High-rate anaerobic treatment of digestate using fixed film reactors

Environmental Pollution 252 (2019) 1622e1632

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High-rate anaerobic treatment of digestate using fixed film reactors*
-Demirer c, Go € ksel N. Demirer d, *, 1 Nilüfer Ülgüdür a, 1, Tuba H. Ergüder b, Sibel Uludag a

Department of Environmental Engineering, Düzce University, 81260, Düzce, Turkey Department of Environmental Engineering, Middle East Technical University, Ankara, Turkey c Department of Biosystems & Agricultural Engineering, Michigan State University, East Lansing, USA d School of Engineering and Technology, Central Michigan University, USA b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 December 2018 Received in revised form 12 June 2019 Accepted 27 June 2019 Available online 28 June 2019

The effluent stream of the anaerobic digestion processes, the digestate, accommodates high residual organic content that needs to be further treated before discharge. Anaerobic treatment of digestate would not only reduce the residual organic compounds in digestate but also has a potential to capture the associated biogas. High-rate anaerobic reactor configurations can treat the waste streams using lower hydraulic retention times which requires less footprint opposed to the conventional completely stirred tank reactors. This study investigated the high-rate anaerobic treatment performance and the associated biogas capture from the digestate of a manure mixture composed of 90% laying hen and 10% cattle manures in fixed-film reactors. The results indicated that it was possible to reduce total chemical oxygen demand content of the digestate by 57e62% in 1.3e1.4 days of hydraulic retention time. The corresponding biogas yields obtained were in the range of 0.395e0.430 Lbiogas/g VSadded which were found to be comparable to many raw feedstocks. Moreover, significant total phosphorus reduction (36e47%) and greenhouse gas capture (over 14.5e18.1 tCO2e/d per m3 digestate) were also recorded in the anaerobic fixed-film reactors. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Digestate Management High-rate Anaerobic Treatment Biogas

1. Introduction Anaerobic digestion has historically been applied for the treatment and stabilization of the high-strength wastes with a profitable outcome, renewable energy production. Even though biogas generated promotes the sustainability of the anaerobic digestion processes, the overall sustainability is grounded on good management practices developed for the digestate. However, there are still significant concerns regarding the management and disposal of digestate which necessitate the development of new approaches and uses (ÐurCevi c et al., 2018). Treatment and nutrient recovery processes offered for digestate management included vacuum evaporation and membrane processes (Fechter and Kraume, 2016), flocculation-aerationchemical oxidation (Camarero et al., 1996), struvite precipitation

* This paper has been recommended for acceptance by Dr. Sarah Harmon. * Corresponding author. E-mail address: [email protected] (G.N. Demirer). 1 At the time of the study, the author was affiliated with the Department of Environmental Engineering, Middle East Technical University, Ankara, Turkey.

https://doi.org/10.1016/j.envpol.2019.06.115 0269-7491/© 2019 Elsevier Ltd. All rights reserved.

(Uludag-Demirer et al., 2005) and ammonia (NH3) stripping (Drosg et al., 2015). The requirement for the addition of chemicals and/or the high energy input for these processes (Drosg et al., 2015) are the main drawbacks associated with their applicability. Even though nutrient removal from digestates using microalgal cultures has extensively been studied, large scale application is limited due to harvesting costs of microalgal biomass related to the dilute nature of the microalgal biomass (Gudin and Thepenier, 1986; Larronde-Larretche and Jin, 2016; Quijano et al., 2017). Thus, digestate still lacks feasible and viable treatment or nutrient recovery methods. Digestate has traditionally been applied on land as a fertilizer or soil conditioner (McPhail et al., 2012; Monnet, 2003; Romero-Güiza et al., 2016; Xia and Murphy, 2016). The nutrients in digestate content can be recycled and consumption of chemical fertilizers can be reduced by substitution of chemical fertilizers with digestate in agriculture (Romero-Güiza et al., 2016). On the other hand, digestate commonly leaves the digesters not fully stabilized due to the lack of optimization of digestion processes which typically have shorter hydraulic retention times (HRTs) and higher organic loading rates (OLRs). The use of incompletely stabilized digestate on land or even the storage of these digestates has a potential to

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create problems related to odor emissions, toxic organic compounds, pathogens and phytotoxicity (Nkoa, 2014; WojnowskaBaryła et al., 2018). Additionally, greenhouse gasses such as carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O) and general atmospheric pollutants such as NH3 can be emitted to the atmosphere during the storage or land application (Menardo et al., 2011). Digestate is thus required to be applied on land after being stabilized to prevent or at least to minimize the problems associated with its instability. Even though post-digestion tanks (closed stirred storage tanks) has been previously proposed to stabilize the digestate before land application (Wojnowska-Baryła et al., 2018), the footprint of such tanks would be large depending on the postdigestion periods of the digestate in the related studies between 28 € l€ days (Banks et al., 2013) and 125e136 days (Seppa a et al., 2013). Large area reservation for post-digestion tanks or even storing the digestate may be an additional concern for the plants where limited site is available. Residual biodegradable organic matter content of digestates asserts itself with high chemical oxygen demand (COD) concentrations. A previous study on anaerobic treatability of the digestates of animal manures and the mixtures of organic wastes and animal manures indicated that total chemical oxygen demand (CODt) content could be further reduced by 21e84% in batch reactors (Ülgüdür and Demirer, 2019). Moreover, additional biogas can be generated from digestates as a consequence of the decomposition of residual organics. The studies on the residual biogas production from the various digestate samples illustrated that 0.021e0.381 L/g VS biogas yield (Banks et al., 2013; Menardo et al., 2011; Wojnowska-Baryła et al., 2018) and 0.013e0.318 L/g VS methane yield (Garoma and Pappaterra, 2018; Hansen et al., 2006; Lindner et al., 2015; Maynaud et al., 2017; Rico et al., 2011; Ruile et al., €la € et al., 2013; Thygesen et al., 2015; Sambusiti et al., 2015; Seppa 2014) can potentially be recovered from various digestates. These potential yields of biogas and CH4 also address the potential energy loss by the disposal of the digestate. The additional biogas potential of digestates has been used to quantify the degradation efficiency of the biogas plants, the stability of the digestate and the effects of operating conditions on residual biogas production (Banks et al., 2013; Ruile et al., 2015; Sepp€ al€ a et al., 2013). The residual biogas produced from the digestate has been proposed to be captured in a storage or a closed post-digestion tank (Menardo et al., 2011; Rico et al., 2011; Wojnowska-Baryła et al., 2018). Moreover, residual biogas potential (RBP) has also been investigated for the purpose of the recycling of the digestate with or without pretreatment (Garoma and Pappaterra, 2018; Lindner et al., 2015; Sambusiti et al., 2015; Thygesen et al., 2014). Besides, high-rate anaerobic reactors have a potential to be applied for the treatment of digestates and to capture the associated biogas produced from the decomposition of the residual organic matters. Uncoupling HRT from solids retention time (SRT), high-rate reactors can be operated at short HRTs and high OLRs which in turn reduces the footprint of the installations (Abbasi et al., 2012; Barber and Stuckey, 1999). This study investigated further anaerobic treatment potential and associated biogas capture from digestates using a high-rate anaerobic reactor configuration. To this purpose, a digestate sample obtained from a full-scale anaerobic digester operated with 90% laying hen and 10% cattle manure was treated using anaerobic fixed-film reactors (AFFRs). To date, RBP of digestates has been studied in batches with the aim of capturing extracted biogas in storage or in closed stirred tanks or recycling of digestates to the main digester. This study brings about a novel insight into the reuse and treatment of digestates by high-rate anaerobic treatment with the specific emphasis on its further treatability.

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2. Materials and methods 2.1. Liquid digestate The digestate of an anaerobic digester operated with a mixture of 90% laying hen and 10% cattle manures was used as a feed for AFFRs. The plant of digestate sampling had 48e50 days of HRT and 83 tons/d digestate production and an installed capacity of 1.8 MW. The yearly electricity production was 12,691,000 kWh. The digestate previously obtained from this plant had the highest residual biogas yield (0.326 ± 0.009 Lbiogas/g VS) and 37e60% CODt reduction without nutrient supplementation among five digestate samples previously tested in batch reactors for 70 days of operation (Ülgüdür and Demirer, 2019). The digestate sample was settled for one day and the liquid portion after settling (liquid digestate) was treated using AFFRs. The digestate (before settling) and the liquid digestate were characterized for total solids (TS), volatile solids (VS), CODt, soluble chemical oxygen demand (CODs), total kjeldahl nitrogen (TKN), ammonium nitrogen (NHþ 4 -N), total phosphorus (TP), dissolved reactive phosphorus (DRP) and intermediate (IA), partial (PA) and total alkalinity (TA) (Table 1). The liquid digestate was kept at approximately 4  C and brought to room temperature before used. 2.2. Anaerobic seed sludge Anaerobic seed sludge was obtained from the same digester that the digestate sample was collected and settled for 1 day. The concentrated portion after settling was sieved from 1 mm mesh to remove large particles and then used as a seed for AFFRs (will be further referred as seed sludge). 500 mL of seed sludge was used to inoculate the AFFRs corresponding to 63.0% and 57.5% of the effective volume of the AFFRs named by R1 and R2, respectively. An enriched culture of anaerobic microorganisms allows for the development of biofilm in AFFRs (Acharya et al., 2008) as well as a rapid start-up (Salkinoja-Salonen et al., 1983). 2.3. Analytical methods Wastewater quality parameters of TS, VS, CODt, CODs, TKN, NHþ 4N, TP and DRP were analyzed according to the procedure given in Standard Methods (APHA, 2005). CODs and DRP were measured after filtering the samples from 0.45 mm pore-sized filters. Alkalinity measurement was performed according to the procedure described by Ripley et al. (1986). pH was monitored by Oakton pH/ CON 450 pH meter. Nitrogen (N2), CO2 and CH4 contents of biogas were determined using Agilent Technologies 6890N Gas Chromatograph with thermal conductivity detector (TCD). The device was equipped with a HP-Plot Q capillary column with dimensions of 30 m  530 mm x 40 mm. The composition of the biogas was measured three times in the last cycle with 2e3 days intervals when steady-state COD removal was achieved. Both the wastewater quality parameters and biogas composition measurements were done in duplicate. The results of the related measurements were given as average ± standard deviation. 2.4. Experimental setup Experimental setup was composed of a glass cylindrical reactor, influent and effluent lines and a biogas collection unit (Fig. 1). The effective volume and height of glass cylindrical reactors (AFFRs) were 793 mL and 56 cm for R1 and 870 mL and 55.5 cm for R2, respectively. R1 and R2 reactors were set as duplicate of each other. Polypropylene bio-filter media with 500 m2/m3 surface to volume

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Table 1 Seed sludge and digestate characterization. Parameter

pH Density (g/L) TS (mg/L) VS (mg/L) Solid content (%) CODt (mg/L) CODs (mg/L) TKN (mg/L) NHþ 4 - N (mg/L) TP (mg/L) DRP (mg/L) TA (mg/L as CaCO3) NHþ 4 - N/TKN

Seed sludge

Digestate

8.40 1035 ± 5 88,455 ± 425 38,065 ± 125 8.54 ± 0.00 74,991 ± 1458 19,460 ± 449 12,236 ± 0 7434 ± 42 18,992 ± 292 253 ± 1 23,275 ± 247 61%

Before settling

After settling (liquid digestate)

7.85 1025 ± 1 57,670 ± 240 34,625 ± 135 5.62 ± 0.02 76,795 ± 548 33,006 ± 196 7092 ± 85 6339 ± 53 8242 ± 42 157 ± 2 21,406 ± 472 89%

8.01 997 ± 5 40,138 ± 400 22,640 ± 294 4.03 ± 0.02 65,066 ± 1527 40,304 ± 1051 6977 ± 189 6637 ± 140 7180 ± 100 151 ± 0 19,248 ± 116 95%

Fig. 1. Experimental setup.

ratio and 0.96e0.98 g/cm3 density were used to immobilize the biomass within each reactor. Bio-filter media were fixed to a spiral cord extending through the reactor to prevent moving and floating of the media inside the reactor. Media fixed inside AFFRs provide a surface for the attachment of biomass (Mohana et al., 2013). Attached microorganisms uptake the components from the wastewater for their growth as the wastewater flows through the reactor (Shete and Shinkar, 2013). Biofilm growth enables high concentrations of active microorganisms to be retained within the reactors. Thus, the anaerobic reactor can be operated with a large SRT and a low HRT (Habouzit et al., 2014; Liu et al., 1991). Reactors were purged with nitrogen before start-up to ensure the strict anaerobic conditions developed within the reactor after inoculated with seed sludge. The liquid digestate was renewed daily and continuously stirred using a magnetic stirrer during feeding. It was fed into AFFRs using a peristaltic pump (Masterflex) in upflow direction. The effluent was collected into a graduated cylinder through a U-shaped pipe path. The biogas produced was

collected from the AFFRs by a gas-liquid-solid (GLS) separator and then transmitted into a gas-meter where the total volume of biogas was quantified. The solution used in gas-meter contained 270 g/L of salt and was acidified to pH 2 using concentrated H2SO4 (Walker et al., 2010). 2.5. Operation of anaerobic fixed-film reactors Two AFFRs were operated in parallel in continuous mode. The operation temperature was kept at 35 ± 2  C at a constant temperature room. The total duration of the experiment was 81 days with six cycles applied. The duration of the cycles, HRT and OLR applied at each cycle are given in Table 2. OLR was calculated based on CODt load applied per unit effective volume of AFFR (Chernicharo, 2007). OLR was incrementally increased by decreasing the dilution of the liquid digestate at the end of cycles 1 and 2 and by increasing the inflow rate between the cycles 3e6 (Table 2). The liquid digestate was diluted by 1/12, 1/6 and 1/3 with

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Table 2 Operational parameters of AFFRs. Reactor

Cycle

Time (d)

Flow rate (mL/min)

HRT (d)

OLR (g/(L.d))

Dilution ratio

R1

1 2 3 4 5 6 1 2 3 4 5 6

0e7 7e19 19e34 34e49 49e64 64e81 0e7 7e19 19e34 34e49 49e64 64e81

0.1 0.1 0.1 0.2 0.3 0.4 0.1 0.1 0.1 0.2 0.3 0.4

5.09 5.09 5.09 2.53 1.69 1.27 5.64 5.64 5.64 2.81 1.88 1.41

1.07 2.13 4.28 8.56 12.83 17.11 0.96 1.92 3.86 7.71 11.57 15.42

1/12 1/6 1/3 1/3 1/3 1/3 1/12 1/6 1/3 1/3 1/3 1/3

R2

tap water at the cycles 1, 2 and 3e6 (Table 2) which corresponded to a solid content of 0.34, 0.67 and 1.34%, respectively. It was previously suggested to operate the AFFRs at a solid content less than 2% in the influent (Wilkie, 2005). The OLR was increased when more than 50% CODt removal was achieved in two consecutive measurements. RBP test previously conducted in our laboratory for the digestate sample obtained from the same digester yielded 37e60% CODt removal efficiency (Ülgüdür and Demirer, 2019). Therefore, 50% efficiency was approximated to be representative of an average attainable CODt removal. The performance of the AFFRs were evaluated in terms of TS, VS, CODt, CODs, TKN, NHþ 4 -N, TP and DRP concentrations. The removal efficiencies were calculated based on the removed amounts of constituents with respect to the influent concentrations. Steady-state conditions were evaluated for both CODt and CODs removal at the 6th cycle and defined as the ones after five turnovers of HRT and when the effluent CODt and CODs removal efficiencies did not vary more than 5%. Discussions related to removals of the constituents were carried out considering end-cycle measurements unless otherwise stated. End-cycle measurements indicate the second data point that falls into the cycle field (Fig. 3). 3. Results and discussion 3.1. Hydraulic retention time, organic loading rate, pH and alkalinity HRT and OLR given in Table 2 were calculated based on the influent flow rate applied to the AFFRs. HRT was gradually reduced from 5.09 to 1.27 days for R1 and from 5.64 to 1.41 days for R2 through the 81 days of operational period (Table 2). The corresponding OLRs increased from 1.07 g/(L.d) to 17.11 g/(L.d) for R1 and from 0.96 g/(L.d) to 15.42 g/(L.d) for R2. The maximum OLRs applied were slightly above the typical OLR of 10e15 g/(L.d) reported for AFFRs (Hall, 1992). HRT and OLR were re-calculated depending on the volume collected from the effluent line within specific time period during operation (Fig. 2). These two operational parameters had slight oscillations compared to those calculated from influent flow. It is probable to observe such oscillations during the operation of high-rate anaerobic reactors when these operational parameters are calculated based on the volume collected from the effluent line (S¸en and Demirer, 2003). The stability of the operation of AFFRs was evaluated in terms of pH and alkalinity. The initial pH of the liquid digestate increased from 8.01 to 8.39 ± 0.14 for R1 and to 8.41 ± 0.13 for R2 in the effluent during the course of operation (Fig. 2). The influent alkalinities were 1604, 3208 and 6416 mg/L as CaCO3 for the dilution ratios of 1/12, 1/6 and 1/3, respectively. The alkalinity concentrations of the effluents were also observed to be higher than that of

the influents (6251 ± 0; 4274 ± 291; 7943 ± 206 for R1 and 6541 ± 58; 4335 ± 236; 7940 ± 177 mg/L as CaCO3 for R2, respectively) (Fig. 2). The increase in pH and alkalinity can be attributed to the methanogenic activity due to the consumption of hydrogen and hydronium ions (Acharya et al., 2008). The pH of the effluents of AFFRs (approximately 8.40) was higher than the tolerable pH range of 6.5e8.0 for anaerobic digestion processes (Cioabla et al., 2012). On the other hand, the pH levels of the effluents were almost stable during the course of operation (8.39 ± 0.14 for R1 and 8.41 ± 0.13 for R2). Moreover, the ratio of intermediate to partial alkalinity (IA/PA) of the effluents was lower than 0.3 (in the range of 0.05e0.16 for R1 and 0.06e0.16 for R2). IA/PA ratios lower than 0.3 indicated the stability of the anaerobic digestion processes (Alcaraz-Gonzalez et al., 2015). Thus, pH levels reported did not affected the operational stability depending on the stable pHs and the indicative IA/PA ratios of the effluents. Even though alkalinity concentrations for both R1 and R2 decreased at the 2nd cycle compared to those of 1st cycle, pH levels were approximately maintained (Fig. 2). The decrease in alkalinity was probably due to formation or presence of carbonic acids and other acids (i.e. volatile fatty acids). Alkalinity is mainly dependent on the presence of salts of weak acids and strong bases, and other compounds that can buffer a pH drop in a digestion environment € n, 2009). On the other hand, alkalinity concentrations (Scho measured during the 2nd cycle were in the range of 3983e4571 mg/L as CaCO3 for both reactors. Typically, an alkalinity concentration of 2000e4000 mg/L as CaCO3 is required to maintain the pH at or near neutral in anaerobic digestion (Tchobanoglous et al., 2003). The measured alkalinity concentrations, which were comparable to upmost typical value (4000 mg/L as CaCO3), and stable pH levels indicated that alkalinity concentration in the digestion environment was sufficient to prevent a probable pH drop. As a consequence, AFFR treatment of the digestate did not require any alkalinity dosing depending on the highly alkaline composition of the effluents and the stability of the reactors. The operational costs related with the chemical consumption can be reduced in the treatment of digestates in AFFRs which is profitable for the plant economics. 3.2. Total and soluble chemical oxygen demand The effluent CODt concentrations (7827 ± 117 for R1 and 9638 ± 234 mg/L for R2) were higher than the influent concentrations (5422 mg/L) at the 1st cycle of operation which was an indication of the wash-out of seed sludge from the reactor. Wash-out of seed sludge resulted in the calculation of negative removals for the constituents. Negative removals of all constituents given in the caption of Fig. 3 indicate this wash-out period observed at the 1st

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Fig. 2. The changes in HRT, OLR, pH and alkalinity during the operation of AFFRs based on the measurements on the collected effluents.

cycle. Wash-out of seed sludge at the initial stages of the operation helps to remove finely dispersed and poorly settleable particles from the reactor (de Zeeuw, 1984), thus, can aid in the development of well settleable biomass within the reactors. This cycle lasted for 7 days and was ended by increasing the OLR. The influent CODt concentrations were 10844 and 21689 mg/L in cycles 2 and 3e4, respectively. Even though OLR was increased by 4 folds (Table 2), CODt reduction was almost preserved during the cycles 2e4 for both reactors considering the end-cycle measurements (53e57% for R1 and 51e59% for R2) (Fig. 3). An additional increase in OLR by 50% resulted in an increased CODt removal efficiency at the 5th cycle (62e63% and 64e66% for R1 and R2, respectively) when the influent CODt concentration was 21689 mg/ L. The CODt concentration of the influent stayed the same once more at the 6th cycle, but the influent flowrate was increased by 33.3%. The applied OLRs were thus 17.11 and 15.42 g/(L.d) for R1 and R2, respectively, at the last cycle. The CODt removal efficiencies in the first measurement at the 6th cycle (57-57% for R1 and 55e56% for R2) (Fig. 3) were observed to be slightly lower than the ones obtained at the 5th cycle. However, these removal efficiencies were obtained in the application of 1.33-fold higher OLR in cycle 6 (17.11 g/(L.d) for R1 and 15.42 g/(L.d) for R2) compared to those of cycle 5 (12.83 g/(L.d) for R1 and 11.57 g/(L.d) for R2). This indicated that optimum loading rate was achieved at the 6th cycle. Since the removal of CODt did not significantly alter between 5th and 6th cycle, the operation of AFFRs with higher OLRs may be preferable to further decrease the footprint requirement for installations. OLR was not further increased to avoid probable wash-out of the microorganisms. The steady-state CODt removal at the 6th cycle was observed between 74 and 81 days of operation which corresponded to a CODt removal efficiency of 61.5 ± 1.12% for R1 and

59.5 ± 2.5% for R2. The CODt removal obtained in the treatment of the liquid digestate in AFFR (in the range of 56e63%) was found to be comparable to the CODt removal of the whole digestate obtained from the same plant in batches at the end of 70 days (37e60%) (Ülgüdür and Demirer, 2019). The treatment of the liquid digestate using AFFRs with an HRT of 1.3e1.4 days requires approximately 7e38 times less volume when compared to the conventional digesters with 10e50 days of HRT. Therefore, anaerobic treatment of the liquid digestate in AFFR would yield less footprint and decrease the associated costs. The removal efficiencies of CODt obtained at the 6th cycle were also comparable to that of obtained in the treatment of dairy wastewater (a raw feedstock, not the digestate) using semi-continuous anaerobic fixed film bed reactor (Nikolaeva et al., 2013). The authors achieved 46.2% COD removal at an OLR and HRT of 12 g/(L.d) and 2 days, respectively. Similar CODt removals were also recorded for anaerobic digestion of dairy manure using bio-based additives (51.4e67.8%) (Yun et al., 2018) and Niobium (Nb)-based additives (56.1e65.2%) (Zhang et al., 2017) to improve biogas yield and digestate stability. CODs removal improved at each increase in the organic loading rate despite almost constant CODt removal rates during the cycles 2e4 (Fig. 3). 58.5, 76.0, 79.5 and 84.5% CODs removal were recorded for R1 at the end of the cycles 2e5. While, CODs removal rates of 67.0, 81.0, 69.0 and 79.5% were observed for R2 at the end of the cycles 2e5 (Fig. 3). The steady-state CODs removal at the 6th cycle was reached between the days of 74e81 with an efficiency in the range of 86e88% considering both R1 and R2. CODs removal was found to be comparable to that of obtained in the treatment of acetic acid based synthetic wastewater (83%) using a downflow AFFR with an OLR of 17.10 g COD/L.d and an HRT of 1.3 days (Hamoda and Kennedy, 1987).

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Fig. 3. The removal profiles of the constituents during the operation of AFFRs. The removals of CODt, CODs, NHþ 4 -N, TKN, DRP and TP were 44, 11, 256, 249, 244 and 13% for R1 and -78, 22, 276, 274, 222 and 16% for R2, respectively, at the 1st cycle.

The influent carried 13435 and 21689 mg/L soluble and total COD at the 6th cycle, respectively, representing a CODs/CODt ratio of 62%. The soluble portion of the removed CODt (CODs/CODt ratio) was 85e90% for R1 and 88e94% for R2 which indicated that the removal of COD was mainly due to its soluble content. The CODs degradation was in the range of 11113e11862 mg/L considering both reactors. The degradation of organic matters as the removal of TS and VS suggested (Section 3.5) also expected to contribute to the CODs concentration during decomposition. Fermentative bacteria solubilizes the complex organic compounds (Chernicharo, 2007)

which would lead to increase in CODs concentration. Thus, CODs degradation could be speculated to be higher when the solubilized COD from the organic content of the digestate was considered. Anaerobic fixed-film treatment of the liquid digestate can therefore be applied in relatively fast degradation of the CODs content and interrelatedly in the extraction of the associated biogas. It therefore becomes necessary to analyze CODs content of the digestates as well as CODt before any application on the further high-rate anaerobic treatment.

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3.3. Ammonium and total kjeldahl nitrogen NHþ 4 -N concentrations of the influent were 553, 1106 and 2212 mg/L during the cycles 1, 2 and 3e6, respectively. NHþ 4 -N concentration applied in the cycles 3e6 (2212 mg/L) was higher than the inhibitory concentration reported as 1700e1800 mg/L when the inoculum was not acclimated (Yenigün and Demirel, 2013). Moreover, TKN concentrations of the influent were between 581 and 2326 mg/L through the cycles which were also higher than the previously reported appropriate TKN range of 186e1551 mg/L (Li et al., 2018). Excessive concentrations of TKN can also have adverse effect on anaerobic digestion (Huang et al., 2016). On the other hand, the stability of the reactors in AFFR treatment indicated no inhibition arising from the increase of inflow ammonium content relying on the pH and alkalinity measurements (Section 3.1). The respectively lower concentrations applied during the cycles 1 and 2 for approximately 13 days may have provided the acclimation of the microorganisms. Besides acclimation during the reactor operation, the seed sludge was obtained from the same digester of digestate sampling which may have already been acclimated to digestate. Inhibitory total ammonia nitrogen concentrations can be up to 5000 mg/L if the microorganisms are acclimated to high ammonium concentrations (Yenigün and Demirel, 2013). The digestate had an ammonification ratio (NHþ 4 -N/TKN) of 89% before settling (Table 1). The high ammonification of the digestate was probably due to the raw feedstock composition of the digester (90% laying hen and 10% cattle manure). The poultry manures have € ller and Müller, 2012). The high NHþ 4 -N to total nitrogen ratios (Mo settling of the digestate resulted in higher ammonification in the liquid phase (95%) which suggested the partial removal of the organic nitrogen by the settled and removed phase (U.S.EPA, 2007). The AFFR treatment of the liquid digestate slightly increased the ammonification from 95% to 96e98% for R1 and 95e97% for R2 according to the end-cycle measurements. The treatment of poultry slaughterhouse wastewater using AFFRs previously reported to have ammonification ratios in the range of 85e96% (Del Pozo et al., 2000) which were found to be comparable with this study. 2212 mg/L of NHþ 4 -N and 2326 mg/L of TKN was applied at the 6th cycle. The removal of NHþ 4 -N was by 9e15% and 10e12% and that of TKN was 12e16% and 11e14% for R1 and R2, respectively at the 6th cycle (Fig. 3). The removed NHþ 4 -N concentrations were lower than that of TKN. TKN is the summation of NHþ 4 -N and organic nitrogen and degradation of organic nitrogen releases ammonium (Ghyselbrecht et al., 2019). Lower NHþ 4 -N removals than that of TKN indicated the removal of organic nitrogen. Thus, NHþ 4 -N and organic nitrogen were simultaneously removed from the digestate content. The pH range of the effluent of AFFRs (8.39 ± 0.14 for R1 and 8.41 ± 0.13 for R2) were lower than the acidity constant (pKa) which was 8.95 at 35  C (Martinelle and €ggstro €m, 1997). NHþ Ha 4 -N can potentially be removed from the system via volatilization of NH3 even if volatilization is expected to have a minor impact at pHs lower than pKa (Al-Nozaily, 2001). Additionally, NHþ 4 -N can be oxidized via catalase enzymatic activity of microorganisms and further removed by autotrophic and/or heterotrophic denitrification in the presence of organic matter (Sabumon, 2007). 3.4. Dissolved reactive and total phosphorus concentrations The change in phosphorus concentrations was investigated with DRP and TP constituents. The influent DRP and TP concentrations ranged between 13-50 and 598e2393 mg/L, respectively, during cycles 1e6. DRP and TP concentrations were observed to be removed during the operation without any exact pattern as well as

NHþ 4 -N and TKN concentrations (Fig. 3). These fluctuations observed were probably due to alterations in OLR applied at the end of each cycle, since the removal efficiencies of the nutrients are dependent on the composition and load of the influent (Singh and Srivastava, 2011; Vymazal, 2007). Similar fluctuations were also observed in the treatment of opaque beer brewery wastewater using a full-scale upflow anaerobic sludge blanket reactor (UASB) (Parawira et al., 2005). DRP removal obtained at the 6th cycle of operation was in the range of 54e64% and 48e66% for R1 and R2, respectively, even though anaerobic digesters are known to reduce negligible amounts of nutrients (Demirer and Chen, 2005). 28e78% reduction in dissolved phosphate concentration was previously obtained in the treatment of synthetic sewage wastewater using a hybrid sludge bed/fixed film reactor (Keating et al., 2016). The authors claimed that the phosphate removal was achieved through the formation of intracellular inorganic polyphosphate (polyP) granules mediated by biofilm and fixed-film unit. Moreover, the precipitation of the calcium phosphate molecules such as hydroxyapatite, calcium phosphate hydrate and carbonated hydroxyapatite was observed during the treatment of black waters in UASB reactors (Tervahauta et al., 2014). Calcium phosphate precipitates were also claimed to act as a nuclei for granular formations on which a surface was provided for the attachment of microorganisms (Cunha et al., 2018). Thus, DRP removal in the anaerobic treatment of liquid digestate can also be attributed to the biologically mediated intracellular inorganic polyPs and the formation of calcium phosphate precipitates. The removal of TP was in the range of 33e48% in R1 and 34e47% in R2 at the 6th cycle (Fig. 3). The removed DRP concentrations (24e33 mg/L) were much lower than that of TP (870e1132 mg/L). This fact indicated the removal of different forms of phosphorus from the liquid digestate at high proportions other than DRP. As dissolved unreactive phosphorus (DUP), dissolved organic phosphorus (DOP) and particulate phosphorus (PP) are the other components of TP (Alaica, 2012), the AFFR treatment of the liquid digestate also enabled the removal of phosphorus forms other than DRP. The effluent of AFFRs had still high concentrations of TP (1353 ± 25 for R1 and 1291 ± 29 mg/L for R2) and NHþ 4 -N (1985 ± 1 and 1975 ± 1 mg/L for R1 and R2, respectively) at the last measurement. This fact may prevent the discharge of AFFR effluent depending on regulatory perspectives. On the other hand, the effluent of AFFRs can be considered as ‘the digestate of a digestate’. As a consequence of the fact that digestates can be used as a feed for microalgal species, AFFR treatment has a potential to be coupled with a microalgal nutrient removal process. Microalgal biomass obtained can then be valorized in biofuel production (Xia and Murphy, 2016) on condition of reduced harvesting costs of biomass. 3.5. Total and volatile solids Liquid digestate had 40,138 ± 400 mg/L TS, 22,640 ± 294 mg/L VS concentration and 4.03 ± 0.02% solid content at the initial characterization (Table 1). The influent of the AFFRs carried a TS and VS concentration of 13,379 mg/L and 7547 mg/L at the last cycle, respectively (Fig. 4). TS concentration was reduced by 10e24% for R1 and 11e20% for R2 whereas those of VS were 24e33% for R1 and 19e30% for R2 at the last cycle. TS and VS removals were comparable to those obtained in anaerobic digestion of cow manure using steel slag as accelerant (14.7e26.2% and 10.8e28.6%, respectively) (Han et al., 2019). TS removal in our study was mainly due to destruction of VS during steady-state COD removal period (between 74th and 81st day of operation) based on the VS/TS ratios (78e96%) of the removed TS concentration. Since VS is an

N. Ülgüdür et al. / Environmental Pollution 252 (2019) 1622e1632

Fig. 4. TS and VS concentrations of the influent and effluent of AFFRs.

approximation to quantify organic matters (Mata-Alvarez, 2002), it can thus be concluded that the removal of TS mainly dependent on the degradation of the residual organic matters in the digestate content.

3.6. Biogas production and yield Negligible biogas production was observed in the first two cycles for both of the reactors (Fig. 5). Acclimation and adaptation of bacteria can result in lower biogas production at the initial stages of incubation (Acharya et al., 2008). No or negligible biogas production at the initial stages of the start-up of bio-film reactors was also

Fig. 5. Daily biogas production per volume of digestate in R1 and R2.

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previously noted (Michaud et al., 2002). Biogas production progressively increased from the third to the sixth cycle. The production was 1.0 ± 0.61, 1.6 ± 0.35, 2.6 ± 0.46, 3.3 ± 0.27 for R1 and 0.3 ± 0.22, 1.0 ± 0.38, 2.3 ± 0.66 and 3.0 ± 0.42 L/L digestate for R2 in the cycles 3e6, respectively. The progressive increase in the biogas production together with the CODt removals attained in the range of 51e69% during cycles 2e6 (Fig. 3) suggested the catabolism of organic compounds by the anaerobic bacteria for respiration rather than anabolic activity for biopolymer synthesis (Michaud et al., 2002). CH4 content of the biogas was in the range of 77.5e80.3% and 70.7e78.0% for R1 and R2, respectively, during steady-state COD removal period at the 6th cycle (Fig. 6). The corresponding CO2 content ranged between 9.0 and 17.0% for R1 and 13.0e19.0% for R2. CH4 contents were higher than those of obtained in the range of 13e46% from the digestates of various mixtures of animal wastes and energy crops (Menardo et al., 2011). On the other hand, CH4 contents were found to be comparable with the ones obtained from an untreated digestate sample of a full-scale digester which was operated with a mixture of liquid and solid manure, maize and grass silage and grain (77.5 ± 6.8%) (Lindner et al., 2015). When the average daily biogas production for each reactor was converted into terms of CH4, daily CH4 production was found as 2.12e2.65 L/L digestate (1.88e2.35 L/L digestate at standard conditions) based on the maximum and minimum CH4 contents obtained from both of the reactors. It was also calculated that 0.274e0.343 kW power could be generated from a cubic meter of digestate via further highrate anaerobic digestion of the digestate (assumptions: lower heating value of CH4 ¼ 36 MJ/m3 at standard conditions, electrical conversion efficiency ¼ 35% (Manyuchi et al., 2018)). 21.9e27.4 kW additional power could be obtained considering a daily digestate production of 80 m3. The power generation capacity from the digestate corresponded to 1/53e1/66 of the existing power output of the anaerobic digester of the digestate sampling (1449 kW). As the power output for the plant was calculated based on the daily volume of digestate produced, the increase in the digestate production would potentially increase the power generation capacity from the digestate. Biogas yields relative to the removed CODt (CODr) and the added amount of volatile solids by the influent (VSadded) are given in Table 3. Each increase in the OLR resulted in an increase in the average biogas yield during operation. Average biogas yields were 0.430 Lbiogas/g VSadded for R1 and 0.395 Lbiogas/g VSadded for R2 at the 6th cycle. These yields corresponded to 0.333e0.345 L CH4/g VSadded and 0.279e0.308 L CH4/g VSadded for R1 and R2,

Fig. 6. N2, CH4 and CO2 composition of biogas during steady state COD removal period at the 6th cycle (Error bars indicate standard deviations).

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N. Ülgüdür et al. / Environmental Pollution 252 (2019) 1622e1632

Table 3 Average biogas yields obtained in R1 and R2 at 35 ± 2  C. Cycle

Average biogas yields R1

2 3 4 5 6

R2

L/g CODr

L/g VSadded

L/g CODr

L/g VSadded

0.030 0.071 0.136 0.198 0.249

0.053 0.125 0.218 0.342 0.430

0.003 0.019 0.094 0.146 0.235

0.005 0.034 0.148 0.303 0.395

*The yields in cycle 1 were excluded from the calculations due to wash-out of the seed sludge.

respectively, in terms of CH4. The CH4 yields were much higher than those of obtained from a digestate sample of a full-scale digester operated with a mixture of animal manures, maize and sorghum silages and olive waste (Sambusiti et al., 2015). The authors reported a CH4 yield in the range of 0.042e0.106 NL/g VSadded for the untreated, thermally, enzymatically and alkali treated digestate sample. The yields of total biogas produced in our study (0.395e0.430 Lbiogas/g VSadded) were also found to be comparable to many raw feedstocks of the main anaerobic digesters such as municipal wastewater sludge (0.3e0.5), pig stomach content, sheep excreta and vegetable wastes (0.3e0.4), straw from cereals and pig excreta (0.2e0.5), liquid cattle manure (0.1e0.8) given by Zupan ci c and Grilc (2012) and molasses, maize and potato distillery slops (approximately 0.4) given by (Braun, 2007)(biogas yields given in L/ g VSadded). Therefore, high-rate anaerobic treatment of the liquid digestate using AFFRs has a potential to yield high residual biogas based on the comparable biogas yields with many raw feedstocks utilized in anaerobic digestion processes.

the anaerobic digester of digestate sampling. The increase in volumetric digestate production by the increase in installed capacity would potentially increase the GWP of the biogas captured. The capture of the associated gasses would also enhance the reduction of GWP of the digestate if the contents of the biogas produced is properly managed, sequestered or recovered. 4. Conclusions The CODt content of the liquid digestate could be reduced by 56e63% at an HRT of 1.3e1.4 days and OLR of 15e17 g/(L.d) in AFFRs. The applicability of 1.3e1.4 days of HRT has a potential to reduce the volume required for the installations aiming at further anaerobic treatment of the digestate. Anaerobic fixed-film treatment of the liquid digestate can decompose mainly the soluble portion of the COD (85e94%). Yet, it is still possible to decompose VS portion and remove it in AFFR via CODs removal. DRP and TP removal were also found to be at appreciable levels (47e66% DRP and 36e47% TP). The associated biogas yields obtained from the COD decomposition were in the range of 0.395e0.430 Lbiogas/g VSadded which were comparable to many raw feedstocks. This study further revealed that further high-rate anaerobic treatment of the liquid digestate has a potential to prevent a yearly emission of 14.5e18.1 tCO2e/m3 digestate (CH4þCO2) if the residual biogas produced from the liquid digestate is properly managed. An AFFR can thus be used for the digestates with high CODs concentrations for further anaerobic treatment, biogas production and capturing the associated greenhouse gas emissions as a cost-efficient digestate management option. Declarations of interest None.

3.7. Global warming potential of the captured biogas from digestate Anaerobic digestion processes are known to have a potential to reduce the greenhouse gasses since it captures CH4 from the wastes before emitted to the atmosphere (Bracmort, 2010). However, the positive climate effect of the anaerobic digestion processes can be repressed by the additional greenhouse gas release during disposal, land application or storage of the digestates. Global warming potential (GWP) of the biogas produced was therefore quantified depending on the measured average daily biogas production per unit volume of digestate and the maximum and minimum CO2 and CH4 contents of the biogas produced in both reactors (9.0e19.0% CO2, 70.7e80.3% CH4, respectively). 100-year GWP of CH4 was taken as 28 and that of CO2 was 1 (Myhre et al., 2013). GWP of the residual biogas captured from a cubic meter of liquid digestate was found to be in the range of 39.6e49.7 kg CO2e/d in terms of overall CO2 and CH4 emissions. Anaerobic treatment of a cubic meter of the liquid digestate in AFFRs was found to be capable of preventing CH4 emissions equivalent to 38.9e48.6 kg CO2e/d. The development of anaerobic conditions may enhance further decomposition of the residual organics and thus CH4 production (Menardo et al., 2011) during disposal, storage or land application of the digestate. The anaerobic digester of digestate sampling had an approximately 80 m3 daily digestate production. The yearly GWP of the captured CH4 was calculated as in the range of 1136e1419 tCO2e. Total emissions from anaerobic lagoons in terms of CH4 and N2O were previously reported as 703 ± 195 kg CO2e/m2.yr (Owen and Silver, 2015). The potential of an AFFR to capture CH4 for the plant of sampling was calculated to be comparable to CH4 and N2O emissions from anaerobic lagoons with a surface area of 1616e2018 m2. It should be noted that the emissions captured were calculated based on the current digestate production volumes of

Conflicts of interest statement The authors report no potential conflict of interest. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Acknowledgements We would like to thank CTP Engineering Corp. for their supply of bio-filter media. References Abbasi, T., Tauseef, S.M., Abbasi, S.A., 2012. Anaerobic digestion for global warming control and energy generation - an overview. Renew. Sustain. Energy Rev. 16, 3228e3242. https://doi.org/10.1016/j.rser.2012.02.046. Acharya, B.K., Mohana, S., Madamwar, D., 2008. Anaerobic treatment of distillery spent wash - a study on upflow anaerobic fixed film bioreactor. Bioresour. Technol. 99, 4621e4626. https://doi.org/10.1016/j.biortech.2007.06.060. Al-Nozaily, F., 2001. Performance and Process Analysis of Duckweed-Covered Sewage Lagoons for High Strength Sewage- the Case of Sana'a. Delft University of Technology, Yemen. Alaica, A.L., 2012. On-Site Total Phosphorus Removal from Wastewater. Civil Engineering. Ryerson University. Alcaraz-Gonzalez, V., Fregoso-Sanchez, F.A., Seyer, J.-P., Mendez-Acosta, H.O., Gonzalez-Alvarez, V., Sandoval, P.G., 2015. Exponential regulation of alkalinity and VFA in continuous anaerobic digestion processes under uncertain operational conditions. WSEAS Trans. Syst. Control 10, 453e460. APHA, 2005. Standard Methods for the Examination of Water and Wastewater. American Water Works Association, Water Environment Federation. Banks, C.J., Haeven, S., Zhang, Y., Sapp, M., Thwaites, R., 2013. Review of the Application of the Residual Biogas Potential Test. Project Code: OMK002-014.

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