8
Energy production from microalgae biomass: carbon footprint and energy balance Diego Lima Medeiros * , Emerson A. Sales, Asher Kiperstok Industrial Engineering Graduate Program (PEI) at Federal University of Bahia (UFBA), Escola Polit ecnica, Rua Aristides Novis, n 2, 6 Andar e Federaç~ ao, EP-UFBA, CEP 40.210-630, Salvador, BA, Brazil article info Article history: Received 22 September 2013 Received in revised form 16 May 2014 Accepted 15 July 2014 Available online xxx Keywords: Microalgae Nannochloropsis sp. Life cycle analysis Greenhouse gas Net Energy Ratio abstract Bioenergy sources are promising alternatives for sustainable energy production. Nevertheless, signicant research and detailed analysis are necessary to identify the circumstances under which such energy sources can contribute to sustainability. This paper reviews the literature of Life Cycle Assessment (LCA) of microalgae-to-energy technologies and focuses in two categories, Greenhouse Gas (GHG) emissions and Net Energy Ratios (NER). The analysis is illustrated with a case study of microalgae biomass com- bustion to produce heat and compares the inuence of different electricity sources with respect to GHG emissions and NER along the supply chain. Selected fossil energy sources were used as reference con- ditions. The methodology was LCA based on ISO 14044 standard, and most of the data used were extracted from a review of relevant scientic publications. Heat production from microalgae showed higher GHG emissions than those from fossil fuels with United States' electricity grid, but lower than those with the Brazilian one. The NER of heat from microalgae combustion life cycle is still disadvan- tageous compared to most of fossil options. However, the observation that fossil fuel options performed slightly better than microalgae combustion, in the two categories analyzed, must be understood in the context of a mature fossil energy technology chain. The fossil technology has less potential for im- provements, while microalgae technology is beginning and has signicant potential for additional innovations. © 2014 Elsevier Ltd. All rights reserved. 1. Introduction The world relies on a continuous supply of energy to maintain the economic growth. The risk of an energy crisis may be reduced with more diversity of energy sources. Fossil fuels supply approx- imately 80% of the world's energy demand and are relatively inexpensive. However, the use of these fuels has added GHG to the atmosphere, thus contributing to global climate change. Biofuels are fuels derived from living matter, i.e. plants, animals, bacterias and fungi. Fossil fuels releases most of their GHG emis- sions in the combustion step while biofuels do from cultivation and processing steps (Zah et al., 2009). New technologies of biomass-to- energy conversion are currently in development and will play a decisive role in the world energy sector (Dovì et al., 2009). Microalgae-to-energy processes have being studied in recent de- cades, and industrial plants are currently being built to begin commercial generation of fuels from this source (Bahadar and Bilal Khan, 2013). On the other hand, Davis et al. (2011) declared that the near-term economic viability of algal biofuels is uncertain due to speculation surrounding the processes of scaling-up this emerging industry. Some researches are interested in analyzing the NER and GHG emissions of microalgae-to-energy technologies (Lam and Lee, 2012; Lam et al., 2012). The reason is that methods, to grow and process algae, vary according to the location, species of algae being grown, and the products intended to be taken. This paper reviews some of the latest discoveries in this eld and explores a simulated case study. 2. Microalgae-to-energy 2.1. Cultivation The rst step in algal bioenergy production, the microalgae biomass growth, is often a decisive step, as it demands most of the inputs in the entire process chain. A comparative assessment of microalgae cultivation was conducted to characterize the range of * Corresponding author. Tel.: þ55 71 3283 9800; fax: þ55 71 3283 9801. E-mail address: [email protected] (D.L. Medeiros). Contents lists available at ScienceDirect Journal of Cleaner Production journal homepage: www.elsevier.com/locate/jclepro http://dx.doi.org/10.1016/j.jclepro.2014.07.038 0959-6526/© 2014 Elsevier Ltd. All rights reserved. Journal of Cleaner Production xxx (2014) 1e8 Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

Energy production from microalgae biomass: carbon footprint and energy balance

  • Upload
    asher

  • View
    215

  • Download
    1

Embed Size (px)

Citation preview

lable at ScienceDirect

Journal of Cleaner Production xxx (2014) 1e8

Contents lists avai

Journal of Cleaner Production

journal homepage: www.elsevier .com/locate/ jc lepro

Energy production from microalgae biomass: carbon footprint andenergy balance

Diego Lima Medeiros*, Emerson A. Sales, Asher KiperstokIndustrial Engineering Graduate Program (PEI) at Federal University of Bahia (UFBA), Escola Polit�ecnica, Rua Aristides Novis, n� 2, 6� Andar e Federaç~ao,EP-UFBA, CEP 40.210-630, Salvador, BA, Brazil

a r t i c l e i n f o

Article history:Received 22 September 2013Received in revised form16 May 2014Accepted 15 July 2014Available online xxx

Keywords:MicroalgaeNannochloropsis sp.Life cycle analysisGreenhouse gasNet Energy Ratio

* Corresponding author. Tel.: þ55 71 3283 9800; faE-mail address: [email protected] (D.

http://dx.doi.org/10.1016/j.jclepro.2014.07.0380959-6526/© 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: MedeiroJournal of Cleaner Production (2014), http:/

a b s t r a c t

Bioenergy sources are promising alternatives for sustainable energy production. Nevertheless, significantresearch and detailed analysis are necessary to identify the circumstances under which such energysources can contribute to sustainability. This paper reviews the literature of Life Cycle Assessment (LCA)of microalgae-to-energy technologies and focuses in two categories, Greenhouse Gas (GHG) emissionsand Net Energy Ratios (NER). The analysis is illustrated with a case study of microalgae biomass com-bustion to produce heat and compares the influence of different electricity sources with respect to GHGemissions and NER along the supply chain. Selected fossil energy sources were used as reference con-ditions. The methodology was LCA based on ISO 14044 standard, and most of the data used wereextracted from a review of relevant scientific publications. Heat production from microalgae showedhigher GHG emissions than those from fossil fuels with United States' electricity grid, but lower thanthose with the Brazilian one. The NER of heat from microalgae combustion life cycle is still disadvan-tageous compared to most of fossil options. However, the observation that fossil fuel options performedslightly better than microalgae combustion, in the two categories analyzed, must be understood in thecontext of a mature fossil energy technology chain. The fossil technology has less potential for im-provements, while microalgae technology is beginning and has significant potential for additionalinnovations.

© 2014 Elsevier Ltd. All rights reserved.

1. Introduction

The world relies on a continuous supply of energy to maintainthe economic growth. The risk of an energy crisis may be reducedwith more diversity of energy sources. Fossil fuels supply approx-imately 80% of the world's energy demand and are relativelyinexpensive. However, the use of these fuels has added GHG to theatmosphere, thus contributing to global climate change.

Biofuels are fuels derived from living matter, i.e. plants, animals,bacterias and fungi. Fossil fuels releases most of their GHG emis-sions in the combustion step while biofuels do from cultivation andprocessing steps (Zah et al., 2009). New technologies of biomass-to-energy conversion are currently in development and will play adecisive role in the world energy sector (Dovì et al., 2009).Microalgae-to-energy processes have being studied in recent de-cades, and industrial plants are currently being built to begincommercial generation of fuels from this source (Bahadar and Bilal

x: þ55 71 3283 9801.L. Medeiros).

s, D.L., et al., Energy product/dx.doi.org/10.1016/j.jclepro.2

Khan, 2013). On the other hand, Davis et al. (2011) declared that thenear-term economic viability of algal biofuels is uncertain due tospeculation surrounding the processes of scaling-up this emergingindustry. Some researches are interested in analyzing the NER andGHG emissions of microalgae-to-energy technologies (Lam and Lee,2012; Lam et al., 2012). The reason is that methods, to grow andprocess algae, vary according to the location, species of algae beinggrown, and the products intended to be taken. This paper reviewssome of the latest discoveries in this field and explores a simulatedcase study.

2. Microalgae-to-energy

2.1. Cultivation

The first step in algal bioenergy production, the microalgaebiomass growth, is often a decisive step, as it demands most of theinputs in the entire process chain. A comparative assessment ofmicroalgae cultivation was conducted to characterize the range of

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e82

inputs required in this step for open and closed systems, Tables 1and 2 respectively.

The data varies significantly between authors. Uncertainty inenergy inputs at cultivation affects the NER and consequently theGHG emissions (Rogers et al., 2013). Handler et al. (2012) did asimilar comparison between LCA studies and found variations inenergy use at cultivation step of two orders of magnitude. Furthercomments on these tables are in the discussion section.

2.2. Scaling up of microalgae production

Significant improvements to reduce the infrastructure and oper-ational costs, in order to scale-upmicroalgae production chain,mustbe performed to produce commercially viable products frommicroalgae. P�erez-L�opez et al. (2013a,b) found the usage of com-mercial fertilizer and electricity as the major contributors to theenvironmental impacts of microalgae products. A defined set oftechnology breakthroughs will be required to optimize the produc-tion of microalgae biofuels at scale (Singh and Olsen, 2011; Um andKim, 2009). Table 3 summarizes most of the current challenges andopportunities related to commercial exploitation of algal biofuels.

Biofuels based on algal biomass may play a decisive role infuture energy production chains if technological breakthroughs canaddress challenges mentioned in Table 3. Koller et al. (2012) statethe possibility of mixotrophic cultivation of microalgae, combiningremoval of pollutants from wastewater in a heterotrophic phaseand production of high added value products in an autotrophicphase. Therefore, the carbon dioxide input required to nourish themicroalgae growth can be supplied from low cost sources such asflue gases from boilers, furnaces or power plants (Sander andMurthy, 2010; Campbell et al., 2010). In addition, combustionproducts such as nitrogen oxides and sulfur oxides can be effec-tively used by microalgae as nutrients (Um and Kim, 2009; Packer,2009; Yoo et al., 2010). Also, most of the nutrients needed for algalgrowth, except carbon, may be obtained from municipal waste-water with the function of nutrient removal (Yang et al., 2011; U.S.DOE, 2010; Park et al., 2011; Pittman et al., 2011; Itoiz et al., 2012;Olguín, 2012; Fenton and �OhUallach�ain, 2012). In Table 4 are pre-sented the conclusions of selected literature related to energybalance of different microalgae biofuels.

The studies in Table 4 found both, favorable and unfavorable,energy balances over the biofuel life cycle depending on the tech-nological scenario modeled. According to Singh and Olsen (2011) itis difficult to identify preferred routes of biofuel production fromalgal biomass at the current stage of development. Holma et al.(2013) affirm the results of the microalgae production chain are

Table 1Inputs in open pond microalgae cultivation per kilogram of produced dry biomass.

Method Open ponds

Authors Chisti,2007.

Lardon et al.,2009.

Lardon et al.,2009.

Jorqueraet al., 2010

Species Chlorellavulgaris

Chlorella vulgaris,normal

Chlorella vulgaris,less N

Nannochloropsp.

Processparameters

Unit Quantity

Energy kWh e 0.35 0.42 1.05CO2 kg 1.83 1.75 1.97 e

N kg 0.07 0.046 0.01 e

P kg 0.01 e e e

Water m3 7.1 e e 2.8Growth g/m2

daye 25 19 11

Concentration kg/m3 0.1 0.5 0.5 0.35Oil content % 30 18 40 30

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

uncertain due to the early development stage of the technology andthe assumptions made concerning the electricity grid, which canvary significantly between different sites.

Clarens et al. (2011) compared three different routes of energyproduction from microalgae biomass for transportation purposes,such as: combined biodiesel and electricity production from biogas,combined biodiesel and electricity production from biomass com-bustion, and electricity production from biomass combustionalone. The authors identified the most advantageous NER camefrom the third route. Some studies concluded that microalgae lipidextraction is an energy intensive process (Clarens et al., 2011;P�erez-L�opez et al., 2013a).

3. Methods

The case study aimed to evaluate the environmental and ener-getic performance of thermal recovery from biomass combustionusing microalgae cultivated in Open Ponds (OP) and Flat PlatePhotobioreactors (FPP). We modeled the GHG emissions and NERover the life cycle and compared themwith selected fossil sources.Most of the data used in this analysis came from scientific litera-ture, as the authors were not aware of any commercial industrialplant producing bioenergy photosynthetically from microalgae asof the writing of this article.

3.1. Goal and scope definition

This study was based on the methodology of Life Cycle Assess-ment (LCA) according to ISO 14044 (2006). Each production chainconsidered two scenarios for cultivation:

OP1 e algal biomass, open pond, flue gas.OP2 e algal biomass, open pond, flue gas and wastewater.FPP1 e algal biomass, flat plate, flue gas.FPP2 e algal biomass, flat plate, flue gas and wastewater.

The cut-off rule was applied to waste streams, flue gas andwastewater. This assumption means that treatment gains or envi-ronmental loads fromwaste streams productionwere not recorded.Scenarios OP1 and FPP1 were supplied by tailing water fromdesalination, as the algae genus used was Nannochloropsis, amicroalgae originally from the sea. Scenarios OP2 and FPP2 usedtwo sources of water, tailing water from desalination and waste-water as a nutrient source. This practice has been found to replacethe use of chemical fertilizers without any productivity loss (Yanget al., 2011; Jiang et al., 2011; Perelo et al., 2012).

Campbellet al., 2010.

Clarens et al.,2010.

Stephensonet al., 2010.

Quinnet al., 2011

Razon andTan, 2011.

sis Dunaliella Mix ofmicroalgae

Chlorellavulgaris

Nannochloropsisoculata

Nannochloropsissp.

0.2 0.19 0.8 e 12.71.69 e e e e

0.008 e 0.024 e 0.0070.0056 e e e 0.0130.7 e 0.7 e e

30 15 30 15 16

e 1 1.67 3 0.13e e 40 51 30

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

Table 2Inputs in photobioreactors microalgae cultivation per kilogram of produced dry biomass.

Method Tubular Flat-plate Polyethylene bags Hybrid, FPP and OP

Author Chisti,2007.

Collet et al.,2011.

Stephensonet al., 2010.

Jorqueraet al., 2010

Batan et al.,2010.

Khoo et al.,2011

Razon andTan, 2011.

Species Chlorellavulgaris

Chlorellavulgaris

Chlorellavulgaris

Nannochloropsissp.

Nannochloropsissalina

Nannochloropsissp.

Haematococcuspluvialis

Processparameters

Unit Quantity

Energy kWh e 0.23 7.27 1.94 0.455 0.972 5.77CO2 kg 1.83 1.17 e e e 1.83 e

N kg 0.07 0.01 0.0236 e 0.147 0.15 0.0128P kg 0.01 0.002 e e 0.02 0.01 0.013Water m3 0.25 e 0.134 0.37 0.134 2125 e

Growth g/m2

daye 25 75 27 25 e 16

Concentration kg/m3 4 0.5 8.3 2.7 e 0.5 0.43Oil content % 30 e 40 30 e e 25

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8 3

3.2. Inventory

The reference flow adopted was 1 kg of biomass with a LowerHeating Value (LHV) of 18.26 Mega Joules (MJ), calculated forNannochloropsis biomass in Appendix I. The functional unit forcomparison with fossil fuels was 20 MJ of LHV. The infrastructurematerials for the cultivation and harvesting step were neglected inthese calculations, as the impact was assumed to be negligible overthe lifespan of the building (Grierson et al., 2013). The followingassumptions were used for the definition of the system model:

3.2.1. CultivationThe electricity consumption in the cultivation stage is primarily

due to flue gas pressurization and pumping into the culture me-dium, water pumping for recirculation, and water pumping forcooling in the FPP scenarios (Jorquera et al., 2010). The electricitysources used were the medium voltage electricity grid from UnitedStates (U.S.) and Brazil (BR) from Ecoinvent (2013).

The flue gas andwastewaterwere assumed to be located close tothe microalgae farms, thus needing no further transport re-quirements as Rickman et al. (2013) point. The water may comefrom the sea or saline aquifers, which are common in the semiaridregion of Brazil and showed a favorable growth medium for Nan-nochloropsis in combination with wastewater after secondarytreatment (Perelo et al., 2012; Jiang et al., 2011). The reason tochoose this algae was the capacity to cultivate it in OP withoutusing pesticides, as the salt water may inhibt predors. The waterevaporation losses in the OP systems were neglected, as all of thewater usedwas previously wastewater. The OP1 and FPP1 scenariosused commercial fertilizers manufactured in Europe.

The biomass concentrations at the point of harvest were 0.35 kg/m3 in OP and 2.7 kg/m3 in FPP according to Jorquera et al. (2010),and the maximum algae concentration is achieved with a growthperiod of 7 days. These data were used to estimate the volume ofcultivation medium needed for each kilogram of microalgaebiomass harvested.

1 The acronym RER means Europe Region.

3.2.2. HarvestingIt was considered three harvesting steps (flocculation, decan-

tation and centrifugation) and a drying stage (solar-greenhouse) toset the biomass suitable for energy recovery through combustion togenerate heat. The products used in flocculation process wereassumed to be produced in Europe.Weschler et al. (2014) identifiedthermal drying as an undesirable process, it offsets most of possibleGHG and NER gains. The solar-greenhouse does not require any

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

significant direct input other than sunlight, reason why this stepwas neglected from the inventory.

3.2.3. CombustionThere is lack of data on microalgal biomass combustion process.

The inventory of a thermoelectric power plant fueled by perishablehousehold waste was selected as a representative inventory formicroalgal biomass combustion from Ecoinvent (2013).

4. Results

4.1. Inventory

Table 5 presents the inventory of Nannochloropsis sp. drybiomass production used to analyse the GHG emissions and NER.

More analysis of the inventory, Table 5, are in the discussionsection.

4.2. Greenhouse Gases (GHG)

Fig. 1 presents the GHG emissions of the production chains, OP1,OP2, FPP1 and FPP2, and selected fossil fuel options obtained fromthe Ecoinvent (2013) as follows: Heat, at hard coal industrial furnace1-10 MW/RER1; Heat natural gas, at industrial furnace > 100 kW/RER1;Heat, heavy fuel oil, at industrial furnace 1MW/RER1;Heat, lightfuel oil, at industrial furnace 1 MW/RER.1

The GHG emissions from microalgae scenarios varied signifi-cantly, with cases better than most fossil fuel options as BR OP2 orworse like U.S. FPP1.

In Fig. 2 is shown the GHG contribution of U.S. OP1 productionchain. The production chains of the other microalgae scenarios aresimilar.

It is noticeable that the processes which contributed most toGHG emissions were N fertilizer, electricity and aluminium sul-phate with 16%, 37% and 28% respectively. More analysis of theseresults, Figs. 2 and 3, are hereafter in the next subsection.

4.3. Net Energy Ratio (NER)

The energy balance or NER was calculated as the energy con-tained in the final product, the output energy (E Out) of the system,divided by the Cumulative Energy Demand (CED) along the

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

Table 3Challenges to commercial-scale implementation of microalgae-to-biofuel schemes.

Cultivation Opportunities Obstacles

CO2 Available at low cost from energy-intensive industrial plantsa Land shortage around these industrial areasb

Nutrients Available at low cost from secondary wastewater treatment plants Not well studied yetc

Water Can be recirculated This practice is not well established yetd

Infrastructureand Operation

Offer more control to the processes High cost and currently is intensive in energye

Sun/light Arid areas are one promising source The resources should be transported through long distancesand it needs investment in infrastructure

Temperature Sites surrounding mountains, rainforests, or large water bodiesoften have temperatures amenable to production

Normally these places are protected. In arid areas temperaturecontrol may impose a challengef

Species Several wild types of algae have been used without selection ormodification

The algae will have to be domesticatedh

Oil productivity Starve algae from nitrogen increase lipid's productivityj Slow down growth yield and consequently operation costsContamination Microalgae from lab did not stand under robust conditions

encountered in the fieldAllow a contaminant native to the area take over the pondsf

Harvesting There are many technologies being used and in development It has to be adapted for a specific specie, medium anddownstream processg

Lipid extraction There are promising technologies being developed It will depend on the specie of algae and how it was grownh

Biomass It can be converted in many forms of biofuels. Not all of them have being successful tested in pilot scale yeti

a Campbell et al. (2010).b Pate et al. (2011).c Park et al. (2011); Christenson and Sims (2011).d Yang et al. (2011).e Norsker et al. (2011).f Sheehan et al. (1998).g Uduman et al. (2010); Mata et al. (2010); Udom et al. (2013).h Rawat et al. (2011); Benemann (2010).i Singh and Olsen (2011).j Lardon et al. (2009).

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e84

production chain, the input energy (E In) of the system (Delrueet al., 2012; Zhang and Colosi, 2013). The results are shown in Fig. 3.

NER ¼ E Out.X

E In (1)

The OP2 and FPP2 scenarios performed more favorable resultsthan the OP1 and FPP1 scenarios in both categories assessed, GHGand NER, due to the elimination of commercial fertilizers, whichrequire significant energy inputs for their production and trans-portation, while wastewater contains the same nutrients “for free”.

Table 4Comparison of energy balances for microalgae biofuel production over the life cycle.

Studies Description NER � 1 NER < 1

Lardon et al. (2009) Biodiesel productionfrom microalgae

X

Clarens et al. (2010) Biomass productionfrom microalgae

X

Liu and Ma (2009) Methanol productionfrom microalgae

X

Scott et al. (2010) Biodiesel productionfrom microalgae

X

Jorquera et al. (2010) Biomass productionusing different methods

X X

Liu et al. (2011) Biodiesel producedfrom six microalgae(raceway) models

X X

Razon and Tan (2011) Biodiesel and methaneproduced from microalgae

X

Itoiz et al. (2012) Biodiesel productionfrom microalgae

X

Delrue et al. (2012) Biodiesel and Biogasproduction from microalgae

X X

Delrue et al. (2013) Biodiesel production frommicroalgae

X

Quinn et al. (2013) Biodiesel and Biogasproduction from microalgae

X X

Khoo et al. (2013) Biooil and Biogas productionfrom microalgae

X X

Passell et al. (2013) Biodiesel production frommicroalgae

X

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

The substitution of reclaimed wastewater for commercial fertilizersreduced the GHG emissions by 22% U.S. OP, U.S. FPP 16%, BR OP 35%,BR FPP 33% and increased the NER by 24% U.S. OP, U.S. FPP 19%, BROP 34%, BR FPP 29%. Nevertheless, the emissions associated withmicroalgae production and combustion are not significantlydifferent from those of most fossil fuels, due to the significant un-certainties associated with both fuel sources.

It is noteworthy that electricity from the U.S. grid, which ispredominantly derived from fossil fuels, is more GHG intensive andless efficient in the energy conversion compared to the Brazilianone. It was identified in the Ecoinvent (2013) with the method CEDthat each MJ of electricity from the medium voltage electrical griddemands 3.55 MJ in US and 1.4 MJ in BR. The reason is that

Table 5Global inventory for the production of 1 kg (dry matter) of Nannochloropsis biomassin Open-ponds (OP) and Flat-plate photobioreactors (FPP).

Processparameters

OP FPP Unit Source

CultivationNitrogen (N) 0.07 0.07 kg/kg This studyPhosphorus (P) 0.01 0.01 kg/kg This studyPotassium (K) 0.01 0.01 kg/kg This studyFertilizers transportation 0.02 0.02 t.km EstimatedCarbon dioxide (CO2) 1.83 1.83 kg/kg Chisti 2007Water 2857.14 370.37 kg/kg Jorquera

et al., 2010Electricity 1.05 1.94 kWh/kg Jorquera

et al., 2010Microalgae þ Water 2858.14 371.37 kg/kgFloculationAluminum Sulfate Al2(SO4)3 1.3 1.3 kg/kg Razon and

Tan, 2011Hydrochloric Acid HCL (15%) 0.3 0.3 kg/kg Razon and

Tan, 2011Flocculent transportation 0.16 0.16 t km Estimated

Microalgae þ moisture 8 1.04 kg/kg CalculatedCentrifugationElectricity 0.06 0.001 kWh/kg Brentner

et al., 2011

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

Fig. 1. GHG emissions of 20 MJ LHV from Nannochloropsis under scenarios OP1, OP2, FPP1 and FPP2 as compared to representative fossil fuels. Source: method IPCC (2007) GWP100a.

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8 5

hydroelectricity is less GHG intensive and more efficient thanthermoelectricity from fossil fuels.

The influence of the electricity input in the outcomes of thedifferent scenarios in the cultivation step were identified. The GHGemissions for BR scenarios for OP1, OP2, FPP1 and FPP2 decreasedby 32%, 38%, 42% and 50% respectively, while their NER improved28%, 36%, 42% and 55% respectively, in comparison to the US sce-narios. Inputs such as fertilizers and flocculants were assumed toretain their original electrical grid from Europe, as most of theseproducts are typically imported.

In the cultivation step under scenarios OP1 and FPP1, the use ofelectricity and fertilizers accounted for the greatest contributions toGHGemissions (Fig. 2). The largest contribution among the differentfertilizers used was the nitrogenous fertilizer. In scenarios OP2 andFPP2, with no commercial fertilizers used, electricity input was themajor source of GHG emissions of the production chain. In theharvesting step the aluminum sulfate flocculent usedwas themajor

Fig. 2. GHG contribution along the production chain of heat production

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

source of GHG emissions due to the high electricity consumptionrequired for the production of this input, presumably from the Eu-ropean electrical grid, with its predominant fossil fuel matrix.

5. Discussion

The literature review showed that electricity is a key input in thecultivation of microalgae due to pumping of flue gases and water inthe culture medium. In disagreement with the findings of Clarenset al. (2011) we found that the cultivation of microalgae biomassfor combustion and thermal recovery is not viable from an energybalance perspective, NER<1. Surprisingly, the fossil fuel options alsoproved to be unviable despite the significant uncertainty ranges ofthe results (Fig. 3).

Several optimization opportunities exist in microalgae-to-energy production chain to reduce the environmental impactsand costs, such as those shown in Table 3. Even though microalgae

from Nannochloropsis under scenario U.S. OP1. Source: SimaPro 8 ®.

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

Fig. 3. NERof 20MJ LHV fromNannochloropsisunder scenariosOP1, OP2, FPP1 and FPP2 as compared to representative fossil fuels. Source:method CED, Jungbluth and Frischknecht (2007).

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e86

biomass is not yet an established alternative fuel source for energyproduction. Studies like the current one and those ones in Table 4are valuable in directing further efforts to develop and implementeconomically viable and environmentally sustainable microalgae-to-energy technologies.

Key differences in the input and output parameters can beobserved comparing the data from literature studies reviewed inTables 1 and 2 with the present case study. For example, the con-sumption of electricity per kg of microalgae dry biomass in OPcultivation step of the present study was 1.05 kWh, while, despitethe use of different species of microalgae, most authors' estimatesranged from 0.19 to 0.42 kWh, with the exception of Stephensonet al. (2010) and Razon and Tan (2011). Using these most commonliterature values for this parameter would reduce the electricityinputs for this stepby60e80%. Such a substitutionwould result in aneven greater difference in FPP cultivation step, as the current studyused an electricity consumption of 1.94 kWh per kg of dry micro-algae,whereasmost authors have published values ranging from0.3to 0.94 kWh, again with the exception of Stephenson et al. (2010)and Razon and Tan (2011). These differences represent a potentialreduction of 52%e85% in electricity consumption.

A possible 70% reduction in electricity consumption at thecultivation stage under the best U.S. scenario analysed, U.S. OP2,would reduce the estimatedGHGbyapproximately 42%, resulting inan emission of 0.85 kg CO2e per 20MJ LHV. This changewouldmakethis scenario appear more favorable in comparison with any fossilfuel options. Regarding the NER, applying the same reduction inelectricity consumption for U.S. OP2 scenario would constitute atechnological breaking even point, when NER equals 1. In this case,the microalgae production chain would be able to supply its wholedemand along the life cycle and lower GHG emissions close to zero.This is because U.S. scenarios havemost of the energy inputs comingfrom fossil fuels. A scenario of microalgae-to-energy with NER > 1would be able to supply the entire production chain, producing realgains and reducing GHG emissions considerably. This simulationdemonstrates how the microalgae-to-energy technology couldbecome economically viable and environmentally sustainable.

There is little room to reduce GHG emissions along the fossil fuelproduction chain, as most of these emissions happen in the com-bustion step, and the current technology is mature. Moreover, thecosts and emissions associated with extracting fossil energy sour-ces are likely to increase as these fuel sources become scarcer. Bycontrast, microalgae combustion has significantly lower GHGemissions, due to the fact that the GHG emitted at this stage isconsidered renewable. Therefore, microalgae bioenergy technolo-gies offer greater opportunities to minimize GHG emissions alongthe supply chain in the near future.

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

6. Conclusion

The results of this paper confirm the potential of microalgaebiomass as an energy source, but demonstrate the need to decreasethe use of electricity, fertilizers and other inputs, such as chemicalflocculants. The starting point for the economic and environmentalviability of energy production from microalgae biomass is theachievement of a favorable energy balance, NER � 1. This studydemonstrates that the use of flue gas, residual nutrients fromwaste-water and cleaner electricity grids enables significant reductions inGHG emissions and improvements in the energy balance associatedwith microalgae-to-energy. The influence of country electricity gridsto GHG emissions and NER over themicroalgae life cycle analysis wasdecisive when compared to fossil fuels. These actions increase theopportunities for competitive commercialization of microalgae en-ergy products. The fact that the Brazilian energy matrix is less GHGintensive and more efficient in NER compared to the world averageplaces the country in a better position to promote the production ofalgal biomass as a renewable energy source. Topics that should beexplored further in future research include the assessment of otherroutes for biofuel production such as biodiesel, biomethane and bio-ethanol, local productivity rates, comparison with other renewableenergy sources, and the evaluation of other environmental LCA cate-gories like land use impacts, resources depletion and eutrofization.

Acknowledgments

This research study was supported by the program InstitutosNacionais de Ciencia e Tecnologia (INCT) of the Conselho Nacionalde Desenvolvimento Científico e Tecnol�ogico (CNPq/MCT) andCoordenaç~ao de Aperfeiçoamento de Pessoal de Nível Superior(CAPES) for their research scholarships, the Ecoinvent for theinternship supervised by Mireille Faist, and the company ACVBrasilon behalf of Pr�e Consultants for concession of the educational li-cense for Simapro with Ecoinvent database.

Appendix A

The calculation of the Lower Heating Value (LHV) was based onthe cellular composition ofmicroalgae biomass, CO0,48H1,83N0,11P0,01,given by Grobbelaar (2004 apud Chisti, 2007). The stoichiometricbalance of combustion is CO0,48H1,83N0,11P0,01 þ 2O2 /

1CO2 þ 0.91H2O þ 0.11NO2We neglected the contribution of P in the stoichiometric bal-

ance. The water vaporization enthalpy (DHvapH2O) at 20 �C wastaken as 44.016 kJ/g mol. See the calculation table of LHV fromNannochloropsis sp., Table A.1.

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

C O H N Comments Lines

Atomic weight 12 16 1 14 1Microalgae biomass

molecularcomposition

1 0.48 1.83 0.11 Grobbelaar 2004 apud Chisti 2007 2

Multiplication 12 7.68 1.83 1.54 Line 1 items � Line 2 items 3Sum 23.05 g/g mol Result of Line 3 operation 4

1000 g or1 kg

5

Number of gmols of biomass

43.38 g mols Line 5/Line 4 6

Higher HeatingValue (HHV)

20 MJ/kg Sforza et al., 2011 7

1 g mol ofbiomass

0.91 g mol H2O 8

Vaporizationenthalpy of H2O

44.02 kJ/g mol 9

40.05 kJ Line 8 � Line 9 101 Kg of biomass 1737.72 kJ Line 10 � Line 6 11or 1.73 MJ 12Lower Heating Value (LHV) 18.26 MJ/kg Line 7 e Line 12 13LHV/HHV 0.91 Line 13/Line 7 14or 1 LHVequivalent to

1.10 HHV 1/Line 14 15

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8 7

References

Bahadar, A., Bilal Khan, M., 2013. Progress in energy from microalgae: a review.Renew. Sustain. Energy Rev. 27, 128e148. http://dx.doi.org/10.1016/j.rser.2013.06.029.

Benemann, J., 2010. AIM Interview: Dr. John Benemann by David Schwartz. AlgaeIndustry Magazine. Available at: http://www.algaeindustrymagazine.com/the-aim-interview-dr-john-benemann/.

Batan, L., Jason, Q., Bryan, W., Thomas, B., 2010. Net energy and greenhouse gasemission evaluation of biodiesel derived from microalgae. Environ. Sci. Technol.44 (20), 7975e7980. http://www.ncbi.nlm.nih.gov/pubmed/20866061.

Brentner, L.B., Eckelman, M.J., Zimmerman, J.B., 2011. Combinatorial life cycleassessment to inform process design of industrial production of algal biodiesel.Environ. Sci. Technol. 45 (16), 7060e7067. http://dx.doi.org/10.1021/es2006995.

Campbell, P.K., Beer, T., Batten, D., 2010. Life cycle assessment of biodiesel pro-duction from microalgae in ponds. Bioresour. Technol. http://dx.doi.org/10.1016/j.biortech.2010.06.048.

Chisti, Y., 2007. Biodiesel from microalgae. Biotechnol. Adv. 25 (3), 294e306. http://dx.doi.org/10.1016/j.biotechadv.2007.02.001.

Christenson, L., Sims, R., 2011. Production and harvesting of microalgae for waste-water treatment, biofuels, and bioproducts. Biotechnol. Adv. 29 (6), 686e702.http://dx.doi.org/10.1016/j.biotechadv.2011.05.015.

Clarens, A.F., et al., 2011. Environmental impacts of algae-derived biodiesel andbioelectricity for transportation. Environ. Sci. Technol. 45, 7554e7560.

Clarens, A.F., Resurreccion, E.P., White, M.A., Colosi, L.M., 2010. Environmental lifecycle comparison of algae to other bioenergy feedstocks. Environ. Sci. Technol.44 (5), 1813e1819. http://dx.doi.org/10.1021/es902838.

Collet, P., H�elias, A., Lardon, L., et al., 2011. Life-cycle assessment of microalgaeculture coupled to biogas production. Biores. Technol. 102, 207e214. http://dx.doi.org/10.1016/j.biortech.2010.06.154.

Davis, R., Aden, A., Pienkos, P.T., 2011. Techno-economic analysis of autotrophicmicroalgae for fuel production. Appl. Energy 88 (10), 3524e3531. http://dx.doi.org/10.1016/j.apenergy.2011.04.018.

Delrue, F., Li-Beisson, Y., Setier, P., et al., 2013. Comparison of various microalgaeliquid biofuel production pathways based on energetic, economic and envi-ronmental criteria. Bioresour. Technol. 136, 205e212. http://dx.doi.org/10.1016/j.biortech.2013.02.091.

Delrue, F., Setier, P., Sahut, C., et al., 2012. An economic, sustainability, and energeticmodel of biodiesel production from microalgae. Bioresour. Technol. 111,191e200. http://dx.doi.org/10.1016/j.biortech.2012.02.020.

Dovì, V.G., Friedler, F., Huisingh, D., Kleme�s, J.J., 2009. Cleaner energy for sustainablefuture. J. Clean. Prod. 17 (10), 889e895. http://dx.doi.org/10.1016/j.jclepro.2009.02.001.

Ecoinvent v2.2, 2013. Life Cycle Inventory Database. Available at: www.ecoinvent.org.

Fenton, O., �Oh Uallach�ain, D., 2012. Agricultural nutrient surpluses as potentialinput sources to grow third generation biomass (microalgae): a review. AlgalRes. 1 (1), 49e56. http://dx.doi.org/10.1016/j.algal.2012.03.003.

Grierson, S., Strezov, V., Bengtsson, J., 2013. Life cycle assessment of a microalgaebiomass cultivation, bio-oil extraction and pyrolysis processing regime. AlgalRes. 2 (3), 299e311. http://dx.doi.org/10.1016/j.algal.2013.04.004.

Handler, R.M., Canter, C.E., Kalnes, T.N., et al., 2012. Evaluation of environmentalimpacts from microalgae cultivation in open-air raceway ponds: analysis of the

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

prior literature and investigation of wide variance in predicted impacts. AlgalRes. 1 (1), 83e92. http://dx.doi.org/10.1016/j.algal.2012.02.003.

Holma, A., Koponen, K., Antikainen, R., Lardon, L., Leskinen, P., Roux, P., 2013. Cur-rent limits of life cycle assessment framework in evaluating environmentalsustainability e case of two evolving biofuel technologies. J. Clean. Prod. 54,215e228. http://dx.doi.org/10.1016/j.jclepro.2013.04.032.

ISO 14044, 2006. International Standard. Environmental Management e Life CycleAssessment e Requirements and Guidelines. International Organization forStandardization, Geneva, Switzerland.

Itoiz, E.S., Fuentes-Grünewald, C., Gasol, C.M., et al., 2012. Energy balance andenvironmental impact analysis of marine microalgal biomass production forbiodiesel generation in a photobioreactor pilot plant. Biomass Bioenergy 39,324e335. http://dx.doi.org/10.1016/j.biombioe.2012.01.026.

Jiang, L., Luo, S., Fan, X., Yang, Z., Guo, R., 2011. Biomass and lipid production ofmarine microalgae using municipal wastewater and high concentration of CO2.Appl. Energy 88 (10), 3336e3341. http://dx.doi.org/10.1016/j.apenergy.2011.03.043.

Jorquera, O., Kiperstok, A., Sales, E.A., Embiruçu, M., Ghirardi, M.L., 2010. Compar-ative energy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors. Bioresour. Technol. 101 (4), 1406e1413. http://dx.doi.org/10.1016/j.biortech.2009.09.038.

Jungbluth, N., Frischknecht, R., 2007. Part II, 2 cumulative energy demand. ecoin-vent report No. 3, v2.0. In: Frischknecht, R., Jungbluth, N., Althaus, H.-J., et al.(Eds.), Implementation of Life Cycle Impact Assessment Methods. Swiss Centrefor Life Cycle Inventories, Dübendorf.

Khoo, H.H., Koh, C.Y., Shaik, M.S., et al., 2013. Bioenergy co-products derived frommicroalgae biomass via thermochemical conversionelife cycle energy balancesand CO2 emissions. Bioresour. Technol. 143, 298e307. http://dx.doi.org/10.1016/j.biortech.2013.06.004.

Khoo, H.H., Sharratt, P.N., Das, P., et al., 2011. Life cycle energy and CO2 analysis ofmicroalgae-to-biodiesel: preliminary results and comparisons. Biores. Technol.http://dx.doi.org/10.1016/j.biortech.2011.02.055.

Koller, M., Salerno, A., Tuffner, P., Koinigg, M., B€ochzelt, H., Schober, S., Braunegg, G.,2012. Characteristics and potential of micro algal cultivation strategies: a review.J. Clean. Prod. 37, 377e388. http://dx.doi.org/10.1016/j.jclepro.2012.07.044.

Lam, M.K., Lee, K.T., 2012. Microalgae biofuels: a critical review of issues, problemsand the way forward. Biotechnol. Adv. 30 (3), 673e690. http://dx.doi.org/10.1016/j.biotechadv.2011.11.008.

Lam, M.K., Lee, K.T., Mohamed, A.R., 2012. Current status and challenges onmicroalgae-based carbon capture. Int. J. Greenh. Gas Control 10, 456e469.http://dx.doi.org/10.1016/j.ijggc.2012.07.010.

Lardon, L., H�elias, A., Sialve, B., Steyer, J.P., Bernard, O., 2009. Life-cycle assessment ofbiodiesel production from microalgae. Environ. Sci. Technol. 43 (17),6475e6481. http://dx.doi.org/10.1021/es900705j. American Chemical Society.

Liu, J., Ma, X., 2009. The analysis on energy and environmental impacts ofmicroalgae-based fuel methanol in China. Energy Policy 37 (4), 1479e1488.

Liu, X., Clarens, A.F., Colosi, L.M., 2011. Algae biodiesel has potential despiteinconclusive results to date. Bioresour. Technol. http://dx.doi.org/10.1016/j.biortech.2011.10.077.

Mata, T.M., Martins, A.A., Caetano, N.S., 2010. Microalgae for biodiesel productionand other applications: a review. Renew. Sustain. Energy Rev. 14, 217e232.

Norsker, N.H., Barbosa, M.J., Vermu€e, M.H., Wijffels, R.H., 2011. Microalgal produc-tion e a close look at the economics. Biotechnol. Adv. 29 (1), 24e27. http://dx.doi.org/10.1016/j.biotechadv.2010.08.005.

ion from microalgae biomass: carbon footprint and energy balance,014.07.038

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e88

Olguín, E.J., 2012. Dual purpose microalgae-bacteria-based systems that treatwastewater and produce biodiesel and chemical products within a biorefinery.Biotechnol. Adv. 30 (5), 1031e1046. http://dx.doi.org/10.1016/j.biotechadv.2012.05.001.

Packer, M., 2009. Algal capture of carbon dioxide: biomass generation as a tool forgreenhouse gas mitigation with reference to New Zealand energy strategy andpolicy. Energy Pol. 37 (9), 3428e3437. http://dx.doi.org/10.1016/j.enpol.2008.12.025.

Park, J.B.K., Craggs, R.J., Shilton, A.N., 2011. Wastewater treatment high rate algalponds for biofuel production. Bioresour. Technol. 102 (1), 35e42. http://dx.doi.org/10.1016/j.biortech.2010.06.158.

Passell, H., Dhaliwal, H., Reno, M., et al., 2013. Algae biodiesel life cycle assessmentusing current commercial data. J. Environ. Manag. 129, 103e111. http://dx.doi.org/10.1016/j.jenvman.2013.06.055.

Pate, R., Klise, G., Wu, B., 2011. Resource demand implications for US algae biofuelsproduction scale-up. Appl. Energy 88 (10), 3377e3388. http://dx.doi.org/10.1016/j.apenergy.2011.04.023.

Perelo, L.W., Sousa, L.L., Hora, D.S., 2012. Crescimento da microalga Nannochloropsissp. em �agua salina do semi-�arido com adiç~ao de esgoto domestico como fontede nutrientes. II Congresso Baiano de Engenharia Sanit�aria e Ambiental, Feira deSantana e BA, Brazil.

P�erez-L�opez, P., Gonz�alez-García, S., Ulloa, R.G., Sineiro, J., Feijoo, G., Moreira, M.T.,2013a. Life cycle assessment of the production of bioactive compounds fromTetraselmis suecica at pilot scale. J. Clean. Prod., 1e9. http://dx.doi.org/10.1016/j.jclepro.2013.07.028.

P�erez-L�opez, P., Gonz�alez-García, S., Jeffryes, C., Agathos, S.N., McHugh, E., Walsh, D.,Moreira, M.T., 2013b. Life cycle assessment of the production of the red anti-oxidant carotenoid astaxanthin by microalgae: from lab to pilot scale. J. Clean.Prod. http://dx.doi.org/10.1016/j.jclepro.2013.07.011.

Pittman, J.K., Dean, A.P., Osundeko, O., 2011. The potential of sustainable algalbiofuel production using wastewater resources. Biores. Technol. 102 (1), 17e25.http://dx.doi.org/10.1016/j.biortech.2010.06.035.

Quinn, J.C., Smith, T.G., Downes, C.M., et al., 2013. Microalgae to biofuels lifecycleassessment d Multiple pathway evaluation. Algal Res., 1e7. http://dx.doi.org/10.1016/j.algal.2013.11.002.

Quinn, J., Winter, L., Bradley, T., 2011. Microalgae bulk growth model with appli-cation to industrial scale systems. Biores. Technol. 102 (8), 5083e5092. http://dx.doi.org/10.1016/j.biortech.2011.01.019.

Rawat, I., Ranjith, R.K., Mutanda, T., Bux, F., 2011. Dual role of microalgae: phycor-emediation of domestic wastewater and biomass production for sustainablebiofuels production. Appl. Energy 88 (10), 3411e3424. http://dx.doi.org/10.1016/j.apenergy.2010.11.025.

Razon, L.F., Tan, R.R., 2011. Net energy analysis of the production of biodiesel andbiogas from the microalgae: Haematococcus pluvialis and Nannochloropsis. Appl.Energy 88 (10), 3507e3514.

Rickman, M., Pellegrino, J., Hock, J., et al., 2013. Life-cycle and techno-economicanalysis of utility-connected algae systems. Algal Res. 2 (1), 59e65. http://dx.doi.org/10.1016/j.algal.2012.11.003.

Rogers, J.N., Rosenberg, J.N., Guzman, B.J., et al., 2013. A critical analysis ofpaddlewheel-driven raceway ponds for algal biofuel production at commercialscales. Algal Res. http://dx.doi.org/10.1016/j.algal.2013.11.007.

Please cite this article in press as: Medeiros, D.L., et al., Energy productJournal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2

Sander, K., Murthy, G.S., 2010. Life cycle analysis of algae biodiesel. Int. J. Life CycleAss. 15, 704e714. http://dx.doi.org/10.1007/s11367-010-0194-1.

Scott, S.A., Davey, M.P., Dennis, J.S., et al., 2010. Biodiesel from algae: challenges andprospects. Curr. Opin. Biotechnol. 21 (3), 277e286. http://dx.doi.org/10.1016/j.copbio.2010.03.005.

Sforza, E., Bertucco, A., Morosinotto, T., Giacometti, G.M., 2011. Photobioreactors formicroalgal growth and oil production with Nannochloropsis salina: from lab-scale experiments to large-scale design. n. December Chem. Eng. Res. Des.,1e8. http://dx.doi.org/10.1016/j.cherd.2011.12.002. Institution of ChemicalEngineers.

Sheehan, J., Dunahay, T., Benemann, J., Roessler, P., 1998. A Look Back at the U.S.Department of Energy’s Aquatic Species ProgramdBiodiesel from Algae. Na-tional Renewable Energy Laboratory (NREL). Available at: http://www1.eere.energy.gov/biomass/pdfs/biodiesel_from_algae.pdf.

Singh, A., Olsen, S.I., 2011. A critical review of biochemical conversion, sustainabilityand life cycle assessment of algal biofuels. Appl. Energy. http://dx.doi.org/10.1016/j.apenergy.2010.12.012.

Stephenson, A.L., Kazamia, E., Dennis, J.S., et al., 2010. Life-cycle assessment ofpotential algal biodiesel production in the United Kingdom: a comparison ofraceways and air-lift tubular bioreactors. Energy Fuels 24 (7), 4062e4077.http://dx.doi.org/10.1021/ef1003123.

U.S. DOE, 2010. National Algal Biofuels Technology Roadmap. U.S. Department ofEnergy, Office of Energy Efficiency and Renewable Energy, Biomass Program.Available at: http://biomass.energy.gov.

Udom, I., Zaribaf, B.H., Halfhide, T., et al., 2013. Harvesting microalgae grown onwastewater. Bioresour. Technol. 139, 101e106. http://dx.doi.org/10.1016/j.biortech.2013.04.002.

Uduman, N., Qi, Y., Danquah, M.K., Forde, G.M., Hoadley, A., 2010. Dewatering ofmicroalgal cultures: a major bottleneck to algae-based fuels. Renew. Sustain.Energy 2, 012701. http://dx.doi.org/10.1063/1.3294480.

Um, B.H., Kim, Y.S., 2009. Review: a chance for Korea to advance algal-biodieseltechnology. J. Ind. Eng. Chem. 15 (1), 1e7. http://dx.doi.org/10.1016/j.jiec.2008.08.002.

Weschler, M.K., Barr, W.J., Harper, W.F., et al., 2014. Process energy comparison forthe production and harvesting of algal biomass as a biofuel feedstock. Bioresour.Technol. 153, 108e115. http://dx.doi.org/10.1016/j.biortech.2013.11.008.

Yang, J., Xu, M., Zhang, X., et al., 2011. Life cycle analysis on biodiesel productionfrom microalgae: water footprint and nutrients balance. Bioresour. Technol.http://dx.doi.org/10.1016/j.biortech.2010.07.017.

Yoo, C., Jun, S.Y., Lee, J.Y., Ahn, C.Y., Oh, H.M., 2010. Selection of microalgae for lipidproduction under high levels carbon dioxide. Bioresour. Technol. 101 (1),S71eS74. http://dx.doi.org/10.1016/j.biortech.2009.03.030.

Zah, R., B€oni, H., Gauch, M., Hischier, R., Lehmann, M., W€ager, P., 2009. Life CycleAssessment of Energy Products: Environmental Impact Assessment of Biofuels.Executive Summary. Empa, Technology and Society Lab, Lerchenfeldstrasse 5,CH-9014 St. Gallen, Switzerland.

Zhang, Y., Colosi, L.M., 2013. Practical ambiguities during calculation of energy ra-tios and their impacts on life cycle assessment calculations. Energy Policy 57,630e633. http://dx.doi.org/10.1016/j.enpol.2013.02.039.

ion from microalgae biomass: carbon footprint and energy balance,014.07.038