Science of the Total Environment 765 (2021) 142717

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

A spatially explicit assessment of sugarcane vinasse as a

sustainable by-product
Luz Selene Buller a,⁎, Cristhy Willy da Silva Romero b, Rubens Augusto Camargo Lamparelli c,
Samuel Fontenelle Ferreira a, Ana Paula Bortoleto d, Solange I. Mussatto e, Tânia Forster-Carneiro a
a
School of Food Engineering, University of Campinas (UNICAMP), Rua Monteiro Lobato, 80, 13083-862, Campinas, São Paulo, Brazil
b
School of Agricultural Engineering, University of Campinas (UNICAMP), Avenue Cândido Rondon, 501, 13083-875 Campinas, Sao Paulo, Brazil
c
Interdisciplinary Center of Energy Planning (NIPE), University of Campinas (UNICAMP), Rua Cora Coralina, 13083-896 Campinas, São Paulo, Brazil
d
School of Civil Engineering, Architecture and Urban Design, University of Campinas (UNICAMP), Rua Saturnino de Brito, 224, 13083-889 Campinas, São Paulo, Brazil
e
Department of Biotechnology and Biomedicine, Technical University of Denmark, Søltofts Plads, Building 223, 2800, Kongens Lyngby, Denmark

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Vinasse application in sugarcane crop is

limited by local environmental laws.
• Biodigested vinasse replaces 30% of
mineral nitrogen and 46% of phospho-
rous.
• GIS modeling is a powerful strategy to
apply vinasse in safe environmental
levels.
• Energy production and nutrient
recycling from vinasse contribute to
decarbonization.

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

Article history: This study evaluates the benefits of mineral fertilizers replacement for biodigested vinasse. Data from experimen-
Received 23 July 2020 tal anaerobic digestion (AD) of vinasse were applied to support the analysis. Based on previous experiments, this
Received in revised form 21 September 2020 assessment assumed that vinasse production could reach 2.38 × 107 m3/year generating around 66,585 MWh/
Accepted 25 September 2020
year of electric energy from biogas burning in the Administrative Region of Campinas (ARC). This amount of en-
Available online 7 October 2020
ergy could supply more than 103,000 inhabitants and avoid 35,892 tCO2eq/year (from electric energy replace-
Editor: Huu Hao Ngo ment). The biodigested vinasse might also reduce the total N, P, and K mineral fertilizers demand per hectare
of sugarcane crop in 30%, 1%, and 46%, respectively, avoiding additional greenhouse gas emissions of 111,877
Keywords: tCO2eq/year. There is no biodigested vinasse surplus for a moderate fertigation rate of 100 m3/ha, complying
Biogas with local environmental laws related to nutrients excess side effects in areas destined to sugarcane crop. Not-
Renewable energy withstanding, a Geographic Information System analysis for a small adjacent area to ARC indicated nine different
Biofertilizer fertigation rates, ranging from 50 to 100 m3/ha. Even though the general analysis for ARC shows high NPK re-
GHG mitigation placement levels, the fertigation practices should be subsidized for robust soil analysis and adequate to safe en-
Environmental conservation
vironmental levels. A management tool can be designed using the results here presented to subsidize
investments for AD widespread adoption by the sugarcane industry to catch a reasonable practice from the eco-
nomic and environmental perspectives.
© 2020 Elsevier B.V. All rights reserved.

Abbreviations: AD, anaerobic digestion; APBR, anaerobic packed-bed reactors; ARC, Administrative Region of Campinas; CO2, carbon dioxide; COD, chemical oxygen demand; GHG,
greenhouse gas; GIS, Geographic Information System; GWP, Global Warming Potential; IPCC, Intergovernmental Panel on Climate Change; K, potassium; N, nitrogen; N2O, nitrous
oxide; P, phosphorous; SDGs, Sustainable Development Goals; UASB, Upflow Anaerobic Sludge Blanket; UNFCC, United Nations Framework Convention on Climate Change; VFA, volatile
fatty acids.
⁎ Corresponding author.
E-mail address: selene@unicamp.br (L.S. Buller).

https://doi.org/10.1016/j.scitotenv.2020.142717
0048-9697/© 2020 Elsevier B.V. All rights reserved.
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al.
1. Introduction
Fossil-derived fuels have brought several environmental issues and
oil price fluctuation (Moraes et al., 2014; Ranjan et al., 2013; Srirangan
et al., 2012). Industrial and urban waste, and crop and agricultural by-
products require long-term management strategies to properly manage
and/or recycle (Palomar et al., 2019). In addition, residual biomass is an
abundant source for developing a renewable economy in the partial re-
placement of petroleum-based energy (Yamakawa et al., 2018). Still,
bioenergy production costs must be reduced to be competitive and
widespread (Bugge et al., 2016). Among the agro-industrial by-
products, vinasse generated during the ethanol distillation process
after the fermentation of sugarcane juice is especially interesting. En-
ergy recovery from the anaerobic digestion (AD) of vinasse can reduce
greenhouse gases (GHG) emissions and may produce positive impacts
on socioeconomic regional, and local levels (Dias et al., 2013; Ekman
et al., 2013; Moraes et al., 2014; Leme and Seabra, 2016; Fuess et al.,
2018a; da Silva Neto et al., 2020).
Brazil is the worldwide leader in sugarcane ethanol production, and
São Paulo State is the primary national producer. After the petroleum
crisis in the 1970s, some countries developed programs to increase
their energy autonomy (De Pretto et al., 2018; Soccol et al., 2005), and
Brazil fostered the ProAlcool Program. Through it, the ethanol industry
was supported by the development of automotive engines specially de-
signed for this fuel and by the establishment of a successful first-
generation sugarcane ethanol technology.
Vinasse is the main by-product of sugarcane ethanol, ranging from
12 to 20 L for 1 L of ethanol (Bonomi et al., 2012). The primary use of
vinasse is so far as soil fertilizer (Fuess et al., 2018b; Moraes et al.,
2014). However, there are limits for the soil's vinasse disposal, which
is regulated by the Environmental Protection Agency of São Paulo
State, according the organic compounds level presented (MAPA,
2009). Indiscriminate vinasse disposal may cause severe environmental
side-effects such as soil salinization, metal ion, and sulfates saturation
and, in general, nutrient leaching and percolation, among other undesir-
able damages (Fuess and Garcia, 2014; Christofoletti et al., 2013;
Madejón et al., 2001). AD can largely reduce the vinasse chemical oxy-
gen demand (COD), and the produced biogas can be converted into
electric and thermal energy (i.e., biogas burning in stationary engines)
or can be purified to biomethane (ANP, 2015; Leme and Seabra, 2016;
Awe et al., 2017). Biogas can be included in the Brazilian energy matrix
as a competitive alternative to natural gas for vehicle fuel, heating pur-
poses, and cooking, contributing to air quality improvement and health
promotion (Mulenga and Siziya, 2019).
AD technology allows the conversion of wastewater and solid resi-
dues with high organic matter into biofertilizer and biogas (composed
of 50 to 70% methane and 30 to 50% carbon dioxide) (Pokhrel and
Viraraghavan, 2004; Memon and Memon, 2020). Anoxic vertical biore-
actors, such as the Upflow Anaerobic Sludge Blanket (UASB), can be
used for AD with the advantage of requiring a smaller area when com-
pared to other technologies such as aerated and horizontal flow anaer-
obic lagoons. UASB can also work with high organic load and smaller
sludge production than conventional aerobic biological treatments
(Forster-Carneiro et al., 2012). New reactors arrangements aiming at
better technical performance are, however, in constant evolution
(Barros et al., 2017; Del Nery et al., 2018), as is the case of the Anaerobic
Packed-Bed Reactors (APBR) (Fuess et al., 2017a; Fuess and Zaiat, 2018).
AD of vinasse is relevant from the economic, energetic, and environ-
mental perspectives (Leme and Seabra, 2016; Parsaee et al., 2019; da
Silva Neto et al., 2020). Biogas has high heat content from the energy
side and can be used as fuel for electric energy generation or heat for
boilers in production processes. In Brazil, the National Electric Energy
Agency Resolution n.482 (ANEEL, 2015) allows decentralized energy
production encouraging the use of biogas as a source of electricity.
Moreover, increased dissemination of AD is expected after establishing
the National Biofuels Policy (RenovaBio), an initiative of the Brazilian
2
Science of the Total Environment 765 (2021) 142717
Ministry of Mines and Energy launched in December 2016 (MME,
2017) that supports the expansion of biofuel production based on envi-
ronmental, economic, and social sustainability.
Environmentally, biodigested vinasse is more advantageous for crop
fertilization then vinasse in natura because it contains nitrogen (N) in a
chemical form more easily absorbed by the plant. During the AD pro-
cess, the organic-N is converted into ammonia-N, which avoids such
transformation in the soil. This conversion can be a source of green-
house gas (GHG) emissions (Moraes et al., 2017). Nitrous oxide (N2O)
has a Global Warming Potential (GWP) 265 higher than carbon dioxide
(CO2) (IPCC, 2013). As a result of managed soils, N2O can be originated
from direct N applications for soil fertilization and from indirect emis-
sions related to soil organic matter contents associated to land-use
change and priming effect, which also depends on tillage/non-tillage
practices (Tubiello et al., 2015). Biodigested vinasse can supply more
N for sugarcane crop reducing mineral applications and, consequently,
N2O emissions. The proper vinasse fertigation rate, depending on soil
chemistry and previous land-use (which determine Nitrogen, Phospho-
rous, and Potassium (NPK) requirements), ranges from 60 to 250 m3/ha
(van Raij et al., 1996). Besides the issue related to N2O emissions, K's
particular excess in over-fertigated sugarcane soils requires attention.
Although sugarcane presents high K requirement as a quality aspect re-
lated to its final sugar content, excess of K is directly related to leaching
side-effects.
Despite there are various possibilities for different agro-industrial
AD arrangements and specific project requirements (depending on cli-
mate and substrate characterization among other features), biogas ver-
satility figures as a promising solution to the Brazilian biofuel industry
(da Silva Neto et al., 2020). AD is efficient in reducing the organic load
of vinasse, reaching more than 85% of reduction depending on the reac-
tor technology (Moraes et al., 2014). It also optimizes bioenergy recov-
ery from biogas, reaching over 30% of electric energy surplus, enhancing
both the environmental and economic aspects (Fuess et al., 2018b).
Moreover, AD technology might provide outstanding GHG mitigation,
close to 48%, when biodigested vinasse is applied before its storage
and transportation to soil disposal (Moraes et al., 2017), and as much
as 27% when biomethane replaces diesel in a given scenario recently
assessed by da Silva Neto et al. (2020).
Thorough AD, it is possible to generate electric energy from biogas
burning, as well as to mitigate GHG from both the fertilizer replacement
and the additional electric power, which can be inserted in the grid. This
study also presents a mineral NPK replacement route with thermophilic
biodigested vinasse, a biofertilizer that fulfills Brazilian sugarcane soil
characteristics and its nutrients disposal limits. This proposal can, spa-
tially explicitly, support the management of products that could cause
pollution into solutions, at local and regional levels, to improve the en-
vironmental and health quality. The present research is connected to
the Sustainable Development Goals (SDGs), which are intimately tied
to a sustainable and inclusive future for humanity. The current Covid-
19 crisis seriously exposed that time matters enormously to save lives,
and the same is valid for the environment. A sustainable development
strategy is mandatory worldwide to avoid unnecessary risks and fragil-
ities related to the massive environmental destruction and its related
decline in economic activity that accentuates the existing inequalities
(Sachs et al., 2020), especially in developing countries.
This article provides a critical analysis of vinasse disposal and en-
ergy/nutrients recycling, mainly to subsidize the current fertigation
practices to support safe environmental vinasse management in the
field. The article is structured as follows: (i) experimental sugarcane
vinasse thermophilic anaerobic digestion, (ii) biogas and biodigested
further applications, (iii) GHG mitigation from electric energy genera-
tion, (iv) sugarcane agronomic nutritional requirements and calculation
of fertigation rates, (v) sugarcane soil NPK replacement, (vi) GHG miti-
gation from soil emissions for in natura and biodigested vinasse, and
(vii) GIS modeling to assess NPK replacement and additional require-
ments for a typical ARC sugarcane soil.
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

2. Materials and methods

The research methodology used in this paper is summarized in Fig. 1.
2.1. Experimental reactor configuration
A lab-scale semi-continuous reactor (capacity of 4.3 L) was kept in
continuous operation for 58 days. The reactor was initially fed with
1.93 L of vinasse. Then, 50 mL of diluted vinasse sample (containing
65% of pure vinasse) was added every three days. Vinasse and inoculum
used for the experimental trial were obtained from an ethanol-
producing plant located at the Administrative Region of Campinas
(ARC) in the State of São Paulo, Brazil. Physicochemical analysis of the
substrates was done according to the Standard Methods for the Exami-
nation of Water and Wastewater (APHA, 1999): pH (4500-H+ B); total
alkalinity (2320B); total solids (2540B); total volatile solids (2540E);
ammonium nitrogen (45000NH3-C) using a digester block (Mark Mar-
coni, model MA 4025), and chemical oxygen demand (4520D). Total
Kjeldahl Nitrogen was determined according to method 978.02 from
the Official Methods of Analysis (AOAC, 1997). Biogas samples were col-
lected in duplicates directly from the reactor and analyzed in a gas chro-
matograph (GC 2014, Shimadzu Corporation, Japan), equipped with a
thermal conductivity detector and a packed column for compound sep-
aration (Shin Carbon ST 50/80 mesh). The biogas composition was de-
termined under the following conditions: drag gas nitrogen (35 mL/
min, 5 bars), 200 °C, thermal conductivity detector at 200 °C, and sample
injected volume of 0.5 mL.
2.2. Biogas production and potential of electric energy generation
EG ¼ Q biogas ∗LCV CH4 ∗C m ∗ne ∗CMW ð1Þ
where EG is the potential of electricity generation (MWh/m3 of
vinasse); Qbiogas is the volume of biogas (Nm3 of biogas/m3 of vinasse
fed to the reactor) according to the experimental data; LCVCH4 is the
lower calorific value of methane (8500 kcal/Nm3); Cm is the percentage
of methane in biogas (%) according to the experimental data; ne is the
engine efficiency (%), assumed as 38%; and CMW corresponds to kcal
conversion to MWh.
2.3. Environmental impact assessment
Two scenarios were designed for the environmental impact as-
sessment. The first one evaluated the climate change impacts of elec-
tric energy generation from biodigested vinasse, and the second, the
use of the biofertilizer compared to the vinasse in natura. Impacts re-
lated to the transportation of the vinasse were not considered since,
for both scenarios, it was assumed the use of the same irrigation
equipment for transport and distribution, and the same distance
and land coverage.
2.3.1. GHG mitigation from electric energy generation
The mitigation of GHG emissions/m3 of vinasse due to the avoidance
of electricity consumption from the grid (due to the additional electric-
ity generated from biogas burning) was estimated from Eq. (2) using
the average CO2 emission factor for the electricity dispatch to the grid
from January 2018 to December 2018 (12 months) of 0.539 tCO2eq/
MWh (MCTIC, 2018). Refer to Supplementary material for additional in-
formation on monthly emission factors.

The experimental biogas volume and its methane content were used
to estimate the biogas potential for electric energy generation in a sta- tCO2eq
GHG emissions ¼ 0:539  EG ð2Þ
tionary engine, according to Eq. (1) (Campello et al., 2020): MWh

Sugarcane vinasse

Experimental
Thermophilic
Anaerobic
Digestion
Typical sugarcane crop
NPK requirements for the
Biogas Biodigested study area (according to
soil class)

Stationary
Engine
Fertigation rates for use as Soil NPK Database
biofertilizer in sugarcane crop for the study case
area
Theoretical Electric
Energy Generation
Theoretical GHG Fertigation rates
Emissions Mitigation NPK Replacement spacialization for
Estimations vinasse use and
NPK replacement
Theoretical GHG
Emissions From Soil

GIS Maps for the

study case area

Fig. 1. Flowchart of the general research methodology used in the present study.

3
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

Fig. 2. Administrative Region of Campinas' typical soil (A), sugarcane plantation areas and sugar mills location (B).

2.3.2. NPK replacement and direct and indirect GHG emissions from soil
Table 1
To calculate of the total volume of vinasse produced in the study
Nutritional needs for sugarcane growth cycles: plant cane and ratoon.
area, a production mix of 56% of sugar and 44% of ethanol was obtained
from data reported for 2015 for the 21 sugarcane mills located in ARC Plant cane
(PROCANA, 2015). For soil emissions from vinasse application, the Expected productivity N P-resin (mg/dm3)
whole area destined to sugarcane cultivation in ARC, São Paulo, Brazil, 0–6 7–15 16–40 >40
was considered (see Fig. 2B), which comprehends 21 sugarcane mills.
t/ha N, kg/ha P2O5 kg/ha
In the 2017/2018 harvest season, the whole sugarcane crop area
corresponded to 513,123.30 ha for productivity of 82.60 t/ha (IEA, <100 30 180 100 60 40
100–150 30 180 120 80 60
2019).
>150 30 – 140 100 80
Sugarcane agronomic nutritional requirements were obtained
from the fertilizer and liming recommendations for the State of São Plant cane
Paulo (van Raij et al., 1996). They vary according to the expected Expected productivity K+ (mmolc/dm3)
productivity, local soil chemistry, and macronutrient contents. The
0–0.7 0.8–1.5 1.6–3.0 3.1–6.0 >6.0
nutritional requirements change during the sugarcane growth cycle
(plant cane and ratoon) depending on soil P and K levels, according t/ha K2O kg/ha
to Table 1. >100 100 80 40 40 0
In the study area, the sugarcane soil is predominantly a ferralsol 100–150 150 120 80 60 0
(Fig. 2A), with intermediary Presin level from 7 to 15 mg/dm3 and K+ >150 200 160 120 80 0

ranging from 1.6 to 3.0 mmolc/dm3 (Fig. 3A, field data for 517 soil sam- Ratoon
ples in an ARC adjacent area). The whole NPK requirement was calcu-
Expected productivity N P-resin K+ (mmolc/dm3)
lated since the study area, and adjacent regions were predominantly
(mg/dm3)
similar to this typical soil chemistry (Fig. 3B) (ferralsol). Finally, the re-
0–15 > 15 0–1.5 1.6–3.0
placement level for mineral fertilizers was evaluated (refer to Supple-
mentary material). t/ha N kg/ha P2O5 kg/ha K2O kg/ha
Considering the United Nations Framework Convention on Climate >60 60 30 0 90 60
Change (UNFCCC) methodologies for National Greenhouse Gas Invento- 60–80 80 30 0 110 80
ries, the direct and indirect emissions were calculated according to the 80–100 100 30 0 130 100
>100 120 30 0 150 120
Intergovernmental Panel on Climate Change (IPCC) Guidelines. The

4
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al.
methods and models (Tier 1) were selected from Chapter 11 - Volume
4: Agriculture, Forestry, and Other Land Use (IPCC, 2006).
Direct emissions of N2O followed Eq. (3) (IPCC, 2006):
N2 ODirect −N ¼ N2 O−N N inputs þ N2 O−NOS þ N 2 O−NPRP
where N2ODirect − N = annual direct N2O-N emissions from managed
soils, t N2O-N year−1; N2O − NN inputs = annual direct N2O-N emissions
from N inputs managed soils, t N2O-N year−1; N2ODirect − NOS = annual
direct N2O-N emissions from managed organic soils, t N2O-N year−1;
N2ODirect − NPRP = annual direct N2O-N emissions from urine and
dung inputs to grazed soils, t N2O-N year−1.
Due to the specific characteristics of Brazilian cultivations, it is not
common to have pasture and sugarcane. Thus, N2ODirect − NPRP is
neglected in the face of N2O − NN inputs. Also, sugarcane is a very tradi-
tional crop in the São Paulo state, dating to the beginning of coloniza-
tion, explaining why there is no emission from the organic matter
natural to the soil and N2O − NOS is considered null. The conversion of
N2O–N emissions to N2O emissions for reporting purposes was per-
formed by using Eq. (4).
N2 O ¼ N2 O–N∗44=28
The conversion to GHG emissions was obtained by multiplying the
emissions of N2O for its GWP (265 kg CO2eq/kg N2O), as presented in
Eq. (5).
GHGemissions ¼ N2O∗GWPN2 O
The indirect emissions of N2O are: fossil fuel combustion-related to
the agricultural process, and the N2O produced through the leakage of
NO−3 in the underground (thus, subsequent transformation into N2O is
also taken into account). Eq. (6) (IPCC, 2006) presents the calculation
of the N2O produced from atmospheric deposition of N volatilized
from managed soils. N2O emissions from N leaching/runoff from man-
aged soils were disregarded in the present assessment.
N2 OðATDÞ −N ¼ ½ðF SN  FracGASF Þ þ ððF ON þ F PRP Þ  FracGASM Þ  EF 4
where N2O(ATD)–N = annual amount of N2O–N produced from atmo-
spheric deposition of N volatilized from managed soils, t N2O–N year−1;
FSN = annual amount of synthetic fertilizer N applied to soils, t N
year−1; FracGASF = fraction of synthetic fertilizer N that volatilizes as
NH3 and NOx, kg N volatilized (t of N applied)−1; FON = annual amount
of managed animal manure, compost, sewage sludge and other organic
N additions applied to soils, t N year−1; FPRP = annual amount of urine
and dung N deposited by grazing animals on pasture, range and pad-
dock, t N year−1; FracGASM = fraction of applied organic N fertilizer
materials (FON) and of urine and dung N deposited by grazing animals
(FPRP) that volatilizes as NH3 and NOx, t N volatilized (t of N applied or
deposited)−1; EF4 = emission factor for N2O emissions from atmo-
spheric deposition of N on soils and water surfaces, [t N–N2O (kg
NH3–N + NOx–N volatilized)−1].
Adding urea to soils for fertilization can lead to loss of the CO2 fixed
during the industrial process. Urea (CO(NH2)2) is converted into NH+
OH−, and HCO− 3 in the presence of water and urease enzymes. Eq. (7)
(IPCC, 2006) was used to calculate the carbon emitted from urea
fertilization.
CO2 −C Emission ¼ M∗EF
where CO2–CEmission = annual C emissions from urea application, t C
year−1; M = annual amount of urea fertilization, t year−1; EF = emission
factor, t of C (t of urea)−1.
2.4. Fertigation rates and NPK replacement study case
The ARC adjacent area selected to show the fertigation rates map
and NPK replacement level (Fig. 4) considered 112 soil data collected
Science of the Total Environment 765 (2021) 142717
in 2017 in field experiments. From a Geographic Information System
(GIS), a geostatistical interpolation method was used, which is essen-
tially a method of estimation by local weighted averaging (Oliver,
1990), represented in Eq. (8):
ð3Þ
N
Z ðS0 Þ ¼ ∑i¼1 λi Z ðSi Þ, ð8Þ
where Z(Si) is the measured value at the ith location; λi is a weight fac-
tor for the measured value at the ith location; S0 is the prediction loca-
tion; and N is the number of measured values.
The kriging method assumes that at least some of the spatial varia-
tion observed in natural phenomena can be modeled by random pro-
cesses with spatial autocorrelation, as well as requires that the spatial
autocorrelation be explicitly modeled (Burrough, 1986; Heine, 1986;
McBratney and Webster, 1986; Press et al., 1988). This method defines
which of the input points will be used to interpolate the value for each
cell in the output raster, and is often used in soil science and geology.
3. Results and discussion
ð4Þ 3.1. Vinasse AD chemical and analytical parameters
Table 2 presents the characterization of in natura and biodigested
vinasse. All the physicochemical parameters from the initial characteri-
zation agree with the results reported in the literature (Fuess et al.,
ð5Þ 2018a). In general, vinasse has a high organic matter concentration, rep-
resented by chemical compounds such as residual sugars, organic acids,
and glycerol. The reactor mixture (vinasse and inoculum) had a pH of
8.36 and an alkalinity of 727.1 mg/L after 58 days of operation. These
conditions are considered favorable for the growth of methanogenic ar-
chaeas. Additionally, after this period, the variations in ammonia
reached 344.93 mg/L, the C:N dropped to 2.84, the Volatile Suspended
Solids/Total Suspended Solids ratio (VSS:TSS) was 0.83 and COD
8407.1 mgO2/L. These results were similar to those presented by Cruz-
Salomón et al. (2017) for AD of vinasse in UASB reactor with a final
ð6Þ
COD of 6500 mgO2/L, and by Ferraz Júnior et al. (2016) where the pH
was 8.3, and COD remained from 5700 to 8400 mgO2/L after 180 days
of the experiment.
The evolution of biogas composition, ammoniacal and total nitrogen,
methane yield, and COD can be seen in Fig. 5. From day 28, methane
production increased steadily to reach a composition of 49% on day 58
(Fig. 5A). These results are consistent with other sugarcane vinasse
treatment findings in an anaerobic fluidized bed reactor (dos Reis
et al., 2015). It is noticeable the increase from 126 mg/L to 345 mg/L
(Fig. 5B), which can be attributed to the microbial activity on sugarcane
vinasse proteins and melanoidins. The dead bacteria proteins can be
subsequently used as a source of nitrogen through endogenous metab-
olism. The quick solubilization of ammonia in water can also explain the
high levels in the final solution. The wide range of inhibiting ammonia
concentrations is probably due to the differences in substrates and inoc-
ulum composition, environmental conditions, temperature, and pH
(Rajagopal et al., 2013). Chen et al. (2008) found that ammonia toler-
4 ,
ance for AD processes in levels up to 4000 mg/L could cause an apparent
inhibition of the methanogenic phase.
The lower initial pH does not favor methanogenic bacterial commu-
nity growth. As a consequence, the gradual build-up of volatile fatty
ð7Þ acids (VFAs) inhibits methane synthesis. Besides, VFAs production and
consumption, and the ammonia presence may cause, to some extent,
the generation of sulfuric acid by the action of some sulfur-reducing
bacteria, which could be present in anaerobic gel immobilized sludge
at UASB reactors startup (Del Nery et al., 2018; Whitman et al., 2014).
On days 14, 28 and 39; 6 N NaOH was added to keep the pH above 8.0
to favor the AD process. In terms of vinasse alkalization, to favor the me-
thanogenic phase in APBR reactor, Fuess (2017) used NaOH and
NaHCO3 throughout the first 50 days of the operational period. The in-
crease in methane content may be related to the pH increase from 8.0
5
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

Fig. 3. (A) Soil typical P and K levels in the study area, (B) pedological map in the study region.
(Source: Adapted from Rossi (2017).)

6
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al.
Fig. 4. Graphic location of the experimental area with sampling points collected.
to 8.5, which is more suitable for the growth of thermophilic methano-
genic archaeas. During the methane yield increments along the
60 days, it is worth observing that COD dropped from 10,584 mgO2/L
to 8407 mgO2/L, corresponding to 20.5% organic load reduction
(Fig. 5C). The theoretical COD values for some compounds in AD steps,
obtained by stoichiometric analysis of each compound's complete com-
bustion reaction in equivalent COD (gO2/mol), are glucose 192.77; hy-
drogen 16.0; acetic acid 32.0; propanoic acid 111.85; butyric acid 160.0.
The analysis of acidogenic reactions and their effects over the ini-
tial parameters of vinasse (Fig. 5, Table 2) shows that the initial
values did not change. So, propanoic acid synthesis from glucose
(C6H12O6 + 2H2 → 2CH3CH2COOH + 2H2O) could be the predomi-
nant reaction accounting for the increasing COD in the reaction mix-
ture. Accordingly, hydrogen, mainly insoluble in an aqueous
medium, is quickly consumed by the hydrogen trophic, an essential
electron carrier in several reduction reactions (Fang and Zhang,
2015; Prakash et al., 2018; Stams et al., 2003; Whitman et al.,
2014). Therefore, the biodigested from anaerobic fermentation
could be assumed as a valuable fertilizer due to its increased nitrogen
availability for a better short-term soil fertilization action.
7
Science of the Total Environment 765 (2021) 142717
3.2. Biogas production and electricity generation potentials
From the methane yield of 3800 ml for a total 2547.50 ml of vinasse
fed to the experimental reactor, the theoretical electric energy genera-
tion in a stationary engine burning biogas (see Eq. (1)), with an effi-
ciency of 38%, reaches 0.0028 MWh/m3 of vinasse. This value is 20%
lower than that obtained by Silva dos Santos et al. (2018), and equal
to the result reported by Moraes et al. (2014). Vinasse production
from the ethanol production process, estimated as 15 L per each liter
of ethanol produced, for the sugarcane crop area in ARC, São Paulo,
Brazil (513,123.30 ha for 2017/18 harvest season), accounted for
2.38 × 107 m3/year, for the assumption yield of 85 L of ethanol per ton
of milled sugarcane. Further, assuming the AD of the whole vinasse po-
tential production, the electric energy generation for the referred har-
vest season could reach 66,585 MWh/year.
In Brazil, ethanol sugarcane refineries usually sell their electric
energy surplus, contributing to a more renewable energy matrix.
Thereby, the additional electricity generated could represent a socially
positive impact. According to the National Energy Balance, the average
electricity consumption was 0.646 MWh/person in 2018 (EPE, 2018),
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

Table 2 study area (Moraes et al., 2014). However, this rate is slightly lower
Characterization of the initial and final contents of thermophilic anaerobic digestion pro- than that reported by Fuess et al. (2018a). They assessed the biodigested
cess (0 and 60 days of experiment, respectively).
vinasse application rates for 210 harvesting days (for the 2014/15 São
In natura Biodigested in Biodigested in Paulo State harvest period), and the seasonal characterization of vinasse
vinasse (day the the for two different AD arrangements (fixed bed reactors in single and in
0) reactor (day 0) reactor (day 60)
two-phase). For the fertigation rate here reported, there is no vinasse
COD (mgO2/L) 20,866.52 10,584.47 8407.10 surplus to be destined to a sugarcane region outside the study area.
N-NH3 (mg/L) 13.06 126.27 344.93
The reduction in NPK mineral fertilizer requirements from biodigested
TN (mg/kg) 414.44 838.13 987.56
TS (g/kg) 36.92 32.75 30.93 vinasse compared with in natura vinasse is 65%, 1%, and 100% per hect-
STS (%ST) 58.47 56.85 61.16 are of sugarcane crop fertigated. The net reduction of NPK accounts for
SVS (g/kg) 14.13 18.61 19.19 30%, 1%, and 46%, respectively. For the vinasse production and
DTS (g/kg) 0.89 5.30 8.30 fertigation rate obtained in the present study, 46% of the total sugarcane
DVS (g/kg) 0.89 4.40 5.70
Density (g/mL) 1.01 1.00 1.00
area (based on K requirements) can be adequately fertilized according
pH 4.67 6.11 8.36 to both plant cane and ratoon's nutritional needs.
Total alkalinity a
189.04 727.10 Notwithstanding, the general analysis for ARC regarding fertigation
(mgCaCO3/L) rates and NPK replacement levels should be understood as an approxi-
TOC (mg/L) 6955.50 3528.16 2802.40
mated catch for management purposes. The results for ARC should be
C:N 16.78 4.21 2.84
P (mg P2O5/L) 17.00b a
32.00 considered as the maximum potential for sugarcane vinasse application
K (mg K2O/L)b 1400.00b a
1400.00 to sugarcane soils. The GIS analysis and kriging maps for an adjacent
a
Not detected.
area to ARC identified 9 (nine) different fertigation rates ranging from
b
Data for phosphorus (P) and potassium (K) were obtained from Salomon (2007). 50 to 110 m3/ha, depending on soil original NPK contents and land-
use history. Fig. 6 presents the potential of harnessing biogas production
into nutrient recycling. The potential mineral N and P replacement for
corresponding to an estimation of more than 103,000 inhabitants who both in natura and biodigested vinasse can be observed in Fig. 6A (I
could be ‘locally’ supplied by the energy yield here reported. and II) and B (I and II), respectively. It is possible to easily observe
both the additional need for N and P in fertigated soils under sugarcane,
3.3. Environmental impact assessment as well as the percentage of mineral fertilizers replacement (Fig. 6A (III
and IV), and B (III and IV)). The GIS presentation makes possible a direct
3.3.1. GHG emissions mitigated from electric energy generation comparison of nutrient recycling improvement. The reduced N and P
From the potential electric energy estimated from vinasse AD in the surpluses and increased nutrient use efficiency would increase crop
comprehended area, it would be possible to dispatch to the energy grid production from arable land similarly to previously reported
a total amount of 66,585 MWh/year for the 2017/18 harvest season. The biodigested fertigation reported in the scientific literature for other
avoided GHG emissions from the input of the locally renewable energy crops (Buller et al., 2015; Koppelmäki et al., 2019).
in the grid could reach 35,893 t CO2eq per year, corresponding to Finally, GHG emissions for in natura vinasse fertigated soils and
0.00085 t CO2eq/ton sugarcane milled. It represents 14% of the avoided biodigested vinasse are presented in Fig. 7. For both cases, 89% of the
emissions of the Bagasse Cogeneration Project at “Usina Alta Mogiana total emissions correspond to the direct soil emissions, from which di-
S/A”, a Brazilian sugarcane mill certified for a Clean Development Mech- rect N2O emissions are the majority accounting for 69% of the total emis-
anism (UNFCCC, 2005a) that aims at the reduction of 11,183.57 t CO2eq/ sions. Compared with the use of in natura vinasse, the fertigation with
year for 1.8 × 106 ton of milled sugarcane both for ethanol and sugar biodigested vinasse could reduce GHG emissions in 111,877 t CO2eq/
production. It represents 12% for ethanol and sugar production com- year. The detailed emissions (direct and indirect) can be observed in
pared to “Usina Colombo S/A” - Bagasse Cogeneration Project Table 3, according to the UNFCC-IPCC methods selected for the estima-
(UNFCCC, 2005b), which has as a target 28,018.29 t CO2eq/year for tions (Section 2.3.2). The outstanding N2O emissions abatement from
3.9 × 106 ton of milled sugarcane. biodigested vinasse use in sugarcane soils and the associated savings
on mineral fertilizers acquisition costs (for the replacement of NPK)
3.3.2. Mineral NPK replacement and GHG emissions mitigated from are supportive pathways for a circular economy for the sugar and etha-
biodigested vinasse use for fertigation nol supply chain.
The two usual growth cycles of harvesting, ratoon, and plant cane The present study shows the importance of using bio-products from
were considered to evaluate the whole harvest season's nutritional re- the sugarcane production (sugar and/or ethanol) for generating
quirements. Refer to Supplementary material for detailed gathered in- biofertilizer, as indicated by B.M.M.N. Borges et al. (2019). Moreover,
formation regarding soil condition, NPK and the liming requirements it collaborates in decreasing GHG emissions, mainly from N alternative
for both growth cycles. Overall, liming, a practice to reduce soil acidity fertilization (C.D. Borges et al., 2019). On the other hand, this work
aiming to improve plant growth, is applied depending on the soil base put focus on the spatial analyses, variable still few studied opening
balance of Ca2+ and Mg2+ ions. Urea addition, the less expensive N and paving ways for “Precision Agriculture”, which can develop more
soil fertilizer (Worldbank, 2019), produces CO2 emissions derived deeply assessments for improving the variable rate application
from the fixed amount in its industrial production process (Tubiello (Amaral et al., 2015; de Castro et al., 2017). This kind of work can de-
et al., 2015). In the presence of water and urease enzymes, urea is con- crease the management costs at the same time increase sustainability.
− −
verted into ammonium (NH+ 4 ), OH and bicarbonate (HCO3 ), the latter
evolves into CO2. P application is intimately related to soil classification, 3.3.3. Additional remarks
and its presence is not associated with GHG emissions. On the other Considering that all the potential vinasse production for the stud-
hand, P excess is directly associated with soil eutrophication and ied area was treated in anaerobic reactors and the generated electric
water bodies leaching. For K excessive application, apart from leaching energy might be enough to supply 8% of the total inhabitants of the
risks, another side effect is the plant's lower Ca absorption, which com- study area (ARC). Currently, in the State of São Paulo, the sugarcane
promises its growth. industry is already providing energy from bagasse burning to the en-
Taking into account the vinasse production from sugarcane ethanol, ergy grid. The energy surplus obtained from biogas burning could
2.38 × 107 m3/year, the local crop's fertigation rate was estimated in 100 represent a competitive advantage for the whole sugar and ethanol
m3/ha, which agrees with previous studies and current practices in the sector associated with using of an alternative biofertilizer instead

8
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

(A)

% O2 %CH4 %CO2

100
90
80

Biogas Composition (%)

70
60
50
40
30
20
10
0
0 4 8 12 16 20 24 28 32 36 40 44 48 52 56 60 64 68

Days

(B)

%CH4 N-NH3
100 400
90 350
80
Biogas Composition (%)

300
70
60 250

N-NH3 (mg/L)
50 200
40 150
30
100
20
10 50

0 0
0 4 8 12 16 20 24 28 32 36 40 44 48 52 56 60 64 68

Days

(C)

%CH4 COD
100 20800
90
80
Biogas Composition (%)

15800
70
mg O2/L

60
50 10800
40
30
5800
20
10
0 800
0 4 8 12 16 20 24 28 32 36 40 44 48 52 56 60 64 68
Days

Fig. 5. (A) Evolution of biogas composition, (B) ammoniacal nitrogen and CH4 percentage, (C) chemical oxygen demand (COD) and CH4 concentration with time of reactor operation.

of the simple vinasse disposal in sugarcane crop. Theoretically, UASB efficient for vinasse treatment when considering the associated
reactors produce around 10 Nm3 of biogas/m3 of vinasse, which is al- costs such as operational stability, organic matter removal, and
most 10-fold higher than the experimental yield. Previous studies methane (CH4) production; despite UASB reactors being efficient
(Fuess, 2017; Fuess et al., 2017b) indicate that APBR reactors are and slightly less expensive than APBR reactors.

9
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

Fig. 6. Maps presenting the potential of harnessing biogas production related to nutrient recycling: (A) for vinasse in natura, and (B) for biodigested vinasse.
10
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al. Science of the Total Environment 765 (2021) 142717

180
160
140

tCO2eq.y-1 (x103)
120
100
80
60
40
20
0
N2ODirect N2OIndirect CO2 from Urea Total GHG
emissions
In Natura Biodigested

Fig. 7. Soil GHG emissions for in natura and biodigested vinasse and the potential mitigation obtained from the last.

Although the cleaning and purification of biogas into biomethane is a
bottleneck (Leme and Seabra, 2016; Awe et al., 2017), previous studies
have shown that the end-use of biomethane in heavy vehicles presents
the best environmental performance (Ferreira et al., 2019). Moreover,
biomethane is compatible with natural gas. The existing infrastructures
and technologies could be employed to boost fossil fuels' direct substi-
tution in transport, reducing CO2 emissions by 50% (Pääkkönen et al.,
2019). Hence, the use of biomethane for the agricultural fleet is also
an outcome of a better vinasse treatment and management. Still, a bet-
ter biomethane destination, for the energy grid, city buses fleet, or truck
supply requires further assessment and substantial investments to sup-
port a national biogas strategy to ensure considerable access for afford-
able and clean energy to the country's totality population.
Another critical aspect to be highlighted for the Brazilian scenario is
the RenovaBio governmental Law. This state policy aims to recognize all
types of biofuels' strategic role in the Brazilian energy matrix, both for
energy security and GHG mitigation. RenovaBio can provide an essential
contribution to Brazilian commitments to the Paris Agreement. Its em-
phasis is on regularity aspects, including carbon credit creation, CBios
(Decarbonization Certificates). Previously established targets related
to the production of fossil fuels by each distributor will oblige them to
offset the emissions buying CBios. The adhesion to RenovaBio is manda-
tory, under penalty of sanctions by the Brazilian National Agency of Pe-
troleum, Natural Gas, and Biofuels (MME, 2019).
Romero et al. (2019) assessed the bioenergetics potential using agri-
cultural residues (sugarcane straw and eucalyptus residues) as raw ma-
terial to produce bioethanol and bioelectricity, to diversify the energy
matrix and replacement of fossil fuels of ARC. Besides the fossil energy
replacement in ARC, a GIS study case, like the one here presented, con-
tributes to a better environmental management and the development
of new policies to address the sugarcane residues. Although vinasse
and biogas conversion into electricity and biomethane are not standard
practices in Brazil, the AD technology presents an outstanding potential
to improve the environmental and energetic sugarcane chain operation
(da Silva Neto et al., 2020). Furthermore, other industries and countries
present successful experiences with AD commercial technologies to
support a broad adoption of vinasse AD, biogas use and biodigested ap-
plication in the sugarcane Brazilian production chain.
4. Conclusions
This study shows that in natura vinasse substitution by biodigested
vinasse is a suitable strategy for N fertilization in sugarcane crops. Biogas
burning may also provide electric energy surplus to the grid, so impor-
tant for green economic development in Brazil and other countries. Be-
sides, it would be possible to expand the Brazilian sugar and ethanol
industry's competitive advantage, which is already in an outstanding stra-
tegic level since the 1970s. AD potential still needs further studies to

Table 3
Direct and indirect GHG emissions (without LUC).

Equation Parametersa In natura vinasse (N input = 45,440.15 t year−1)b Biodigested vinasse (N input = 16,032.02 t year−1)c

Eq. (3) N2O − NN inputs (t year−1) 454.40 160.32

N2O − NOS (t year−1) 0 0
N2O − NPRP (t year−1) 0 0
N2ODirect − N (t year−1) 454.40 160.32
N2ODirect (t CO2eq year−1) 120,549.71 42,484.85
Eq. (6) FSN 45,440.15 16,032.02
FracGASF 0.1 0.1
FON 0 0
FPRP 0 0
FracGASM 0 0
EF4 0.01 0.01
N2O(ATD) − N (tN2O–N year−1) 71.45 25.19
N2OInirect (t CO2eq year−1) 18,922.58 6676.19
Eq. (7) M 45,440.15 16,032.02
EF 0.20 0.20
CO2 from Urea (t CO2eq year−1) 33,322.78 11,756.81
Total direct GHG emissions (t CO2eq year−1) 153,872.49 54,241.67
Total indirect GHG emissions (t CO2eq year−1) 18,922.58 6676.19
Total GHG emissions (t CO2eq year−1) 172,795.07 60,917.86
a
Parameters from IPCC (2006) default values – Tier 1.
b
According to sugarcane crop N requirement and in natura vinasse characterization for a fertigation rate of 99 m3 ha−1.
c
According to sugarcane crop N requirement and biodigested vinasse characterization for a fertigation rate of 100 m3 ha−1.

11
L.S. Buller, C.W.S. Romero, R.A.C. Lamparelli et al.
explore its full potential. Governmental subsidies to research and expand
its adoption among ethanol and sugar producers may advance a renew-
able energy grid in Brazil. Fostering a low-carbon energy grid will contrib-
ute to sustaining new business models benefiting all stakeholders and,
consequently, sustainable cities. Supply chains need to be based on circu-
lar economy principles as land-use strategies need to promote urban-
rural integration. A management tool may be designed using this study's
results to subsidize investments for the sugarcane industry to adopt AD.
Additionally, the GIS analysis shows different fertigation rates, varying
by soil chemical characteristics, in a smaller area of Sao Paulo State. The
fertigation rate from 50 to 110 m3/ha suggests that vinasse application
should be better implemented with advanced tools, such as Precision Ag-
riculture and Spatial Analysis. These tools also allow precise management
to comply with environmental laws and avoid side-effects from the wide-
spread fertigation in sugarcane crops.
Beyond the environmental benefits, our findings also suggest a
method that, once applied, can exploit vinasse embodied energy and
nutrients available within the sugarcane production chain. The ap-
proach integrating GIS and UNFCC-IPCC models may support to reach
at least two of the seventeen UN Sustainable Development Goals: af-
fordable and clean energy and climate action.
CRediT authorship contribution statement
Luz Selene Buller: Conceptualization, Methodology, Writing - origi-
nal draft preparation, Writing - review & editing. Cristhy Willy da Silva
Romero: methodology, data curation, validation, writing- original draft
preparation. Rubens Augusto Camargo Lamparelli: Methodology, For-
mal analysis, Data curation, Validation, Resources, Funding acquisition.
Samuel Fontenelle Ferreira: Experimental investigation. Ana Paula
Bortoleto: Writing - review & editing, Validation. Solange I. Mussatto:
Writing - review & editing, Validation, Funding acquisition. Tânia
Forster-Carneiro: Resources, Validation, Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
The authors acknowledge Paulo Magalhães, Mauro Donizeti Berni
and Bruna de Souza Moraes (Interdisciplinary Center of Energy Planning
(NIPE), University of Campinas) for the valuable soil chemical database
and recommendations on this work. Authors also acknowledge the
financial support from the Brazilian Science and Research Foundation
(CNPq, Brazil); Coordination for the Improvement of Higher Education
Personnel (CAPES, Brazil), Finance code 001; São Paulo Research
Foundation – FAPESP (2018/05999-0; 2018/14938-4, and FAPESP-
BBSRC (2015/50612-8)); and Novo Nordisk Foundation, Denmark
(grant number: NNF20SA0066233). T. Forster-Carneiro thanks CNPq
for the productivity grant (302473/2019-0).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2020.142717.
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