Bioresource Technology 169 (2014) 439–446

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Bioresource Technology

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Comparison of solid-state anaerobic digestion and composting of yardtrimmings with effluent from liquid anaerobic digestion

http://dx.doi.org/10.1016/j.biortech.2014.07.0070960-8524/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel.: +1 330 263 3855.E-mail address: li.851@osu.edu (Y. Li).

Long Lin a,b, Liangcheng Yang a, Fuqing Xu a,b, Frederick C. Michel Jr. a, Yebo Li a,⇑a Department of Food, Agricultural and Biological Engineering, The Ohio State University, Ohio Agricultural Research and Development Center, 1680 Madison Ave., Wooster, OH44691, USAb Environmental Science Graduate Program, The Ohio State University, 3138A Smith Lab, 174 West 18th, Columbus, OH 43210, USA

h i g h l i g h t s

� Solid-state anaerobic digestion (SS-AD) and composting were compared.� High total solids content negatively

affected performance of SS-AD andcomposting.� The preferred feedstock/effluent ratio

for SS-AD was 4–6.� The total carbon loss during

composting was up to 50% greaterthan that in SS-AD.� Both SS-AD and composting

generated nutrient-rich (N, P, K) endproducts.

g r a p h i c a l a b s t r a c t

Solid-state anaerobic digestion (SS-AD) and composting of yard trimmings with effluent from liquidanaerobic digestion were conducted at TS content of 22–30% and 35–55%, respectively. Carbon losswas compared at feedstock to effluent ratio ranged from 4 to 6. The greatest total carbon loss wasobserved at 35% TS in composting, which was about 50% higher than that in SS-AD; while, using SS-AD, more than half of the degraded carbon was converted to methane as a renewable energy carrier.

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Article history:Received 13 May 2014Received in revised form 30 June 2014Accepted 1 July 2014Available online 9 July 2014

Keywords:Solid-state anaerobic digestionCompostingThermophilicBiogasCarbon loss

a b s t r a c t

Solid-state anaerobic digestion (SS-AD) and composting of yard trimmings with effluent from liquid ADwere compared under thermophilic condition. Total solids (TS) contents of 22%, 25%, and 30% were stud-ied for SS-AD, and 35%, 45%, and 55% for composting. Feedstock/effluent (F/E) ratios of 2, 3, 4, 5, and 6were tested. In composting, the greatest carbon loss was obtained at 35% TS, which was 2–3 times of thatat 55% TS and was up to 50% higher than that in SS-AD. In SS-AD, over half of the degraded carbon wasconverted to methane with the greatest methane yield of 121 L/kg VSfeedstock. Methane production fromSS-AD was low at F/E ratios of 2 and 3, likely due to the inhibitory effect of high concentrations of ammo-nia nitrogen (up to 5.6 g/kg). The N–P–K values were similar for SS-AD digestate and compost with dif-ferent dominant nitrogen forms.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Municipal solid waste (MSW) has become one of the largestenvironmental concerns in recent decades due to its increasingquantity. Besides recycling, there are globally four methods used

440 L. Lin et al. / Bioresource Technology 169 (2014) 439–446

for the management of MSW: landfilling, incineration, composting,and anaerobic digestion (AD). In 2012, about 228 million tonnes ofMSW were generated in the United States, and yard trimmingswere the third largest component comprising 13.5% (USEPA,2012). However, current policy aims to divert yard trimmings fromlandfills and incinerators due to potential pollution. More than 50%of yard trimmings were diverted by composting in the U.S. (USEPA,2012). Furthermore, yard trimmings may also serve as a feedstockof anaerobic digestion for renewable biogas production (Liew et al.,2012). However, AD or composting using yard trimmings may behindered by high carbon to nitrogen (C/N) ratios (Forster-Carneiro et al., 2008; Li et al., 2011a). This problem can be solvedby introducing a nitrogen-rich amendment.

AD is a widely used technology that produces biogas, a renew-able fuel, through decomposition of organic matter in the absenceof oxygen by consortia of microorganisms. Most commercialdigesters in the United States are liquid anaerobic digestion (L-AD) systems that contain less than 15% total solids (TS) and arefed with manure, sewage sludge, or food waste (USEPA, 2013).The by-product of L-AD, also known as L-AD effluent, usually hasa high water content and is expensive to transport long distances.Thus energy intensive dewatering processes are often employed.However, L-AD effluent is rich in nitrogen and active microbialconsortia, which could likely improve the rate of yard trimmingsconversion in both composting and anaerobic digestion (Xu et al.,2013).

With respect to digesting yard trimmings, solid-state anaerobicdigestion (SS-AD), which operates with TS content higher than15%, is a better option than L-AD, because problems of floating andstratification of fibrous materials in L-AD can be addressed in SS-AD (Chanakya et al., 1999). Furthermore, due to the lower watercontent, the by-product of SS-AD, also known as digestate, is mucheasier to transport than the L-AD effluent (Li et al., 2011a). Recently,SS-AD has been tested as a method to use L-AD effluent as an inocu-lum and nitrogen source for the production of methane from yardtrimmings (Liew et al., 2012). L-AD effluent was found to be a betterinoculum source for SS-AD than aerobic waste activated sludge,rumen fluid, or manure, as it provided a balanced microbial consor-tium with greater methanogenic activity (Forster-Carneiro et al.,2007; Kim and Speece, 2002). In addition, digestion at thermophilictemperatures (55 �C) has been reported to be more efficient indecomposing organic wastes and destroying pathogens than at mes-ophilic temperatures (37 �C) (Shi et al., 2013). One concern withthermophilic SS-AD is its high energy demand to maintain processtemperature and sensitivity of thermophilic AD microbial commu-nities to environmental disturbances, such as pH (Shi et al., 2013).

In contrast, composting is an aerobic biological process todegrade organic matters by consortia of microbes. It has also beenused to treat L-AD effluent by adding bulking agents such as saw-dust and produces a solid saleable end product (Bustamante et al.,2013). Composting generally proceeds through two phases: initialand thermophilic, followed by a mesophilic maturation or curing(Fogarty and Tuovinen, 1991; Liang et al., 2003). Upon completionof these phases, most pathogens have been destroyed (Grewalet al., 2006), thereby converting L-AD effluent and bulking agentsto a solid soil amendment (Bustamante et al., 2013). The key fac-tors affecting the performance of composting process are aeration,TS content, and C/N ratio (Fogarty and Tuovinen, 1991). TS con-tents in the range of 30–40% (60–70% moisture content) have beenreported to provide maximum microbial activities (Liang et al.,2003). When L-AD effluent is used to provide nitrogen for com-posting without additional buffers or nutrient supplements, thefeedstock to effluent (F/E) ratio is the sole parameter that deter-mines the pH, alkalinity, and C/N ratio of the mixture to be com-posted. The optimal C/N ratio for composting has been reportedto be in the range of 26–35 (Fogarty and Tuovinen, 1991).

SS-AD and composting have different advantages and disadvan-tages in treating solid wastes. SS-AD is more complicated andrequires a larger investment compared to composting (Li et al.,2011a). However, SS-AD produces renewable biogas as a fuel,while composting does not (Walker et al., 2009).The compostingprocess usually requires a larger area and can emit odor, whileSS-AD usually operates under controlled systems with a relativelysmaller area (Bustamante et al., 2013). Both SS-AD and compostingof yard trimmings have been reported in the literature (Chanakyaet al., 1999; Fogarty and Tuovinen, 1991; Liew et al., 2012); how-ever, no side-by-side comparison of thermophilic SS-AD and com-posting of yard trimmings with L-AD effluent has been reported.The objectives of the present study were to: (1) compare the rateof biogas/CO2 production from thermophilic SS-AD/composting ofyard trimmings amended with L-AD effluent; (2) evaluate theeffects of TS content and F/E ratio on the performance of SS-ADand composting; and (3) compare carbon loss, degradation oforganic compounds, and the fertilizer values of the end productsgenerated from SS-AD and composting.

2. Methods

2.1. Yard trimmings and L-AD effluent

Yard trimmings consisting of wood chips (30% w/w), lawn grass(20% w/w), and maple leaves (50% w/w) were used as the feedstockfor SS-AD and composting tests. Yard trimmings have a more bal-anced C/N ratio of around 30 than that of the individual component(Liew et al., 2012). Wood chips, lawn grass, and maple leaves wereobtained in June, 2011 from the Ohio Agricultural Research andDevelopment Center (OARDC) campus in Wooster, OH, USA. Thesefeedstocks were dried at 40 �C for 48 h in a convection oven (Pre-cision Thelco Model 18, Waltham, MA, USA) to a moisture contentof less than 10%, then ground with a hammer mill to pass through a9 mm screen sieve (Mighty Mac, MacKissic Inc., Parker Ford, PA,USA), and stored in air-tight containers. Effluent and centrifugedeffluent were collected from a mesophilic liquid anaerobic digesterthat processed municipal sewage sludge (KB BioEnergy, Inc., Akron,OH, USA). Centrifuged effluent was produced with a D5LL solidbowl decanter centrifuge (ANDRITZ AG, Graz, Austria) at the facil-ity and was used to achieve the designed TS contents for compost-ing tests. Both effluents were stored in air-tight buckets at 4 �C.Prior to use, they were acclimated at 55 �C for 1 week.

2.2. SS-AD

A full factorial design with three TS contents (22%, 25%, and30%) and three F/E ratios (4, 5, and 6) was used for the SS-ADexperiments. Two additional F/E ratios of 2 and 3 were includedat the TS content of 22%. The yard trimmings, deionized (DI) water,and effluent were mixed using a hand-mixer (Black & Decker, 250-watt mixer, Towson, MD, USA), and then loaded into 1 L glassreactors and incubated for up to 45 days in a 55 ± 0.3 �C incubator(BioCold Environmental, Inc., Fenton, MO, USA). Triplicate reactorswere tested for each condition. Effluent without any feedstockaddition was used as a control. Biogas was collected in 5 L Tedlargas bags (CEL Scientific, Santa Fe Springs, CA, USA) connected tothe outlets of each reactor. Biogas composition and volume weremeasured every 2–3 days.

2.3. Composting

For the composting experiments, a similar full factorial designwith three TS contents (35%, 45%, and 55%) and three F/E ratios(4, 5, and 6) was used. The yard trimmings, effluent, and/or

L. Lin et al. / Bioresource Technology 169 (2014) 439–446 441

centrifuged effluent were mixed and loaded into 4 L PVC reactorsand incubated for up to 45 days at 55 ± 0.3 �C as described byGrewal et al. (2006). To simulate the aerobic composting process,pre-heated and pre-humidified air was conveyed through flowrestrictors and a manifold to the bottom of the reactors at a rateof 100 mL/min. Off-gas from the top of each reactor passed througha water bath at 9 �C to condense moisture, and the de-watered off-gas was then analyzed for CO2 content (Vaisala, GMT 220, SouthBurlington, VT, USA). Each reactor was also equipped with a K-typethermocouple that measured temperatures at the center of eachreactor. Room temperature and humidity were also measured (Vai-sala, HMP 235, South Burlington, VT, USA). Data were automati-cally recorded on a data logger (Campbell Scientific, CR23X,Logan, UT, USA) every hour. Triplicate reactors were tested for eachcondition, and effluent without any feedstock addition was used asa control.

2.4. Analytical methods

Samples from the reactors were collected at the beginning andthe end of the 45-day incubation. The TS, VS, pH, and alkalinitywere measured according to Standard Methods Examination ofWater and Wastewater (APHA, 2005). Samples for the pH and alka-linity measurements were prepared by diluting 5 g of samples with50 mL of DI water and then measured using an auto-titrator con-nected with a pH meter (Mettler Toledo, DL22 Food & BeverageAnalyzer, Columbus, OH, USA). Total carbon (TC), total nitrogen(TN) and sulfur (S) contents were determined by an elemental ana-lyzer (Elementar Vario Max CNS, Elementar Americas, Mt. Laurel,NJ, USA). Total ammonia nitrogen (TAN), including NH3 and NH4

+,

was measured based on a modified distillation and titration method(ISO 5664, 1984) using 4% boric acid instead of 2% boric acid with aKjeldahl Distillation Unit B-324 (Buchi Labortechnik AG, Switzer-land) and the auto-titrator mentioned above. Total content of vola-tile fatty acids (VFAs) (acetic, propionic, isobutyric, butyric,isovaleric, and valeric acid) was measured using a gas chromato-graph (GC) system (Shimadzu, 2010PLUS, Columbia, MD, USA)equipped with a 30 m � 0.32 mm � 0.5 lm Stabilwax polar phasecolumn and a flame ionization detector according to methodsdescribed by Shi et al. (2013).

Extractives of raw materials and digested materials were mea-sured based on the NREL Laboratory Analytical Procedure (Sluiteret al., 2008). Extractive-free samples were used to determine thestructural carbohydrates with a two-step acid hydrolysis method(Sluiter et al., 2012). Monomeric sugars (glucose, xylose, galactose,arabinose, and mannose) and cellobiose were analyzed using ahigh-performance liquid chromatography (HPLC) system

Table 1Characteristics of yard trimmings and L-AD effluent.

Parameters Wood chips Lawn grass Maple lea

TS (%) 89.6 ± 0.1 90.0 ± 0.1 83.4 ± 0.1VS (%) 86.9 ± 0.1 83.3 ± 0.1 73.1 ± 0.2TC (%) 46.4 ± 0.3 43.8 ± 0.7 41.5 ± 0.1TN (%) 0.6 ± 0.0 3.1 ± 0.1 1.2 ± 0.0C/N ratio 75.4 ± 2.4 14.2 ± 0.2 35.8 ± 0.8pH ND ND NDAlkalinity (g CaCO3/kg) ND ND NDVFAs (g/kg) ND ND NDTAN (g N/kg) ND ND NDExtractives (%)a 15.5 ± 0.1 30.5 ± 1.2 15.7 ± 0.6Cellulose (%)a 27.5 ± 0.3 23.8 ± 0.3 12.2 ± 0.1Hemicellulose (%)a 15.6 ± 0.1 15.8 ± 0.2 9.9 ± 0.2Lignin (%)a 26.9 ± 0.4 12.7 ± 0.0 36.1 ± 0.2Crude protein (%)a 5.4 ± 1.2 8.8 ± 1.2 5.0 ± 3.7

a Based on TS of sample; the others are based on total weight of sample; ND = not deb Yard trimmings included wood chips (30% w/w), lawn grass (20% w/w), and maple l

(Shimadzu, LC-20AB, Columbia, MD, USA) equipped with a BioradAminex HPX-87P column and a refractive index detector. Waterwas used as the mobile phase at a flow rate of 0.3 mL/min. Thetemperatures of the column and detector were kept at 60 �C and55 �C, respectively. Extractive-free samples were also used todetermine total Kjeldahl nitrogen (TKN) with the modified Kjeldahlnitrogen method (ISO 5663, 1984) using a Tecator™ Digester(FOSS, Eden Prairie, MN, USA) with the distillation unit and auto-titrator mentioned above. Crude protein content was obtained bymultiplying total organic nitrogen (TON, TKN minus TAN) by a fac-tor of 6.25 (Hattingh et al., 1967). The concentrations of 16 ele-ments (P, K, Na, Mg, Al, Ca, Fe, Si, Mn, Ni, Co, Cu, Zn, As, Se, Mo,Cd, Hg, Pb) in digestate and compost were measured using aninductively coupled plasma-mass spectrometer (ICP-MS) (Agi-lent,7500cx, Santa Clara, CA, USA) (USEPA, 2007). Fecal coliformswere determined by the most probable number (MPN) multipletube procedure (USEPA, 2010). Concentrations were calculatedfrom a standard MPN table according to the number of tubes thatindicated growth of fecal coliforms.

The volume of biogas was measured with a drum-type gasmeter (Ritter, TG 5, Bochum, Germany) and the composition(CO2, CH4, N2, and O2) was analyzed with a GC system (Agilent,HP 6890, Wilmington, DE, USA) equipped with a 30 m �0.53 mm � 10 lm Rt-Alumina BondKCl deactivation column anda thermal conductivity detector. Helium gas was used as a carriergas at a flow rate of 5.2 mL/min. The temperature of the detectorwas kept at 200 �C.

Carbon loss for SS-AD was determined as the produced gas-phase carbon (CO2-C and CH4-C) divided by the initial total carbon.Carbon loss for composting was determined as the CO2-C dividedby the initial total carbon.

2.5. Statistical analysis

Average results and standard errors were reported based ontriplicates for each treatment, with two exceptions. For SS-AD,two reactors (at F/E ratios of 5 and 6) with TS content of 30% wereupset and their results were not included. Statistical significancewas tested by analysis of variance (ANOVA) using R-project soft-ware 3.0.2 version with a threshold value of 0.05.

3. Results and discussion

3.1. Chemical composition of yard trimmings and L-AD effluent

Wood chips, lawn grass, and maple leaves were determined tohave different C/N ratios (75.4, 14.2 and 35.8, respectively) but

ves Yard trimmingsb Effluent Centrifuged effluent

86.6 ± 0.1 12.2 ± 0.0 30.1 ± 0.379.3 ± 0.1 6.6 ± 0.0 15.9 ± 0.143.4 ± 0.3 4.4 ± 0.0 10.2 ± 0.31.38 ± 0.0 0.6 ± 0.0 1.0 ± 0.031.5 ± 1.1 7.6 ± 0.1 10.4 ± 0.2ND 8.4 ± 0.0 9.0 ± 0.1ND 16.16 ± 0.8 19.2 ± 0.1ND 3.6 ± 0.0 0.5 ± 0.0ND 5.2 ± 0.1 6.3 ± 0.118.6 ± 0.5 13.4 ± 0.0 11.2 ± 0.819.1 ± 0.2 1.4 ± 0.0 1.4 ± 0.112.8 ± 0.2 0.6 ± 0.1 0.2 ± 0.128.7 ± 0.2 ND ND5.9 ± 2.0 11.6 ± 0.2 13.8 ± 1.3

termined.eaves (50% w/w).

Fig. 1. Effect of TS content and F/E ratio on daily CH4 and CO2 yields during SS-AD ofyard trimmings with L-AD effluent. (a) F/E = 4, (b) F/E = 5, and (c) F/E = 6.

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Fig. 2. (a) Effect of TS content and F/E ratio on total CH4 yield, and (b) effect of F/Eratio on daily CH4 yield and CH4 content at 22%TS.

442 L. Lin et al. / Bioresource Technology 169 (2014) 439–446

similar TC contents (41.5–46.4%) as shown in Table 1. The mixtureof these three components resulted in yard trimmings with a bal-anced C/N ratio of 31.5. Wood chips had the highest holocellulosecontent (43.1%, cellulose and hemicellulose combined); while lawngrass had the highest extractives content (30.5%, water and ethanolsolutes combined) and crude protein content (8.8%). Extractivesinclude compounds such as free sugars, oligosaccharides, andorganic acids (Chen et al., 2007), which are easily degradable forbiogas generation (Liew et al., 2012). Leaves had the highest lignincontent (36.1%). The presence of lignin usually reduces the biodeg-radation rate of organic feedstocks (Liew et al., 2012). Yard trim-mings containing all three components have not only a balancedC/N ratio, but also extractives, holocellulose, and crude protein.Centrifuged effluent increased the TS content of effluent from12.2% to 30.1%. Due to the low TS content of the effluent, centri-

fuged effluent was needed to adjust the TS content to 35% andabove in composting.

3.2. Effect of TS content and F/E ratio on the performance of SS-AD

During SS-AD, the methane production rate showed a bell shapewith a short lag phase (Fig. 1), which was consistent with the typ-ical dynamics of anaerobic batch reactors (Li et al., 2011b; Xu et al.,2013). The methane production rate had a single peak, while thecarbon dioxide production rate had two peaks. The first peak ofcarbon dioxide production rate was during the initial 2 days andthe second one was synchronous with the peak of methane pro-duction rate between days 8 and 16. This profile indicated thatduring SS-AD there were three distinct stages dominated by differ-ent consortia of microorganisms (Appels et al., 2011; Fernándezet al., 2010). Hydrolytic, acidogenic, and acetogenic microbes dom-inated during the initial 2 days when carbon dioxide was dominantin the biogas (80% CO2), indicating the fast hydrolysis of easilydegradable organics in the beginning. Methanogenic activityincreased after the initial 2 days, when both methane and carbondioxide were produced and the ratio of these gases was in agree-ment with the typical composition of biogas (65–75% CH4)(Appels et al., 2011; Forster-Carneiro et al., 2008).

Reactors with higher TS contents (lower moisture contents) hadprolonged lag phases, delayed peaks in methane production, and

Table 2pH, total VFAs, alkalinity, and TAN from SS-AD initial and final materials.

pH VFAs (g/kg) Alkalinity TAN (g N/kg)

Initial Final Initial Final Initial Final Initial Final

TS = 22% F/E = 2 8.2 ± 0.0 8.5 ± 0.1 3.0 ± 0.3 4.6 ± 1.2 13.2 ± 1.0 16.1 ± 0.5 4.3 ± 0.0 5.6 ± 0.0F/E = 3 8.2 ± 0.0 8.4 ± 0.1 2.4 ± 0.0 2.9 ± 0.3 9.0 ± 0.6 14.1 ± 1.0 3.4 ± 0.2 4.6 ± 0.2F/E = 4 8.1 ± 0.1 8.4 ± 0.0 2.0 ± 0.0 2.0 ± 0.3 7.1 ± 0.2 13.3 ± 1.5 2.8 ± 0.0 3.8 ± 0.1F/E = 5 8.0 ± 0.0 8.4 ± 0.0 1.7 ± 0.1 0.8 ± 0.3 5.6 ± 0.3 10.8 ± 0.6 2.4 ± 0.1 3.6 ± 0.0F/E = 6 7.9 ± 0.1 8.5 ± 0.0 1.4 ± 0.0 0.4 ± 0.1 4.6 ± 0.1 9.5 ± 0.0 2.1 ± 0.0 2.8 ± 0.3

TS = 25% F/E = 4 8.1 ± 0.1 8.5 ± 0.0 2.2 ± 0.0 3.2 ± 0.4 7.0 ± 0.3 12.6 ± 0.8 3.2 ± 0.0 4.3 ± 0.0F/E = 5 8.2 ± 0.0 8.5 ± 0.0 1.9 ± 0.2 2.5 ± 0.1 6.5 ± 0.1 10.9 ± 0.2 2.7 ± 0.0 3.8 ± 0.0F/E = 6 7.9 ± 0.0 8.5 ± 0.0 1.6 ± 0.0 1.5 ± 0.3 4.8 ± 0.3 10.1 ± 0.5 2.4 ± 0.0 3.2 ± 0.0

TS = 30% F/E = 4 8.1 ± 0.0 8.5 ± 0.0 2.7 ± 0.0 5.4 ± 0.6 7.7 ± 0.2 14.1 ± 1.7 3.8 ± 0.0 4.8 ± 0.0F/E = 5 7.9 ± 0.0 8.6 ± 0.0 2.3 ± 0.0 4.9 ± 0.1 5.7 ± 0.2 11.9 ± 0.4 3.3 ± 0.1 4.7 ± 0.1F/E = 6 8.0 ± 0.0 8.3 ± 0.0 2.0 ± 0.0 5.3 ± 0.3 6.6 ± 0.0 7.8 ± 0.0 2.8 ± 0.1 4.0 ± 0.3

All the data are based on total weight of sample.

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Fig. 3. Changes of temperature in the center of composting reactors during 45-daycomposting and room temperature at an F/E ratio of 6.

Fig. 4. Effect of TS content on daily CO2 yield during composting of yard trimmingswith L-AD effluent. (a) F/E = 4, (b) F/E = 5, and (c) F/E = 6.

L. Lin et al. / Bioresource Technology 169 (2014) 439–446 443

decreased peak values of biogas production (Fig. 1). For example, atan F/E of 4, no obvious lag phase was observed for 22% TS and themethane production rate was high on day 4 (Fig. 1a). In contrast, at30% TS, the lag phase was prolonged to day 8. The peak values ofboth methane and carbon dioxide decreased with increasing TScontent. Similar trends were observed at F/E ratios of 5 and 6(Fig. 1b and c). Mass transfer or diffusion coefficients have beenfound to decrease drastically with increases of TS content(Abbassi-Guendouz et al., 2012; Xu et al., 2014). On the other hand,water content is important for microbial activity, the lower watercontent at a higher TS content might have inhibited microbialactivity (Abbassi-Guendouz et al., 2012; Fernández et al., 2010).

The total methane yield decreased significantly (p < 0.05) by25–38% when the TS content increased from 22% to 30% at F/Eratios of 4, 5, and 6 (Fig. 2a). This result is consistent with previousstudies (Forster-Carneiro et al., 2008; Li et al., 2011b). In additionto mass transfer limitations, the lower methane yield at a higherTS content could be attributed to the inhibitory effects of by-prod-ucts, e.g. VFAs, which can result from imbalances among hydroly-sis, acidogenesis, acetogenesis, and methanogenesis reactions, andinhibit methanogenesis (Ahring et al., 1995). An accumulation ofVFAs was observed in SS-AD at 30% TS (Table 2). One of the tripli-cates at 30% TS and F/E ratios of 5 and 6 failed due to a low pH (�5),suggesting that 30% TS is a threshold for SS-AD inhibition.

ANOVA test showed that F/E ratios ranging from 4 to 6 had nosignificant effect on the total methane yield (p > 0.05), nor theinteraction between TS content and F/E ratio. However, whenlower F/E ratios of 2 and 3 were included at 22% TS, the F/E ratio

was a significant factor (Fig. 2a). The methane yield increased by50% when the F/E ratio increased from 2 to 4. These results werein agreement with a previous study, which showed that an F/E

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Fig. 5. Comparison of total carbon loss in SS-AD and composting (4, 5, and 6 on x axis represent F/E ratios).

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Fig. 6. Degradation of extractives, cellulose, hemicellulose, and crude protein in (a) SS-AD, and (b) composting reactors at an F/E ratio of 4. (⁄Note: no detectable cellulose andhemicellulose degradation at 30% TS in SS-AD).

444 L. Lin et al. / Bioresource Technology 169 (2014) 439–446

ratio of 4.58 resulted in more rapid biogas production as comparedto 2.43 for thermophilic digestion (Li et al., 2011b). The low dailymethane yield at F/E ratios of 2 and 3 could be attributed to theinhibition of high concentrations of TAN that was originated from

the effluent (5.2 g N/kg) and/or degradation of crude protein due tothe relatively low C/N ratios (14–16) of the mixture in the reactors.Although the inhibitory level of TAN varies, studies demonstratedthat 5.6 g N/L can lead to a 50% decrease in biogas for thermophilic

Table 3Elementary analysis of residues from SS-AD and composting at an F/E ratio of 4.

SS-AD (TS = 22%) Composting (TS = 35%)

Percentage (%)

Ash content 22.4 ± 2.5 28.2 ± 1.0TC 37.1 ± 1.4 38.0 ± 1.7TN 3.3 ± 0.1 3.4 ± 0.2C/N ratio 11.1 ± 0.8 11.3 ± 1.2TAN 1.9 ± 0.1 0.9 ± 0.0TON 1.4 ± 0.2 2.5 ± 0.2NO3-N 0.03 ± 0.0 0.1 ± 0.0NO2-N 0.002 ± 0.0 0.01 ± 0.0S 1.8 ± 0.4 1.2 ± 0.1P 0.6 ± 0.0 0.6 ± 0.0K 0.5 ± 0.0 0.6 ± 0.0Na 0.1 ± 0.0 0.6 ± 0.1Mg 0.3 ± 0.0 0.3 ± 0.0Al 0.03 ± 0.0 0.04 ± 0.0Ca 5.5 ± 0.2 5.0 ± 0.0Fe 1.1 ± 0.0 1.1 ± 0.1

ppm

Si 146 ± 3 122 ± 14Mn 1361 ± 43 1227 ± 55Ni 92.1 ± 2.9 89.3 ± 0.5Co 1.1 ± 0.0 1.0 ± 0.0Cu 222.6 ± 1.1 182.6 ± 0.0Zn 678.0 ± 14.9 1338.0 ± 92.9As 3.9 ± 0.0 4.0 ± 0.0Se <0.0 <0.0Mo 2.3 ± 0.0 2.7 ± 1.2Cd 1.4 ± 0.0 1.4 ± 0.0Hg <0.0 <0.0Pb 5.0 ± 0.0 3.3 ± 1.8

aNote: based on total weight of samples; the others are based on TS of samples.

L. Lin et al. / Bioresource Technology 169 (2014) 439–446 445

digestion (Chen et al., 2008). In this study, TAN concentrationswere 4.6–5.6 g N/kg at F/E ratios of 2 and 3 (Table 2), which werehigher than their initial values due to degradation of proteins,and may have caused the low methane yields in these treatments.While at F/E ratios of 4–6, the TAN levels were not greater than3.8 g N/kg. The highest methane yield of 121 L/kg VSfeedstock

(104 L/kg VSinitial) was observed at a TS content of 22% and an F/Eratio of 6. This value was close to the previously obtained methaneyield of 143 L/kg VSfeedstock for mesophilic digestion of yard trim-mings at a low F/E ratio of 0.5 and a substrate concentration of2 g VSfeedstock/L (Owens and Chynoweth, 1993).

3.3. Effect of TS content and F/E ratio on the performance ofcomposting

A typical composting process consists of a thermophilic phaseduring which most of the organic matter conversion occurs, fol-lowed by a mesophilic or curing phase (Fig. 3). In this study onlythe thermophilic phase was simulated by incubating the reactorsat 55 �C. The composting temperatures increased above the setpoint initially due to microbial activity, and then gradually stabi-lized. The maximum temperatures were 62.4 �C, 60.8 �C, and56.9 �C for TS contents of 35%, 45%, and 55%, respectively, at anF/E ratio of 6. Similar temperature profiles were observed for F/Eratios of 4 and 5 (data not shown).

The carbon dioxide production rate during composting increasedrapidly and reached a peak during days 2–4, and then declined(Fig. 4). The carbon dioxide peaks coincided with the temperatureincreases in the reactors (Fig. 3), and occurred earlier than the peaksof biogas production in SS-AD reactors (Fig. 1). Most of the carbondioxide (80–95%) during composting was produced in the first16 days, indicating that microbial degradation mainly occurred dur-ing this period. There was still oxygen in the off-gas, indicating thatthe composting process was aerobic (Grewal et al., 2006).

Similar to SS-AD, the maximum carbon dioxide production rateof composting decreased as TS content increased (Fig. 4). Thegreatest peak value of 36.52 L/kg VSinitial/d was observed at a TScontent of 35% and an F/E ratio of 4 (Fig. 4a), which was consistentwith composting literature that maximum microbial activitieswere observed in the range of 60–70% moisture content (Lianget al., 2003). Unlike SS-AD, a shift in the peak of carbon dioxideproduction was not observed during composting at high TS con-tents. When the F/E ratio increased from 4 to 6, the carbon dioxideproduction rate showed a lower peak value with a slightly widerbell shape at the TS content of 35%, but similar peak values in reac-tors with TS contents of 45% and 55%.

The total carbon dioxide yields at the three F/E ratios were 241–298, 162–184, and 90–109 L/kg VSinitial for TS contents of 35%, 45%,and 55%, respectively. The total carbon dioxide yield decreased sig-nificantly with an increase of TS content (p < 0.05), but the effect ofF/E ratio was not significant (p > 0.05). Due to high mass transferlimitations associated with low water content in high TS treat-ments, as discussed in the previous section, the activity of aerobicmicrobes might be limited. The minor effect of F/E ratio on the car-bon dioxide production rate may be attributed to the fact that C/Nratio was a more important factor during composting than inocu-lum size (Fogarty and Tuovinen, 1991). Thus, in this study, for allcomposting reactors with a narrow range of C/N ratios from 17to 20, the F/E ratio might not be an important factor affecting thecomposting rate.

3.4. Comparison of SS-AD and composting

3.4.1. Carbon lossStatistical analysis showed that TS content significantly affected

carbon loss in both SS-AD and composting (p < 0.05), while the F/E

ratio did not (p > 0.05) (Fig. 5). For SS-AD, the greatest carbon lossof 15.2% occurred at a TS content of 22%, followed by TS content of25% TS (12.7% loss), and 30% TS (9.2% loss). A similar phenomenonwas observed during composting and the total carbon lossdecreased from 23.3% to 9.1% as the TS content increased from35% to 55%. Overall, the greatest carbon loss during compostingwas observed at 35% TS content, versus at 22% for SS-AD. Thisresult may be due to the effective oxygen mass transfer duringcomposting, and was consistent with previous research that foundcomposting was a faster degradation process compared to AD(Bustamante et al., 2013; Walker et al., 2009). However, 60% ofthe total carbon loss during SS-AD was converted to methane,while no methane was detected in composting.

3.4.2. Degradation of organic componentsCellulose, hemicellulose, extractives, crude protein, and lignin

are the major components in yard trimmings, and consequently,their biodegradation is essential to both SS-AD and compostingprocesses. Except for negligible degradation of lignin (data notshown), both SS-AD and composting showed considerable degra-dation of the other four components, although the degradation ofcellulose and hemicellulose were negligible at 30% TS in SS-AD(Fig. 6). As expected, extractives had the greatest extent of degra-dation in both SS-AD and composting (Chen et al., 2007; Liewet al., 2012). Composting had slightly higher extents of celluloseand hemicellulose conversion than those in SS-AD, which wasprobably due to its stronger microbial activities that decomposecellulose and hemicellulose (Walker et al., 2009). In contrast, SS-AD showed a greater removal of crude protein. A possible reasoncould be that crude protein was degraded by microbes to smallmolecules, such as ammonium, which could be further utilizedby microbes for protein synthesis through cell growth. Aerobicmicrobes generally have higher growth rates than anaerobicmicrobes, thus more cell protein was synthesized in the compost-

446 L. Lin et al. / Bioresource Technology 169 (2014) 439–446

ing process and the measured net removal of crude protein (Kjel-dahl nitrogen based) for composting was lower. Furthermore,degradations of holocellulose were approximately 30% and 20%at TS of 22% and 25% in SS-AD, respectively, which were muchhigher than the results from a previous mesophilic SS-AD studyin which only 5% degradation was obtained at a TS content of18–19% and F/E ratio of 3 (Liew et al., 2012). This result could bebecause thermophilic digestion was more favorable for cellulolyticand xylanolytic microbes than was mesophilic digestion (Shi et al.,2013).

3.4.3. Analysis of digestate and compostBoth SS-AD digestate and compost have the potential to be used

as fertilizers. Table 3 shows that the TC and TN contents were sim-ilar between the SS-AD digestate and compost, while the forms ofnitrogen differed. TAN (57%, including NH3-N and NH4

+-N) domi-nated in SS-AD digestate, while TON (74%) was the predominantform in compost. Although both of these forms of nitrogen areavailable forms for plant uptake, TON may contribute to long-termnitrogen turnover in the soil, while TAN may be rapidly lostbecause of plant uptake, ammonia volatilization, or nitrificationand nitrate leaching (Tambone et al., 2010). Thus SS-AD digestateand compost might require different land application methods.Furthermore, the concentrations of P, K, and S as well as heavymetals were comparable in the SS-AD digestate and compost(Table 3). The concentrations of heavy metals were one to twoorders of magnitude lower than the regulated levels based on theUS EPA 40 CFR Part 530 Class A Biosolids. No fecal coliforms weredetected in either the SS-AD digestate or the finished compostsamples (data not shown). Therefore, while SS-AD digestate andcomposting have different forms of nitrogen, they were compara-ble in terms of other fertilizer value, did not harbor indicatorpathogens, had low heavy metal concentrations, and could be usedas a substitute for inorganic fertilizer.

4. Conclusions

Both SS-AD and composting successfully degraded organics inyard trimmings and L-AD effluent. Increased TS content negativelyimpacted the performance of SS-AD and composting, while F/Eratio had minor effects. Daily CO2 production peaked within thefirst 2 days for both composting and SS-AD (first peak), while thesecond CO2 peak in SS-AD was synchronous with the peak ofmethane. Composting had higher total carbon loss than SS-AD,while over half of the degraded carbon was converted to methanein SS-AD. Nutrient-rich (N, P, K) end products with non-detectablecoliform were generated from both SS-AD and composting.

Acknowledgements

This project was funded by the USDA NIFA Biomass Researchand Development Initiative Program (Award No. 2012-10008-20302) and USDA NIFA Hatch Program. The authors would like tothank Mrs. Mary Wicks (Department of Food, Agricultural andBiological Engineering, OSU) for reading through the manuscriptand providing useful suggestions.

References

Abbassi-Guendouz, A., Brockmann, D., Trably, E., Dumas, C., Delgenès, J.-P., Steyer,J.-P., Escudié, R., 2012. Total solids content drives high solid anaerobic digestionvia mass transfer limitation. Bioresour. Technol. 111, 55–61.

Ahring, B.K., Sandberg, M., Angelidaki, I., 1995. Volatile fatty acids as indicators ofprocess imbalance in anaerobic digestors. Appl. Microbiol. Biotechnol. 43, 559–565.

APHA, 2005. Standard Methods for the Examination of Water and Wastewater, 21sted. American Public Health Association, Washington, D.C..

Appels, L., Lauwers, J., Degrève, J., Helsen, L., Lievens, B., Willems, K., Van Impe, J.,Dewil, R., 2011. Anaerobic digestion in global bio-energy production: potentialand research challenges. Renewable Sustainable Energy Rev. 15, 4295–4301.

Bustamante, M.a., Restrepo, A.P., Alburquerque, J.a., Pérez-Murcia, M.D., Paredes, C.,Moral, R., Bernal, M.P., 2013. Recycling of anaerobic digestates by composting:effect of the bulking agent used. J. Clean. Prod. 47, 61–69.

Chanakya, H., Srikumar, K., Anand, V., Modak, J., Jagadish, K., 1999. Fermentationproperties of agro-residues, leaf biomass and urban market garbage in a solidphase biogas fermenter. Biomass Bioenergy 16, 417–429.

Chen, S.-F., Mowery, R.a., Scarlata, C.J., Chambliss, C.K., 2007. Compositional analysisof water-soluble materials in corn stover. J. Agric. Food Chem. 55, 5912–5918.

Chen, Y., Cheng, J.J., Creamer, K.S., 2008. Inhibition of anaerobic digestion process: areview. Bioresour. Technol. 99, 4044–4064.

Fernández, J., Pérez, M., Romero, L.I., 2010. Kinetics of mesophilic anaerobicdigestion of the organic fraction of municipal solid waste: influence of initialtotal solid concentration. Bioresour. Technol. 101, 6322–6328.

Fogarty, A., Tuovinen, O., 1991. Microbiological degradation of pesticides in yardwaste composting. Microbiol. Rev. 55, 225–233.

Forster-Carneiro, T., Pérez, M., Romero, L.I., 2008. Influence of total solid andinoculum contents on performance of anaerobic reactors treating food waste.Bioresour. Technol. 99, 6994–7002.

Forster-Carneiro, T., Pérez, M., Romero, L.I., Sales, D., 2007. Dry-thermophilicanaerobic digestion of organic fraction of the municipal solid waste: focusing onthe inoculum sources. Bioresour. Technol. 98, 3195–3203.

Grewal, S.K., Rajeev, S., Sreevatsan, S., Michel, F.C., 2006. Persistence ofMycobacterium avium subsp. paratuberculosis and other zoonotic pathogensduring simulated composting, manure packing, and liquid storage of dairymanure. Appl. Environ. Microbiol. 72, 565–574.

Hattingh, W.H.J., Thiel, P.G., Siebert, M.L., 1967. Determination of protein content ofanaerobic digesting sludge. Water Res. 1, 185–189.

ISO 5663, 1984. ISO 5663 Water quality – Determination of Kjeldahl nitrogen –Method after mineralization with selenium.

ISO 5664, 1984. ISO 5664 Water quality – Determination of ammonium –Distillation and titration method.

Kim, M., Speece, R.E., 2002. Aerobic waste activated sludge (WAS) for start-up seedof mesophilic and thermophilic anaerobic digestion. Water Res. 36, 3860–3866.

Li, Y., Park, S.Y., Zhu, J., 2011a. Solid-state anaerobic digestion for methaneproduction from organic waste. Renewable Sustainable Energy Rev. 15, 821–826.

Li, Y., Zhu, J., Wan, C., Park, S.Y., 2011b. Solid-state anaerobic digestion of corn stoverfor biogas production. Trans. ASABE 54, 1415–1421.

Liang, C., Das, K.C., McClendon, R.W., 2003. The influence of temperature andmoisture contents regimes on the aerobic microbial activity of a biosolidscomposting blend. Bioresour. Technol. 86, 131–137.

Liew, L.N., Shi, J., Li, Y., 2012. Methane production from solid-state anaerobicdigestion of lignocellulosic biomass. Biomass Bioenergy 46, 125–132.

Owens, J.M., Chynoweth, D.P., 1993. Biochemical methane potential of municipalsolid waste (MSW) components. Water Sci. Technol. 27, 1–14.

Shi, J., Wang, Z., Stiverson, J.a., Yu, Z., Li, Y., 2013. Reactor performance and microbialcommunity dynamics during solid-state anaerobic digestion of corn stover atmesophilic and thermophilic conditions. Bioresour. Technol. 136, 574–581.

Sluiter, A., Hames, B., Ruiz, R., Scarlata, C., Sluiter, J., Templeton, D., Crocker, D., 2012.Laboratory Analytical Procedure (LAP): Determination of StructuralCarbohydrates and Lignin in Biomass, NREL/TP-510-42618. NationalRenewable Energy Laboratory, Golden, CO, USA.

Sluiter, A., Ruiz, R., Scarlata, C., Sluiter, J., Templeton, D., 2008. Laboratory AnalyticalProcedure (LAP): Determination of Extractives in Biomass, NREL/TP-510-42619.National Renewable Energy Laboratory, Golden, CO, USA.

Tambone, F., Scaglia, B., D’Imporzano, G., Schievano, A., Orzi, V., Salati, S., Adani, F.,2010. Assessing amendment and fertilizing properties of digestates fromanaerobic digestion through a comparative study with digested sludge andcompost. Chemosphere 81, 577–583.

USEPA, 2007. Method 3051A. Microwave assisted acid digestion of sediments,sludges, soils, and oils. Revision 1.

USEPA, 2010. Method 1680: Fecal Coliforms in Sewage Sludge (Biosolids) byMultiple-Tube Fermentation using Lauryl Tryptose Broth (LTB) and EC Medium.EPA-821-R-10-003.

USEPA, 2012. Municipal Solid Waste. http://www.epa.gov/wastes/nonhaz/municipal/.

USEPA, 2013. Operating Anaerobic Digester Projects. http://www.epa.gov/agstar/projects/index.html.

Walker, L., Charles, W., Cord-ruwisch, R., 2009. Comparison of static, in-vesselcomposting of MSW with thermophilic anaerobic digestion and combinationsof the two processes. Bioresour. Technol. 100, 3799–3807.

Xu, F., Shi, J., Lv, W., Yu, Z., Li, Y., 2013. Comparison of different liquid anaerobicdigestion effluents as inocula and nitrogen sources for solid-state batchanaerobic digestion of corn stover. Waste Manag. 33, 26–32.

Xu, F., Wang, Z.-W., Tang, L., Li, Y., 2014. A mass diffusion-based interpretation ofthe effect of total solids content on solid-state anaerobic digestion of cellulosicbiomass. Bioresour. Technol. 167, 178–185.