Energy Policy 60 (2013) 98–105

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Energy Policy

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Modeling of biodiesel production in algae cultivation with anaerobicdigestion (ACAD)

John Morken a,n, Zehra Sapci a,b, Jon Eivind T. Strømme a

a Department of Mathematical Sciences and Technology, Norwegian University of Life Sciences (UMB), PO Box 5003, Drøbakveien 31, Aas, N-1432, Norwayb Department of Environmental Engineering, Faculty of Engineering and Architecture, Bitlis Eren University, 13000 Bitlis, Turkey

H I G H L I G H T S

� The model combines algae cultivation with anaerobic digestion.

� In the model nutrients and carbon dioxide are recycled.� Organic waste is converted into electrical power, biodiesel and organic fertilizer.� Results showed that more energy can be produced by combining the processes.

a r t i c l e i n f o

Article history:Received 20 January 2012Accepted 24 April 2013Available online 13 June 2013

Keywords:Renewable energyModelingBiorefinery

15/$ - see front matter & 2013 Elsevier Ltd. Ax.doi.org/10.1016/j.enpol.2013.04.081

esponding author. Tel.: +4764965459; fax: +4ail address: john.morken@umb.no (J. Morken)

a b s t r a c t

This study presents a model of an ecotechnology that combines algae cultivation with anaerobicdigestion in order to recycle nutrients and to reduce the need for external energy. The concept is toconvert organic waste into several products, such as electricity, biodiesel and organic fertilizer. It islabeled as the ACAD biorefinery. The simulation model of the ACAD biorefinery proved itself to be apowerful tool for understanding the symbioses and dynamics of the system, and therefore also a goodtool for reaching political decisions. The model shows that the ACAD biorefinery could be totallyindependent of external energy supplies. Energy calculations indicate that more energy can be producedby combining the algae cultivation and anaerobic digestion processes. For every unit of energy enteringthe system in feedstock, 0.6 units of energy are exported as either biodiesel or electricity. The exportedelectricity accounts for approximately 30% of the total exported energy, while the remaining 70% isexported as biodiesel. By producing its own energy, the biorefinery improves its renewability and level ofcarbon neutrality.

& 2013 Elsevier Ltd. All rights reserved.

1. Introduction

In just a few hundred years, humans have released the organiccarbon accumulated over hundreds of millions of years. Without achange in policy, the world is on a path leading toward a rise inglobal temperature of up to 6 1C, with catastrophic consequencesfor our climate (CIA, 2009). Continued greenhouse gas (GHG)emissions at or above current rates will cause further warmingand induce many changes in the global climate system during the21st century that would very likely be larger than those observedduring the 20th century (IPCC, 2007). Therefore, the main globalenergy sectors – electricity and general use fuels – will have toachieve significant emission reductions to meet the plannedtargets of international agreements. Currently, the electricitysector accounts for approximately 33% of global energy use and

ll rights reserved.

7 64 96 54 01..

is developing a range of low CO2-emission approaches for elec-tricity production (e.g. nuclear, solar, wind, geothermal, hydro-electric, clean-coal technology). Fuels account for a much largermarket share (67%) of global energy consumption (approximately15.5 TW in 2005) (Schenk et al., 2008). Despite the obviousimportance of fuels, CO2-neutral fuel production systems (biodie-sel, bioethanol, biomethane, etc.) are far less developed than arethe ones for CO2-neutral electricity production. Therefore, bioe-nergy production systems, of which an important intrinsic char-acteristic is carbon neutrality due to its ultimate source, sunlight,are gaining increased attention these days.

One of the virtues of bioenergy is that the time from photo-synthesis to human energy use is short – days or years – and notthe hundreds of millions of years required for fossil fuels(Rittmann, 2008). On the other hand, first generation bioenergyproduction systems cannot contribute in a major way to global fuelrequirements. The problems of first generation biofuels have ledtoward alternatives for second generation bioenergy systems.These have the potential for a much higher net energy balance,

J. Morken et al. / Energy Policy 60 (2013) 98–105 99

can be more water-efficient, and require much less arable land(Schenk et al., 2008). Two different approaches for production ofsecond generation bioenergy are lignocellulosic technologies andthe use of microorganisms such as bacteria and microalgae.

The idea of combining anaerobic digestion (AD) with microalgaecultivation (MC) was proposed and proven to be technically feasiblein the laboratory by Golueke and Oswald (1959). A broader evalua-tion of a tentative microbiological process that converts solar energyto electrical power through algal photosynthesis – methane fermen-tation of algae and thermal combustion of methane – was proposedby Oswald and Golueke (1960). More recently, a revival of thesunlight-to-biogas biological energy conversion system has shownthat anaerobic digestion of microalgae can yield positive effects forthe sustainability of microalgal biodiesel production (Schamphelaireand Verstraete, 2009, and Sialve et al., 2009). The potential of feedingall the algal material into the anaerobic digester, without theproduction of biodiesel from the lipid part of the algae, was alsooutlined (Sialve et al., 2009). They also predicted that the promisingintegration process of coupling anaerobic digestion with microalgalculture will re-emerge in the coming years, either as a required stepto support large scale microalgal culture or as a standalone bioenergyproduction process. The findings of their study confirmed thepotential of microalgae as an energy source, but they also concludedit was necessary to decrease energy and fertilizer consumption.Lardon et al. (2009) suggested anaerobic digestion also of oilcakes(residue after oil extraction) as a way to reduce external energydemand and recycle a part of the mineral fertilizer.

In light of this knowledge, an ecotechnology model thatcombines microalgae cultivation (MC) with anaerobic digestion(AD) is presented here. The goal of the model is to recyclenutrients and to reduce the need for external energy required bythe process. The objective is to build a combined model, whileconsidering the sustainability of algae and anaerobic digestion.The concept, labeled here as the ACAD biorefinery, is to convert

Anaerobic Digestion1.

Flucculatio2.

Scrubbing9.

CHP10.

Digestate

Methane CO2

Biogas

Glyserine

Treated Algal Oilcake

Recycled Water

System Bounderies

Electric Power

Sludge

Waste Paper

Fig. 1. Overview of the

organic waste into several products such as electricity, biodiesel,and organic fertilizer. The model will then be a useful tool forunderstanding the policy instruments that would be suitable forpromoting the production of sustainable fuels from algae. Therequired instruments will, of course, vary country to countryaccording to geographical, social, and economic conditions.

2. Description of the ACAD model

The model of using anaerobic digestion, microalgal cultivation,scrubbing, oil extraction, transesterification, and heat and electricityto produce surplus electricity and biodiesel, will hereafter be referredto as the Algae Cultivation with Anaerobic Digestion (ACAD) bior-efinery. The ACAD biorefinery model is shown in Fig. 1. Organicwastes (sludge, waste paper, algal oilcake, and glycerin) are fed intothe AD (Fig. 1, (1)), and the nutritious effluent from the AD, referredto as digestate, is forced to flocculate with the aid of a coagulant(Fig. 1, (2)). The flocculent is then separated through the dewateringprocess (Fig. 1, (3)). Separated solids are a co-product of the processand can be used as a soil amendment. The remaining filtrate ispumped to a high rate algal pond where it acts as a fertilizer (Fig. 1,(4)). During this stage, algal biomass is grown and harvested from thepond. The harvested algal matter is treated with a coagulant prior toseparation of the solid components from the liquid (Fig. 1, (5 and 6)).The separated solids (algal biomass) are pretreated for extracting thelipids (oil) and producing the oilcake from them (Fig. 1, (7)). Then theoilcake, which is easily consumed by the microorganisms in the AD,is used as a feedstock for the AD (Fig. 1, (1)). The oil goes through anesterification process with the aid of methanol and a base (NaOH)(Fig. 1, (8)). This process produces biodiesel and glycerin residue. Theglycerin is fed back to the AD together with the oilcake and co-digestion matter (sludge and waste paper) (Fig. 1, (1)). The overflowwater from the separation of algae is put under pressure and used to

n Separation3.

MicroalgaeCultivation

4.

Flocculation5.

Separation6.

Oil Extraction7.

Esterification8.

Digestate

enriched Water

Heat

Filtrate

Algal Biomass

Algal Biomass+ flocculator

Algal Biomass

etah

psoh

P,mu

issa

toP

Algal Oil

Solid waste(Organic Fertilizer)

Biodiesel (Algae

Methyl Ester)

Sunlight

ACAD biorefinery.

System Boundaries

SunlightSludgeWaste Paper CO2 Flocuculant Phosphorus NaOH Methanol

Power Biodiesel Water Loss

Solid Waste

GHG Emissions

Fig. 2. Flows in and out of the system boundaries.

J. Morken et al. / Energy Policy 60 (2013) 98–105100

purify the biogas in a scrubbing process (Fig. 1, (9)). The scrubbingprocess increases the methane content of the biogas, and increasesthe carbon content of the water. The carbon rich effluent water isthen pumped back to the algae pond to stimulate its productivity(Fig. 1, (4)). The produced methane goes into a combined heat andpower (CHP) gas engine to produce electricity and heat (Fig. 1, (10)).The heat is used to extract the oil, and to pretreat the biomass priorto the AD, and also ensures an optimal process temperature withinthe AD reactor. The CO2 produced during combustion in the CHP ispumped back to the algal pond to stimulate the production of algalmatter.

In the ACAD model, four different organic substrates enter theAD: wastewater sludge, waste paper, algal oilcake, and glycerin(residue from biodiesel production). These materials reach theoptimal ratio there between carbon and nitrogen (C/N ratio) andsupply enough nitrogen for use in the production of algae. Duringthe entire process, nutrients and carbon are recycled, resulting in aloop for converting sunlight to bioenergy. The system is designedso that no additional nitrogen fertilizer is necessary. The inputsand outputs across the system boundaries are illustrated in Fig. 2.

3. Description of process in the ACAD model

3.1. Anaerobic digestion (AD)

AD is a biological process where organic materials are con-verted into energy-rich biogas (CO2 and CH4). The process alsomineralizes some of the organic nitrogen and phosphorus intoammonium and phosphate that can be used to produce algae. Theproducts of the process are biogas and digestate. The biogas ismainly composed of methane and carbon dioxide, but also tracesof hydrogen sulphide, dinitrogen, dihydrogen and other volatilecompounds (Rasi et al., 2007). In order to simplify the model,biogas is presumed to consist only of CH4 and CO2, and that thereare no emissions from the AD. All of the energy in the biogas isassumed to come from the CH4 fraction.

The rate of degradation of organic matter (OM), referred to asreduction of volatile solids (VS), is of major importance for theoverall performance of the AD process. The maximum VS reduc-tion was reported to be about 45% for algae, compared to about60% for wastewater sludge (Salerno et al., 2009). CH4 productionrates increased by one third when green microalgae biomass waspreheated (Chen and Oswald, 1998). Therefore, because of the cellwall disruption, thermal pretreatment is a strategy for increasingthe digestibility of the biomass. Co-digestion of algal matter withhigh-carbon, low-nitrogen substrates has the potential to increasethe biogas production per unit volume of the digester tank. For theACAD model, the organic matter VS reduction rate is set equal tothe reduction rate for wastewater sludge (Appendix 1). In addition,since the feed material described in the work of Yen and Brune(2007) is closest to the feed material in the ACAD model, theproductivity yields presented in their work are used for the ACAD

model. Their maximum yield was achieved when they mixed 2 gVS l−1 day−1 algal sludge with 3 g VS l−1 day−1 waste paper, givingan algae fraction in the feedstock of 40%.

Together with the resistance to biodegradation of the algaecells, the low C/N ratio of the algal sludge is also a factor that mustbe considered. A low C/N ratio could result in a high total ofammonium nitrogen (TAN) and a high accumulation of volatilefatty acids (VFAs) in the digester. High concentrations of TAN andVFAs in the digester disturb the methanogenesis and, in highconcentrations, it could inhibit anaerobic digestion. Co-digestioncannot only reduce the problems of excess amounts of ammonia,but can also increase the yield of methane. By mixing algal sludgewith waste paper, the optimal C/N ratio for co-digestion was foundto be in the 20–25/1 range (Yen and Brune, 2007). This range isused to calculate the mixture of organic matter entering the AD(sludge, waste paper, glycerin, and oilcake) in our model(Appendix 1).

One challenge in determining the flow rate for the ACAD modelis that of determining how much of the nutrients in the feedstockbecomes available to the algae through the anaerobic process.General figures for the composition of the digestate are hard tofind since the composition is highly dependent on the propertiesof the feedstock and the conditions in the AD reactor. AD results ina strong reduction of the easily degradable fraction of the organicmatter and an accumulation of recalcitrant molecules. The highmineralization of nitrogen and phosphorus may point to thedigestate as a readily available liquid fertilizer for agriculturaluse. The macro-nutrient total tends not to be influenced, or is onlyslightly decreased, during AD processes. As degradable organicmatter is transformed into biogas, the relative content of ammoniain the TS increases proportionately to the biological stability. Thesefindings are interpreted to mean that the mineralization ofammonia is greater than the reduction of VS since the reductionof VS leads to greater biological stability (Schievano et al., 2008). Inthe ACAD model, the conversion rate of organic nitrogen toammonia is therefore set equal to the VS reduction rate (i.e. 60%of the nitrogen entering the AD reactor is converted to liquidammonia). All of this ammonia is also assumed to be algaeavailable. The nitrogen which is not bound into ammonia (40%)crosses the system boundaries in the solid waste. In order to keepthe nitrogen balance within the system, the amount of nitrogenleaving the system must also enter the system, either through theco-digestion material or as fertilizer. Since one of the goals for theACAD concept is to eliminate the need for chemical nitrogenfertilizer, the first strategy is chosen. By co-digesting sewagesludge, waste paper, oilcake and glycerin in a designed mixture,both the nitrogen balance and the optimal C/N ratio can bemaintained.

3.2. Microalgae cultivation (MC)

Productivity is a measure of how much algal biomass isproduced per area per unit of time. Production of up to127,000 kg ha−1 yr−1 can be achieved in high-rate raceway ponds(Chisti, 2007). Productivity rates between 20 and 30 g m−2 day−1

(73–109,000 kg ha−1 yr−1) are in the range of usual open racewayperformance (Lardon et al., 2009). Productivity is estimated to be afunction of photosynthetically active radiation coupled with datafor insolation and radiation (Clarens et al., 2010). However, in theACAD model, fixed figures for algae productivity are utilized. Thesefigures are summarized in Table 1.

It is assumed that all of the nutrients are used with perfectefficiency. Phosphorus is more closely associated with metabolicfunctions (e.g. photosynthesis) than with storage functions (Lardonet al., 2009). The quota of phosphorus in the algae is thereforeassumed to be proportional to the protein content and then

Table 1Average achieved values for algae.

Properties Data References

Algae Biomass Fraction of protein (%) 47 Illman et al. (2000)a

Fraction of carbohydrates (%) 28 Illman et al. (2000)a

Fraction of lipids (%) 25 Huntley and Redalje (2007)a

Algae cultivation Calorific value (MJ kg−1) 22 Illman et al. (2000)a

Growth rate (day−1) 0.25 Illman et al. (2000)a

Dry weight per volume (g m−3) 206 Illman et al. (2000)a

Productivity (g m−2 day−1) 15.1 Illman et al. (2000), Huntley and Redalje (2007), Lardon et al. (2009)

a Is assumed regarding reference.

J. Morken et al. / Energy Policy 60 (2013) 98–105 101

indirectly to the nitrogen fraction of the biomass. The needed levelsof N and P are calculated using the figures for C. vulgaris low-N, andcalculated proportionately to the protein content (Table 1 andAppendix 1). Nutrients other than nitrogen and phosphorus areassumed to be present in sufficient quantities in the pond or thedigested sludge (Wijffels and Barbosa, 2010). By the propertiesgiven in Table 1, the nitrogen and phosphorus content of the algalmatter is calculated to be approximately 7% and 1%, respectively.

It has been reported that the consumption of CO2 per kg algaeis 1.6 kg kg−1 (Clarens et al., 2010). The supply of CO2 to the algaein this system comes from three sources. The first is the overflowwater used to scrub the biogas, the second is from the combustionof methane in the gas engine (CHP), while the last is CO2 derivedexternally. During the anaerobic process, the CO2 content of thedigestate is raised and, therefore, the algae will also have a supplyof CO2 through the digestate. This supply is not included in theACAD model.

The calculation used for evaporation during algae production ina Mediterranean context is also used for evaporation in the ACADmodel (Appendix 1).

3.3. Algal sludge thickening

The algae concentration in the open raceway pond is set to0.206 g l−1 (Huntley and Redalje, 2007). Water from the algae pondis pumped out and coagulated with the aid of aluminum sulfate.The algae sludge and water are separated in a settling tank. Theconcentrations of sludge leaving the settling tank and leaving therotary press are taken from the literature (Appendix 1).

3.4. Oil extraction

Oil extraction using the microwave oven method was identifiedas the simplest, easiest and most effective method among thetested methods (Lee et al., 2010). But since the ACAD model hasexcess heat, this heat can be utilized for thermo-mechanical oilextraction methods. Some 55% of the energy in the methane isconverted to heat through the CHP process. This heat is used toextract the oil and, at the same time, pre-treat the algal oilcakemaking it more bioavailable for fermentation in the AD reactor.Heat for extraction was calculated to be 1.84 GJ kg−1. The modeldetermines the heat balance. The pre-treatment using heat willalso raise the temperature of the feedstock and then contribute toa higher process temperature in the AD reactor. Through the oilextraction process, algal oil is separated from the oilcake andwater, which are fed back to the AD.

3.4.1. EsterificationInputs for the esterification of rape oil (Jungbluth et al., 2007)

were assumed to be valid for the production of biodiesel fromalgae oil. Before starting esterification, the water must be removed

from the oil since its presence causes the triglycerides to hydrolyzeinto soaps instead of undergoing transesterification to give bio-diesel. The algal oil is heated, and brought gradually into contactwith a mixture of sodium hydroxide (NaOH) and methanol. Smallamounts of phosphoric acid and smectite are also used. After anhour of agitation, the mixture is separated into two main compo-nents; methyl esters and glycerin. The glycerin fraction is muchdenser than the biodiesel fraction (methyl esters) and the two canbe separated in a settling vessel or decanter. Once the biodiesel isseparated from the glycerin, the biodiesel can be purified bywashing gently with warm water to remove residual catalyst orsoaps (Mortimer et al., 2003).The glycerin produced in the processis also fed into the AD. The glycerin could have been furtherprocessed to produce pure glycerin, but in order to simplify theconcept, it is recycled back to the AD.

3.5. Water scrubbing

Water scrubbing is used to remove CO2 and H2S from biogassince these gases are more soluble in water than CH4. The biogas ispressurized and fed to the bottom of a packed column wherewater is fed at the top and so the absorption process is operatedcounter-currently (Wheeler and Lindberg, 1999).

CO2 properties data is applied according to the literature(Appendix 1). A scrubbing efficiency of 0.75 is used. In the ACADmodel, the overflow from the settling basin of algal sludge is usedfor scrubbing before the CO2 enriched water is pumped back to thepond as a carbon supply.

3.6. Combined heat and power (CHP) gas engine

The utilization of biogas in internal combustion engines is along established and extremely reliable technology. In the ACADmodel, figures in line with the technical characteristics of the gainsand losses outlined in references are used (Jungbluth et al., 2007).The CHP engine derives all its energy from the methane. In thecombustion process, methane and oxygen are converted to carbondioxide and water as shown in the complete chemical Eq. (1):

CH4 þ 2O2-CO2 þ 2H2Oþ Heat ð1Þ

The combustion within the CHP is assumed to be perfect,meaning that all the carbon in the CH4 finally ends up as CO2.The mass ratio between CH4 and CO2 in the formula is estimated inthe model (Appendix 1). Cooling water for CHP is delivered fromrotary press for the algal sludge. The energy in the heated water isthen utilized for oil extraction, esterification, biomass pre-treat-ment, and for maintaining an optimal process temperature in theAD reactor. The overflow is ultimately pumped back to the pond.

Fig. 3. System overview.

J. Morken et al. / Energy Policy 60 (2013) 98–105102

4. Calculation methodology for the ACAD model

4.1. Methane

Methane production is a central feature of the ACAD model(Fig. 3); this was therefore chosen as the reference for the rest ofthe calculations (Appendix 1). The amount of CH4 produced by anamount of organic matter (in kg VS) that is fed into the AD iscalculated using formula (2):

M¼ B2G�%CH4 � ðXOC þ XS þ XC þ XGÞ ð2Þ

where B2G is the mass of biogas produced per kg VS, %CH4 is theproportion of CH4 in the biogas, and XOC, XS, XC, and XG are themasses for oilcake, sludge, wastepaper and glycerin, respectively.M is the mass of the CH4 produced.

4.2. C/N ratio

The C/N ratio of organic matter in the AD reactor is animportant process parameter. Since the algal matter has a lowC/N it must be mixed with a more carbon rich material in order toreach the optimal C/N ratio (Appendix 1). The mix of algal and co-digestion matter is limited to the optimal C/N range by using thefollowing equations:

CNmin ≤ða� CNOC þ b� CNS þ d� CNC þ k� CNGÞ≤CNmax ð3Þ

ða; b; d; kÞ ¼ 1 ð4Þ

0≤a; b; d; k≤1 ð5Þ

Subscripts OC, S, C, and G stand for oilcake, sludge, waste paperand glycerin, respectively, while a, b, d, and k are the differentpercentages of the respective feedstock masses entering the ADreactor (kg VS).

4.3. Nitrogen balance

By altering the type of, and the mix of, co-digestion materialand algal matter, the nitrogen flow through the system can bebalanced, i.e. the nitrogen leaving the system is made equal to thenitrogen entering the system. ‘Production’ of algae-available nitro-gen (NP) is calculated using Eq. (6).

NP¼ βVS � ðx� NOC þ y� NS þ z� NC þ j� NGÞ ð6ÞβVS is the mineralization factor for nitrogen in the AD. N

indicates the total percentage of nitrogen in the feedstocks, whilesubscripts OC, S, C, and G stand for oilcake, sludge, waste paperand glycerin, respectively. The symbols x, y, z, and j are the weightsof the different feedstocks (kg VS). Assuming perfect efficiency,algae production is calculated based on the available nitrogen inthe AD effluent.

4.4. Carbon balance

There are two sources of CO2 in the system; biogas (PCO2 ), andcombustion of methane in the CHP unit (CHPCO2 ). CO2 is consumedby the algae (MCCO2 ). The production and consumption arecalculated using Eqs. (7)–(9).

PCO2 ¼WCO2 � B2G�%CO2 �M ð7Þ

CHPCO2 ¼ βCO2�WCH4 � B2G�%CH4 �M ð8Þ

MCCO2 ¼ ACO2 � XA ð9Þwhere WCO2 and WCH4 are the weights of CO2 and CH4; B2G is theproduction of biogas (m3) per kg VS; %CO2 and %CH4 are the % ofCO2 and CH4; βCO2

is the weight ratio between CO2 and CH4; and Mis the total mass of the feedstock entering the AD reactor. If theconsumption of CO2 is greater than the production, CO2 must beintroduced from external sources.

Table 3Energy content of the biomass involved.

Feedstock Energy (GJ) Fraction (%)

Algae 97.2 50Sludge 79 40Wastepaper 18.0 9Methanol 2.8 1

Total 197 100

Table 4Algae productivities.

Oilcontent(%)

Oilproductivity(g m−2 d−1)

Biomassproduction(g m−2 d−1)

Energyproduction(kW ha−1)

Averageachievedopen ponda

25 3.8 15.1 24

Maximumachievedponda

25 9.1 36.4 58

J. Morken et al. / Energy Policy 60 (2013) 98–105 103

4.5. Chronology of calculations

Based on the presented parameters, a query can be constructedin the model. The criteria are: (1) CN ratio, and (2) nitrogenbalance within the system. This query then yields information on:(1) amount of VS in the different feedstocks fed into the AD, (2) thefractions in the different feedstocks, and (3) external CO2 needed.

Biogas production and total mass can then be calculated basedon the total VS entering the AD.

Based on biogas production, the amounts of methane, and CO2,and the need for scrubbing, the figures for the combined heat andpower (CHP) can then be estimated.

Based on the amount of oilcake (kg VS), one can calculatebackward to estimate: (1) total algae mass, (2) evaporation, (3)pond area needed, (4) nutrient requirements (N, P, and CO2), (5)flows, and (6) need for coagulant. When total algae mass is known,the amount of oil can be estimated based on the lipid fraction inthe algae. This gives the foundation to estimate: (1) need forphosphoric acid, hexane and smectite for the oil extractionprocess, (2) oil produced, (3) methanol and NaOH for esterifica-tion, (4) crude glyceride produced, and (5) biodiesel produced.

Heat and power consumption can then be estimated based onthe calculated flows. The power that is not consumed within thesystem is exported.

Projectedvaluesa

35 19.8 56.5 101

ACADbiorefinery

25 3.8 15.1 23

a Values taken from Huntley and Redalje (2007).

Fig. 4. Energy flow in the system.

5. Results

The total amount of volatile solids entering the AD is used toestimate the biogas produced. The calculated biogas volume,methane volume, and energy content were 3966 m3, 2372 m3,and 89,584 MJ, respectively. A 4416 kg algal biomass was needed.One of the factors that governs the productivity of algae is solarradiation, which also causes evaporation (18 m3). The productionof algae was calculated to be 55,000 kg ha−1 yr−1. Assuming thatsufficient nutrients are available for the algae, the sunlight neededto support the photosynthetic process might be the limiting factor.

The fertilizer and CO2 requirements to produce the algalbiomass are based on stoichiometric estimations (Lardon et al.,2009; Clarens et al., 2010). The results show that an external Psupply is necessary (Table 2).

The energy content of the biomass is calculated by multiplyingthe amount of feedstock by its gross calorific value (Table 3). Thetotal biomass energy entering the system as sludge, waste paper,and methanol (other inputs are not included due to their lowcontributions) was 99 GJ. Of this 97 GJ is converted to algae(Table 3) and 40 GJ is eventually exported as biodiesel. Table 4shows the total energy flow of the system.

Related to the total energy in the biomass, the distribution ofthe different forms of energy is given in Fig. 4. It can be concludedthat 65% of the energy in the feedstock is used, and the rest is lost,either through CHP or through energy leaving the system in thesolid waste.

Through combustion of methane in the CHP, the systemproduces its own electric power. About 41% of the power producedis consumed within the system boundaries, the rest is assumed tobe exported to a power grid. The heat from the CHP is used in

Table 2Fertilizer and CO2 requirements.

Parameter Needed Internal supply External supply

N (kg) 321 378 NoneP (kg) 73 40 34CO2 (kg) 7065 7110 None

different processes within the system. The scrubber consumes themost power, followed by the anaerobic digester, rotary presses,pumps, and mixers (Table 4). The rest of the processes compriseapproximately 1% of the power consumption. The power that isnot consumed is exported. The scrubbing of the biogas has beenincluded, together with its power consumption.

The heat balance shows that heat production is 49 GJ, whiletotal heat consumption is 31 GJ (for AD, extraction and transester-ification). This shows that heat production is sufficient for theinternal demand.

Table 5Comparison between the closed-loop-concept and ACAD biorefinery concept.

Process proprieties ACAD biorefinery Schamphelaire andVerstraete (2009)

Production, ton VS ha−1 yr−1 55 24–65Concentration in pond, mg VS l−1 206 256–703Biogas production, m3 kg VS−1 0.54 0.38–0.63Biogas quality, % 60 40–65VS destruction, % 60 49–64C/N ratio 25 10–17Calorific value of algae, kJ g−1 20 25Energy production prospects, kW ha−1 23 9–23

J. Morken et al. / Energy Policy 60 (2013) 98–105104

6. Discussion

This study is based on a theoretical model and many techno-logical challenges are still unsolved, some of which are probablynot even identified yet. On the other hand, an attempt to makereasonable assumptions has been made in order to design a betterbiowaste-biogas-microalgal system for the production of bioe-nergy. The results should therefore be interpreted as a preliminarystudy to identify some of the opportunities and challenges.

Setting methane production as the key reference parameter,the flows in the system were calculated using parameters andfigures derived from the literature. By altering the mixture of thefeedstock entering the anaerobic digester, an optimal C/N ratio forthe feedstock and the nitrogen balance for the system wasreached. The model proved itself to be a powerful tool for under-standing the symbioses and dynamics of the concept. Manysymbiotic features were identified: nutrient removal from thedigestate and nutrient supply for the algae cultivation; excess heatand the need for heat in different processes; and production andconsumption of electric power.

The field of microalgae is vast, and the overall data on productiv-ity, nutrient requirements, composition, and energy content willalways be coupled with uncertainties and can always be criticized forbeing too general. But in order to investigate the potential of theACAD concept, general data and rough assumptions were used.

Although the whole algal biomass should be digested when thecell lipid content is below 40% (Sialve et al., 2009), the ACADcalculations found that the two phase approach of both biodieseland biogas yields more energy, in the model, than digesting thewhole biomass even at levels below 40%. Since the oil extractionprocess is also a pre-treatment for the oilcake, the biogas yieldmight be higher than otherwise projected. With regard to envir-onmental issues, biodiesel is a very important energy source sinceit can substitute for fossil diesel directly without major changes inthe infrastructure. There are many renewable and low-carbonsolutions for production of electricity, but not as many for fuels.Because of these reasons, the two-output version has been chosenfor the model.

It can be concluded that the conversion of algal oil intobiodiesel is much more energy efficient than the conversion ofalgal biomass into biogas (Fig. 4). While 100% of the energy in thelipids is exported as biodiesel, only about 12% of the feedstockenergy of the oil cake is exported as electricity. Although theenergy in the biogas also supplies the biodiesel production processwith electricity and heat, the total energy outcome of the bior-efinery increases as the lipid fraction of the algae increases.

Although it does not contribute a large quantity, the electricityfraction is very important in many ways. First, electricity produc-tion makes the system independent of external energy sources,making the system more robust and flexible regarding location,unstable power supply, and fluctuations in energy prices. Anotherbenefit of producing electricity is that, since electricity has ahigher energy quality, it can be used in many both internal andexternal applications not suitable for liquid fuels. If all the outputenergy is summed (electricity, biodiesel and organic waste), comesto 124 GJ, 25 GJ more than the total feedstock energy entering thesystem. The additional energy comes from the algae's ability tocombine CO2, nutrients and sunlight into energy-rich biomass. Inaddition, the nutrients from anaerobic digestion contribute 50% ofthe energy in the internal feedstock (Table 3). The role of theanaerobic digester is therefore primarily to supply nutrients to thealgae, and secondly to produce biogas for heat and electricityproduction.

Increasing the oil yield has been one of the main focal pointsof research since microalgae were suggested as a source of lipidsfor bioenergy production (Sheehan et al., 1998). Two major

government-sponsored research programs in Japan and USA con-cluded that algae technology was not yet feasible and theprograms were terminated after investing millions of US dollars.In contrast to these failures, Huntley and Redalje (2007) reportedthe results of a private initiative that engineered, built andsuccessfully operated a modular, commercial scale (2 ha) produc-tion system for photosynthetic microbes on Hawaii. Theirapproach was to combine photobioreactors and open ponds in atwo-stage process, shifting between nutrient-sufficient conditionsand nutrient-limiting conditions. The first stage (nutrient-suffi-cient conditions) takes place in a photobioreactor that favorscontinuous cell division and prevents contamination; the goal ofthe second stage is to expose the cells to nutrient deprivationand other environmental stresses that lead to synthesis of theproduct of interest: oil. Environmental stresses are applied bytransferring the culture from the photobioreactor to an open pond.By this method, they have managed to achieve microbial oilproduction from Haematococcus pluvialis equivalent to a low of420 GJ ha−1 yr−1 with the prospect of producing 3200 GJ ha−1 yr−1.Their average achieved values are used in the ACAD model.

The productivities used in the ACAD model are shown in Table 4and are compared to the productivities obtained and projected byHuntley and Redalje (2007). Evidence supporting the projected valuelisted in Table 5 can be demonstrated using species with knownperformance characteristics under the conditions that prevailed intheir existing production system. The oil productivity figures used inthe ACAD biorefinery model are the achieved values and thereforemuch lower than the reported high value (Table 4).

An increase in algal biomass productivity and a decrease in lipidcontent for the algae in the ACAD model will shift the production ofenergy from biodiesel into biogas, which again is converted toelectricity and heat. If biodiesel is to be the main output of an ACADbiorefinery, lipid production must be a major focus. As mentionedearlier, the oil productivity depends on both the oil content andproductivity of algal biomass in general. While the first parameteraffects the ratio between ACAD biodiesel and electricity, the secondparameter governs the pond area needed to collect the energy. Thefigure from Huntley and Redalje (2007) for this was chosen for use inthe ACAD model since this was documented on a large scale, whilethe figure from Illman et al. (2000) were lab results. Oil content inmicroalgae can exceed 80% by weight, and levels of 20–50% are quitecommon (Chisti, 2007). But, as mentioned earlier, high oil levelsoften mean low productivity. An alternative way to improve oilproductivity is to use photosynthetic bacteria, such as cyanobacteria;Synechocystis sp. Cyanobacteria accumulate lipids in thylakoid mem-branes, which are associated with high levels of photosynthesis and arapid growth rate (Rittmann, 2008). Vermaas (1998), according toRittmann (2008), managed to genetically improve a single genemutation of Synechocystis sp. that accumulates up to 50% of its dryweight in lipids. The lipid level of 25% used in the ACAD biorefinerymodel is a conservative figure, and higher lipid levels could probablybe achieved by using other suitable microalgae or cyanobacteria.

J. Morken et al. / Energy Policy 60 (2013) 98–105 105

Although the ACAD biorefinery model used in this study differsfrom the model used by Schamphelaire and Verstraete (2009), theresults from their research could indicate the viability of thefigures for the ACAD biorefinery. Their model combined algaecultivation with anaerobic digestion, but they included a microbialfuel cell (MFC) as well. In Table 5, values for their closed-loopsystem and the ACAD biorefinery are compared and show thesame final outputs. Table 5 indicates that, despite lower values forall key components, the biorefinery achieves as high a level ofenergy production as the maximum outlined by them. The outputenergy in their model is the heat of combustion of methane, whilethe output energy from the biorefinery is electricity, which can beconsidered a higher quality energy, and biodiesel.

There are also other and more practical questions that need tobe addressed before a biorefinery can be implemented. How willunwanted substances in the wastewater affect the growth of thealgae? How can the productivity and oil content be maximized?Which strain of algae or cyanobacteria is most suitable? Shouldone use open ponds or photobioreactors or both? Are the assump-tions made in this article viable in the real life? Despite all thequestions, one thing is sure: if the cultivation of microalgae is to beimplemented on a large scale for energy production it cannot relyon chemical fertilizers using today's methods of production with-out creating a large environmental burden attributable to theenergy produced.

7. Conclusion

The construction of the ACAD model outlines both challengesand opportunities within the ACAD concept. Many differentoperational factors and processes are combined, and they haveto function together in order for the model to be balanced.

Energy calculations from the model show that more energy canbe produced by combining processes. For every unit of feedstockenergy entering the system, 0.57 units of energy is exported as eitherbiodiesel or electricity. The energy content of the algae equals theenergy content of the external biomass sources, suggesting that theACAD concept is as much a sunlight-to-bioenergy, as a waste-to-bioenergy system. The roles of the anaerobic digester in the ACADconcept are therefore primarily that of supplying nutrient to thealgae and second, producing biogas for heat and electricityproduction.

The model shows that the ACAD biorefinery could be totallyindependent of external fossil energy supply. Approximately 40%of the electricity produced by the system is used to run the variousprocesses within it; the other 60% is exported. The exported poweraccounts for approximately 30% of the total exported energy, whilethe remaining 70% is in biodiesel. If one manages to design thebiorefinery so that all the nutrients for algae cultivation are madeavailable through the AD process, the biorefinery could be inde-pendent from chemical fertilizer. By producing its own energy, thebiorefinery improves its renewability and level of carbon neutral-ity. By building the biorefinery model, the viability of combiningthe AD with the MC has been strengthened.

The bioenergy concept could produce substantial amounts ofenergy without using arable land, and without the need forchemical nitrogen fertilizer. Using an ecotechnological approachseems to be a key component when building sustainable energyproduction systems, and therefore the model could be a useful toolif a policy for sustainable energy production were to be outlined.

Appendix A. Supporting information

Supplementary data associated with this article can be found inthe online version at http://dx.doi.org/10.1016/j.enpol.2013.04.081.

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