Impacts of European livestock production: Nitrogen, sulphur, phosphorus and greenhouse gas emissions, land-use, water eutrophication and biodiversity

Abstract

Livestock production systems currently occupy around 28% of the land surface of the European
Union (equivalent to 65% of the agricultural land). In conjunction with other human activities,
livestock production systems affect water, air and soil quality, global climate and biodiversity, altering
the biogeochemical cycles of nitrogen, phosphorus and carbon. Here, we quantify the contribution of
European livestock production to these major impacts. For each environmental effect, the
contribution of livestock is expressed as shares of the emitted compounds and land used, as compared
to the whole agricultural sector. The results show that the livestock sector contributes significantly to
agricultural environmental impacts. This contribution is 78% for terrestrial biodiversity loss, 80% for
soil acidification and air pollution (ammonia and nitrogen oxides emissions), 81% for global warming,
and 73% for water pollution (bothNand P). The agriculture sector itself is one of the major
contributors to these environmental impacts, ranging between 12% for global warming and 59% for
Nwater quality impact. Significant progress in mitigating these environmental impacts in Europe will
only be possible through a combination of technological measures reducing livestock emissions,
improved food choices and reduced food waste of European citizens.

Full text

Environ. Res. Lett. 10 (2015)115004 doi:10.1088/1748-9326/10/11/115004
LETTER
Impacts of European livestock production: nitrogen, sulphur,
phosphorus and greenhouse gas emissions, land-use, water
eutrophication and biodiversity
Adrian Leip
1
, Gilles Billen
2
, Josette Garnier
2
, Bruna Grizzetti
1
, Luis Lassaletta
2,3
, Stefan Reis
4,9
,
David Simpson
5,6
, Mark A Sutton
4
, Wim de Vries
7,8
, Franz Weiss
1
and Henk Westhoek
3
1
European Commission, Joint Research Centre (JRC), Institute for Environment and Sustainability, Ispra (VA), Italy
2
CNRS-UPMC, UMR 7619 Metis, BP 105, 4 Place Jussieu, 75005 Paris, France
3
PBL Netherlands Environmental Assessment Agency, PO Box 303, 3720 AH, Bilthoven, The Netherlands
4
NERC Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian, EH26 0QB, UK
5
EMEP MSC-W, Norwegian Meteorological Institute, NO-0313, Oslo, Norway
6
Department Earth and Space Sciences, Chalmers University of technology, SE41308 Gothenburg, Sweden
7
Alterra, Wageningen University and Research Centre (WUR), PO Box 47, 6700 AA Wageningen, The Netherlands
8
Environmental Systems Analysis Group, Wageningen University, PO Box 47, 6700 AA Wageningen, The Netherlands
9
University of Exeter Medical School, Knowledge Spa, Truro, TR1 3HD, UK
E-mail: adrian.leip@jrc.ec.europa.eu
Keywords: livestock production, climate change, air quality, biodiversity loss, coastal eutrophication, soil acidification, European Union
Supplementary material for this article is available online
Abstract
Livestock production systems currently occupy around 28% of the land surface of the European
Union (equivalent to 65% of the agricultural land). In conjunction with other human activities,
livestock production systems affect water, air and soil quality, global climate and biodiversity, altering
the biogeochemical cycles of nitrogen, phosphorus and carbon. Here, we quantify the contribution of
European livestock production to these major impacts. For each environmental effect, the
contribution of livestock is expressed as shares of the emitted compounds and land used, as compared
to the whole agricultural sector. The results show that the livestock sector contributes significantly to
agricultural environmental impacts. This contribution is 78% for terrestrial biodiversity loss, 80% for
soil acidification and air pollution (ammonia and nitrogen oxides emissions), 81% for global warming,
and 73% for water pollution (both N and P). The agriculture sector itself is one of the major
contributors to these environmental impacts, ranging between 12% for global warming and 59% for
N water quality impact. Significant progress in mitigating these environmental impacts in Europe will
only be possible through a combination of technological measures reducing livestock emissions,
improved food choices and reduced food waste of European citizens.
Introduction
Nowadays agricultural land occupies about
180 million hectares or 42% of the land area of the
European Union
10
from which a great portion is used
as grassland and for cultivating feed (FAO 2006).
Historically, livestock helped to transform inedible
materials (grass and waste)into high quality food.
However today livestock production systems affect air
quality, global climate, soil quality, biodiversity and
water quality (Sutton et al 2011b,2011c), by altering
the biogeochemical cycles of nitrogen, phosphorus and
carbon. In particular, reactive nitrogen (N
r
)plays a key
role in several environmental impacts (N
r
represents
all forms of nitrogen other than N
2
, including ammo-
nia (NH
3
), nitrogen oxides (NO
x
), nitrous oxide
(N
2
O), and N losses to water bodies). Nitrogen
cascades or recycles through crop and livestock pro-
duction systems, in form of feed for livestock and of
manure to grow crops, as illustrated in figure 1, leading
to several un-intended flows that give rise to environ-
mental concerns (Sutton et al 2011a, Leip et al 2011a).
OPEN ACCESS
RECEIVED
27 June 2015
REVISED
1 September 2015
ACCEPTED FOR PUBLICATION
15 September 2015
PUBLISHED
4 November 2015
Content from this work
may be used under the
terms of the Creative
Commons Attribution 3.0
licence.
Any further distribution of
this work must maintain
attribution to the
author(s)and the title of
the work, journal citation
and DOI.
10
Data refer to the situation with 27 Member States, in this article
we will use the term ‘Europe’also to refer to the EU27.
© 2015 IOP Publishing Ltd

The emissions from the livestock sector contribute
to five major environmental impacts:
(i)The emissions of ammonia (NH
3
)and nitrogen
oxides (NO
x
=NO+NO
2
)contribute to the
formation of secondary particulate matter (PM)
and tropospheric ozone, both with serious
impacts on air quality. Across Europe, ammo-
nium in particles may account for 5–15% of total
PM
2.5
(Putaud et al 2010). Loss of statistical life
expectancy due to exposure to PM
2.5
is estimated
at 6–12 months for large parts in Europe (Amann
et al 2011).
(ii)Emissions from the livestock sector affect radia-
tive forcing in many ways; long-lived greenhouse
gases (GHGs)occur as methane (CH
4
), nitrous
oxide (N
2
O)and carbon dioxide (CO
2
)from the
use of fossil fuels or through land use and land
use change. Emissions of NO
x
contribute to
tropospheric ozone formation—an important
greenhouse gas in its own right—which reduces
carbon sequestration through damage to vegeta-
tion (Ainsworth et al 2012, Simpson et al 2014).
Conversely, aerosols produced by NO
x
-driven
photochemistry also affect climate, generally
having a cooling effect (Simpson et al 2014,
Shindell et al 2009). The interactions between
atmospheric chemistry, vegetation and aerosols
are complex and only partially understood (Ains-
worth et al 2012, Simpson et al 2014), but overall,
it is estimated that the emissions of N
r
from
Europe lead to a small, but uncertain, cooling
(Butterbach-Bahl et al 2011). Deposition of N
r
contributes also to additional carbon sequestra-
tion in forests by stimulating plant growth and
altering rates of ecosystem respiration, generally
reducing CO
2
concentrations (de Vries
et al 2011a, Zaehle et al 2011). Globally, livestock
systems are estimated to contribute about 14.5%
to total GHG emissions (Gerber et al 2013).
Estimates of the share of GHG emissions from
land use changes to total livestock emissions
range between 9%–35% (FAO 2006,2010,
Lesschen et al 2011, Weiss and Leip 2012).
(iii)Terrestrial biodiversity is affected by livestock
production through land use (including historic
land use changes), ammonia emissions and con-
sequent deposition and climate change. Inten-
sively managed grassland and arable land used to
grow livestock feeds have a low biodiversity,
while extensive grazing avoids shrub encroach-
ment or reforestation and helps maintain land-
scapes of high biodiversity. Habitat changes and
land fragmentation can lead to truncation of
Figure 1. Nitrogen cascade illustrating the central role of agriculture. The figure shows the input of new reactive nitrogen (N
r
)
production, contrasting the intended flows to and from European agriculture (black arrows), the unintended flows as this pass down
the cascade (red arrows), and the resulting environmental concerns (orange boxes). Updated from Sutton et al (2011a).
2
Environ. Res. Lett. 10 (2015)115004 A Leip et al

migratory routes or the replacement of native
species with invasive ones (Reid et al 2010).N
r
deposition reduces species richness through
eutrophication, acidification, direct foliar
impacts, and exacerbation of other stresses (Dise
et al 2011, Bobbink et al 2010).
(iv)Finally, livestock production has a role in the
deterioration of the quality of freshwater and
coastal water, increasing losses of N and phos-
phorus (P)to the water system. There is evidence
that concentrations of 25 mg L
−1
nitrate (NO
3
−
)
in drinking water are related to an increase of
incidences of colon cancer by about 3% (van
Grinsven et al 2010). The stoichiometric excess of
nitrogen and phosphorus in coastal water with
respect to silica (Si), can enhance water eutrophi-
cation (Billen and Garnier 2007, Grizzetti
et al 2011, Voß et al 2011).
In this study we quantified the contribution of
livestock production systems to the above mentioned
five impacts combining new data based on a cradle-to-
gate Life Cycle Assessment (LCA)calculation with
results of other studies on emissions at the European
scale. The results are discussed with respect to total
emissions in the EU27. Although several compounds
are included in the analysis, this paper will give parti-
cular attention to reactive nitrogen flows in agri-
cultural production systems.
Methods
Overall approach
We estimated emissions of CO
2
,CH
4
,N
2
O, NH
3
,
NO
x
,SO
2
, and N and P losses to the hydrosphere
related to livestock production in Europe and inter-
preted the results in the light of the five major
environmental threats. This was done by (i)extending
the LCA approach in the agro-economic Common
Agricultural Policy Regionalised Impact (CAPRI)
modelling system (Britz and Witzke 2012)
11
, devel-
oped for the assessment of GHG emissions and N
footprints, to provide cradle-to-farm gate LCA data
for reactive nitrogen, in combination with (ii)model
results for other compounds (P and SO
2
)to provide a
comprehensive picture of the environmental impact
of EU livestock production. Table 1gives an overview
of emission sources quantified indicating how they are
linked to livestock production systems. As the table
indicates, emissions caused by livestock rearing were
calculated for EU27 only. Emissions from imported
livestock products were not included in the analysis,
while further emissions associated with cultivation,
processing and transport of (non-forage)feed might
occur within or outside the EU.
The CAPRI N-LCA approach
The emissions of GHGs (N
2
O and CH
4
)and reactive
nitrogen (N
r
)to air (NH
3
,NO
x
)and water (N leaching
and runoff)and other N flows (such as trade of food
and feed)were estimated with CAPRI, using the
cradle-to-gate LCA approach implemented for the
estimation of GHG emissions (Weiss and Leip 2012)
and further extended to include the estimation of N
footprints per product group (Leip et al 2014b). Here
we present new data that have been calculated when
further extending the model with flows of all N
r
. All
new data presented here include emissions occurring
within Europe and outside the EU territory for
imported feed and/or land use change (LUC; LUC
emissions were calculated using the land use transition
probabilities of scenario II in Weiss and Leip (2012),
table A1). Also included are credits for carbon
sequestration in managed grassland as well as emis-
sions due to foregone carbon calculation in croplands
according to Weiss and Leip (2012). To analyze
Table 1. Overview of emissions caused by livestock rearing and feed that were quantified in the study.
Livestock rearing Feed
Direct and energy
a
Cultivation excl. energy
b
Energy incl. feed processing and
transport
c
Air quality NH
3
,NO
x
NH
3
,NO
x
NO
x
Climate change CH
4
,N
2
O, CO
2
(NH
3
,NO
x
)
N
2
O, CO
2
(NH
3
,NO
x
)CO
2
Soil quality NH
3
,NO
x
,SO
2
NH
3
,NO
x
NO
x
,SO
2
Terrestrial biodiversity CH
4
,N
2
O, CO
2
,
NH
3
,NO
x
N
2
O, CO
2
,NH
3
,NO
x
,
land use
NO
x
,CO
2
Quality of inland and coastal water N and P losses N and P losses
Note: Direct livestock rearing includes livestock housing and manure management and storage; energy consumption from housing, milking,
buildings etc. Cultivation of forages (grass, fodder maize, fodder beet etc)and other feed includes all direct and indirect emissions not linked
with the consumption of energy.
a
Place of emissions is EU27.
b
Place of emissions is EU27 for forages and both EU27 and rest of the world for other feed.
c
Place of emissions is both EU27 and rest of the world.
11
http://www.capri-model.org/
3
Environ. Res. Lett. 10 (2015)115004 A Leip et al

international N flows to and from EU27, the detailed
trade data matrix of the trade module in the FAOSTAT
database (FAOSTAT 2014)was used taking into
account the N content to the 504 commodities
involved (vegetal, animal and fiber products)(Lassa-
letta et al 2014). Internal flows among EU 27 countries
were calculated and subtracted. The net N import to
EU27 for each world country was estimated by the
difference between total imports and exports.
A general description of the CAPRI model and its
relevant modules can be found in Britz et al (2010),
Jansson and Heckelei (2011), Leip et al (2011b,2011d),
Britz and Wizke (2012)and Perez-Dominguez
et al (2012).
In the CAPRI LCA module (Weiss and Leip 2012,
Leip et al 2014b, Westhoek et al 2015), total agri-
cultural emissions E
agri
were estimated as the sum of
flows caused by agricultural production activities, plus
emissions caused in earlier phases of the products life
cycle, including energy use or land use change. Supple-
mentary Information S1 gives detailed results of the
N-LCA for the main six vegetable and six livestock
product groups to which the data were aggregated.
Differently from Weiss and Leip (2012)and in accor-
dance to Leip et al (2014b)the allocation of flows from
primary crop products to secondary products (e.g.
soya to soybean oil and soybean cakes)is done by
mass. The allocation of emissions from feed produc-
tion to specific livestock products makes use of the
animal budget module in CAPRI where energy and
protein requirements are matched with domestic and
imported feed supply, and data on farm expenditures
for feed (Britz and Witzke 2012, Leip et al 2011d).Ina
first step, emissions from crop activities are converted
into emission intensities and allocated to animal activ-
ities and in a second step to animal products (Weiss
and Leip 2012).
For our purpose, E
agri
was divided into emissions
related to livestock production E
lvst
and those related
to production of crops for other purposes (food, fuel,
fibre)E
crop
.E
lvst
includes emissions from livestock
production systems E
anim
(e.g. CH
4
emissions from
enteric fermentation, emissions from energy use for
milking etc)plus the emissions from feed production,
transport and processing E
feed
.
For each crop product, allocation to food or feed is
done on the basis of the market balance which is avail-
able in CAPRI at the national level (see supplementary
information S2). The share of total quantities of flows
allocated to food crops was calculated on the basis of
total domestic production (gross production)minus
the quantity used for feed, while the share of the flow
used to feed is allocated to livestock products based on
feed intake quantities. Emission sources considered
are given in table 2.1 by Westhoek et al (2015).While
this study is restricted to quantifying emissions from
EU27 agriculture, E
feed
includes both emissions from
domestic feed production E
feedeu
and emissions from
imported feed products E
feedrow
:
EEE
EEEE
.
agri lvst crop
feedrow feedeu anim crop
=+
=+++
Global warming
The contribution to global warming was assessed as
the sum of direct GHG emissions (CO
2
,N
2
O and
CH
4
), indirect N
2
O emissions and C sequestration.
Direct N
2
O and CH
4
emissions were from CAPRI-
LCA, using a global warming potential of
298 kg CO
2
eq (kg N
2
O)
−1
and
25 kg CO
2
eq (kg CH
4
)
−1
(IPCC 2007). Indirect N
2
O
emissions were estimated as 1% of the emitted N
(IPCC 2006). Indirect C sequestration in forests was
calculated using an average carbon uptake (sequestra-
tion)factor of 35 kg C per kg N deposited for Eur-
opean boreal and temperate forests (de Vries
et al 2014,2009)and a fraction of 0.25 kg N deposited
on forest per kg N emitted, based on EU27 total NH
3
–
N emissions from agriculture and NH
3
–N deposition
on forests (de Vries et al 2011b). Other ‘cooling
effects’(Butterbach-Bahl et al 2011)were not included
in the quantification.
Air quality
The contribution to air quality impacts was assessed
on the basis of the sum of NH
3
and NO
x
emissions, as
calculated with CAPRI N-LCA.
Soil acidification
Contribution to soil acidification was assessed on the
basis of the sum of SO
2
,NH
3
and NO
x
emissions. NH
3
and NO
x
emissions were calculated with CAPRI
N-LCA. Total SO
2
emissions were obtained from the
EDGAR data base (European Commission 2011).SO
2
emissions caused by agricultural activities were
approximated by the ratio of CO
2
emissions from
agriculture related to energy use (Weiss and Leip 2012)
and total energy CO
2
emissions in EU27 (EEA 2011).
This gives a share of about 6%, which is associated with
livestock products (4%)and vegetable products (2%),
in accordance with the global estimate of FAO
(FAO 2006).
The contribution of agricultural sources to
emissions of acidifying substances was estimated on
the basis of acidity equivalents (Schöpp and
Posch 2003). This method converts emissions of S,
NO
x
and NH
y
to acidity equivalents on the basis of
the molecular weight m(64, 46, and 17 for SO
2
,
NO
x
,andNH4
+, respectively)and the charge per
mole z(−2, −1, and +1forSO42-,
NO ,
3
-and
NH ,
4
+respectively)to get the conversion factors
0.03125 Geq (Gg SO
2
)
−1
, 0.02174 Geq (Gg NO
2
)
−1
,
and 0.05882 Geq (Gg NH
3
)
−1
.
Terrestrial biodiversity
The contribution of agriculture, livestock and feed to
loss of relative mean species abundance (MSA)was
estimated using shares of land use and emissions of
4
Environ. Res. Lett. 10 (2015)115004 A Leip et al

NH
3
,NO
x
, and net GHG exchange, accounting for C
sequestration, as calculated with the CAPRI-LCA. The
data are linked to the estimates of the effect of the main
drivers for biodiversity loss as calculated with the
GLOBIO-model (Alkemade et al 2009, Kram and
Stehfest 2012, van Vuuren et al 2015). This model gives
an absolute loss of 65% MSA caused by land conver-
sion into arable, grazing and forestry (35%, 15% and
14%, respectively), and to pressures such as N deposi-
tion (2%), climate change (3%)and land fragmenta-
tion (30%)(for details see supplementary
information S3).
Water quality
The contribution of agriculture, livestock and feed to
N
r
losses to the hydrosphere was derived from the
results of CAPRI N-LCA. Contribution of livestock
and feed to dissolved inorganic phosphorus (DIP)
losses has been calculated by applying the share of P in
fertilizers (mineral fertilizer and manure)per crop
from CAPRI LCA to Global NEWS results on total and
agricultural flows of DIP (Mayorga et al 2010).We
were unable to quantify the role of agriculture in the
load of particulate phosphorus (PP).
A quantification of the impact of N and P losses
was done by combining an analysis of potential risk of
eutrophication, based on the Indicator for Coastal
Eutrophication Potential (ICEP, Garnier et al 2010,
Billen et al 2011)with the estimation of livestock con-
tribution to river nutrient loads provided by the model
GREEN (Grizzetti et al 2012)in the different European
coastal areas (see supplementary information S4).
Results
The role of trade in N emissions in EU27 and other
world regions
Nflows from EU27 to other world regions and
vice versa for the year 2004 are illustrated in figure 2.
Much of the proteins grown in Europe are used to feed
livestock. From a total of 16.4 Tg N produced on
agricultural land in the year 2004 only 2.4 Tg N yr
−1
(about 15%)were supplied for direct human con-
sumption or further processing. Most of it was used as
animal feed (8.8 Tg N yr
−1
or 54%)or returned to the
soil as crop residue (5.1 Tg N yr
−1
or 31%). Further-
more, we estimate that livestock received
4.2 Tg N yr
−1
from imports or industry (Leip
et al 2014b, see also details in supplementary informa-
tion S2).
According to FAO trade statistics, EU27 was in
2004 a net importer of agricultural products with soy-
bean products for animal feed produced in Argentina,
Figure 2. Nflows from any EU27 to the other world regions and countries for the year 2004 calculated from FAO database
(FAOSTAT 2014, Lassaletta et al 2014). EU27 marked in black, blue countries are those which are net exporting N to Europe. Yellow,
orange, red countries are those which are net importing N from Europe. Arrows show flows between large regions and EU27. Flows
below 20 GgN are not represented.
5
Environ. Res. Lett. 10 (2015)115004 A Leip et al

Brazil and USA representing 84% of the total net
imports of EU27 (see figure 2; for a comparison of
EU27 and global agricultural structure and emissions
see supplementary information S5)that entails sig-
nificant trade of embodied cropland surface (MacDo-
nald et al 2015). According to calculations based on
FAOSTAT (2014)data, in 2004 about 70% of the Eur-
opean livestock production was used for intra-
national consumption and 18%–27% (respectively for
chicken and cattle meat, expressed in N)was traded
between EU27 countries with significant associated
embodied GHG emissions (Caro et al 2014). The EU
was thus close to self-sufficiency for meat and dairy
products, but the share of pig meat production was
much higher than in the rest of the world, while the
share of ruminant meat was significantly lower (22%
versus 29% globally).
The environmental impact of agriculture and
livestock production in EU27
Table 2shows the results for total agricultural
emissions from the EU27 agricultural sector and
emissions related to livestock production, feed pro-
duction and imported feed. Values are provided for
NH
3
,NO
x
,SO
2
, the combined effect of the three
pollutants converted to acidity equivalents, GHG
emissions (CH
4
,N
2
O, and CO
2
), C-sequestration,
water pollution by emissions of N and P (as dissolved
inorganic P, DIP), the land use and the contribution to
the loss of the MSA. Values reported in table 2refer to
the year 2004. Detailed results of the LCA calculation
(N
r
and GHG emissions)are given in supplementary
information S1.
Total agricultural emissions as compared with the
total EU27 emissions from all sources (Leip
et al 2011a)are given in table 3. Both total and agri-
cultural emissions refer to emissions from EU27 terri-
tory. Therefore, agricultural emissions in table 3do
not include emissions associated with imported feed
(see table 2).
Air quality
Agricultural sources of NH
3
from manure manage-
ment, and manure and mineral fertilizers on soils
totalled 2.8 Tg N yr
−1
in 2004. The contribution of
livestock production to total agricultural emissions
was particularly high for NH
3
(82%)due to the
importance of manure management. The share of
NH
3
emissions linked to livestock feed was 41% of
agricultural emissions, of which about 8% occurred
outside Europe.
Total agricultural NO
x
emissions at 0.46 Tg N yr
−1
were dominated by emissions from fossil fuel used for
farm operations and during processing or transport of
animal feed. The share of energy related emissions was
higher for crop products (88%)than for livestock pro-
ducts (77%)with an overall contribution to emissions
of 85% (0.39 Tg N yr
−1
). As there were only small NO
x
emissions from livestock production systems, most of
the emissions were related to feed production, proces-
sing and transport (0.23 Tg N yr
−1
)and we estimated
that about 51% of those occurred outside the EU terri-
tory or were linked to feed transport.
For the sum of NH
3
and NO
x
emissions, the share
of agricultural emissions from livestock was 80% due
to the dominance of NH
3
emissions. 42% of emissions
were related to feed production, and 10% were asso-
ciated with feed imports.
Global warming
The direct emissions of GHGs from the agriculture
sector itself in 2003–2005 was 483 Tg CO
2eq
yr
−1
,
contributing about 10% of total anthropogenic GHG
emissions in the European Union (EEA 2011). How-
ever, we estimated emissions of more than twice that
amount when including associated emissions that
agriculture causes in other sectors, such as energy,
industry, or land use and land use change (Weiss and
Leip 2012). Overall, 81% of total European agricul-
tural emissions (including associated emissions and
emissions from outside of the EU27)were caused by
livestock production. As much as 39% of agricultural
emissions were estimated to occur outside the EU
territory or from associated emissions. This includes
especially feed imports, feed transport and emissions
from land use change. Carbon sequestration
induced by N deposition on forests was found
to reduce agricultural emissions by about
100 Tg CO
2eq
yr
−1
(i.e., 10%). As agricultural N emis-
sions are closely linked to manure management (see
supplementary information S1), the N benefit for
carbon sequestration was mainly located within
the EU.
Soil quality
Emissions of acidity equivalents were dominated by
NH
3
which accounted for about 85% of the acidity
equivalent emissions for livestock (including asso-
ciated emissions).
Terrestrial biodiversity
Expressed in terms of MSA, we estimated that overall
agriculture, through arable and grazing and emissions
of N and GHG, caused a loss of 34% MSA, i.e., more
than half of the overall loss of biodiversity (Alkemade
et al 2009). Of this agriculture related loss, 76% was
estimated to be caused by livestock, with most of this
through feed production.
Quality of inland and coastal water
Nitrogen
Diffuse N losses from agricultural systems were
estimated at 6.0 Tg N yr
−1
. This represents percolation
of nitrate and organic nitrogen below the rooting zone
in agricultural soils, including both cropland and
pasture land, and run-off from soils or barn yards.
6
Environ. Res. Lett. 10 (2015)115004 A Leip et al

73% of these emissions were associated with livestock,
which was dominated by feed production. The share
of leaching and runoff occurring outside of the EU
territory was estimated at 10%.
Phosphorus
Diffuse losses of DIP from agriculture were estimated
at 0.025 Tg P yr
−1
, while weathering in agricultural
systems contributes an estimated additional
0.003 Tg P yr
−1
(Mayorga et al 2010). By far the
largest share of net P input (P input minus P crop
removal)was retained in the soil, which is considered
abenefit as long as this leads to increased soil fertility,
i.e., with low erosion. We do not have an estimate of
agricultural dissolved organic phosphorus (DOP)or
PP,asitisverydifficult to distinguish sources for
DOPandparticularlyforPPexport.However,most
likely the contribution of agriculture is much higher
for PP than for DIP while PP dominates P export. The
data presented in table 2relate to DIP only and are
therefore to be regarded as a conservative estimate for
the total contribution of agriculture to P flows to
coastal areas in Europe. Phosphorus losses from
livestock were entirely attributed to feed production,
with livestock DIP representing 73% of total agricul-
tural losses, even though some additional losses from
animal housing or manure storage systems might
occur.
We estimate that in Europe the livestock sector
accounts for 23%–47% of the nitrogen river load to
coastal waters, and 17%–26% of the phosphorus river
loads, where the lower limit is calculated considering
the contribution of manure alone and the upper limit
taking into account manure applications plus mineral
fertilizer (see supplementary information S4).
Discussion
To our knowledge, this is the first study to estimate the
contribution of livestock production systems, feed and
Table 2. Share of the livestock sector, feed production and feed imports on the emissions of pollutants due to agriculture in EU27 with
relevance for air quality, global warming, soil quality, biodiversity and water quality for the year 2004.
Air and soil quality Air and soil quality Air quality Global warming
NH
3
NO
x
NH
3
and NO
x
GHG
Emissions Share Emissions Share Emissions Share Emissions Share
[Tg N yr
−1
][Tg N yr
−1
][Tg N yr
−1
][Tg CO
2eq
yr
−1
]
Agriculture 2.8 100% 0.46 100% 3.2 100% 1062 100%
Livestock 2.3 82% 0.30 66% 2.6 80% 861 81%
Feed 1.1 41% 0.23 49% 1.4 42% 560 53%
Feed imports 0.2 8% 0.12 25% 0.3 10% 411 39%
Global warming Global warming Soil quality Soil quality
C-sequestration GHG +sequestration SO
2
NH
3
and NO
x
and SO
2
Emissions Share Emissions Share Emissions Share Emissions Share
[Tg CO
2eq
yr
−1
][Tg CO
2eq
yr
−1
]total [Teq yr
−1
][Teq yr
−1
]
Agriculture −104 100% 958 100% 0.021 100%
a,f
0.19 100%
Livestock −82 80% 779 81% 0.014 67% 0.15 79%
Feed −43 42% 516 54% 0.010 50% 0.08 42%
Feed imports −10 10% 400 42% 0.01 8%
d
Biodiversity
b
Biodiversity
b
Water quality N Water quality P
b
Land Use Loss of biodiversity N DIP
c
Area Share Relative Share Emissions Share Emissions Share
[Mio km
2
]MSA [%][Tg N yr
−1
][Tg P yr
−1
]
Agriculture 2.0 100% −34% 100%
a,e
6.0 100% 0.025 100%
Livestock 1.4 69% −25% 76% 4.4 73% 0.018 73%
Feed 1.4 69% −25% 74% 4.2 71% 0.018 73%
Feed imports 0.2 11% 0.6 10%
Notes
a
Own calculation;
b
Emissions occurring outside Europe not included in these estimates;
c
DIP emissions represent about 50% of total P export to the coastal zones;
d
Not considering SO
2
;
e
Alkemade et al 2009;
f
EEA 2011.
7
Environ. Res. Lett. 10 (2015)115004 A Leip et al

feed imports to total agricultural emissions and their
related environmental impact at a comparable level of
detail. Plausibility of results have been discussed in
depth with regard to GHG emissions (Weiss and
Leip 2012)and N-footprints (Leip et al 2014b). Esti-
mates of the share of N
r
emissions however are
different from those given in Leip et al (2014b), as the
authors calculated the shares on the basis of domestic
consumption (human consumption or processing)
while in this study we calculated the share on the basis
of total production. Below, we first discuss uncertainty
aspects of our emission estimates and estimates of
emission shares, followed by options to reduce the
environmental impact.
Uncertainty of emission estimates
For N, combining NH
3
+NO
x
emissions, our
estimate of 2.6 Tg N yr
−1
from agricultural sources
using the CAPRI model (excluding energy related
NO
x
)is 19% and 7% smaller than official estimates
of the European Union of 3.2 Tg N yr
−1
(EEA 2014)
and the estimate of the MITERRA model of
2.8 Tg N yr
−1
(Westhoek et al 2014), respectively.
The estimated total N excretion in CAPRI, at
8.9 Tg N yr
−1
,is88%oftheofficial estimate in EEA
(2014, EEA 2014).Thisdifferencecanbeexplained
by the fact that CAPRI calculates N excretion on the
basis of a consistent IPCC Tier 2 approach (animal
budget, Leip et al 2011b,IPCC2006)across all
Table 3. Comparison of estimated agricultural emissions in this study (from Table 2)and reported total EU27 emissions.
Total Agricultural LCA
impact within EU27
territory
Total EU27
budget
impact Data source for total EU27 impact
NH
3
emissions
[Tg N yr
−1
]
2.6 2.7 EDGAR data base (European Commission 2011)for
non-agricultural emissions
NO
x
emissions [Tg N yr
−1
]0.3 2.6 EDGAR data base (European Commission 2011)
GHG emissions 651 4889 EU GHG inventory (EEA 2011)
CH
4
+N
2
O+CO
2
emissions
[Tg CO
2eq
yr
−1
]
Carbon sequestration −93 −171 Same method as for agricultural C sequestration
[Tg CO
2eq
yr
−1
]
SO
2
[Teq yr
−1
]
0.021 0.3 EDGAR data base (European Commission 2011)
Land Use 1.8 4.2 FAOSTAT
Area
[Mio km
2
]
Air quality 2.9 5.3
NO
x
+NH
3
emissions
[Tg N yr
−1
]
Global warming 558 4718
GHG +C sequestration
[Tg CO
2eq
yr
−1
]
Soil quality 0.18 0.56
NO
x
+NH
3
+SO
2
[Teq yr
−1
]
Loss of biodiversity
[relative MSA]
−25% −65% Alkemade et al (2009)
Water quality N
N
[Tg N yr
−1
]
5.4 9.1 European Nitrogen Assessment (Leip et al 2011a)for
non-agricultural sources (sewage, forest including
background, deposition on water surfaces)
Water quality P 0.025 0.25 Mayorga et al (2010)
DIP
[Tg P yr
−1
]
8
Environ. Res. Lett. 10 (2015)115004 A Leip et al

countries, while national inventories in Europe are
constructed with a large variety of methods and data
quality (Leip 2010). National estimates would be of
higher quality than CAPRI estimates from countries
with good data (Leip et al 2014b),butsome
countries still need to improve their methodology
(EEA 2014). Furthermore, CAPRI uses ammonia
abatement measures from the GAINS model (Kli-
mont and Winiwarter 2011)which may not have
been considered in national inventories (Leip
et al 2010).
In comparison with 4.4 Tg N yr
−1
agricultural
NH
3
emissions in the EDGAR data base, our estimate
of 2.6 Tg N yr
−1
for EU27, excluding emissions from
imported feed, is lower. The reason for this might be
the lower excretion estimates, although the NH
3
emis-
sions are in line with estimates by the MITERRA
model.
While 85% of NO
x
emissions were related to
energy use, only 0.07 Tg N yr
−1
were from non-energy
sources. A quality check of the total agricultural emis-
sion estimate for NO
x
is difficult as no comparable
study exists including both NO
x
budget flows and NO
x
emissions related to energy consumption in agri-
cultural systems. Energy consumption in agriculture is
calculated in CAPRI with a dedicated energy module
which is also used for GHG emission estimates (Kem-
pen and Kraenzlein 2008, Weiss and Leip 2012); this is
also the basis of the estimated contribution of SO
2
emissions. The share of agricultural NO
x
and NH
3
to
total emissions is within −6% to +16% of earlier esti-
mates (Leip et al 2011a).
Our estimate for the share of agricultural GHG
emissions to total GHG emissions based on table 3is
about 13%. It ranges between the value of the official
EU GHG inventory (10%, EEA 2014)and other esti-
mates on the shares of agriculture or even livestock
production on total GHG emissions (Gerber
et al 2013, FAO 2006, Weiss and Leip 2012). The offi-
cial GHG inventory considers only emissions reported
in the agriculture sector, whereas LCA studies also
include emissions from Land Use Change (LUC)and
from imported feeds, which amounted to 39% of total
agricultural emissions (see table 2).
Our estimate for N
2
O emissions from agricultural
soils is considerably lower than official estimates; a
comparison of N
2
O emissions between various mod-
els (de Vries et al 2011b)showed overall satisfying
agreement. No methodology is able to capture the
huge variability of N
2
O emissions caused by changing
soil and climate conditions. In view of the general lack
of experimental observations, even process-based
models are not able to achieve a closer match than
independent calculations using inverse methods (Leip
et al 2011c).
LUC is certainly one of the most difficult sources
to quantify, as it requires data (or good assumptions)
on how much LUC is occurring as a consequence of EU
agricultural and livestock production, as well as what
kind of LUC is triggered. Indeed, the debate on the best
method to estimate LUC emissions from agricultural
products is still ongoing (European Commis-
sion 2013). The method developed in the CAPRI
model (Leip et al 2010, Weiss and Leip 2012)was based
on the assumptions that the agricultural market is very
fluid and no differentiation between direct and indir-
ect LUC is possible. The approach considers only LUC
linked to an expansion of harvested area, very similar
to the methods proposed by recent guidelines (Food
SCP RT 2013, leap 2014). We used unique LUC factors
for imports from a country outside the EU as weighted
average for all importing countries accounting for
globally connected and substitutable trade flows.
We are aware of the debate on the permanency of
carbon sequestration in grassland (Smith 2014), how-
ever the approach by Weiss and Leip (2012)is based on
the observation that enhanced carbon sequestration
rates in grassland are observed also after the 20 years
equilibrium time usually used by IPCC methodologies
(IPCC 2006), which is also consistent with recent
simulations with the CENTURY model (Lugato
et al 2014).
Carbon sequestration in forests has been estimated
earlier at the scale of the EU27 for the year 2000 by
multiplying an estimated N deposition caused by agri-
cultural NH
3
emissions of 0.61 Tg N yr
−1
with a C
response of 50 kg C per kg N deposited leading to a C
sequestration near 30 Tg C yr
−1
or 112 Tg CO
2
yr
−1
(de Vries et al 2011a), being very close to our estimate
of 104 Tg CO
2
yr
−1
. In our study the estimated N
deposition was larger (0.82 Tg N yr
−1
)while the C:N
response was estimated at 35 kg C perkg N deposited.
Estimates of agricultural N-leaching range from
2.0 to 5.7 Tg N yr
−1
(de Vries et al 2011b), the higher
value being also found in the EU GHG inventory
(EEA 2014). Possible reasons for these differences—in
addition to those already discussed—are available cali-
bration data for nitrate concentrations which might
neglect flows of organic nitrogen to water, and the split
of total N between the highly uncertain N
2
emissions
and N leaching/runoff (de Vries et al 2011b). Our esti-
mate of nitrate leaching at 5.4 Tg N yr
−1
is consistent
with the estimate of the European Nitrogen Budget
(Leip et al 2011a)which is used in table 3for total N
input to water. Although livestock dominated overall
agriculture P flows (73%), agriculture is responsible
for only 10% of the total riverine P export (table 3).
This is because point sources from human wastewater
dominate (accounting for 0.21 Tg P yr
−1
out of a total
riverine DIP export of 0.25 Tg P yr
−1
). The contribu-
tion of agriculture to the total P load (including DIP,
dissolved organic P, DOP and particulate P, PP)may
however be larger, specifically for PP, which is about
40% of the total P export to waters in Europe (50% is
DIP and 10% is DOP). The share of agriculture in PP
export is determined by (i)surface runoff of P in parti-
cles of fertilizer and manure, (ii)agricultural practices
(e.g. tillage)that affect the erosion rate and (iii)
9
Environ. Res. Lett. 10 (2015)115004 A Leip et al

elevated P contents of soil material eroded from agri-
cultural fields due to application of P fertilizers and
animal manure. The effects of agriculture on PP
export are likely to occur much faster than the strongly
delayed effect of DIP export through the soil systems
but these mixed contributions make it very hard to
assess what the agricultural contribution to the PP
load is.
Finally, we have used the MSA indicator as a mea-
sure for terrestrial biodiversity. MSA represents an
index of the naturalness of an ecosystem. Compared
with more traditional measures (e.g. monitoring spe-
cies changes), this measure has two main advantages: it
is possible to attribute biodiversity loss to certain sec-
tors (PBL 2014), and the effect of alternative scenarios
on biodiversity can be quantified (PBL 2012,2014).
The patterns of change indicated by the MSA are lar-
gely similar to those indicated by other measures as the
living planet index as developed by WWF or red list
indices (SCBD 2014). A limitation of the MSA indi-
cator is that it does not yield comprehensive informa-
tion on the actual distribution and abundance of
species, such as the status of endangered or threatened
endemic species.
Uncertainty of the estimated shares
While some uncertainty is associated with the indivi-
dual emission estimates, other parameters might
dominate the uncertainty of the estimated shares. For
example, while the estimate of N
2
O emission factors
might be associated with an uncertainty of up to 50%
(at the European scale), the uncertainty around the
estimated share of crops that is used as feed determines
the uncertainty of livestocks’contribution on total
agricultural N
2
O emissions. A bias in the total feed
translates directly into a bias of the estimated share of
emissions from livestock production, as it not only
determines the share of crops used as feed, but also the
amount of CH
4
emissions from enteric fermentation
in ruminants and manure excretion (which is calcu-
lated on the basis of animal retention data)and
consequent emissions from manure management.
This value is obtained from statistical sources (market
balances)and is further constrained by energy and
nutrient requirement calculations for major livestock
types.
No data are available whether farmers prefer
domestically produced crops or imported crops for
feed; therefore this value is highly uncertain. Because
of the lack of information, we considered equal pre-
ference. However, this uncertainty concerns only pri-
mary crops that are used for both food and feed, which
make only 12% of the total feed, while the rest comes
from non-marketable crops (82%), such as grass, fod-
der maize and beet, or secondary crops (6%). Non-
marketable crops are all domestically produced; sec-
ondary feed stuff is dominated by imported soya bean.
Options for reducing the environmental impact of
livestock production
There are two main routes to reduce the environmen-
tal impacts of livestock production:
(i)technical measures (reduce emissions intensity/
land use intensity and
(ii)lower livestock production in the EU with
demand side measures, i.e., a reduction of food
losses and wastes and/or dietary shifts.
Our study presents a ‘status quo’analysis (attribu-
tional LCA)and does not examine emissions without
(or with less)livestock production (case ii). What
would happen if livestock production is reduced in
Europe has been discussed in depth in Westhoek et al
(2014,2015). Based on the observation that the intake
of protein as well as saturated fats by European inhabi-
tants is far above the maximum recommended level
(WHO 2007, Westhoek et al 2011), the authors
showed that reducing the consumption of meat, dairy
and eggs in the EU27 by 50% would lead to a decrease
of N
r
emissions by 40% and a reduction of GHG emis-
sions by 25%–40% with expected substantial health
benefits (Westhoek et al 2014,2015). Those results
hold for two contrasting scenarios on the use of the
‘freed’land that would not anymore be required for
feed production, i.e., a ‘greening scenario’with
enhanced production of bio-energy and a ‘high price’
scenario with increasing export of cereals. They can be
regarded as conservative scenarios, as beneficial envir-
onmental effects outside Europe had not been quanti-
fied, such as the subsequent prevention of land
conversion outside Europe (Stehfest et al 2013), or the
reduction of GHG emissions from bio-energy produc-
tion (or other options such as afforestation).
From the production side many technical, struc-
tural or policy mitigation options are being dis-
cussed, addressing feed production (e.g., precision
agriculture and agronomic nitrogen use efficiencies),
livestock production (e.g. grazing and feeding man-
agement and feed supplements, improved herd
structures), or housing and manure management
(Thornton and Herrero 2010,Gerberet al 2013,
Golub et al 2013,USDA2013,Cohnet al 2014,Havlík
et al 2014,Houet al 2014, Van Middelaar et al 2014,
Winiwarter et al 2014, Van Doorslaer et al 2015).The
benefits of sustainable extensification practices have
also recently been explored for Europe (van Grinsven
et al 2015).Bouraouiet al (2014)have shown that
high reductions of nitrogen losses to water could be
achieved in Europe by an optimized use of organic
manure. Additional emission reductions could be
achieved by decreasing the wastage of the supplied
proteins (Westhoek et al 2011, Bellarby et al 2013,
Grizzetti et al 2013).
10
Environ. Res. Lett. 10 (2015)115004 A Leip et al

Conclusions
This analysis shows that, while agricultural activities
are a major source of pollutants and land use change,
livestock production systems dominate the environ-
mental consequences. For the five threats considered
here, livestock production contributed between 73%
(water quality)to about 80% (biodiversity, air quality,
soil acidification and global warming)of the overall
agricultural impact.
The results point to the fact that in Europe serious
efforts in mitigating the major environmental pro-
blems for Europe from agriculture need to address the
livestock sector. While technical measures can clearly
contribute significantly to emission reductions, they
cannot alone be sufficient (Bellarby et al 2013, Bajželj
et al 2014, Eshel et al 2014, Leip et al 2014a, Witzke
et al 2014, Pierrehumbert and Eshel 2015, Vanham
et al 2015). The issues of what European citizens eat
and their food waste also need to be addressed. For
example, recent scenarios showed that all these actions
would be necessary to achieve a stabilization in global
N
2
O emissions (UNEP 2013).
Moreover, while a shift of production from Eur-
ope to other world regions might make Europe ‘clea-
ner’, this would possibly come at the cost of higher
emission intensities in other regions of the world
where production systems might be less optimised
(FAO 2010, Cederberg et al 2011, Gerber et al 2013);
this could increase the environmental footprint of
products consumed in Europe, unless additional
actions were taken to address this.
Our study shows that there are intimate links
between key environmental threats, emissions of N
r
to
the environment, the production of animal products
and our diet choices.
Acknowledgments
The authors would like to thank the European
Commission funded research projects NitroEurope-
IP (FP6-017841), ANIMALCHANGE (FP7-266018),
and ECLAIRE (FP7-282910)for supporting the
research and collaboration underpinning the results
presented in this paper. We also like to thank Dr Jean
Philippe Putaud (EC-JRC)for helpful discussion on
the aerosol phenomenology and Dr Faycal Bouraoui
(EC-JRC)for discussion on the results of the model
GREEN.
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