Access to this full-text is provided by Springer Nature.
Content available from The International Journal of Life Cycle Assessment
This content is subject to copyright. Terms and conditions apply.
https://doi.org/10.1007/s11367-021-01929-7
LCA FORAGRICULTURE
Assessing life cycle environmental impacts ofinoculating soybeans
inArgentina withBradyrhizobium japonicum
AngelicaMendozaBeltran1 · ClausNordstrømScheel2· NualaFitton3· JannickSchmidt4· JesperHedalKløverpris2
Received: 8 July 2020 / Accepted: 18 May 2021
© The Author(s) 2021
Abstract
Purpose To estimate life cycle impacts from introducing the yield-enhancing inoculant containing the nitrogen-fixing bacte-
rium Bradyrhizobium japonicum and the signal molecule lipochitooligosaccharide (LCO) in Argentinian soybean production.
The study focuses on soybeans grown in rotation with corn in the Buenos Aires province. We also provide the life cycle
impact assessment for the inoculant production. The study represents a novel scope in terms of the studied crop, inoculant
type, and location.
Methods Consequential LCA is used to assess the cradle-to-gate soybean production systems with and without inoculant use.
Stepwise is used for quantification of 16 impacts at mid-point level. Also, the LCA-based guidance of Kløverpris etal.(2020)
is followed, and we divide the change in impacts caused by the inoculant’s use into four effects. The field effect accounts for
changes in field emissions. The yield effect accounts for additional soybean production in the inoculant system that displaces
soybean production elsewhere (system expansion). The upstream effect covers the inoculant production and the downstream
effect covers post-harvest changes such as soybean transport and drying. Small plot field-trials data is applied in the biogeo-
chemical model DayCent to estimate field emissions, among others.
Results and discussion The use of this inoculant reduces environmental impacts from soybean production in all studied
impact categories. The main contributing factor is the yield effect, i.e., reduced impacts via avoided soybean production
elsewhere including reduced pressure on land and thereby avoided impacts in the form of indirect land-use-change (iLUC).
The field effect is the second-largest contributor to the overall impact reduction. Upstream and downstream effects only had
minor influence on results. The yield and field effects are closely tied to the yield change from the inoculant use, which was
not fully captured in the DayCent modeling. Thereby, a potential underestimation of the environmental benefits of roughly
10% can be expected, corresponding to the difference of empiric yield data and the modeled yield data in DayCent.
Conclusion and recommendations The use of this inoculant shows environmental benefits and no trade-offs for the 16 impacts
assessed. Results depend primarily on avoided soybean production (the yield effect) which entails iLUC impacts in Brazil
and USA, and to a lesser degree on field emissions modelled with DayCent. Better data and parametrization of DayCent, to
better capture the change in yields and estimate field emissions, economic modelling for the system expansion assumptions,
and accounting for uncertainty in iLUC modelling could improve the assessment.
Keywords Environmental impact· N-fixation· Inoculant· Soybean· Agricultural practices
Communicated by Greg Thoma.
* Jesper Hedal Kløverpris
jklp@novozymes.com
Angelica Mendoza Beltran
angelica.mendoza@uab.cat
1 Institute ofEnvironmental Science andTechnology (ICTA),
Universitat Autonoma de Barcelona (UAB), Barcelona,
Spain
2 Novozymes A/S, Biologiens vej 2, 2800Kgs.Lyngby,
Denmark
3 Institute ofBiological andEnvironmental Sciences,
University ofAberdeen, Cruickshank Building, 23
St. Machar Drive, AberdeenAB243UU, UK
4 Department ofPlanning, Aalborg University, Rendsburggade
14, room 1.431, 9000Aalborg, Denmark
/ Published online: 2 August 2021
The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
1 Introduction
In the past, the main goals of agricultural optimization were
solely related to productivity improvement. For instance,
yield enhancements and economic optimization were pri-
oritized without further considering potential environmen-
tal trade-offs that some practices could give rise to (Foley
etal. 2011; van Noordwijk and Brussaard 2014). Today, the
drive for productivity is increasingly combined with a need
for agricultural sustainability (Leggett etal. 2017). This
implies that an important additional aim is to minimize
environmental impacts of food consumed. Some alterna-
tives to achieve this are for instance, reducing land use and
chemical use, or ensuring optimal nutrient and carbon bal-
ances in agricultural soils (Horrigan etal. 2002). Sustain-
able agricultural practices have already been widely docu-
mented (Tilman etal. 2001; Godfray etal. 2010; Rockström
etal. 2017) and inoculants—also known as biofertilizers—
is a technology combining agricultural optimization with
a sustainability focus (Santos etal. 2019). Agricultural
inoculants have been known for more than a century and
are broadly used while still holding further potential for
widespread use (Santos etal. 2019). Soybean inoculation
is largest in South American countries while in the USA
only about 15% of the area with soybean cultivation has
been inoculated (Santos etal. 2019).
Generally, inoculants contain microorganisms that tar-
get specific processes in growing plants or the surrounding
soil to enhance the health and growth of plants (Nadeem
etal. 2013) and therefore may change productivity. For
instance, the microbial phosphate inoculant P. bilaiae aids
the uptake of soil nutrients in corn plants causing higher
yields (Leggett etal. 2015) and overall environmental
benefits such as reduction of global warming and nutri-
ent enrichment impacts (Kløverpris etal. 2020). Likewise,
there is a specific type of agricultural inoculants within
the nitrogen (N) fixing category that focuses on symbi-
otic N-fixation. Availability of N is often the limiting soil
nutrient factor for plant growth (Andrews etal. 2003),
and thus, the symbiotic relation between the plant and the
microorganism that enhances N-fixation has potential to
increase crop yields. That is the case for the symbiosis
between soybean and the bacterial inoculant made with
Bradyrhizobium (Keyser and Li 1992). Several reviews
have shown the positive effects of a range of N-fixing bac-
teria, among others, on plant nutrient uptake and N avail-
ability (Andrews etal. 2003; Adesemoye and Kloepper
2009; Di Benedetto etal. 2017; Backer etal. 2018).
In addition to the productivity debate (Adesemoye and
Kloepper 2009; Backer etal. 2018), a broader environ-
mental assessment of the use of inoculants would be more
relevant for agricultural sustainability assessments. Recent
research has focused on identifying possible ways in which
inoculants may help in the reduction of environmental
impacts. For instance, Nadeem etal. (2013) reviewed
the potential of bacterial inoculants in future sustainable
agriculture and suggests that inoculants could reduce the
impact of biotic and abiotic stress factors such as pathogen
attach and extreme temperature, and thereby increase, for
instance, climate resilience of crops. Alori and Babalola
(2018) identified the additional potential of inoculants use
to reduce agro-chemicals such as pesticides and chemi-
cal fertilizers, similar to the study by Alves etal. (2003)
who found that N fertilizer could be completely avoided
for soybean produced in Brazil when properly inoculated
with Bradyrhizobium. The knowledge on the mechanisms
of action of the microbial inoculants plays a vital role in
their use for sustainable agriculture. For instance, under-
standing their relationship with nutrient flows, yields and
agricultural inputs, is vital information to understand their
environmental impacts. Yet, to our knowledge, only one
study quantified the environmental effects of introducing
inoculants in agricultural practices.
Kløverpris etal. (2020) use life cycle assessment (LCA),
as per ISO 14040 (ISO 2006), as a basis for articulating
specific methodological guidance (detailed in Sect.2.2)
with respect to assessing the environmental consequences
of alternative agricultural practices. With this methodology,
they assess the effects of introducing a microbial phosphate
inoculant as a yield-enhancer in the production of corn in
the USA. Results show that the environmental consequences
of introducing a microbial phosphate inoculant to corn are
significant environmental benefits with no trade-offs, in par-
ticular reduction of climate change, eutrophication and land
use change impacts. These benefits come from reduction in
direct emissions from the cropland and from reduced use of
land and other agricultural inputs elsewhere when more crop
can be grown on the same field. Besides this application of
the methodological guidance of Kløverpris etal. (2020), no
other crops, inoculant types and locations have been studied
with it or with LCA more broadly.
In the present study, we apply the LCA-based method-
ological framework described by Kløverpris etal. (2020)
to a new inoculant, crop rotation, and region. We study
soybean production in a corn-soybean rotation, with and
without the use of a novel N-fixing inoculant in the Buenos
Aires region of Argentina. The inoculant contains a natu-
rally occurring, root-nodulating, microsymbiotic N-fixing
bacterium called Bradyrhizobium japonicum and a signal
molecule called lipochitooligosaccharide (LCO). The inocu-
lant is manufactured by Novozymes and is nowadays mar-
keted under the name Nitragin Optimize® II (from here on
referred to as the inoculant) in Argentina. The signal mol-
ecule (LCO) increases the consistency and effectiveness of
1571The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
the rhizobium-soybean symbiosis. This molecule initiates
nodulation, stimulates the root system, and enhances nod-
ule development leading to enhanced N-fixation (Leggett
etal. 2017). The inoculant action on soybean cultivation
follows several steps. Newly emerged soybean plants rely
on their cotyledon leaves as a source of N. Once that supply
is exhausted, the N-deficient plant exudes flavonoid signal
molecules. The rhizobia bacteria in the soil sense the fla-
vonoids and release their own unique signal molecule, the
LCO molecule (nod factor). This signal molecule initiates
a process of root cell elongation and cell division creating
infection sites for the symbiotic rhizobia bacteria within the
soybean roots. This inoculant replaces the need for the plants
to wait until the nodulation cycle is complete by bypassing
the need to release the flavonoids from the plants and/or the
release of LCO. The LCO molecule is present on the seed
as well as the rhizobia inoculant, starting the growth process
and rhizobia nodulation at emergence. Nodulation timing,
root length, and volume can increase greatly. This changes
N and carbon (C) nutrient cycles, crop yields (Leggett etal.
2017), and general plant growth, thereby also affecting the
amount of plant residues.
This study will not only provide an assessment of
the environmental impacts of the use of LCO-fortified
Bradyrhizobium japonicum in soybean production in Buenos
Aires, Argentina but also the life cycle impact assessment
for the inoculant production which could be of use in other
LCA studies.
In the following sections, we first explain how we imple-
ment and capture the mode of action of the inoculant within
the goal, scope and life cycle inventory of the LCA. We then
present the results and discuss the limitations and uncertain-
ties around the LCA. Finally, we conclude and recommend
further improvements and research.
2 Methods
2.1 Goal andscope
The goal of this study is to quantify environmental conse-
quences of introducing an inoculant containing Bradyrhizo-
bium japonicum and LCO in conventional soybean produc-
tion from cradle-to-gate using a consequential LCA. The
functional unit is one metric ton (Mg) of dried soybeans
at farm, ready for the market (13% moisture at harvest and
11% moisture after drying). The soybean is cultivated in the
province of Buenos Aires, Argentina (referred to as AR)
in a corn-soybean rotation. The geographic scope is at the
province level, as the corresponding largest multi-annual
dataset for yields (n = 58) is available at this level (Leggett
etal. 2017). Field data collection took place between 2009
and 2013, and the temporal scope of the study is within the
short-term future. Figure1 shows the data flows from field
trial data to life cycle inventory data. The full inventory and
its calculation are described in coming sections.
The method used for life cycle impact assessment (LCIA)
is Stepwise 2006, version 1.7. The method is described and
documented in Annex II of Weidema etal. (2008) and in
Weidema (2009), and updates for nature occupation in
Schmidt and Saxcé (2016). The characterization module of
Stepwise is based on a combination of the Impact 2002+
method (Jolliet etal. 2003) and the EDIP 2003 method
(Hauschild and Potting 2005). For the detailed description
of the impact categories and methods in Stepwise, see the
electronic supplementary material (ESM), Sect.1.2. Results
are presented at mid-point level of impact, i.e., without nor-
malization and weighting.
2.2 Four environmental effects fromtheuse
ofBradyrhizobium japonicum
Two systems are compared as this study focuses on the
changes in environmental impacts from introducing the
inoculant. In the reference system (Ref), soybean is grown
conventionally in rotation with corn. Here, standard agricul-
tural inputs are applied to the field and then harvested and
dried to get an output of corn in year 1 and soybean in year 2.
The second system is the inoculant system which considers
soybean grown with Bradyrhizobium japonicum (referred to
as B.j-LCO) in year 2 following conventional corn produc-
tion in year 1. It is assumed that the corn output in uneven
years (year 1, 3, 5, …, 99) is unaffected by the introduction
of the inoculant for the biogeochemical modelling period of
100 years, as will be detailed further.
Following the approach by Kløverpris etal. (2020), the
two systems are divided into four categories, i.e., upstream,
field, yield, and downstream and the difference in impact
between the two systems within each category is referred
to as an “effect.” The upstream effect includes the produc-
tion of the inoculant in the inoculant system. The field effect
includes a change in direct emissions from the field in the
inoculant system in comparison with the reference system.
The yield effect considers the higher output of soybean in
the inoculant system per unit of area compared to the refer-
ence system. To ensure that the two systems provide the
same output, i.e., that the two systems are “equivalent” and
therefore comparable, the inoculant system is expanded to
include displacement of marginal soybean production else-
where. Finally, the downstream effect accounts for changes
in drying and transport from field to farm in the inoculant
system compared to the reference. See the ESM, Sect.1.1,
for details on the equations to calculate each effect.
Figure2 shows the reference and the inoculant systems.
Figure2 also shows the cultivated area in both systems (A),
the output of soybeans from area A in the reference system
1572 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
(Q), the increase in soybean output from area A when the
inoculant is used (∆Q) and the area of soybean produc-
tion displaced when the inoculant is used (B). These are
all important parameters to determine the individual effects
(ESM, Sect.1.1).
2.3 Inventory
The inventory data and assumptions for the effects’ model-
ling are described here. Details for the area A in the ref-
erence system and the inoculant system are available in
Table1.
2.3.1 Upstream effect: theinoculant production
The inoculant production takes place in a fermentation facil-
ity and has three main stages: the laboratory, the fermenta-
tion, and the post-fermentation stage. In general, all inven-
tory flows are estimated based on the inoculant’s production
of the total volume of liquid processed at the fermentation
facility in 2017. For the materials, energy, transport, emis-
sions, waste streams, and capital goods and services that are
included in this inventory, see the ESM, Sect.2.1.
Finally, the amount of inoculant used in the inoculant
system is 0.15 kg per ha, as estimated based on the rec-
ommended dose for all Nitragin Optimize® II products
for South America and the assumed standard seeding rate
(USDA 2019).
2.3.2 Field effect
Soybean cultivation and biogeochemical modelling with
DayCent The DayCent model was used to simulate the use
of the inoculant in the soybean production (Del Grosso etal.
2001, 2006; Parton etal. 2001). Initially, DayCent simu-
lates the corn-soybean rotation for the reference scenario.
For this, input parameters include temperature, precipitation,
soil texture, plant growth, and management events such as
fertilization and harvests. Data for these parameters were
obtained from a regional calibration of data for soybean
after corn production, combining typical productivity and
management practices sourced from agronomic experts from
Novozymes, with soil (most dominant soil type) and climate
(daily climate data averaged across the region) parameters
sourced from the Harmonized World Soil Database (HWSD)
and National Aeronautics and Space Administration (NASA)
databases, respectively.
Two additional assumptions were made to model the
inoculant mode of action system. First, the average per-
centage change in soybean yield achieved by the inocu-
lant system and simulated in DayCent is based on data
obtained from the field data for Buenos Aires (Sect.2.3.3).
Second, the effect of the inoculant in plant growth and N
uptake by the plant was simulated by gradually increas-
ing the parameter in DayCent that defines the maximum
amount of N fixed per gram of C fixed via net primary
production (NPP), if there is insufficient N within the
soil. This parameter is called the SNFXMX parameter
and it was gradually increased until the average percent-
age change in soybean yield with inoculant use from the
field was achieved in the simulations. Modification of this
parameter is used as a simple yet representative proxy to
characterize the inoculant’s mode of action, particularly
capturing the effect the inoculant has on plant growth and
on N uptake within the model. The baseline rate of N-fixa-
tion without the use of the inoculant had a value of 0.003 g
N/g C NPP i.e. this is the SNFXMX value for the reference
system. Simulations for both systems run for a 100-year
period. More details on DayCent modelling are provided
in the ESM, Sect.2.2.1. The key DayCent outputs were
the nutrient balances shown in the ESM, Sect. 2.2.2. These
are the base for the inventory of the cultivation process
emissions as explain below.
Cultivation emissions based on DayCent simulations DayCent-
modelled outputs include soil organic carbon (SOC) content,
CH4 emissions from aerobic and anaerobic reactions, N in
plant grain, as well as N-related emissions to air, i.e., N2O
(direct), NH3, NO, N2, and NO3
− emissions to water for the ref-
erence and inoculant systems. SOC changes between systems
were used to estimate CO2 emissions (see below). Change in
N2O emissions are observed because the inoculant can pro-
mote root growth and plant productivity. Over a long period of
time, the increase in plant productivity returns higher C inputs
into the soil, resulting in a higher soil C level in the inoculant
system compared to the reference system. This in turn results
in a slight increase in the corn yields (~0.4%) over the 100-year
period, too. Soil C and its retention within the soil is key to
soil health and its relationship with crop yields is well estab-
lished (Oldfield etal. 2019). Therefore, the modelled change
in corn yields may also be expected. However, the increase in
corn yield has conservatively been omitted in the LCA as it
is assumed that corn production inputs and outputs (including
emissions) remain the same in both systems. This is because,
while corn yields increase, the level of increase is so small
(~0.4%), it cannot be safely assumed that fertilizer applica-
tion or any other management activates around corn would
change due to the presence of the inoculant. Table1 shows the
emissions based on DayCent simulations as used in the inven-
tory for soybean, as well as the simulated emissions for corn,
for indication. The ESM, Sect.2.2.2, shows the uncertainty
parameters of the DayCent modelled emissions.
SOC‑related emissions The SOC emissions are calculated
with a time-independent approach elaborated by Schmidt
1573The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Table 1 Inventory of soybean production in a corn-soybean rotation, with (B.j-LCO) and without (Ref) the use of inoculant. All flows normal-
ized to 1 ha
Flow Unit Ref B.j-LCO Data source (section)
Output Value σg
2 (pedigree
scores)***
Value σg
2 (pedigree scores)***
Soybean yield (DayCent) Mg 2.626 2.29 2.747* 2.13 Selected data from Leggett
etal. (2017), Sect.2.3.3
Inputs
Pesticide application ha 4.30 - 4.30 - Leggett etal. (2017),
Sect.2.3.2
Combine harvesting ha 0.30 - 0.30 - Ecoinvent v3.4, Sect.2.3.2
Tillage ha 0 - 0 - Leggett etal. (2017),
Sect.2.3.2
Sowing ha 1.00 - 1.00 - Ecoinvent v3.4, Sect.2.3.2
Fertilizing ha 1.00 - 1.00 - Leggett etal. (2017),
Sect.2.3.2
Phosphate fertilizer, as P2O5kg 11.45 - 11.45 - Selected data from Leggett
etal. (2017), Sect.2.3.2
Packaging, for fertilizers and
pesticides
kg 12.37 - 12.37 - Calculated proxy
Pyrethroid-compound kg 0.06 - 0.06 - Ecoinvent v3.4, Sect.2.3.2
Organophosphorus-compound,
unspecified
kg 0.53 - 0.53 - Ecoinvent v3.4, Sect.2.3.2
Phenoxy-compound kg 0.30 - 0.30 - Ecoinvent v3.4, Sect.2.3.2
Glyphosate kg 0.003 - 0.003 - Ecoinvent v3.4, Sect.2.3.2
Triazine-compound, unspecified kg 0.02 - 0.02 - Ecoinvent v3.4, Sect.2.3.2
Seeds kg 65.6 - 65.6 - (USDA 2019), Sect.2.3.2
Water l 0 - 0 - Leggett etal. (2017),
Sect.2.3.2
Transport field to farm tkm 41.55 3.18 (4,4,4,4,4,2.0) 43.46 3.18 (4,4,4,4,4,2.0) Calculated proxy, Sect.2.3.4
Drying of soybean l 68.22 2.46 (4,4,4,4,4,1.05) 71.36 2.46 (4,4,4,4,4,1.05) Calculated proxy, Sect.2.3.4
Inoculant kg 0 1.55 (2,2,1,2,1,1.05) 0.150 1.55 (2,2,1,2,1,1.05) Recommended dose,
Sect.2.3.1
Land occupation ha year−1 1 - 1 - Area A, Sect.2.3.2
Market for arable land {GLO} ha year 1 - 1 - iLUC, Sect.2.3.2
Avoided production
Soybean {GLO}| market for kg 0 - −121 28.9 Avoided production,
Sect.2.3.3
Emissions for soybean
NH3-N emissions to air kg N 3.66 3.47 3.67 3.45 DayCent, Sect.2.3.2
NO-N emissions to air kg N 0.76 4.83 0.77 4.79 DayCent, Sect.2.3.2
N2O-N emissions (direct) to air kg N 0.576 4.75 0.582 4.68 DayCent, Sect.2.3.2
N2-N emissions to air kg N 0.25 8.01 0.16 15.52 DayCent, Sect.2.3.2
CH4 emissions to air kg CH42.17 1.12 2.16 1.12 DayCent, Sect.2.3.2
N2O-N emissions (indirect)
to air
kg N 0.1067 - 0.1072 - IPCC, Sect.2.3.2
NO3
--N emissions to water kg N 8.33 10.28 8.37 10.13 DayCent, Sect.2.3.2
Phosphate emission to water kg P 0 - 0 - Dalgaard etal. (2006),
Sect.2.3.2
SOC CO2 emissions to air kg CO20 - −18.3 1.37*** DayCent, Sect.2.3.2
Emissions from corn**
NH3-N emissions to air kg N 5.42 - 5.56 - DayCent, Sect.2.3.2
NO-N emissions to air kg N 1.41 - 1.41 - DayCent, Sect.2.3.2
N2O-N emissions (direct) to air kg N 0.93 - 0.94 - DayCent, Sect.2.3.2
N2-N emissions to air kg N 0.17 - 0.28 - DayCent, Sect.2.3.2
1574 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
and Brandão (2013), building on the time-independent,
decay-function-based CO2 characterization factors described
by Petersen etal. (2013). Kløverpris etal. (2020) recom-
mends the use of the time-independent approach which
looks at the change in radiative forcing related to a single
event, in this case, one year of soybean production with
inoculant use. The inoculant application impacts the trend
of SOC over the subsequent time period. This trend can be
compared to the trend in the reference scenario (without
inoculant) and, in this way, changes can be estimated. The
estimated change in SOC emission are −18.3 in kg CO2 ha−1
year−1 for the 100-year modelled period (ESM, Sect.2.2.3,
and Appendix II). An additional annualized approach to
calculate SOC emissions (for 20 and 50 years) is described
in the ESM, Sect.2.2.3, and it is used in the sensitivity sce-
narios (see ESM, Sect.4).
Residues The LCA follows DayCent modelling of biomass
from residues (Abodeely etal. 2012). At harvest, DayCent
separates the entire above and belowground biomass into
grain and “other biomass.” The other biomass is divided into
a fraction returned to the field, i.e., left behind (residues)
and adding nutrients to either soy or corn (thus accounted
for in the nutrient balances), and the remaining is removed
from the field. The fraction removed has been set to 70%
of the total residues following previous DayCent runs from
Fitton etal. (2014, 2017). The difference of removed resi-
dues between inoculant and reference systems in Mg dry
matter ha-1 yr-1 for corn is 0.02 and 0.16 for soybean (ESM,
Sect.2.2.4). No inventory assumption was made on the
treatment of these removed residues because it is not clear
what happens to them after being removed and the range of
treatment options is large, as discussed in the ESM. This is
a cutoff of the system. More data collection from the field
practices could improve the assessment.
Other field emissions Other field emissions included in the
inventory were indirect N2O emissions to air and phosphate
emissions to water (Table1). Indirect N2O emissions were esti-
mated using the IPCC 2006 Guidelines for National Greenhouse
Gas Inventories Tier 1 (De Klein etal. 2006)and N-related
parameters calculated with DayCent, i.e., N-volatilization,
N-redeposition, N-leaching, ammonia emissions, NOx emis-
sions, and nitrate emission to water. Calculation details are
shown in the ESM, Sect.2.2.5.
Phosphate emissions are calculated based on Dalgaard
etal. (2006) as a fraction of 2.9% of the surplus of P, esti-
mated as the difference between phosphate fertilizer input
and phosphorus removal in the crop. Similar to DayCent
emissions, these emissions are only estimated for soybean
production as corn cultivation is assumed to remain the same
between systems. More details of this calculation are shown
in the ESM, Sect.2.2.5.
Other inputs to soybean cultivation Other inputs to soy-
bean cultivation considered are as follows: seeds, fertiliz-
ers and packaging, pesticides and packaging, energy use for
crop management (plant protection applications, harvest-
ing, tillage, ploughing, sowing, and fertilizing), and water
use (Table1). Assumptions and background processes used
for each input are described in the ESM, Sect.2.2.6. These
inputs remain the same on area A, for the reference and inoc-
ulant systems, and were added, for completeness. Land-use-
change (LUC) was also added for completeness and remains
equal between systems. It is accounted in the form of direct
* To avoid double counting, the yield entered in the SimaPro software for the inventories is 2.626 Mg/ha * year. The table shows the actual yields
to display the change between systems
** DayCent modelled emissions for corn are shown for indication here. It was assumed no inputs or outputs of corn production changed between
systems
*** Uncertainty information for selected flows of the reference and inoculant systems in AR. σg
2 is included in SimaPro together with lognormal
distribution for all flows to characterize their uncertainty, except for SOC for which the assumed distribution for CO2 emissions is normal in
order to account for the negative emissions
Table 1 (continued)
Flow Unit Ref B.j-LCO Data source (section)
Output Value σg
2 (pedigree
scores)***
Value σg
2 (pedigree scores)***
CH4 emissions to air kg CH42.08 - 2.08 - DayCent, Sect.2.3.2
N2O-N emissions (indirect)
to air
kg N 0.163 - 0.165 - IPCC, Sect.2.3.2
NO3
−-N emissions to water kg N 12.63 - 12.74 - DayCent, Sect.2.3.2
Phosphate emission to water kg P n.a - n.a - Dalgaard etal. (2006),
Sect.2.3.2
1575The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
and indirect land use change (dLUC and iLUC) and has the
same magnitudes for the reference and inoculant systems i.e.
one ha yr-1 of occupied arable land for dLUC and one ha
yr for iLUC, linked to the global marginal market for land
(ESM, Sect.2.2.7, and Schmidt etal. 2015) and (Table1).
For more details on LUC accounting and modelling, see the
ESM, Sect.2.2.6.
2.3.3 Yield effect
Yield modelling Field trial data (Leggett etal. 2017) was
collected for nine provinces in Argentina (ESM, Sect.2.3.1).
Yields had a relative increment of 6.4% due to the inoculant
use. These data were refined to a smaller dataset via a plot
analysis (ESM, Sect.2.3.1), resulting in a dataset that con-
tains data only from Buenos Aires, Argentina, with a relative
increment of yields of 5.1% (n = 58). The final relative yield
increment used in the LCA was determined with this dataset
and with DayCent simulations as explained in Sect.2.3.2.
The resulting modelled yield increase was 4.6% in Buenos
Aires. All yield-related values are shown in Table2. The
difference between change in modelled yields (4.6%) and
change in yields from the plot analysis for Buenos Aires
(5.1%) is about a 10%, yet it is the closest long-term match
achieved by means of the simulations. The impossibility to
replicate the plot analysis yields in DayCent is rooted in two
reasons. First, the annual modelled yield, and yield response
to the presence of the inoculant is not fixed and varies in
relation to the climate, as a consequence interannual vari-
ation in soybean yield is greater than the increase in yield
due to the inoculant use. Secondly, the change in yield, due
to the presence of the inoculant, was smaller in years with
projected lower yields.
The modelled relative change in yields leads to a total
change in production between the systems with and without
inoculant of 0.121 mg DM ha−1 year−1 (Table2). This is the
value used for the system expansion as the avoided soybean
production in the global marginal market of soybean due to
the inoculant use (Table1). We use the DayCent modelled
yields to keep consistency with the modelled emissions
within the LCI, despite them being lower than those from
the plot analysis. The use of lower modelled yields leads to
a conservative assessment of the benefits from the inoculant
use.
Global marginal market of soybean According to the meth-
odology to identify marginal suppliers in LCA described in
Weidema etal. (2009) and Weidema (2003), the marginal
producers (on a country level) are the first to react to changes
in the market, e.g. in demand. Similarly, they would be the
first producers to pause production increases if a new tech-
nology (e.g., a yield-enhancing inoculant) increased sup-
ply elsewhere. Hence, it is assumed that the producers, that
would first react to a change in demand, are located in the
countries with the recently largest increase in production
(i.e., an assumed reaction to increasing demands). Based
on a linear regression of FAOSTAT data from 2012 to 2016
(FAO 2018), the marginal suppliers of soybean in the global
market were assessed to be located in USA and Brazil, where
the largest increases were observed. Together, the two coun-
tries represent about 60% of the global production of soy-
beans. The distribution of 52% soybeans from USA and 48%
soybeans from Brazil in the marginal market corresponds to
a scaled share of global production but only accounting for
these countries (ESM, Sect.2.3.2).
The life cycle inventory for soybean production in the USA
and Brazil for this market is based on data from Schmidt and
De Rosa (2018). It includes inputs such as fertilizer, diesel,
land, irrigation, and outputs such as soybean production and
main field emissions (ESM, Sect.2.3.2). The input of land
is linked with the global marginal market of land used to
model iLUC (ESM, Sect.2.2.7). According to Schmidt etal.
(2015), there is a global market for land concerned with
production capacity of land, instead of land area. Countries
that supply land to this market are all countries that expand
their arable land and countries that intensify their existing
productive land. Thus, there is supply through expansion and
Table 2 Soybean yields with (B.j-LCO) and without (Ref) the use of the inoculant. DayCent modelled yields are used in the LCIs (values in
bold)
* Corresponds to 9 provinces in Argentina
** Corresponds to Buenos Aires, Argentina (number of plots = 58)
*** Arithmetic standard deviation
Yields [Mg dry matter ha−1 year−1]
Field trials (Leggett etal. 2017) Plot Analysis Modelled by DayCent
Ref B.j-LCO Change in yield
(ΔQ = B.j-LCO
– Ref)
Change in soybean
yield (%)
Change in soybean
yield (%)
Ref B.j-LCO Change in yield
(ΔQ = B.j-LCO
– Ref)
Change in
soybean yield
(%)
2.55* 2.72* 0.17 +6.4* + 5.1** 2.626 (0.66)*** 2.747 (0.69)*** 0.121 +4.6
1576 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
intensification. In fact, the global market of land operates
with different markets for land, i.e., (1) arable land, (2) inten-
sive forest land, (3) extensive forest land, and (4) grassland.
This delimits land types with different potential uses. Land
use change (LUC) can be direct (dLUC) if the reference use
of land is directly changed or indirect (iLUC) if it is induced
via the market i.e. the use of land by the crop under study is
what is considered as dLUC, while the supply of new land
caused by the need for compensating the production capac-
ity of the land required by the new demand is considered as
iLUC. In our case, the avoided production of soybean in the
global marginal market of soybean is linked to the global
marginal market of land as it is expected for the marginal
producers to avoid the need for new agricultural land.
2.3.4 Downstream effect—soybean transport anddrying
Once harvested, the transport of soybeans from field to farm
by tractor is added for both systems. Such transport has been
calculated as the yield in wet weight times the distance from
field to farm. Moisture at harvest is 13% and the distance
field-farm is 14 km (ecoinvent v3.4. data for soybean pro-
duction for Argentina). Similarly, the impact of transporting
soybean from field to farm in the global marginal market of
soybean, i.e., in Brazil and USA (needed for the substituted
soybean production in the inoculant system) was calculated.
The difference between the two systems covers the down-
stream effect of transport (ESM, Sect.2.4.1).
For drying of additional and substituted soybean, mois-
ture at storage was assumed to be 11% for all locations.
For more details on the drying calculations, see the ESM,
Sect.2.4.2.
2.3.5 Background processes
All processes used in the background of the reference and
inoculant systems are from the ecoinvent v3.4 database,
consequential model (Wernet etal. 2016). The two back-
ground processes that are not drawn from this database are
the global marginal market of soybean (Sect.2.3.3) and the
global marginal market of land used for iLUC modelling
(ESM, Sect.2.2.7, and Schmidt etal. 2015).
2.3.6 Uncertainty analysis andsensitivity scenarios
An uncertainty analysis was conducted to account for
parameter uncertainty among which for DayCent emis-
sions, yields, inoculant use and substituted soybean (see
ESM, Sect.5, for all details and Table1). Pairwise Monte
Carlo simulations are run, and based on these, we calcu-
late the discernibility analysis count per impact and the
statistical significance using a null hypothesis testing by
means of a paired t-test, for all impacts as well. This analy-
sis aims to show whether the mean of the relative impacts
of two systems are significantly different from each other.
For the sensitivity analysis, we performed the three one-
at-the time scenarios: (1) 20- and 50-year annualized SOC
emissions (as described by Kløverpris etal.2020) instead
of the time-independent approach, (2) higher impacts in
the production of the inoculant to address the missing
feedstocks in the inventory of this activity, and (3) exclud-
ing iLUC emissions that appeared as key contributors to
the impacts (ESM, Sect.4).
2.4 Impacts notincluded intheLCA
Two important environmental impacts are not explicitly
quantified in this study and deserve further research: soil
microflora and water impacts. Microbial inoculants can
impact the soil microflora temporarily and in the long
term, and these effects are still not well understood and
need further research (Trabelsi and Mhamdi 2013). The
effect of the inoculant, on synergistic effects, interactions
and co-inoculation of B.j-LCO and other microorganisms
on soybean productivity has been studied (Chibeba etal.
2015; Egamberdieva etal. 2016; Meena etal. 2018). Also,
the competitive behavior of the inoculant with indigenous
microorganisms has been studied, finding that it can be
used to enhance N-fixation and productivity in organic
soybean and may save chemical fertilizer use (Abou-
Shanab etal. 2017). To our knowledge, no studies cover
specifically the impacts of the use of B.j-LCO inoculant
on soil microflora and it would be an impact that needs
further developments in LCA.
For water impacts, the development of bigger crops with
higher yields will likely lead to higher evapotranspiration
from the specific field and thereby a higher “green” water
footprint (Mekonnen and Hoekstra 2011). In case the crops
are fully rain-fed, this is not a major issue, e.g., in Buenos
Aires soybean (Leggett etal. 2017). Also, higher yields due
to the inoculant use avoid more soybean production else-
where. Hence, the net water use is likely to be more or less
unaffected per Mg of soybean produced, although this will
depend on the efficiency of water use in the different loca-
tions. Besides irrigation water, some water is used in produc-
tion of the inoculant (upstream effect). This is likely off-set
by the water saved through the yield effect. We included the
use of water in the inoculant production and no irrigation
was assumed in the marginal producers of soybean. With
data for specific locations, this impact could be added to the
LCA impacts.
1577The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
3 Results
3.1 Life cycle impact assessment results
Table3 shows the LCIA results per kg of inoculant as
implemented in this study.
Table4 shows the effects of introducing the inoculant
in soybean cultivation for the 16 environmental impact
categories considered. The total impacts for the reference
system are shown for comparison as well as the relative
changes in impacts caused by the inoculant. Impacts are
reduced for all impact categories in the inoculant system
with respect to the reference system. Among the four
effects, the yield effect is dominating the impact reduc-
tions. The field effect also contributes to impact reduc-
tions, particularly of global warming, whereas upstream
and downstream effects are relatively insubstantial.
Figure3 shows the contribution of different activities to
each impact category and each effect, for the two systems.
Negative contributions (i.e., reduction of impacts) are
shown for the avoided soybean production. These results
correspond with the yield effect and are therefore only vis-
ible for the inoculant system. Field emissions are the only
contributor to the field effect. The inoculant production
contributes to the upstream effect and finally, drying and
transport correspond with the downstream effect. More
detailed results for the contribution analysis, contribu-
tion of effects and total impacts are available in the ESM,
Sect.3.1.
3.2 Sensitivity anduncertainty analysis results
Here, we briefly describe key results for the sensitivity and
uncertainty analysis. Detailed results can be found in the
ESM, Sects. 4 and 5, respectively. For the first sensitivity
scenario, field CO2 emissions related to changes in SOC
are higher (less negative) than when estimated using the
annualized approach. Therefore, global warming impacts
are higher for the scenarios when the annualized estimates
are used. Thus, the field effect increases (is less negative)
and therefore the benefits of using the inoculant reduce. For
the second scenario, the upstream effect is less than 15%
of the total change in impacts, when the impacts per kg of
inoculant are 10 times the initially established. These results
suggest that including further feedstocks on the production
of the inoculant would have to increase more than 10 times
the impacts per kg of inoculant in order to meaningfully
change the upstream effect. Finally results for the third sen-
sitivity scenario show that all effects remain the same except
for the yield effect that substantially increases (is less nega-
tive) because iLUC emissions (CO2 emissions) are the larg-
est contributor to this effect and have been excluded in the
scenario. Global warming impacts reduce from around 7%
when excluding iLUC to 4% when including iLUC.
For the uncertainty analysis the discernibility analysis
shows that for all impacts (except for nature occupation),
results are not discernible, meaning that when accounting
for uncertainty it is difficult to assert whether the inoculant
system has better results than the reference. Yet, results for
the paired t-test show that for a p value of 5% and a cor-
rected p value of 2.9%, 16 out of 16 impacts are significantly
different. This means that the mean of the distribution of
the difference of impacts between reference and inoculant
systems, are significantly different from zero which is the
hypothesized mean, and therefore impacts are significantly
reduced in the inoculant system compared to the reference.
4 Discussion
4.1 Effects discussion
Results showed that the field and yield effects are the largest
contributors to the overall benefits of using the inoculant in
soybean grown with corn as previous crop. Upstream and
downstream effects contribute insubstantially to the change
in impacts from introducing the inoculant.
The field effect depends entirely on changes in soil emis-
sions from the area A as modelled in DayCent, because
emissions related to iLUC, field work, fertilizer, pesticides,
seeds, and other inputs do not change between the systems
for the area A. The field effect is negative (reduced impacts)
Table 3 LCIA of the production of one kg of inoculant for Stepwise
impacts at mid-point level
Impact category Unit Value per kg inoculant
Human toxicity, carcinogens kg C2H3Cl-eq 1.991E−02
Human toxicity, non-carc. kg C2H3Cl-eq 5.548E−03
Respiratory inorganics kg PM2.5-eq 2.974E−04
Ionizing radiation Bq C-14-eq 7.084E−01
Ozone layer depletion kg CFC-11-eq 2.997E−08
Ecotoxicity, aquatic kg TEG-eq w 1.014E+01
Ecotoxicity, terrestrial kg TEG-eq s 1.594E+00
Nature occupation PDF*m2a −8.375E−04
Global warming kg CO2-eq 3.523E−01
Acidification m2 UES 1.956E−02
Eutrophication, aquatic kg NO3
-
-eq 3.534E−04
Eutrophication, terrestrial m2 UES 2.267E−02
Respiratory organics pers*ppm*h 2.425E−04
Photochemical ozone,
vegetat.
m2*ppm*h 2.431E+00
Non-renewable energy MJ primary 1.143E+01
Mineral extraction MJ extra 8.587E−03
1578 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
for three impacts: global warming, respiratory organics, and
photochemical ozone formation impact on vegetation. Other
impacts have a positive field effect, i.e., the inoculant use
does not lead to reductions compared to the reference. A
closer look at global warming, for instance, shows that N2O
emissions from the area A have the largest increase with the
use of the inoculant and SOC-related CO2 emissions the
largest reduction, leading to a net reduction in greenhouse
gas (GHG) emissions from the area A (ESM, Table17). N2O
and SOC emissions/sinks are influenced by the increase in
biomass (plant and root growth) stimulated by the inoculant
and modeled in DayCent, not just for soybeans but also for
corn. The slight increase in corn yield over the 100-year
simulation period increases the return of carbon and nitrogen
to the soil via plant inputs, as a consequence this induces
additional carbon storage and nitrogen-related emissions.
Because these results for the field effect depend entirely on
the DayCent model outputs, uncertainties, and limitations
of this modelling approach are further discussed (Sect.4.2).
The yield effect is the largest contributor among the
effects. The yield effect is negative for all impact categories
by definition as it consists of avoiding the impacts of soybean
production in the global marginal market of soybean. The
larger the yield increase in the inoculant system compared
to the reference, the more impacts will be avoided and the
more negative the yield effect will be (direct proportion-
ality). These results depend primarily on the yield change
between systems, which is based on experimental data from
Leggett etal. (2017) and also on how this change was cap-
tured in DayCent (see Sect.4.2 for limitations). Also, the
benefit of avoiding soybean produced in this market is larger
when accounting for iLUC (0.86 kg CO2eq Mg−1 soybean)
compared to when not, i.e., excluding iLUC (0.24 kg CO2eq
Mg−1 soybean). N2O and CO2 emissions from iLUC are the
two main contributors to total GHG emissions of avoided
soybean production in this market (ESM, Table17). iLUC
modeling is thus important as are its limitations and uncer-
tainties, for instance data and identification of marginal land.
More strengths and weaknesses of the model are discussed,
also in comparison to other iLUC models, in De Rosa etal.
(2016). Among the most important strength is the suitabil-
ity of the model to be used within an LCA framework. For
instance, there is no conflict with the usual assumption of
full price elasticity in the markets (Weidema 2003), and the
Table 4 Effects of the use of inoculant on the impacts of soybean production per Mg soybean. Negative values refer to improvement compare to
the reference
Impact category Unit Upstream
effect (Eq.1)
Field effect
(Eq.2)
Yield effect
(Eq.3)
Down-stream
effect (Eq.4)
Total inoculant
effect (Eq.5)
Total ref. without
inoculant incl.
iLUC
Changewith B.j-
LCO versus ref
incl. iLUC (%)
Human toxicity,
carcinogens
kg C2H3Cl-eq 1.14E−03 0.00E+00 −2.21E−01 1.86E−03 −2.18E−01 5.53E+00 −4.0%
Human toxicity,
non-carc.
kg C2H3Cl-eq 3.19E−04 1.94E-04 −2.24E−01 6.39E−03 −2.17E−01 1.14E+01 −1.9%
Respiratory
inorganics
kg PM2.5-eq 1.71E−05 4.62E−04 −3.36E−02 2.07E−03 −3.10E−02 1.19E+00 −2.6%
Ionizing radiation Bq C-14-eq 4.07E−02 0.00E+00 −1.71E+01 1.40E−01 −1.70E+01 3.59E+02 −4.7%
Ozone layer
depletion
kg CFC-11-eq 1.72E−09 0.00E+00 −1.24E−06 5.91E−09 −1.23E−06 2.70E−05 −4.6%
Ecotoxicity,
aquatic
kg TEG-eq w 5.83E−01 1.49E−02 −6.14E+02 5.35E+00 −6.09E+02 8.79E+03 −6.9%
Ecotoxicity, ter-
restrial
kg TEG-eq s 9.17E−02 3.73E−02 −5.33E+01 8.35E−01 −5.24E+01 1.48E+03 −3.5%
Nature occupation PDF*m2a −4.82E−05 0.00E+00 −4.41E+01 −1.78E−02 −4.41E+01 1.34E+03 −3.3%
Global warming kg CO2-eq 2.03E−02 −6.06E+00 −3.97E+01 2.09E−01 −4.56E+01 1.12E+03 −4.1%
Acidification m2 UES 1.12E−03 1.14E−01 −5.70E+00 1.84E−02 −5.56E+00 1.84E+02 −3.0%
Eutrophication,
aquatic
kg NO3
−
-eq 2.03E−05 2.18E−02 −1.63E+00 4.69E−05 −1.61E+00 3.52E+01 −4.6%
Eutrophication,
terrestrial
m2 UES 1.30E−03 5.33E−01 −2.45E+01 2.09E−02 −2.39E+01 8.14E+02 −2.9%
Respiratory
organics
pers*ppm*h 1.39E−05 −1.45E−04 −5.98E−03 1.13E−04 −6.00E−03 2.88E−01 −2.1%
Photochemical
ozone, vegetat.
m2*ppm*h 1.40E−01 −1.18E+00 −7.44E+01 1.33E+00 −7.41E+01 3.49E+03 −2.1%
Non-renewable
energy
MJ primary 6.57E−01 0.00E+00 −1.51E+02 2.29E+00 −1.48E+02 3.56E+03 −4.1%
Mineral extrac-
tion
MJ extra 4.93E−04 0.00E+00 −7.77E−01 6.07E−03 −7.70E−01 2.05E+01 −3.8%
1579The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
accounting for land use emissions over time is being handled
by means of the global warming potential (GWP) concept in
line with the characterization of greenhouse gases usually
applied in LCA.
The displacement of marginal soybean production in Bra-
zil and the USA is important as much of the overall environ-
mental benefits of the inoculant are driven by this effect. It
is hence warranted to pay further attention to American soy-
bean markets. Studies show that the largest producers of soy-
bean namely Brazil, USA, and Argentina, affect one another
when changing their production as a consequence of price
and demand changes (Plato and Chambers 2004; Boerema
etal. 2016; Yao etal. 2018). For instance, an increased sup-
ply in South America reduces the soybean price in the USA
(Plato and Chambers 2004). This suggests that increased
supply in Argentina may change production in Brazil and
USA, but how production will change depends not only
on the price change but also on the demand, on production
costs, as well as on the stimulus for farmers to remain pro-
ducing soybean at a lower market price, among others. Cap-
turing such complexities and better estimating the short-term
effects that additionally produced soybean in Argentina will
have on the global market and marginal producers, would
require more sophisticated economic modelling, for instance
by a partial-equilibrium model. Such modelling can better
inform the assumptions made for the system expansion, i.e.,
determining the marginal producers and the effect that addi-
tionally produced soybean will have in the global marginal
market; thus, this is a matter for further research. Yet, we
believe the system expansion presented here is plausible and
representative of the dynamics of the global soybean market.
The upstream effect is positive for all impacts because
producing the inoculant is associated with an impact (in the
inoculant system) that is not part of the reference system.
Although the inoculant production inventory covers most
materials, transport, energy, and emissions reported by
Novozymes, three relevant materials are not included due
to lack of available relevant inventories for these materials.
A sensitivity scenario is explored to account for the possi-
ble effect of these inventories (ESM, Sect. 4). The scenario
confirms the relatively small contribution of this effect com-
pared to the other effects.
Finally, the downstream effect was either positive or
negative depending on the impact and the location. For
transport, we assumed the same distance from field to farm
for all locations thus the difference in impacts reflects only
the difference in yields. Similarly, for drying we assumed
the same moisture content of soybean in all countries;
thus, the difference in impacts only reflects the differ-
ence in yields. Estimates of the downstream effect would
improve with more location representative data on soybean
moisture and distances from field to farm.
4.2 DayCent uncertainties andlimitations
There are uncertainties and limitations around the replica-
tion of the inoculant action on soybean, as observed in the
field, within DayCent. The main assumption made is that the
inoculant only impacts soybean yield. This assumption could
lead to misrepresentations of some observed field behav-
ior and thus of the modelled emissions. For instance, the
field trial dataset reports yield and yield changes induced
Fig. 1 Data flows from field trials to life cycle inventories of reference and inoculant systems
1580 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
by the inoculant use. From the two, DayCent simulations
in this study reflect yield changes, misrepresenting, e.g.,
long-term soil or crop processes indirectly induced due to
the presence of the inoculant. Also, as detailed in Leggett
etal. (2017), the presence of the inoculant does not trigger
a unique response by the soybean crop. Yet, yield responses
to the inoculant within DayCent modelling in this study,
indicated an increase in yield always, possibly misrepre-
senting years where the yield decreased, as it reached its
genetic maximum (Leggett etal. 2017). In the absence of
ReferenceSystem(Ref)
InoculantSystem(B.j-LCO)
DisplacedMaterial/energy flow
Process
System expansion
Material/energyflow
Legend
Functional Unit
Displacedprocess
Energy (Fuel)
Capitalgoods
(machinery)
Corn Cultivation
(AR)
Area A(ha)
Freshcorn
Fertilizers
Energy (Fuel)
Capitalgoods
(machinery)Emissions
Crop residues
NetCO
2
-uptake
Land
Pesticides
Year 1
SoybeanCultivation
(AR)
Area A(ha)
Emissions
Crop residues
NetCO
2
-uptake
Year 2
Seeds
Fertilizers
Land
Pesticides
Seeds
Inputs
Inputs
Fresh Soybeans
Drying
Soybeans to market (Q)
Energy
Drying
Energy
Corn (Mg/ha *yr)
System expansion
Corn Cultivation
(AR)
Area A(ha)
Emissions
Crop residues
NetCO
2
-uptake
Year 1
SoybeanCultivation
(AR)
Area A(ha)
Emissions
Crop residues
NetCO
2
-uptake
Year 2
Inputs
Otherinputs
Coated
Seeds
Inoculant
production
Energy
Rawmaterials
Soybean
Cultivation
Area B
Inputs Fresh
soybeans
FreshSoybeans
Drying
Drying
Soybeans to market(Q+∆Q)
Energy
Soybeans to market (-∆Q)
Energy
Freshcorn
Drying
Energy
Corn (Mg/ha *yr)
Fig. 2 Reference (Ref) and the inoculant (B.j-LCO) systems for soybean production in a corn-soybean rotation
1581The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
more detailed experimental information that could be used
for model parameterizations and upgrade model predic-
tions, the approach adopted here is valid in providing an
understanding of the impact caused by the inoculant on
emissions as the assumptions underpinning model simu-
lations and implementation are in line with established
Fig. 3 Contribution analysis of the impacts of soybean production with (B.j-LCO) and without (Ref) the inoculant. A negative contribution
means a reduction of the impact. The field effect includes impacts from (in blue): field emissions, iLUC, field work, fertilizers, pesticides and
seeds; the downstream effect includes impacts from (in green) transport and drying; the yield effect includes impacts from the avoided soybean
(in yellow) and the upstream effect includes impacts from the inoculant (in black)
1582 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
modelling methodologies outlined in other studies (Fitton
etal. 2017). Besides, we expect that using yield changes
as the key DayCent model driver could represent well the
interactions between the inoculant, the plant, the yields and
hence the modelled emissions because of model-intercom-
paring studies (Fitton etal. 2019), that show that outputs
from DayCent matched both the emissions field-data and
also data for more complex models that could explicitly
model the relationship examined.
Moreover, the method used here to implement yield
changes within DayCent is also uncertain. As the inoculant
aims to promote the uptake of N from the soil by the soybean
plant, replication of this effect was undertaken by modify-
ing the maximum amount of N fixed per gram of C fixed
via net primary production (NPP) if there is insufficient N
within the soil. Gradual increase of this parameter was used
to characterize the effect the inoculant has on plant N uptake
in DayCent. All other inputs such as soil, climate, manage-
ment including fertilization, chemical treatment and residue
production and treatment, and corn and soybean growth
parameters remained constant. Thus, only one parameter
change represents the inoculant mode of action. A limita-
tion of this approach is that it was not possible to achieve
the exact percentage change in yield observed on the field,
and values presented in this analysis are based on the closest
long-term match. Moreover, other parameters could change
in reality due to the effect of the inoculant, and thus, they
could be misrepresented by the approach leading to a misrep-
resentation of emissions too, as discussed for the field effect.
Additional field data on such parameters could help improve
this limitation.
4.3 LCA uncertainty andsensitivities
Results of the uncertainty analysis confirm the improve-
ments in soybean cultivation impacts due to the inoculant
use including parametric uncertainty. No trade-offs appear,
i.e., 16 out of 16 impact categories are significantly lower
in the inoculant system when accounting for uncertainty.
The results to the three scenarios can be found in ESM,
Sect.4. The first scenario shows that annualized approaches
to calculate SOC emissions lead to lower benefits in global
warming impacts than the time-independent approach.
Thus, the field effect increases and therefore the benefits
of using the inoculant reduce if the annualized approach
is used. The second scenario was already discussed in
Sect.3.1. The third scenario shows that all effects remain
the same except for the yield effect that substantially
increases as iLUC emissions are the main contributor to this
effect, i.e., CO2 emissions from iLUC. Particularly, Brazil
has a high conversion rate of forests into arable land mainly
for cattle ranching and more recently for soybean cultivation
(Boerema etal. 2016).
4.4 Rough perspectives forinoculant use inall
Argentinian soybean production
The average production of soybeans in Argentina from 2015
to 2018 was 53 million metric tons (FAO 2020). The inocu-
lant is currently used on 5.5% of Argentinian soybean fields
but is expected to have the potential to give a yield response
on 80% of these fields if applied at full scale (D’Alessio
2020). If the inoculant were applied at this scale, the global
warming benefit would correspond to a reduction in green-
house gas emissions of 1.9 million Mg CO2e [i.e., 80%,
53 million Mg 45.6 kg CO2e Mg−1]. While this is a rough
extrapolation of the results for the Buenos Aires province
to the rest of the country, it gives an indication of total ben-
efits the inoculant could potentially provide (order of mag-
nitude). An important assumption behind these estimates is
an increasing demand of soybean. Since mid-1990s, imports
of soybean by China, the largest world importer, have been
increasing. Nonetheless, in the last couple of years, imports
by China show a more stable behavior (FAO 2021) so this
may be an assumption to revise for the short-term future.
5 Conclusions
We compared the life cycle environmental impacts of soy-
bean cultivation with and without the use of an inoculant
containing Bradyrhizobium japonicum and the signal mol-
ecule lipochitooligosaccharide (LCO) in the Buenos Aires
province of Argentina. This cradle-to-gate assessment
included the cultivation of soybean, the inoculant produc-
tion, and the postharvest activities including transport from
field to farm and drying of soybean until ready for market.
The environmental benefits from introducing the inoc-
ulant were assessed by investigating the effect of this
inoculant in four main stages. The upstream effect covers
the inoculant production. The field effect consists of the
change in field emissions triggered by the increased pro-
duction per ha in the inoculant system. The yield effect
accounts for the fact that additional production in the inoc-
ulant system is expected to replace soybean production
in the global marginal market of soybean and its linked
impacts. The downstream effect compares the postharvest
impacts of the additional production in the inoculant sys-
tem and in soybean production elsewhere (avoided).
The inoculant use in soybean production in Buenos Aires,
Argentina, reduced all studied environmental impacts.
Hence, the use of this inoculant leads to overall environmen-
tal benefits and no trade-offs. This is a key finding contrib-
uting to knowledge about environmental impacts emerging
from inoculants’ use. The main contributor to this benefit is
the yield effect. Most of these avoided impacts come from
iLUC CO2 emissions, which result from the assumed system
1583The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
expansion. Avoiding soybean production in Brazil and USA
is crucial for the environmental benefits found in this study.
Hence, the marginal soybean producers and the effect of the
additional production of soybean induced by the inoculant
use should be carefully determined and is a matter for further
research. The field effect is the second largest contributor
to the overall reduction in GHG emissions, mostly due to
the effect of the increased SOC activated by the inoculant
use, as modelled by DayCent in this study. DayCent results
carry uncertainties and limitations of modelling the mode
of action of the inoculant given the parametrization of the
model. In the absence of field data to better model emis-
sions and dynamics of nutrients in DayCent, uncertainties
remain, and these results represent a modelling explorative
exercise valid to understand possible dynamics and environ-
mental impacts driven by the inoculant use. The downstream
and upstream effects contribute insubstantially to the total
change in impacts when using the inoculant. These conclu-
sions hold for this particular inoculant used in the province
of Buenos Aires, Argentina, in a corn-soybean rotation.
Some of the limitations of this study and topics for fur-
ther research that could further refine calculations and help
improve the robustness of conclusions include addressing
missing data on the supply chains of some feedstocks to
produce the inoculant, further study of the assumption of
avoided soybean production taking place at the global mar-
ginal market of soybean which could be tested with more
sophisticated economic models, additional field data col-
lection to better parameterize modelled field emissions in
DayCent, field data collection on the residues production
and treatment, and including uncertainty of iLUC emis-
sions. Finally, other impacts such as water, biodiversity
and microflora impacts should also be considered in order
to have more complete environmental assessments of inoc-
ulants use, with broader focus besides productivity gains.
Supplementary information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s11367- 021- 01929-7.
Declarations
Conflict of interest Jesper H. Kløverpris is employed by Novozymes
who produce and market microbial inoculants as part of a larger port-
folio of biological solutions. Claus Nordstrøm Scheel was employed by
Novozymes when the study was conducted.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
References
Abodeely J, Muth D, Bryden KM (2012) Integration of the DAY-
CENT biogeochemical model within a multi-model framework.
In: iEMSs 2012 - Managing Resources of a Limited Planet: Pro-
ceedings of the 6th Biennial Meeting of the International Envi-
ronmental Modelling and Software Society
Abou-Shanab RAI, Wongphatcharachai M, Sheaffer CC etal (2017) Com-
petition between introduced Bradyrhizobium japonicum strains and
indigenous bradyrhizobia in Minnesota organic farming systems.
Symbiosis 73:155–163. https:// doi. org/ 10. 1007/ s13199- 017- 0505-4
Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in
enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol
85:1–12. https:// doi. org/ 10. 1007/ s00253- 009- 2196-0
Alori ET, Babalola OO (2018) Microbial Inoculants for Improving
Crop Quality and Human Health in Africa. Front Microbiol.
https:// doi. org/ 10. 3389/ fmicb. 2018. 02213
Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in
soybean in Brazil. Plant Soil 252:1–9. https:// doi. org/ 10. 1023/A:
10241 91913 296
Andrews M, James EK, Cummings SP etal (2003) Use of nitrogen
fixing bacteria inoculants as a substitute for nitrogen fertiliser
for dryland graminaceous crops: progress made, mechanisms of
action and future potential. In: Symbiosis
Backer R, Rokem JS, Ilangumaran G etal (2018) Plant growth-promoting
rhizobacteria: Context, mechanisms of action, and roadmap to com-
mercialization of biostimulants for sustainable agriculture. Front
Plant Sci 871:1–17. https:// doi. org/ 10. 3389/ fpls. 2018. 01473
Boerema A, Peeters A, Swolfs S etal (2016) Soybean trade: balancing
environmental and socio-economic impacts of an intercontinental
market. PLoS One 11:e0155222. https:// doi. org/ 10. 1371/ journ al.
pone. 01552 22
Chibeba AM, Guimarães MDF, Brito OR etal (2015) Co-inoculation
of soybean with Bradyrhizobium and Azospirillum promotes early
nodulation. Am J Plant Sci 6:1641–1649
D’Alessio (2020) Senior manager: Personal communication.
Novozymes
Dalgaard R, Halberg N, Kristensen IS, Larsen I (2006) Modelling
representative and coherent Danish farm types based on farm
accountancy data for use in environmental assessments. Agric
Ecosyst Environ 117:223–237. https:// doi. org/ 10. 1016/j. agee.
2006. 04. 002
De Klein C, Novoa RSA, Ogle S, Smith KA, Rochette P, Wirth, TC,
McConkey BG, Mosier A, Rypdal K, Walsh M, Williams SA
(2006) IPCC Guidelines for National GHG Inventories. Chap-
ter11: N2O Emissions From Managed Soils, and CO2 Emissions
From Lime and Urea Application
De Rosa M, Knudsen MT, Hermansen JE (2016) A comparison of land
use change models: challenges and future developments. J Clean
Prod 113:183–193. https:// doi. org/ 10. 1016/j. jclep ro. 2015. 11. 097
Del Grosso SJ, Parton WJ, Mosier AR etal (2006) DAYCENT
National-Scale Simulations of Nitrous Oxide Emissions from
Cropped Soils in the United States. J Environ Qual 35:1451–1460.
https:// doi. org/ 10. 2134/ jeq20 05. 0160
Del Grosso SJ, Parton WJ, Mosier AR, etal (2001) Simulated inter-
action of carbon dynamics and nitrogen trace gas fluxes using the
DAYCENT model. In: Schaffer M, Hansen LM (eds) Modeling
carbon and nitrogen dynamics for soil management. CRC press,
Boca Raton, Florida
1584 The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Di Benedetto NA, Corbo MR, Campaniello D etal (2017) The role of
Plant Growth Promoting Bacteria in improving nitrogen use effi-
ciency for sustainable crop production: a focus on wheat. AIMS
Microbiol 3:413–434. https:// doi. org/ 10. 3934/ micro biol. 2017.3. 413
Egamberdieva D, Jabborova D, Berg G (2016) Synergistic interactions
between Bradyrhizobium japonicum and the endophyte Stenotropho-
monas rhizophila and their effects on growth, and nodulation of
soybean under salt stress. Plant Soil 405:35–45. https:// doi. org/ 10.
1007/ s11104- 015- 2661-8
FAO (2018) FAOSTAT. Food and Agriculture Organisation of the United
Nations. http:// faost at. fao. org/. Accessed 20 Jul 2003
FAO (2020) FAOSTAT. Food and Agriculture Organisation of the United
Nations. http:// faost at. fao. org
FAO (2021) FAOSTAT. Food and Agriculture Organization of the United
Nations. http:// faost at. fao. org/. Accessed 15 Mar 2021
Fitton N, Bindi M, Brilli L etal (2019) Modelling biological N fixation
and grass-legume dynamics with process-based biogeochemical
models of varying complexity. Eur J Agron 106:58–66. https:// doi.
org/ 10. 1016/j. eja. 2019. 03. 008
Fitton N, Datta A, Cloy JM etal (2017) Modelling spatial and inter-
annual variations of nitrous oxide emissions from UK cropland and
grasslands using DailyDayCent. Agric Ecosyst Environ 250:1–11.
https:// doi. org/ 10. 1016/j. agee. 2017. 08. 032
Fitton N, Datta A, Hastings A etal (2014) The challenge of modelling nitro-
gen management at the field scale: simulation and sensitivity analysis
of N 2 O fluxes across nine experimental sites using DailyDayCent.
Environ Res Lett. https:// doi. org/ 10. 1088/ 1748- 9326/9/ 9/ 095003
Foley JA, Ramankutty N, Brauman KA etal (2011) Solutions for a cul-
tivated planet. Nature 478:337
Godfray HCJ, Beddington JR, Crute IR etal (2010) Food security: the
challenge of feeding 9 billion people. Science (80- ) 327:812–8.
https:// doi. org/ 10. 1126/ scien ce. 11853 83
Hauschild MZ, Potting J (2005) Spatial Differentiation in Life Cycle
Assessment: The EDIP2003 Methodology. Copenhagen
Horrigan L, Lawrence RS, Walker P (2002) How sustainable agriculture
can address the environmental and human health harms of industrial
agriculture. Environ Health Perspect 110:445–456. https:// doi. org/ 10.
1289/ ehp. 02110 445
ISO (2006) ISO 14044. Environmental management - Life cycle assess-
ment - Requirements and guidelines. Switzerland
Jolliet O, Margni M, Charles R etal (2003) IMPACT 2002+: A new
life cycle impact assessment methodology. Int J Life Cycle Assess
8:324. https:// doi. org/ 10. 1007/ BF029 78505
Keyser HH, Li F (1992) Potential for increasing biological nitrogen fixa-
tion in soybean. In: Ladha JK, George T, Bohlool BB (eds) Biologi-
cal Nitrogen Fixation for Sustainable Agriculture. Developments in
Plant and Soil Sciences. Springer, Dordrecht, The Netherlands
Kløverpris JH, Scheel CN, Schmidt J etal (2020) Assessing life cycle
impacts from changes in agricultural practices of crop production.
Int J Life Cycle Assess 25:1991–2007. https:// doi. org/ 10. 1007/
s11367- 020- 01767-z
Leggett M, Diaz-Zorita M, Koivunen M etal (2017) Soybean Response
to Inoculation with Bradyrhizobium japonicum in the United States
and Argentina. Agron J 109:1031–1038. https:// doi. org/ 10. 2134/
agron j2016. 04. 0214
Leggett M, Newlands NK, Greenshields D, West L, Inman S, Koivunen,
ME (2015) Maize yield response to a phosphorus-solubilizing
microbial inoculant in field trials. J Agric Sci. https:// doi. org/ 10.
1017/ S0021 85961 40011 66
Meena RS, Vijayakumar V, Yadav GS, Mitran T (2018) Response and
interaction of Bradyrhizobium japonicum and arbuscular mycorrhi-
zal fungi in the soybean rhizosphere. Plant Growth Regul 84:207–
223. https:// doi. org/ 10. 1007/ s10725- 017- 0334-8
Mekonnen MM, Hoekstra AY (2011) The green, blue and grey water
footprint of crops and derived crop products. Hydrol Earth Syst Sci
15:1577–1600. https:// doi. org/ 10. 5194/ hess- 15- 1577- 2011
Nadeem SM, Naveed M, Zahir ZA, Asghar HN (2013) Plant–microbe
interactions for sustainable agriculture: fundamentals and recent
advances. In: Arora NK (ed) Plant microbe symbiosis: fundamentals
and advances. Springer India, New Delhi, p 459
Oldfield EE, Bradford MA, Wood SA (2019) Global meta-analysis of the
relationship between soil organic matter and crop yields. Soil 5:15–32.
https:// doi. org/ 10. 5194/ soil-5- 15- 2019
Parton WJ, Holland EA, Del Grosso SJ etal (2001) Generalized model
for NO x and N 2 O emissions from soils. J Geophys Res Atmos
106:17403–17419. https:// doi. org/ 10. 1029/ 2001J D9001 01
Petersen BM, Knudsen MT, Hermansen JE, Halberg N (2013) An approach
to include soil carbon changes in life cycle assessments. J Clean Prod
52:217–224. https:// doi. org/ 10. 1016/j. jclep ro. 2013. 03. 007
Plato GE, Chambers W (2004) How does structural change in the global
soybean market affect the U.S. price?
Rockström J, Williams J, Daily G etal (2017) Sustainable intensification
of agriculture for human prosperity and global sustainability. Ambio.
https:// doi. org/ 10. 1007/ s13280- 016- 0793-6
Santos MS, Nogueira MA, Hungria M (2019) Microbial inoculants:
reviewing the past, discussing the present and previewing an out-
standing future for the use of beneficial bacteria in agriculture. AMB
Express 9:205. https:// doi. org/ 10. 1186/ s13568- 019- 0932-0
Schmidt J, Brandão M (2013) LCA screening of biofuels – iLUC, bio-
mass manipulation and soil carbon. Aalborg, Denmark
Schmidt J, De Rosa M (2018) Comparative LCA of RSPO certified and
non-certified palm oil – revised final draft after 1st round critical
review dated 19th March 2019. Aalborg, Denmark
Schmidt J, Saxcé DM (2016) Arla Foods Environmental Profit and Loss
Accounting 2014. Copenhagen
Schmidt JH, Weidema BP, Brandão M (2015) A framework for modelling
indirect land use changes in Life Cycle Assessment. J Clean Prod
99:230–238. https:// doi. org/ 10. 1016/j. jclep ro. 2015. 03. 013
Tilman D, Fargione J, Wolff B, etal (2001) Forecasting agriculturally
driven global environmental change. Science (80- ) 292:281 LP –
284. https:// doi. org/ 10. 1126/ scien ce. 10575 44
Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on
soil microbial communities: a review. Biomed Res Int 2013:1–11.
https:// doi. org/ 10. 1155/ 2013/ 863240
USDA (2019) Economic Research Service. https:// data. ers. usda. gov/
repor ts. aspx? ID= 17883. Accessed 20 Sep 2004
van Noordwijk M, Brussaard L (2014) Minimizing the ecological foot-
print of food: closing yield and efficiency gaps simultaneously? Curr
Opin Environ Sustain 8:62–70. https:// doi. org/ 10. 1016/j. cosust.
2014. 08. 008
Weidema B (2003) Market information in life cycle assessment
Weidema B, Hauschild M, Jolliet O (2008) Preparing characterisation
methods for endpoint impact assessment. In: Weidema BP, Wesnae
M, Hermansen J, etal. (eds) Environmental improvement potentials
of meat and dairy products. Institute for Prospective Technological
Studies, Seville
Weidema BP (2009) Using the budget constraint to monetarise impact
assessment results. Ecol Econ. https:// doi. org/ 10. 1016/j. ecole con.
2008. 01. 019
Weidema BP, Ekvall T, Heijungs R (2009) Guidelines for application of
deepened and broadened LCA, Deliverable D18 of work package 5
of the CALCAS project
Wernet G, Bauer C, Steubing B etal (2016) The ecoinvent database ver-
sion 3 (part I): overview and methodology. Int J Life Cycle Assess
21:1218–1230. https:// doi. org/ 10. 1007/ s11367- 016- 1087-8
Yao G, Hertel TW, Taheripour F (2018) Economic drivers of telecou-
pling and terrestrial carbon fluxes in the global soybean complex.
Glob Environ Chang 50:190–200. https:// doi. org/ 10. 1016/j. gloen
vcha. 2018. 04. 005
Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
1585The International Journal of Life Cycle Assessment (2021) 26:1570–1585
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com
Available via license: CC BY 4.0
Content may be subject to copyright.