates.
2.3. Analytical methods Total ammonia, total Kjeldahl nitrogen (TKN), total solids, ash and chemical oxygen demand (COD), were determined by standard methods (APHA, 1995). Volatile fatty acids (VFA) were determined on the supernatant of centrifuged (10 min in 5000 rpm) samples according to Montgomery et al. (1962). Organic carbon was measured according to Yeomans and Bremner (1988). The ratio of carbon to nitrogen (C/N) of the samles was calculated as the ratio of the organic carbon to the TKN, which represents the total nitrogen (organic and inorganic) content of the samples. Biogas was trapped inside a vessel contained aqueous solution, which was replaced during biogas production. Solution of 0.1 N H2SO4 was used in order to avoid the dissolution of CO2 into the solution. Bio-methane was measured by passing biogas into a solution 5% NaOH. The NaOH solution absorbed the CO2 of the biogas and the difference between the volume before and after CO2 absorption was considered as the volume of produced bio-methane. The pH values were measured with a pH 209 (Hanna Instruments) pH meter. All analyses were made for two continuously feds in
Table 1 Physicochemical characterization of raw poultry litter, after their anaerobiosis, and after ammonia stripping. Parameter
Raw
After anaerobiosis of 60 days
After ammonia stripping
pH (1:10 H2O) Total solids (%) Ash (% TS) COD (mg-O2/g) TKN (mg-N/g) Ammoniac nitrogen (mg/g) Organic carbon (mg/g) C/N ratio
6.74 23.3 ± 0.55 27.6 ± 1.51 990 ± 55 52.5 ± 0.1 11.2 ± 1.1
8.29 19.71 ± 0.34 30.2 ± 1.90 960 ± 26 51.0 ± 0.5 36.4 ± 1.7
6.63 – 32.6 ± 1.51 860 ± 173 25.3 ± 0.1 1.86 ± 0.31
336 ± 26 6.4
312 ± 12 6.11
296 ± 11 11.7
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
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triplicates for each run (n = 12), except biogas, which measurement were recorded for three continuously feds once per run (n = 6). 3. Results and discussion In order to be a mono-digestion of PL feasible, a strategy for the lowering ammonia nitrogen concentration in the digestion liquor is required (Abouelenien et al., 2014). In the present study PL was treated on the first stage by storing it under anaerobic conditions for the degradation of organic nitrogen (proteins and uric acid) and the accumulation of ammonia. After 60 days of storing the ammonia nitrogen of TPL was increased considerable, by a factor of three, i.e. from about 11 mg/g to 36 mg/g (Table 1). This increase in ammonia caused an increase of the substrate pH, which reached a value about 8.3. This increase of pH was desired because it would favor the formation of FA and its easier removal by stripping. After the second phase of ammonia stripping, the TPL contained ammonia nitrogen less than 2 mg/g, a fact that indicates that ammonia stripping from substrate through heating was very effective. After the whole process, the C/N ratio was increased from 6.4 to 11.7. This C/N ratio, though is still significantly lower than the desired range of 20–30:1. Due to ammonia stripping the pH of the substrate decreased again reaching almost the value of the raw PL. However, a consequence of the whole process was an around 15% decrease of the COD values of the substrate. This indicates that some organic matter was degraded and lost, probably as methane, CO2 and water during the storage of PL under anaerobic conditions and their heating for 24 h. After ammonia stripping, the TPL with lower nitrogen content were used as mono-substrate for their anaerobic digestion. The anaerobic digestion was performed with four different TS loads (5%, 10%, 15% and 20%). An additional experimental series with the digestion of raw PL with the same four TS loads was used to serve as control runs for comparison purposes. As was mentioned before, during anaerobic digestion the organic matter is degraded by the anaerobic microflora. The methanogenic process is accomplished through four main phases, (i) hydrolytic phase, in which macromolecules, such as proteins, carbohydrates and fats, are broken down to amino acids, sugars and fatty acids, respectively (ii) acidogenic phase, in which sugars, amino acids, and fatty acids are converted to VFA, (iii) acetogenic phase, in which acetate, H2 and CO2, are formed, and (iv) methanogenic phase, in which acetate, H2 and CO2, are used as substrates for the production of biogas. During the acidogenic phase, the nitrogenous organic compounds are also degraded into VFA, CO2, H2 and ammonia. As higher the organic nitrogen content so higher the final ammonia concentration inside the digester. However, the tolerance of the digester to the TA depends on various parameters, such as pH, acclimatization of microflora, temperature etc., and it is hard to define the TA levels as an indicator to the state of an anaerobic process. Nonetheless, for an unhindered anaerobic digestion, TA concentration should not exceed 2.5–3 g/L (Chen et al., 2008; Yenigün and Demirel, 2013). As shown in Fig. 2, as expected, the ammonia concentrations in the digestion liquor of the control digesters were considerable higher compared to the series with TPL after ammonia stripping. In the most of the control digesters (with 10%, 15% and 20% TS loads), TA concentration exceeded 2.5–3 g/L. The general trend was increasing TA concentration as TS loads increased. Such high TA concentrations are typically reported by works dealing with anaerobic digestion of PL (Abouelenien et al., 2009b; Bujoczek et al., 2000). In contrast, in the series with TPL after ammonia stripping, TA concentrations were much lower than 2.5–3 g/L. The treatment of PL applied in the study resulted as expected to the decrease of TA concentration in the digester liquor about 62%,
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67%, 69% and 73% compared to the corresponding control digesters. The pH values of the digestion liquor was higher in the series with PL than with PLT after ammonia stripping. The pH of the liquor was 7.81 ± 0.01, 7.99 ± 0.04, 8.06 ± 0.03 and 8.00 ± 0.06, for raw PL and 7.55 ± 0.03, 7.70 ± 0.06, 7.73 ± 0.12 and 7.77 ± 0.04 for TPL after ammonia stripping for TS loads of 5%, 10%. 15% and 20%, respectively. A consequence of the accumulation of TA is the inhibition of methanogens, lowering their acetoclastic and hydrogenotrophic methanogenic activity. Inhibited methanogens can not consume the produced VFA during acidogenesis/acetogenesis, while VFA still continue to be produced and accumulated in the digestion liquor. The accumulation of TA along with VFA have a finally negatively synergetic effect on the biogas production (Franke-Whittle et al., 2014; Lü et al., 2013; Yenigün and Demirel, 2013). Nonetheless, as like TA concentration, it is not easy to define which VFA levels effect the state of an anaerobic digestion process, because different systems can tolerate different levels of VFA (Franke-Whittle et al., 2014). In any case, all digesters in the series with raw PL displayed considerable higher VFA concentrations compared to the series with TPL after ammonia stripping (Fig. 2). Especially, as the TS load increased the differences of the accumulated VFA between the experimental series were much higher. Obviously this is a consequence of the higher TA concentrations at higher TS loads that inhibits methanogens in higher degree. VFA in the series of TPL after ammonia stripping were about 41%, 41%, 66% and 51% lower compared to the corresponding control digesters. This indicates that the VFA produced during acidogenesis/acetogenesis were consumed by the methanogens, keeping their concentrations in relative low levels. COD is a parameter to determine the organic load of a substrate. Higher COD values correspond to higher organic loads. Consequently, the higher the removal of COD the higher the removal of organic matter, which could be translated to higher biogas and bio-methane yields. Moreover, higher removal of COD means lower organic load to the effluents, having lower post-treatment requirements for their disposal. As shown in Fig. 2, in the series with raw PL, the COD removal was higher as the TS load decreased, while the residual COD was higher at higher TS loads. In contrast, in the series with TPL after ammonia stripping, the COD removal was increased as TS load increased up to 15% and decreased considerable at 20% TS load. The differences between the two experimental series indicates that lowering the nitrogen content had a significant positive effect on the organic matter degradation, resulting to the improvement of bio-methane yield (Fig. 3) of 9%, 18%, 46% and 124% for TS loads of 5%, 10%, 15% and 20%, respectively. Bio-methane yields in the TPL after ammonia stripping series were about 193, 196, 215 and 147 LCH4 /kgCOD (based on the COD added), for 5%, 10%, 15% and 20% TS loads, respectively. It is reported that the optimum TS load for PL digestion is about 5% (Bujoczek et al., 2000), which explains the low differences in bio-methane yield between raw PL and TPL after ammonia stripping with 5% TS load. However, increasing TS load it is necessary to reduce the PL nitrogen content, in order a mono-digestion to be feasible. The better anaerobic conditions of the series with TPL after ammonia striping resulted also to a higher bio-methane content in biogas (Fig. 3). This probably was due to the affection of the interaction between the buffering sub-systems of carbonate–bicarbonate, ammonium/ammonia and unionized/ionized VFA (Procházka et al., 2012). Other studies investigating the improvement of biogas production by PL report an increase of 93% when PL was co-digested with carbon rich co-substrates (Abouelenien et al., 2014), over than 195% when phosphorite ore at a concentration of 5% was added to the digester (Krylova et al., 1997), while a bio-methane yield
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
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G. Markou / Bioresource Technology xxx (2015) xxx–xxx
Raw PL
TPL after ammonia stripping
Raw PL
TPL after ammonia stripping
Raw PL
TPL after ammonia stripping
COD removal COD removal
Fig. 2. Concentrations of total ammonia, volatile fatty acids, and residual COD in the liquor of the anaerobic digestion of (a) raw and (b) pre-treated poultry litter after ammonia stripping with four different total solids loads (5%, 10%, 15% and 20%).
Raw PL
TPL after ammonia stripping
CH4 content (%)
CH4 content
CH4 content
Fig. 3. Bio-methane yield and CO2 content in biogas of (a) raw and (b) pre-treated poultry litter after ammonia stripping with four different total solids loads (5%, 10%, 15% and 20%).
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067
G. Markou / Bioresource Technology xxx (2015) xxx–xxx
of 195 ml/g of volatile solids was obtained through removing ammonia by biogas recycle in thermophylic digesters (Abouelenien et al., 2010) and a bio-methane yield of 104 ml/g of volatile solids using multiple ammonia stripping phases during thermophylic dry-digestion of PL (Abouelenien et al., 2009a). A significant issue however, related to the present approach is the energy consumption for the pre-treatment of the substrate. It is probably that the energy (direct or indirect) consumption by this approach would be higher compared to other methods for the improvement of biogas production from PL (Abouelenien et al., 2010, 2009b, 2014; Dong and Tollner, 2003; Krylova et al., 1997). Nevertheless, an energy consumption comparison between the methods is not applicable mainly due to the lack of detailed information. In any case, a potential advantage of the present approach is that waste thermal energy derived from the electrical energy production of biogas combustion could be used, minimizing the input of energy for the pre-treatment of PL. It would be of interest to investigate if this approach could be used also for solid or high solid substrates with low C/N, such as livestock manures (from pigs, cows, etc.), slaughterhouse wastes or fish wastes. Also it would be interesting to investigate whether this approach is applicable also to liquid substrates (wastewaters) with low C/N ratio. 4. Conclusions In the present study the effect of lowering of the nitrogen content of PL on the biogas production performance was investigated. PL with low nitrogen content displayed generally lower ammonia (62–73%) and VFA (41–65%) concentrations in the digestion liquor compared to digesters with raw PL, while bio-methane yield increased from 8% up to 124%, depending on TS load of the digesters. Bio-methane yields were about 193, 196, 215 and 147 LCH4 /kgCOD, based on the COD added, for 5%, 10%, 15% and 20% TS loads, respectively. The results indicate that lowering nitrogen content using the suggested process improves bio-methane yields significantly. Acknowledgements This research project is funded under the Action ‘‘Research & Technology Development Innovation projects (AgroETAK)’’, MIS 453350, in the framework of the Operational Program ‘‘Human Resources Development’’. It is co-funded by the European Social Fund and by National Resources through the National Strategic Reference Framework 2007–2013 (NSRF 2007–2013) coordinated by the Hellenic Agricultural Organisation ‘‘DEMETER’’ (Institute of Soil and Water Resources/Scientific supervisor: Dr. Dimitris
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Oiconomou). Vassilis Kompoulis is kindly acknowledged for providing the poultry litter. References Abouelenien, F., Fujiwara, W., Namba, Y., Kosseva, M., Nishio, N., Nakashimada, Y., 2010. Improved methane fermentation of chicken manure via ammonia removal by biogas recycle. Bioresour. Technol. 101, 6368–6373. Abouelenien, F., Kitamura, Y., Nishio, N., Nakashimada, Y., 2009a. Dry anaerobic ammonia–methane production from chicken manure. Appl. Microbiol. Biotechnol. 82, 757–764. Abouelenien, F., Nakashimada, Y., Nishio, N., 2009b. Dry mesophilic fermentation of chicken manure for production of methane by repeated batch culture. J. Biosci. Bioeng. 107, 293–295. Abouelenien, F., Namba, Y., Kosseva, M.R., Nishio, N., Nakashimada, Y., 2014. Enhancement of methane production from co-digestion of chicken manure with agricultural wastes. Bioresour. Technol. 159, 80–87. APHA, 1995. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC. Bujoczek, G., Oleszkiewicz, J., Sparling, R., Cenkowski, S., 2000. High solid anaerobic digestion of chicken manure. J. Agric. Eng. Res. 76, 51–60. Chen, Y., Cheng, J.J., Creamer, K.S., 2008. Inhibition of anaerobic digestion process: a review. Bioresour. Technol. 99, 4044–4064. Dong, X., Tollner, E.W., 2003. Evaluation of Anammox and denitrification during anaerobic digestion of poultry manure. Bioresour. Technol. 86, 139–145. Franke-Whittle, I.H., Walter, A., Ebner, C., Insam, H., 2014. Investigation into the effect of high concentrations of volatile fatty acids in anaerobic digestion on methanogenic communities. Waste Manage. 34, 2080–2089. Jiang, A., Zhang, T., Zhao, Q.-B., Li, X., Chen, S., Frear, C.S., 2014. Evaluation of an integrated ammonia stripping, recovery, and biogas scrubbing system for use with anaerobically digested dairy manure. Biosyst. Eng. 119, 117–126. Kelleher, B., Leahy, J., Henihan, A., O’dwyer, T., Sutton, D., Leahy, M., 2002. Advances in poultry litter disposal technology–a review. Bioresour. Technol. 83, 27–36. Kirchmann, H., Witter, E., 1989. Ammonia volatilization during aerobic and anaerobic manure decomposition. Plant Soil 115, 35–41. Krylova, N.I., Khabiboulline, R.E., Naumova, R.P., Nagel, M.A., 1997. The influence of ammonium and methods for removal during the anaerobic treatment of poultry manure. J. Chem. Technol. Biotechnol. 70, 99–105. Lü, F., Hao, L., Guan, D., Qi, Y., Shao, L., He, P., 2013. Synergetic stress of acids and ammonium on the shift in the methanogenic pathways during thermophilic anaerobic digestion of organics. Water Res. 47, 2297–2306. Montgomery, H., Dymock, J.F., Thom, N.S., 1962. The rapid colorimetric determination of organic acids and their salts in sewage sludge liquor. The Analyst 87, 947–952. Niu, Q., Qiao, W., Qiang, H., Hojo, T., Li, Y.-Y., 2013. Mesophilic methane fermentation of chicken manure at a wide range of ammonia concentration: stability, inhibition and recovery. Bioresour. Technol. 137, 358–367. Procházka, J., Dolejš, P., Máca, J., Dohányos, M., 2012. Stability and inhibition of anaerobic processes caused by insufficiency or excess of ammonia nitrogen. Appl. Microbiol. Biotechnol. 93, 439–447. Rajagopal, R., Massé, D.I., Singh, G., 2013. A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour. Technol. 143, 632–641. Serna-Maza, A., Heaven, S., Banks, C.J., 2014. Ammonia removal in food waste anaerobic digestion using a side-stream stripping process. Bioresour. Technol. 152, 307–315. Yenigün, O., Demirel, B., 2013. Ammonia inhibition in anaerobic digestion: a review. Process Biochem. 48, 901–911. Yeomans, J., Bremner, J.M., 1988. A rapid and precise method for routine determination of organic carbon in soil 1. Commun. Soil Sci. Plant Anal. 19, 1467–1476.
Please cite this article in press as: Markou, G. Improved anaerobic digestion performance and biogas production from poultry litter after lowering its nitrogen content. Bioresour. Technol. (2015), http://dx.doi.org/10.1016/j.biortech.2015.07.067