Bioresource Technology 194 (2015) 21–27

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Reducing the life cycle GHG emissions of microalgal biodiesel through

integration with ethanol production system
Henrique Leonardo Maranduba a,⇑, Sabine Robra a, Iracema Andrade Nascimento b, Rosenira Serpa da Cruz a,
Luciano Brito Rodrigues c, José Adolfo de Almeida Neto a
a
State University of Santa Cruz, Campus Soane Nazaré de Andrade, Rodovia Jorge Amado, km 16, CEP 45662900 Salobrinho, Ilhéus, Bahia, Brazil
b
Institute of Biology, Federal University of Bahia, Campus Ondina, Rua Barão de Geremoabo, 147, CEP 40170290 Ondina, Bahia, Brazil
c
State University of Bahia Southwest, Campus Itapetinga, Praça Primavera, 40, CEP 45700000 Primavera, Itapetinga, Bahia, Brazil

h i g h l i g h t s

 Microalgal biodiesel is environmentally unfeasible, as an isolated production process.

 Algal digested cake as nutritional input does not ensure the feasibility of biodiesel production.
 The use of ethanol co-products improves the carbon footprint of microalgal biodiesel.

a r t i c l e i n f o a b s t r a c t

Article history: Despite environmental benefits of algal-biofuels, the energy-intensive systems for producing
Received 1 May 2015 microalgae-feedstock may result in high GHG emissions. Trying to overcome energy-costs, this research
Received in revised form 21 June 2015 analyzed the biodiesel production system via dry-route, based on Chlorella vulgaris cultivated in race-
Accepted 22 June 2015
ways, by comparing the GHG-footprints of diverse microalgae-biodiesel scenarios. These involved: the
Available online 2 July 2015
single system of biomass production (C0); the application of pyrolysis on the residual microalgal biomass
(cake) from the oil extraction process (C1); the same as C0, with anaerobic cake co-digested with cattle
Keywords:
manure (C2); the same conditions as in C1 and C2, by integrating in both cases (respectively C3 and C4),
Biofuels
Nutrient recycling
the microalgae cultivation with an autonomous ethanol distillery. The reduction of GHG emissions in sce-
Carbon footprint narios with no such integration (C1 and C2), compared to CO, was insignificant (0.53% and 4.67%, respec-
Integrated biorefineries tively), whereas in the scenarios with integration with ethanol production system, the improvements
were 53.57% for C3 and 63.84% for C4.
Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction by governmental incentives via mandatory blends with

The expansion of biodiesel production from land crops may
result in negative environmental impacts, not only on biodiversity,
but also due to land use changes, which in turn can promote the
release of nitrogen and CO2 from the organic carbon stored in bio-
mass and soils. These represent additional greenhouse gas (GHG)
emissions, which can counteract the potential benefits of biofuels
in mitigating those emissions (Kim and Dale, 2011; Naik et al.,
2010). Furthermore, the increasing production of first generation
biofuels (i.e. biofuels produced from food commodities) stimulated
⇑ Corresponding author at: Grupo Bioenergia e Meio Ambiente (BioMA), Univer-
sidade Estadual de Santa Cruz (UESC), Campus Soane Nazaré de Andrade, Rodovia
Jorge Amado, km 16, CEP 45662900 Salobrinho, Ilhéus, Bahia, Brazil. Tel.: +55 73
3680 5274.
E-mail address: henrique.leo@gmail.com (H.L. Maranduba).
petroleum-based fuels, extends the dispute ‘‘arable areas to pro-
duce fuels or food?’’. Therefore, major efforts for the production
of biofuels from oleaginous microorganisms are undertaken, which
may avoid such limitations (Naik et al., 2010).
Microalgae appear as potential feedstock for biofuels produc-
tion, due to their higher productivity, and higher carbon capture
and sequestration (CCS), when compared to terrestrial crops
(Delrue et al., 2012; Moncada et al., 2014; Nascimento et al.,
2015, 2014). The cultivation of algal biomass does not compete
for arable land with other cultures, in particular, food production
(Naik et al., 2010). Furthermore, algae can be cultivated in a wide
range of aquatic environments such as fresh water, salt water, or
wastewater with high organic loads (Mata et al., 2010).
Although the harvesting and transportation costs of the inputs
and products may be lower if derived from integrated algal

http://dx.doi.org/10.1016/j.biortech.2015.06.113
0960-8524/Ó 2015 Elsevier Ltd. All rights reserved.
22 H.L. Maranduba et al. / Bioresource Technology 194 (2015) 21–27
biorefinery operations than those from terrestrial cultures (Souza
et al., 2015), at present, microalgae production systems are
energy-intensive, which may result in high GHG emissions, thus
reducing the otherwise favorable aspects of algal biofuels (Lardon
et al., 2009; Mata et al., 2010; Singh and Olsen, 2011).
Additionally, the costs of the CO2 supply during cultivation can
amount up to 50% of the overall costs, which may turn algal biodie-
sel more expensive than petroleum-based diesel (Cheng et al.,
2009). Such economic considerations are fomenting the search
for alternative and cheaper materials and processes with sufficient
availability to produce algae-based biodiesel in a more economical
way (Marques et al., 2013; Nascimento et al., 2014; Osundeko and
Pittman, 2014).
The ‘‘Integrated biorefineries’’ concept may be considered as a
way to overcome the above mentioned limitations and to ensure
the viability of large scale microalgal biodiesel production
(Adesanya et al., 2014; Alam et al., 2012; Slade and Bauen, 2013).
This integrated approach aims to develop an industry capable of
converting a wide range of waste and biomass feedstock into bio-
fuels, bioenergy and bioproducts. Integrated production intends to
optimize the inputs and outputs of materials and energy, and also
to reduce the environmental impacts and production costs
(Cabanelas et al., 2013b; Lohrey and Kochergin, 2012; Uggetti
et al., 2014).
The integrated use of co-products from the sugarcane industry,
including CO2, bagasse, straw, electricity, etc., increases the supply
of suitable feedstock for production of microalgal biodiesel
(Martines-filho et al., 2006; Szymanski et al., 2010). In Brazil, for
instance, the growing sugarcane ethanol production resulted in
increased amounts of stillage, the main co-product of this industry.
The environmentally friendly disposal of stillage is difficult, not
only because of its large quantities, but mainly due to its high pol-
lution potential (Cortez, 2010; Szymanski et al., 2010). Depending
on the process, the composition of stillage can vary, but it contains
considerable amounts of potassium, calcium, nitrogen, phospho-
rus, sulfate, as well as organic matter (COD, between 20,000 and
35,000 mg L 1), with pH ranging between 3.7 and 5. Due to these
characteristics, the stillage is mainly used for irrigation of sugar-
cane cultures.
However, the use of this technique requires care, because
the excessive application of stillage can contaminate ground-
water and surface waters, and can lead to changes in the
physical–chemical properties of the soil (Cortez, 2010;
Szymanski et al., 2010). Anaerobic digestion of stillage in
sealed systems, however, improves the fertilizer properties of
the effluent and makes energy production through methane
recovery possible (Moraes et al., 2014; Szymanski et al.,
2010), thus contributing to reduce the GHG footprint of algae,
as biodiesel feedstock.
Thus, a systemic analysis of the potentials of the sugarcane
industry and the production of biodiesel from algae points to a pos-
itive synergistic integration of these production systems, with
effects on the economic and environmental performances of the
respective life cycles of products (Cheng et al., 2009; Lohrey and
Kochergin, 2012; Marques et al., 2013; Nascimento et al., 2015;
Souza et al., 2015). These results, however, are recent and applied
to specific conditions, which must be extended to more diverse
scenarios.
This study analyzed a biodiesel produced by dry route, based on
the microalgae Chlorella vulgaris cultivated in raceways (Xu et al.,
2011), including two technological alternatives for the reuse of
energy from residual biomass (cake): pyrolysis (Xu et al., 2011),
and anaerobic co-digestion with cattle manure (Collet et al.,
2011; Uggetti et al., 2014) and its integrated production with a
sugarcane ethanol distillery.
2. Methods
The methodological principles of Life Cycle Assessment (ISO
14040, 2006; ISO 14044, 2006) scenarios and inventory data were
used in the present work to analyze the energy and material flows,
and to calculate the carbon footprints (IPCC 100 years) of microal-
gal biodiesel, integrated or not with the sugarcane ethanol produc-
tion (autonomous distillery). Thus, this study was focused on the
direct and indirect GHG emissions, addressing the impact category
‘‘Global Warming Potential’’ (GWP). The ‘‘cradle to gate’’ approach
was chosen, starting with the microalgae cultivation and ending
with the biodiesel production.
The GHG emissions of microalgal biodiesel were used to assess
the environmental performances of two technological alternatives
for the reuse of energy. The first one used residual biomass (pyrol-
ysis and anaerobic co- digestion), while the other considered the
synergetic aspects of biodiesel production from microalgae, inte-
grated with a sugarcane ethanol distillery.
2.1. Process description
Both production systems (ethanol and biodiesel) were assumed
to be on a large scale. Data for ethanol production were derived
from Ecoinvent 2.2 (Cultivation Area: 20,223 ha y 1. Ethanol pro-
duction: 90,000 t y 1). Data for biodiesel production were derived
from the system described by Xu et al. (2011) (Cultivation Area:
100 ha y 1. Biodiesel production: 2081 t y 1).
All scenarios for biodiesel production were modeled based on
the system proposed by Xu et al. (2011), via ‘‘dry route’’. The fol-
lowing stages were considered: cultivation of microalgae C. vul-
garis in open ponds (raceways), harvesting via flocculation,
drying (centrifugation, mechanical and thermal drying), solvent
oil extraction (95% of the total oil content). Biodiesel production
was performed by homogeneous base-catalyzed transesterifica-
tion, similar to soybean biodiesel production (Sheehan et al.,
1998; Souza et al., 2015).
According to literature, the green microalgae C. vulgaris is one of
the most studied microalgae species with potential as biodiesel
feedstock (Cabanelas et al., 2013a; Nascimento et al., 2015; Xu
et al., 2011). C. vulgaris strains, which have higher growth rates
and biomass production compared to other microalgae species cul-
tivated under the same period of time and conditions, generally
increase the average lipid concentration (19–23%) in biomass during
the exponential growth phase by 2–3 times during the stationary
phase, when the quantity of triacylglycerols (precursors of biodie-
sel) in lipids also reach their highest values (Chisti, 2007; Gong
and Jiang, 2011; Nascimento et al., 2015). In this study, the assumed
oil content of C. vulgaris was 46% (Scott et al., 2010) referring to the
oil content at the end of the cultivation period (based on Xu et al.,
2011), when the microalgae are subjected to stressful conditions
by nutrient depression (Scott et al., 2010; Xu et al., 2011).
The lipid content, extracted from the dry biomass of this species
reached a maximum productivity of 62 mg L 1 day 1, which may
support a biodiesel production of 42–46 L ha 1 day 1
(Nascimento et al., 2015). It is important to refer to a data from
Gong and Jiang (2011), indicating that oleaginous strains are suit-
able for biodiesel production with no less than 20% (w/w) lipid
content and 40 mg L 1 day 1 lipid productivity (Gong and Jiang,
2011; Nascimento et al., 2015).
Five scenarios were proposed in order to assess the impacts on
GHG emissions of biodiesel from microalgae, by considering differ-
ent technological routes for the energetic recycling of the residual
biomass (cake) and the integration with an autonomous sugarcane
ethanol distillery (Fig. 1):
 H.L. Maranduba et al. / Bioresource Technology 194 (2015) 21–27 23

Electricity
Emissions to air

Heat
- Carbon dioxide (CO2);
Biogas - Methane (CH4);

SUGARCANE
ETHANOL DISTILLERY Stillage
Manure transportation service
in natura CATTLE
MANURE Hydraulic loader and spreader
PRODUCTION
Electricity
- Cogeneration;
Heat Emissions to air
ANAEROBIC - Ammonia (NH3);
Cattle manure
Electricity DIGESTION - Dinitrogen monoxide (N2O);
- Cogeneration; Cattle manure - Methane (CH4);
- Nitric oxide (NO);
- Nitrogen (N);
Fresh water
Stillage biodigested Substrate biodigested Biogas
ANAEROBIC
Fertilizer transportation service DIGESTION
Emissions to air
Urea (N) - Carbon dioxide (CO2);
CULTIVATION - Methane (CH4);
Triple superphosphate (P) Biochar
with water recycling
Potassium nitrate (K)
CO2 (liquid or from distillery)
Electricity (network supply or distillery) Wastewater PYROLYSIS Pyrolysis oil
- Paddle wheel; Biomass and water
- Water pumping;
- CO2 pumping
- Wastewater pumping; Cake
- Sand filter;
Synthetic flocculant Pyrolysis gas
HARVESTING
Lime Wastewater Cake
by flocculation
Electricity (network supply or distillery)
- Biomass and water pumping; Wet Biomass
DRYING TRANS-
Heat OIL BIODIESEL
by centrifugation, ESTERIFICATION
mechanical drying
EXTRACTION
Electricity (network supply or distillery) by homogeneous
Dry Biomass by hexane Oil Glycerine
- Centrifuge; and thermal drying base-catalyzed
- Mechanical dryer

- Sodium methoxide;
- Sodium hydroxide;

- Hydrochloric acid;
Hexane

Heat

Heat
Electricity

Electricity

Chemicals
- Methanol;
INTEGRATED
LEGEND:
PROCESS UNIT
BIOREFINERY INPUT INTERMEDIATE OUTPUT Direct emissions

Permanent flow between process units [occurs in all scenarios] Conditional flow between process units [only occurs in some scenarios]

Output flow (product, byproduct and emissions)

Fig. 1. Flowchart of the systems considered in this study, including external biorefinery (sugarcane ethanol distillery), unit processes, material and energy flows.

 Scenario C0: baseline scenario. Certain changes, such as the phosphorus and potassium. An average fugitive loss of 3% of
reuse of 84% of the entire system’s wastewater (Yang et al., biogas was assumed (Efferbenger et al., 2009). (Co-)products:
2011), and data adjustments according to the Brazilian condi- biodiesel (1 t), glycerin (0.05 t), and biogas with 70% CH4 and
tions (energy matrix and transport distances) were made to 30% CO2 (0.01 t).
the ‘‘dry route’’ proposed by Xu et al. (2011):  Scenario C3: scenario C1 + integration with an ethanol dis-
tillery. For purposes of modeling, the microalgae cultivation,
(i) Microalgae C. vulgaris with 46 wt% DW of oil content, cul- harvesting, drying and oil extraction were considered as occur-
tivated in raceways (0.03 wt% DW). ring near the ethanol distillery, also the distance between the
(ii) Harvesting of the wet microalgal biomass using synthetic microalgae oil extraction and the biodiesel transesterification
flocculant (1.6 wt% DW). refinery was not considered. The following co-products from
(iii) Drying of the wet microalgal biomass in three steps: cen- the distillery were assumed as inputs: CO2 (from bagasse com-
trifuge (16 wt% DW), mechanical (50 wt% DW) and ther- bustion and juice fermentation), stillage, and electricity from
mal (85 wt% DW). cogeneration. (Co-)products: biodiesel (1 t), glycerin (0.05 t),
(iv) Oil extraction of the dry biomass (yield of 95%). and pyrolysis oil (0.8 t).
(v) Transesterification of the extracted oil by base-catalyzed  Scenario C4: scenario C2 + integration with an ethanol distillery.
homogeneous route. The following co-products from the distillery were assumed as
inputs: CO2 (from bagasse combustion and juice fermentation),
In this scenario, processes for the possible energy recovery of stillage (already stabilized by anaerobic co-digestion), and elec-
the cake were not considered. (Co-)products: biodiesel (1 t), glyc- tricity from cogeneration. (Co-)products: biodiesel (1 t), glycerin
erin (0.05 t) and cake (1.35 t). (0.05 t), and biogas with 70% CH4 and 30% CO2 (0.01 t).

 Scenario C1: scenario C0 + pyrolysis of the residual biomass

(cake) from the oil extraction process. The pyrolysis process The method used for the allocation of the burdens among the
was assumed to be ‘‘energetically self-sufficient’’ by the ener- products and co-products of each scenario was based on energy.
getic use of co-products such as biochar and pyrolysis gas (the The relations between the distillery co-products and the inputs
environmental burdens of the conversion were not considered). for microalgae cultivation were established based on mass and
(Co)-products: biodiesel (1 t), glycerin (0.05 t), and pyrolysis oil energy flows. The inventory data were derived from secondary
(0.8 t). sources, such as literature and LCA databases, for instance,
 Scenario C2: scenario C0 + anaerobic co-digestion of residual Ecoinvent 2.2. Calculations were performed using mass and energy
biomass from the oil extraction process, with cattle manure balances of the processes, organized in spreadsheets. The modeling
(for more details about the inputs/outputs inventory, see system and calculations, including the uncertainty analysis by
Supplementary materials), using the anaerobic co-digestion Monte Carlo simulation, were conducted with the proprietary
effluent (substrate biodigested) as source of nitrogen, software SimaPro 8.0Ó (Pré Consultants).
24 H.L. Maranduba et al. / Bioresource Technology 194 (2015) 21–27

Table 1
Inputs/outputs inventory from scenarios C0, C1, C2, C3 and C4, for the production of 1 t of microalgae biodiesel.

Process Input Amount (by scenarios)

C0 C1 C2 C3 C4
Cultivation Fresh water (t)a,b 1182.90 1104.12
Recycled fresh water (t)a,b 6210.21
Water pump (kWh)b 387.07 382.95
Paddle wheel (kWh)b 0.018
CO2 (t)a 2.82
CO2 pump (kWh)b 62.51
Biodigested stillage (t)*,h – – – 83.81
Biodigested effluent (t) – – 1.42 – 1.42
Nitrogen (N) (t)d,h 0.11 0.05 0.06 –
Phosphorus (P) (t)d,h 0.02 0.01 0.02 –
Potassium (K) (t)d,h 0.02 0.01 – –
NPK transportation (tkm)e 22.95 9.38 12.64 –
Flocculation Substrate pump (kWh)c 387.07
Lime (t)d 2.22
Synthetic flocculant (t)d 0.0037
Drying Centrifuge (kWh)c 78.28
Mechanical dryer (kWh)c 144.16
Thermal dryer (MJ)c 4805.4
Water recycling Pump (kwh)c 546.06
Sand filter (kWh)f 208.60
Oil extraction Electricity (kWh)c 161.46
Heat (MJ)c 1826.05
Hexane (t)c 0.0058
Trans-esterification Electricity (kWh)g 102.90
Heat (MJ)g 1837.46
Methanol (t)g 0.0900
Sodium hydroxide (t)g 0.0023
Sodium methoxide (t)g 0.0244
Hydrochloric acid (t)g 0.0077
Pyrolysis Electricity (kWh)c – 259.68 – 259.68 –
Heat (MJ)c – 4099 – 4099 –
Anaerobic co-digestion Cattle manureh – – 0.07 – 0.07
Electricity (kWh)a – – 7.29 – 7.29
Heat (MJ)a – – 45.99 – 45.99

(Co) products Amount (by scenarios)

C0 C1 C2 C3 C4
g
Biodiesel (t) 1.00
Glycerin (t)g 0.05
Residual biomass (cake) (t)c 1.35 – – – –
Pyrolysis oil (t)c – 0.80 – 0.80 –
Biogas (t)a – – 0.01 – 0.01
*
The environmental impacts of the anaerobic co-digestion of stillage were incorporated in the cultivation process (the infrastructure was not considered).
a
Collet et al. (2011).
b
Yang et al. (2011).
c
Steele et al. (2012).
d
Lardon et al. (2009).
e
Calculated (the distances of 67.00 km (nitrogen), 386.00 km (phosphorus) and 323.00 km (potassium) are equivalent to the distances to be covered, assuming that the
location of the integrated production is the Recôncavo Region, in the State of Bahia).
f
Calculated. Sand filter similar to those used in pools: 120 W and 3 m3 h 1.
g
Sheehan et al. (1998).
h
Szymanski et al. (2010).

The inventory data of inputs and outputs, processed and nor-
malized to the functional unit of 1.0 t of microalgal biodiesel, are
shown in Table 1. The Ecoinvent processes used in the modeling
for each input can be found in Supplementary materials.
3. Results and discussion
The results confirm the potential synergy between the two bio-
fuel production systems in the improvement of the microalgal bio-
diesel carbon footprint. The contributions of the co-products to
reduce the GHG emissions of the biodiesel for each proposed sce-
nario are shown in Fig. 2.
According to the functional unit (1 t of microalgal biodiesel), the
C0 (baseline scenario) showed the highest GHG emissions among
the proposed scenarios (5.12 t CO2-eq/t biodiesel). However, the
scenarios C1 and C2, with no integration, showed values very close
to the baseline. The C1 and C2 scenarios presented GHG emissions
of 5.10 and 4.88 t CO2-eq/t biodiesel, respectively.
The three scenarios (C0, C1 and C2) presented very similar
emissions by process unit. The cultivation process showed an aver-
age contribution to the total GHG emissions of about 45.81%. The
harvesting/flocculation, drying, oil extraction and transesterifica-
tion processes contributed with an average of 36.57%, 7.7%,
1.94%, and 7.66%, respectively, to the GHG emissions. The
 H.L. Maranduba et al. / Bioresource Technology 194 (2015) 21–27
contribution of the pyrolysis process (C1) and anaerobic
co-digestion (C2) to the GHG emissions were 0.95% and 0.04%,
respectively.
The scenarios C3 and C4, which proposed the integration with
the ethanol distillery, showed expressive reductions in the GHG
emissions (2.38 and 1.85 t CO2-eq/t biodiesel, respectively), com-
pared to the scenarios without integration. Compared to the base-
line scenario (C0), this reduction signifies an improvement, of
53.57% for C3 and 63.84% for C4. Regarding the contributions of
the process units, the results differed from the scenarios C0, C1
and C2. The cultivation process showed negative GHG emissions
of 0.36 and 0.83 t CO2-eq/t biodiesel for C3 and C4, respectively,
due to the use of the distillery co-products (CO2, stillage and
cogenerated electricity) and the internal recycling of the microal-
gal cake to replace the mineral fertilizers in the system itself.
These negative GHG emissions were considered ‘‘credits’’ for
the system in C3 and C4, for reducing the GHG emissions of the
biodiesel product.
The unit processes harvesting, drying, oil extraction, and trans-
esterification contributed to the GHG emissions with 77.36%,
16.28%, 4.10% and 15.16%, respectively, for C3; and 99.33%,
20.90%, 5.26%, and 19.46%, respectively, for C4.
The contribution of the Pyrolysis unit process in C3 was 2.03% of
the total GHG emissions from the system, while the contribution of
Anaerobic Co-digestion in C4 was only 0.10%.
However, it is also important to consider the GHG emission per
unit of energy output from product (biodiesel) and co-products
(glycerin, cake, pyrolysis oil and biogas), since the principal objec-
tive of the biodiesel system is to produce an energy carrier. Table 2
compares the GHG emissions of the five scenarios calculated per
unit of mass (functional unit) and energy output (GJ).
As shown in Table 2, the GHG emissions per ton of biodiesel
were lowest in C4, followed by C3. The baseline scenario C0 was
the least favorable, followed closely by C1 and C2.
The baseline scenario obtained the best energy output per func-
tional unit (69.75 GJ), while the scenarios C1/C3 and C2/C4 pre-
sented 51.60 GJ and 38.91 GJ, respectively. Per unit of energy
output, the GHG emissions of C0 were improved compared to C1
and C2. Similarly, the pyrolysis scenarios (C1 and C3) improved
compared to the anaerobic digestion scenarios (C2 and C4).
Taking into consideration the energy contained in the biodiesel,
i.e. the emissions by GJ of biodiesel, C0 improved by 4.92%, while
C1 improved by 4.51%, compared to C2, per unit of mass, resulting
in the same t CO2-eq emissions per GJ biodiesel for the three sce-
narios. The integration approach resulted in an improvement of
8.60% for C3 compared to C4 per unit of mass.
Considering the energy from co-products (GJ of bioenergy), the
improvements of C0 and C1 compared to C2 and C3 in relation to
C4
C3
C2
C1
C0
-2.00 -1.00 0.00 1.00 2.00 3.00 4.00 5.00 6.00
t CO2-eq
Cultivation Harvesting/Flocculation Drying
Oil Extraction Transesterification Pyrolysis
Anaerobic Digestion
Fig. 2. Comparison of GHG emissions, distributed by process unit (t CO2-eq/t of
microalgal biodiesel), for the five production scenarios (C0, C1, C2, C3 and C4).
25
C4 are more prominent. Including the energy from the cake, C0
improved by 43.38% while C1 improved by 27.59%, compared to
C2 per unit of mass. Under this perspective, C2 becomes the least
favorable scenario, followed by C1 and C0. Considering the
co-products, C3 and C4 are equal in emissions in respect to GJ of
bioenergy.
Although the baseline scenario C0 is the best in energy produc-
tion, it is the worst in cumulative energy demand (CED) per ton of
biodiesel (86.67 GJ), followed by C1 (85.31 GJ), C2 (82.05 GJ), C3
(49.88 GJ) and C4 (45.64 GJ). This is due to the energy balance
and the correlation existent between CED and GHG emission. The
GHG emissions from the produced bioenergy raise C0 from the
worst scenario to the best in the scenarios without integration.
Still, in terms of GHG emissions this scenario is less favorable than
the scenarios C3 and C4, which consider the integration of microal-
gae biodiesel production with a sugarcane ethanol production
system.
These results highlight the importance of the co-products for
the viability of microalgal biodiesel on large scale. On other hand,
the results indicated no differences between pyrolysis and anaero-
bic co-digestion, in terms of GHG emissions. However, the role of
anaerobic co-digestion in the recycling of the nutrients from
microalgal cake needs to be better studied, since this process
affects the demand of mineral fertilizers, and therefore can reduce
the impacts on other environmental categories.
The comparison of the results for GHG emissions for microalgal
biodiesel obtained in this study with the GHG emissions of com-
peting fuels (fossil diesel and first generation biodiesel) are shown
in Fig. 3.
Considering the GHG emissions, the results for the baseline sce-
nario (C0) were the least favorable, followed by C2 and C1. The
comparison of these results with others from competing fuels con-
firms the current unfeasibility of biodiesel from isolated microal-
gae cultivation as an alternative for the mitigation of greenhouse
gas emissions. The energetic recycling of the nutrients (nitrogen,
phosphorus and potassium) from the cake has improved the GHG
emissions of the microalgal biodiesel system, but not enough to
make it competitive with the first generation biodiesel. Also, the
differences among C0, C1, and C2 could not be confirmed as well,
according to Fig. 3.
The microalgal biodiesel production from the integrated scenar-
ios C3 and C4 resulted in GHG emissions in the range of rape and
soybean biofuels (Microalgae C3), and sunflower and palm biofuels
(Microalgae C4); the latter having the best environmental results
among the first generation biofuels.
According to literature, a large number of studies aim to assess
the microalgae biodiesel production integrated with other systems.
However, studies about the feasibility of microalgae biodiesel
co-produced in an integrated system with the sugarcane industry
are yet incipient. Cheng et al. (2009), evaluated the production of
microalgae biodiesel using sugar cane juice hydrolysate as carbon
source for the microalgae, in order to improve the oil yield and effi-
ciency of carbon conversion. Lohrey and Kochergin (2012)
Table 2
Comparison of GHG emissions from the scenarios C0, C1 C2, C3, and C4 calculated per
unit of mass (t CO2-eq/t biodiesel), per unit of energy from the biodiesel (t CO2-eq/GJ
biodiesel) and per unit of energy from the entire system, biodiesel and co-products, (t
CO2-eq/GJ bioenergy).
Scenarios Emissions by mass Emissions by Emissions by
(t CO2 eq/t of energy (t CO2 eq/GJ energy (t CO2 eq/GJ
biodiesel) biodiesel) bioenergy)
C0 5.12 0.13 0.08
C1 5.10 0.13 0.10
C2 4.88 0.13 0.12
C3 2.38 0.06 0.05
C4 1.85 0.05 0.05
26 H.L. Maranduba et al. / Bioresource Technology 194 (2015) 21–27
0.18
0.16
0.14
0.12
0.10
t CO2-eq / GJ
0.08
0.06
0.04
0.02
0.00
Microalgae C0
Soybean
Microalgae C4
Fig. 3. Comparison of the GHG emissions from biodiesel, on an energetic basis (t CO2-eq/GJ), from scenarios C0, C1, C2, C3, and C4, with other first generation biodiesel and
fossil diesel fuels. The variation coefficient from microalgal biodiesel was estimated with the software Simapro 8.0Ó, by combining the Matrix Pedigree and the Monte Carlo
Simulation (1000 runs; 95%).
investigated a proposal for the integration between microalgae
biodiesel and sugarcane production systems, focusing on the
improvement of the energy balance, using bagasse as feedstock
for heat and CO2 supply for microalgae cultivation. None of these
studies carried out a Life Cycle Inventory, which prevents a com-
parative analysis of GHG emissions with this study.
Souza et al. (2015) conducted a LCA of an integrated Brazilian
algae-sugarcane biorefinery with a similar framework. The results
of GHG emissions presented by Souza et al. (2015) were between
0.020 t CO2-eq/GJ (57% and 37% lower than C3 and C4, respec-
tively) and 0.037 t CO2-eq/GJ (33% lower than C3 and 24% higher
than C4). This substantial variation, well as the failure in consider-
ing the environmental impacts of CO2, the use of two allocations
simultaneously (energy for ethanol-electricity and mass for
biodiesel-cake) and the use of a portion of biodiesel for replacing
the onsite fossil diesel demand, prevent a fair comparison with
the integrated biodiesel evaluated in this work (Souza et al., 2015).
However, microalgal biodiesel has some advantages compared
to first generation biofuels based on terrestrial feedstock that need
to be considered. The problems of land use emissions, competition
for arable land and food production, do not apply to microalgal bio-
diesel. Thus, algae as biodiesel feedstock can be more advanta-
geous than the first generation feedstock, when the scope of
comparison is extended.
The results for the GHG emissions showed no significant differ-
ences between pyrolysis and anaerobic co-digestion of the cake. As
the cultivation stage was responsible for more than 35% of the
GHG emissions of the whole biodiesel production system, the anaer-
obic co-digestion scenario should be considered due to a higher rel-
ative reduction of non-renewable raw materials, when compared to
the pyrolysis scenario. The internal recycling of nutrients, such as
phosphorus, can result in a reduction of the demand of mineral fer-
tilizers, and therefore can affect other important impact categories,
such as abiotic depletion and cumulative energy demand. Therefore,
nutrient recycling in the cultivation of microalgae for biodiesel feed-
stock should be further investigated, in order to shed light on the
economic and environmental consequences of this alternative.
4. Conclusions
The higher GHG emissions from microalgal biodiesel generated
according to the baseline scenario (C0), in comparison with results
Microalgae C2 Microalgae C1 Rape
Microalgae C3 Waste oils and fats Sunflower
Palm Diesel
from competing fuels, confirm the current view about the unfeasi-
bility of biodiesel from isolated microalgae cultivation, as an alter-
native for the mitigation of greenhouse gases emissions.
The biorefinery approach, however, by integration with other
product systems, was shown to be a promising alternative to
improve the environmental feasibility of microalgal biodiesel on
large scale, through the reduction of the GHG emissions, if based
on the use of ethanol sugarcane co-products (CO2, stillage and elec-
tricity) as process inputs.
The results of pyrolysis and anaerobic co-digestion as pathways
for the reuse of microalgal biomass do not add any significant dif-
ference to this previous assumption. However, anaerobic
co-digestion and utilization of the effluent as fertilizer reduce the
demand of mineral fertilizers. Further studies are therefore neces-
sary to analyze other environmental categories, such as ‘‘depletion
of abiotic resources’’, mainly due to the phosphorus recovery.
Acknowledgements
The authors would like to express their thanks to the Brazilian
National Council of Technological and Scientific Development
(CNPq – Brazil) for the financial support (DTI-3) of the projects
CNPq 574712/2008-9 and 551134/2010-0, and for the granting of
master degree scholarship; the authors are also indebted to the
Bahia State Research Support Foundation (FAPESB – Brazil) for
the sponsorship of technical infrastructure, as well as the purchase
of the software licenses.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.biortech.2015.06.
113.
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