Received: 27 July 2020 | Accepted: 31 August 2020

DOI: 10.1111/gcb.15342

RESEARCH REVIEW

Can N2O emissions offset the benefits from soil organic carbon
storage?

Bertrand Guenet1 | Benoit Gabrielle2 | Claire Chenu2 | Dominique Arrouays3 |

Jérôme Balesdent4 | Martial Bernoux5 | Elisa Bruni1 | Jean-Pierre Caliman6 |
Rémi Cardinael7,8,9 | Songchao Chen3 | Philippe Ciais1 | Dominique Desbois10 |
Julien Fouche11 | Stefan Frank12 | Catherine Henault13 | Emanuele Lugato14 |
Victoria Naipal1 | Thomas Nesme15 | Michael Obersteiner12 | Sylvain Pellerin15 |
David S. Powlson16 | Daniel P. Rasse17 | Frédéric Rees2 | Jean-François Soussana18 |
Yang Su2 | Hanqin Tian19 | Hugo Valin12 | Feng Zhou20
1
Laboratoire des Sciences du Climat et de l'Environnement, CEA-CNRS-UVSQ-UPSCALAY, Gif sur Yvette, France
2
UMR ÉcoSys, INRAE, AgroParisTech, Université Paris-Saclay, Paris, France
3
INRAE, InfoSol Unit, Orléans, France
4
Aix-Marseille Université, CNRS, IRD, INRAE, Coll France, CEREGE, Aix en Provence, France
5
Food and Agriculture Organization of the United Nations (FAO), Climate and Environment Division, Rome, Italy
6
SMART Research Institute (SMARTRI), Riau, Indonesia
7
CIRAD, UPR AIDA, Harare, Zimbabwe
8
AIDA, Univ Montpellier, CIRAD, Montpellier, France
9
Crop Science Department, University of Zimbabwe, Harare, Zimbabwe
10
UMR Économie publique, INRAE-AgroParisTech, Université Paris Saclay, Paris, France
11
Institut Agro, LISAH, Univ Montpellier, INRAE, IRD, Montpellier, France
12
IIASA, International Institute for Applied Systems Analysis, Laxenburg, Austria
13
Agroécologie, AgroSup Dijon, INRAE, Univ. Bourgogne Franche-Comté, Dijon, France
14
European Commission, Joint Research Centre (JRC), Directorate for Sustainable Resources, Ispra, Italy
15
ISPA, INRAE, Bordeaux Sciences Agro, Univ. Bordeaux, Villenave d'Ornon, France
16
Department of Sustainable Agriculture Sciences, Rothamsted Research, Harpenden, UK
17
Department of Biogeochemistry and Soil Quality, NIBIO – Norwegian Institute of Bioeconomy Research, Ås, Norway
18
INRAE, Paris, France
19
International Center for Climate and Global Change Research, School of Forestry and Wildlife Sciences, Auburn University, Auburn, AL, USA
20
Sino-France Institute of Earth Systems Science, Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences, Peking University,
Beijing, P. R. China

Correspondence
Bertrand Guenet, Laboratoire des Sciences Abstract
du Climat et de l'Environnement, CEA- To respect the Paris agreement targeting a limitation of global warming below 2°C
CNRS-UVSQ-UPSCALAY, F-91191 Gif sur
Yvette, France. by 2100, and possibly below 1.5°C, drastic reductions of greenhouse gas emissions
Email: [email protected] are mandatory but not sufficient. Large-scale deployment of other climate mitiga-
Present address tion strategies is also necessary. Among these, increasing soil organic carbon (SOC)
Bertrand Guenet, Laboratoire de Géologie stocks is an important lever because carbon in soils can be stored for long periods
de l'ENS, PSL Research University, Paris,
France

See also the Commentary on this article by Davies et al., 27, 218–­219.

Glob Change Biol. 2021;27:237–256. wileyonlinelibrary.com/journal/gcb© 2020 John Wiley & Sons Ltd | 237
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238 GUENET et al.

Funding information
National Natural Science Foundation of and land management options to achieve this already exist and have been widely
China, Grant/Award Number: 41671464; tested. However, agricultural soils are also an important source of nitrous oxide (N2O),
Agence Nationale de la Recherche, Grant/
Award Number: ANR-16-CONV-0003 a powerful greenhouse gas, and increasing SOC may influence N2O emissions, likely
causing an increase in many cases, thus tending to offset the climate change benefit
from increased SOC storage. Here we review the main agricultural management op-
tions for increasing SOC stocks. We evaluate the amount of SOC that can be stored
as well as resulting changes in N2O emissions to better estimate the climate benefits
of these management options. Based on quantitative data obtained from published
meta-analyses and from our current level of understanding, we conclude that the
climate mitigation induced by increased SOC storage is generally overestimated if
associated N2O emissions are not considered but, with the exception of reduced till-
age, is never fully offset. Some options (e.g. biochar or non-pyrogenic C amendment
application) may even decrease N2O emissions.

KEYWORDS
biochar, cover crops agroforestry, erosion, greenhouse gas emissions, land-based mitigation,
organic amendment, soil organic carbon, tillage

1 | I NTRO D U C TI O N C to a depth of 1 m (Ciais et al., 2013). However, the ecosystems

which contain the largest stocks of soil organic carbon (SOC) are un-
The United Nations Framework Convention on Climate Change managed (comprising boreal forests, permafrost soils and wetlands),
(UNFCCC) Paris Agreement adopted in 2015 aimed at keeping global whereas only soils from managed ecosystems, in particular agricul-
warming below 2°C by 2100, and at possibly further limiting the tem- tural soils, may be managed to increase SOC stocks (i.e. carbon se-
perature increase to 1.5°C. This requires not only drastic reductions questration). Agriculture is also a key target sector for the reduction
in GHG emissions in the near future, but also net negative emission of methane (CH4) and nitrous oxide (N2O) emissions (IPCC, 2019;
technologies because not all emissions will be reducible to zero Tian et al., 2016; Wollenberg et al., 2016). Yet, few countries have
within this time scale (Rogelj et al., 2015; Seneviratne et al., 2018). To included agriculture in their nationally determined contributions—a
a large extent, these negative emissions imply land-based mitigation roadmap volunteered by national governments as part of the Paris
strategies (IPCC, 2018), mostly involving the production of organic Agreement to express their efforts to reduce GHG emissions—
matter by plant photosynthesis coupled with carbon storage in living because of potential trade-offs with food production and uncertain-
biomass and/or soil organic matter (SOM; Paustian et al., 2016). ties on achievable potentials (Frank et al., 2017).
A pathway frequently discussed known as bioenergy with car- Recent emphasis on promoting SOC storage has resulted in
bon capture and storage (BECCS) comprises generating energy using international initiatives such as the ‘4 per mil’ initiative launched
biomass, capturing the CO2 evolved from this process and storing by France during the UNFCCC conference of the parties (COP) 21
it in geological reservoirs. The deployment of BECCS faces both (Minasny et al., 2017; Soussana et al., 2019). It relies on the concept
technical challenges and most likely limitations due to high costs and that even a very small relative increase in SOC pools worldwide
adverse environmental impacts such as increased pressure on land could offset a significant fraction of CO2 emissions. Preliminary
and water resources (Obersteiner et al., 2018; Smith et al., 2016). evaluation indicated that increasing global agricultural SOC stocks
On the other hand, the net removal of atmospheric CO2 taken up at an annual rate of 4‰ would result in a C sequestration poten-
by plants in agricultural soils (i.e. carbon sequestration) has recently tial of 2–3 Pg C/year (Minasny et al., 2017). This may contribute
come under sharp focus as a more affordable and practical alter- significantly to the objectives of the land sector to achieve the
native, potentially associated with positive economic outcomes and Paris agreement target (Roe et al., 2019). Moreover, even if it
possibly applicable at large scale in managed lands (Hepburn et al., would not be sufficient to totally offset anthropogenic emissions,
2019; Minasny et al., 2017). SOC increase is generally associated with several positive feed-
The role of soils as a key component of the global carbon cycle backs on biodiversity, crop yields, soil water retention, etc. (Mäder
is now recognized by the scientific community and also by policy- et al., 2002; Soussana et al., 2019). Nevertheless, several stud-
makers (Obersteiner et al., 2018; Smith et al., 2016). Soils have never ies have discussed and criticized the feasibility of enriching soils
been harnessed at large scale for the purpose of sequestering car- at a rate of 4‰ over a sustained period of years (Chabbi et al.,
bon, although they currently make up the largest reservoir of organic 2017; Poulton et al., 2018; Van Groenigen et al., 2017) because:
carbon in the terrestrial biosphere, with a size of 1,500–2,400 Pg (a) it requires large amounts of new organic matter inputs, (b) it
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GUENET et al. 239

requires large amounts of nutrients, (c) it is difficult to achieve this storing practices may incur costs, thus affecting farmers' profitabil-
target rate in all agricultural systems, and (d) it may be hampered ity and implying a need for governmental payments, depending on
by the climate change-induced enhancement of SOC decomposi- CO2 price. Smith et al. (2008) estimated that 47%, 65% and 86% of
tion. Moreover, altered management practices may impact farm- the technical potential SOC storage in agricultural lands could be
ers' income and imply trade-offs with food production (Poulton reached at costs of 20, 50 and 100 USD per ton of CO2 respectively.
et al., 2018). Data from long-term experiments show that it is very The SOC storage potential of the various practices has been exten-
difficult to achieve the 4 per mil rate in temperate arable systems sively assessed in the recent scientific literature (Cardinael, et al.,
without drastic changes in management (Batjes, 2019; Poulton 2018; Chenu et al., 2019; Fujisaki et al., 2018; Ogle et al., 2019;
et al., 2018). Finally, the annual rate of SOC increase generally lev- Paustian et al., 2016; Poulton et al., 2018), and recently revised by
els off over time as the SOC pool increases and approaches a new IPCC in its 2019 report on climate change and land (IPCC, 2019).
equilibrium level (Stewart et al., 2007). However, implications for the N cycle (in particular N2O emissions),
Nevertheless, concrete management options exist to increase and other biogeochemical cycles or crop yields have not been thor-
SOC stocks such as cover crops, tillage management, crop rotations, oughly documented so far (Bossio et al., 2020; Lugato et al., 2018;
organic amendments, agroforestry and biochar amendments with Oldfield et al., 2019). Neither have been the consequences of large-
effects depending on local conditions (Chenu et al., 2019; Corbeels scale deployment of these measures, and constraints related to
et al., 2019; Dignac et al., 2017). These options have socio-economic the nitrogen (N), phosphorous (P) and potassium (K) cycles. These
impacts on farmers and land managers and indirect effects on eco- aspects are important because they determine the overall GHG
system services, through changes in crop yields, water consump- abatement efficiency of mitigation measures and set limits on their
tion, nitrate leaching and CH4 and N2O emissions which have to potential deployment.
be considered when evaluating the feasibility and the relevance of C and N cycles are strongly interlinked (Figure 1) in particular in
implementing SOC storage options. For instance, maintaining SOC soils and, we assume that the deployment of land-based mitigation

F I G U R E 1 A schematic representation of C–N interactions in the terrestrial ecosystem. Note that biological nitrogen fixation and
denitrification are process performed by microorganisms that also need C as substrate and that the schematic is more representative of
agroecosystems
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240 GUENET et al.

options to increase SOC may impact the N cycle and the associ- availability would likely lead to greater primary productivity and
ated N2O emissions. A recent modelling study suggests that mea- inputs of plant-derived organic matter to the soil (Glendining
sure to increase SOC sequestration might be offset by increased et al., 1996). On the other hand, higher N availability also tends
N2O, depending on the crop rotation and on the duration of the to lower the allocation of photosynthates to the root system
land management practices (Lugato, et al., 2018). Recent progress (Pausch & Kuzyakov, 2018). As root-derived C inputs contribute at
in modelling SOC may help to better understand SOC dynam- least 2–3 times more than shoot-derived C inputs to SOC storage
ics and how we can enhance SOC storage (Abramoff et al., 2018; (Kätterer et al., 2011; Rasse et al., 2005), a high soil N availability
Cotrufo et al., 2013; Zhang et al., 2018, 2020), but so far the in- could theoretically increase the plant biomass but the plant bio-
teraction between C and N cycles is still poorly represented in mass produced might not be transformed into SOC as efficiently
models. A better understanding of such interactions is necessary because of a reduced amount of root-derived C entering the soil
to evaluate the benefits of different management practices aimed (Han et al., 2016).
at increasing SOC storage and to predict the full GHG balance of Soil organic matter turnover (i.e. rate of mineralization and
each practice. Nevertheless, measuring N2O fluxes is challenging transformation of SOM) also depends on the availability of N to
and large uncertainties exist due to difficult methodology (Chapuis- microorganisms. While a low mineral N availability may limit
lardy et al., 2007). Indeed, most of the existing data are measured the mineralization rate of plant residues and amendments (Fang
using chamber systems and several authors considered that a net et al., 2018; Recous et al., 1995), the combination of regular inputs
N2O uptake by the soils was due to technical limitation, in partic- of fresh organic C with a low soil N availability can lead to posi-
ular when measurements had been carried out close to detection tive priming effect, that is, a higher rate of SOM mineralization,
limits (Chapuis-lardy et al., 2007). Recent publications using other and a lower SOC storage potential (Chen et al., 2014; Fontaine
methods clearly showed that a net N2O uptake is possible mainly et al., 2004). Moreover, because of the relatively narrow range of
during daytime (Keane et al., 2019; Shurpali et al., 2016). Despite C:N ratios of SOM in mineral layers (Van Groenigen et al., 2017) and
such large uncertainties in the raw measurements of N2O fluxes, because of the importance of soil microbial processing for building
when comparing a given management option against a control we up stable SOM (Cotrufo et al., 2013) in some ecosystems, large
may assume that the methodological bias are similar and the rela- amounts of N are inevitably required to stabilize large amounts of
tive effect is still valid. SOC (Bertrand et al., 2019; Cotrufo et al., 2019). Because of this
Here we focus on the interactions between soil C and nutrient stoichiometric requirement, it might seem acceptable to maintain a
dynamics, and in particular on N dynamics and N2O emissions. The high availability of N in the soil by applying large amounts of min-
aims of the paper are to (a) describe the mechanisms linking the C eral fertilizers. Such a strategy would, however, lead to potential
and N cycles in soils, (b) assess how N2O emissions may be affected N losses, for example, as N2O emissions or nitrate leaching from
by increased SOC pools as a land-based mitigation option, (c) review soil, and further increase GHG emissions during fertilizer produc-
our knowledge on the other impacts of these practices. tion. Thus the modest increases in SOC resulting from N fertilizer
applications up to sensible agronomic rates are welcome in the
context of C sequestration, but it would be counterproductive and
2 | I NTE RT W I N E D S O I L C A R B O N A N D inappropriate to recommend higher rates of N application aimed at
N ITRO G E N C YC LE S promoting an additional increase in soil C.
Input of N to terrestrial ecosystems by biological N2 fixation
Because C and N cycles are tightly coupled in soils, and altering is another example of a close link between C and N resources.
one will affect the other as shown in Figure 1. In soils the C and Root-associated or free-living N2-fixing bacteria depend on the
the N cycles are sometimes totally interdependent, in particular availability of organic C resources for sustaining their heterotro-
when both are in organic forms but are sometimes uncoupled phic needs, which may explain why N2 fixation is only triggered
when C or N are present as minerals. This section summarizes the when the amount of soil mineral N is low. In particular, the en-
main mechanisms explaining how changes in the soil C cycle and ergy cost of N2 fixation represents between 5% and 23% of daily
SOC sequestration interact with N cycle processes, and in par- photo-assimilated C (Lambers, 1987). The associated CO2 losses by
ticular N2O emissions (Figure 1). The first reason why soil C and respiration may therefore decrease the amount of plant C entering
N dynamics are interdependent is that both elements are stored the soil. However, the consequence of this on the potential of SOC
predominantly as organic forms in the soil, sometimes within the storage remains unclear. For example, the presence of leguminous
same compounds (amino acids, proteins, etc.), thus mineralization plants can result in lower below-ground C inputs compared to
generally affects both. Moreover, the availability of mineral N in gramineous plants, leading to lower SOC concentrations (Bessler
the soil controls a number of processes in both cycles and vice et al., 2009; Lange et al., 2015). However, the net inputs of N to
versa. For instance, mineral N transformations depend on carbon soils by leguminous plants have been shown to correlate with a
availability and plant dry matter production is limited by N avail- net accumulation of SOC, by providing the organic N required to
ability. Nitrogen is needed to sustain photosynthesis and other stabilize an additional amount of SOC in soils (Jensen et al., 2012).
physiological processes (Engels et al., 2012); therefore higher N Similarly, crop rotations that include leguminous plants appear
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GUENET et al. 241

to store more SOC than conventional monocultures (Drinkwater a given soil water-filled pore space (WFPS) will usually be lower
et al., 1998), although this effect may be mainly due to longer pe- when the soil mineral N content is low and when soil pH is alka-
riods of plant cover, and to the presence of deeper root systems line or when C availability is reduced. Furthermore, because a low
than to biological N2 fixation itself (Jensen et al., 2012). These soil redox potential (<400 mV; Brettar et al., 2002) is required for
feedbacks also depend on which non-leguminous plants are asso- denitrification, N2O emissions have been suggested to have their
ciated (King & Blesh, 2018) to the N2-fixing plant, and may lead to optimum at 70%–80% WFPS, while prolonged waterlogging condi-
contrasting results in terms of SOC storage (Pellerin et al., 2019). tions may result in complete nitrate reduction to N2 instead of N2O
Of course, obtaining N from legumes, where this is practicable, (Butterbach-Bahl et al., 2013). This view is consistent with the clas-
rather than from N fertilizer does eliminate the GHG emissions as- sical model proposed by Firestone and Davidson (1989) but, recent
sociated with N fertilizer manufacture. results suggest that N2O can be reduced to N2 by non-denitrifier
N2O emissions represent a particular case that illustrates how bacteria (Hallin et al., 2018). Thus, N2O reduction rate might be
the soil N cycle may be influenced by the C cycle. First, as N2O higher than previously assumed explaining some net uptakes some-
mainly originates from the nitrification of ammonium (NH4+) or times observed but generally considered as methodological arte-
−
the denitrification of (NO3 ) by specific groups of microorgan- facts (Chapuis-lardy et al., 2007). N2O uptake is also controlled by
isms, any process that can affect the total amount of mineral N in environmental factors including pH or SOC (Assémien et al., 2019).
soils, such as N uptake by plants or plant residue mineralization, is Therefore, any modifications of soil conditions (e.g. redox potential,
likely to affect N2O emissions. Moreover, fresh C inputs to the soil soil moisture, etc.) due to land management practices may affect
through root exudates or amendments may temporarily decrease N2O uptake.
or increase soil pH, affecting the magnitude of N2O emissions. Several mechanisms can therefore explain why attempts to
Consumption of these organic products by microorganisms may modify the soil C cycle may also affect N2O emissions. On a lon-
also decrease the local concentration of oxygen, leading to anaer- ger timescale, the build-up of SOC by various strategies may be
obic conditions which are favourable to denitrification and N2O expected to increase the retention of water and fertilizer-N in the
emissions (Chen et al., 2013). Furthermore, because organic mate- rooting zone through improved soil properties (e.g. water hold-
rials generally act as electron donors in the denitrification process ing capacity, porosity, hydrophilicity). This might trigger a higher
and because SOM content may lower the redox potential of the soil primary production and enhance further SOC storage, but also
(Quin et al., 2015), increasing the amount of SOM may also increase increase the risk of N2O emissions because of the increase in N
the activity of denitrifiers and therefore increase N2O emissions sources and the shift to soil environmental conditions more fa-
(Brettar et al., 2002; Li et al., 2005). These mechanisms likely ex- vourable to N2O emissions. In the remainder of this paper, we con-
plain why higher SOC contents in soils have indeed been shown to sider possible interactions between increased SOC and changes
correlate with larger N2O emissions (Hénault et al., 2012; Stehfest in N2O emission for a range of management practices designed to
& Bouwman, 2006). As a rule, net N2O emissions from the soil at increase SOC (Table 1).

TA B L E 1 Summary of the effects of management practices on soil organic carbon (SOC) storage and N2O emissions

Management practice Effect on soil C stocks Effect on N2O emissions

Reduced tillage/zero tillage Reduced C loss/increased C inputs to soils when Promote denitrification (anaerobiosis; Mei et al., 2018)
associated with a reduced weed management
(Angers & Eriksen-Hamel, 2008; Virto et al., 2011)
Erosion control (contour Reduced C loss (Moraru & Rusu, 2010) Unclear
plowing, terracing)
Addition of non-pyrogenic Increased C input but in some cases (e.g. manure) Enhanced denitrification rate (via anaerobiosis and
organic amendments rather a transfer from one terrestrial location to the supply of electron donors), and soil N availability
(compost, manure, crop another than a transfer of C from atmosphere to (Charles et al., 2017)
residues) soil (Diacono & Montemurro, 2011)
Use of cover crops Reduced C loss/increased C input (Poeplau & Decreased denitrification because of N uptake by
Don, 2015) plants; may be compensated for by N inputs from
biological nitrogen fixation (Lugato, et al., 2018; Thapa
et al., 2018)
Biochar Increased C input (Lehmann et al., 2006) Decreased nitrification due to adsorption of mineral N
with biochar (Borchard et al., 2019)
Agroforestry Increased C input, reduced C loss, increased Decreased denitrification (lower soil moisture, increased
aggregate stability (Feliciano et al., 2018) soil porosity, increased nitrogen uptake), except for
N2-fixing trees (increasing soil available N; Kim et al.,
2016)
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242 GUENET et al.

3 | H OW S O C S TO R I N G PR AC TI C E S might increase N2O emissions, because: (a) increased organic matter

A FFEC T N 2 O E M I S S I O N S content can increase N2O release (Mei et al., 2018), either because
of increased energy supply to denitrifying organisms or because in-
3.1 | Balancing the nitrogen inputs creased biological activity utilizes oxygen in soil, thus possibly lead-
ing to anoxic conditions at some microsites and (b) reducing tillage
Since mineral N availability drives N2O emissions as well as crop can be associated in the short term with a less porous soil struc-
productivity and C inputs into the soil (Ladha et al., 2011; Wang ture, conducive of anoxy (Linn & Doran, 1984; Table 1). However,
et al., 2019), N fertilization should be carefully managed. A balance increased anoxia may have the opposite effect on N2O emissions by
should be obtained between N inputs (including fertilizers, manures accelerating N2O reduction to N2 as recently shown. This is due to
and biological nitrogen fixation through symbiosis between N2-fixing the complex soil physical structure creating anoxic microsites that
bacteria and some plant species) and N exported in harvested prod- may simultaneously produce more N2O but also accelerate N2O
ucts in order to reduce a N surplus that can be source of N2O, but reduction to N2 (Buchen et al., 2019; Parkin, 1987). The different
without a major negative effect on crop productivity. This N surplus meta-analysis we compiled here (Figure 2) suggest that N2O emis-
should ideally be zero, but it is actually large and positive in many sions may offset the C storage in no-till system when both fluxes are
regions of the world, that have intensive agriculture (e.g. parts of compared in CO2 equivalents. However, there is conflicting evidence
China, India, Europe, North America), and negative in other regions on whether or not this risk is actually realized (Mei et al., 2018; van
(e.g. Africa; Gruber & Galloway, 2008). Excess N associated with a Kessel et al., 2013). Recent meta-analyses suggest that, in the ma-
positive surplus is a major cause of N2O emissions on farms, but also jority of situations, N2O emissions are either unchanged or slightly
of nitrate leaching losses, part of which contributes to indirect N2O decreased under zero or reduced tillage; the result will certainly be
emissions if nitrate is denitrified within surface waters. Overall, N influenced by soil type and local climate and weather conditions so
surplus is a strong driver of N2O emissions, especially when consid- it may not be possible to draw a conclusion that is universally valid
ering that the rate of emission is no longer linear for high N input (Mangalassery et al., 2014; van Kessel et al., 2013). Furthermore, in
(Shcherbak et al., 2014). The relatively low cost of mineral N ferti- some studies, N2O emissions were expressed on both an area basis
lizers in developed countries compared to the price of agricultural and a yield-scaled basis (van Kessel et al., 2013); because crop yields
products incentivizes farmers to apply more N than recommended were slightly decreased under reduced tillage in some environments,
by good practices, as an 'insurance' against unforeseen N losses due N2O emissions per unit of grain (or other product) were sometimes
to climate variability. In some regions of the world, but not all, there increased compared to conventional tillage.
is considerable potential to lower agricultural N2O fluxes in inten-
sive farming by reducing the N surplus without affecting farmers'
incomes (Hoben et al., 2011). Therefore, the use of mineral N to in- 3.3 | Erosion control—Terracing
crease crop productivity may induce an increase of C input into the
soil but a complex balance must be found to avoid excessive N2O Erosion control practices are able to maintain or increase SOC con-
emissions and N leaching. tent at the plot scale (Moraru & Rusu, 2010), although on a larger
scale whether erosion is net C sink or a net source is still debated
(Berhe et al., 2018; Lugato, et al., 2018; Van Oost et al., 2007).
3.2 | Reduced tillage/non tillage Erosion control encompasses a wide range of practices such as pro-
tecting the soil surface with cover crops or unharvested biomass
The effect of reduced tillage has attracted attention as a prac- (pruned fronds and other plant residues), agroforestry, crop rota-
tice leading to increased SOC storage. However, recent meta- tions, conservation tillage, or terracing on steep slopes. Some of
analyses demonstrate only a small positive effect of no-tillage on these practices are already addressed in other sections of this paper
SOC stocks in the topsoil (0–30 cm layer) compared to conven- (3.2, 3.4 and 3.5), and the following focuses on terracing.
tional tillage, while it may vary widely across pedoclimatic situ- Terracing is an ancient form of erosion control and a soil con-
ations (Angers & Eriksen-Hamel, 2008; Luo et al., 2010; Meurer servation method performed for thousands of years in steep land-
et al., 2018; Powlson et al., 2016; Virto et al., 2011). Moreover, scape regions (Dotterweich, 2013; Tarolli et al., 2014). Despite its
it must be recognized that the largest impact of reducing till- importance, studies focusing on quantifying soil erosion rates and
age is a redistribution of SOC towards the soil surface (Angers & the resulting C fluxes and SOC stocks in terraced areas are limited,
Eriksen-Hamel, 2008; Baker et al., 2007; Meurer et al., 2018; Ogle especially at regional scales. Generally, terracing reduces soil ero-
et al., 2019; Powlson et al., 2016). As a consequence, data from sion by reducing the slope gradient and length, and can decrease
field trials must be carefully examined to distinguish between a soil erosion rates by up to 95% (Fu, 1989; Upadhyay et al., 2005).
genuine increase in SOC stocks in the surface soil layers from a It accordingly preserves SOC and nutrients. A meta-analysis on the
simple change in the vertical distribution of SOC concentration. ecosystem benefits of terracing shows that, compared to unterraced
There has been considerable discussion as to whether the in- slopes, soil in terraced slopes contains 28.1% and 41.7% more N and
creased SOC in soil under zero tillage, especially near the surface, C, respectively (Wei et al., 2016). However, the overall net effect
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GUENET et al. 243

F I G U R E 2 Estimation of the soil organic carbon storage and N2O emissions of land-based mitigation options expressed in CO2
equivalents. Negative values indicate a net reduction in GHG emissions in terms of CO2 equivalents, while positive values show a net
increase of CO2 equivalent emissions. All values refer to the difference between the land-based mitigation option in question and a ‘control’
land (e.g. no-tillage vs. conventional tillage). For agroforestry, the control land is cropland and different types of agroforestry systems were
considered. NB: In Kim et al. (2016) the majority of soil C storage data comes from intercropping, improved fallows and rotational woodlots,
which are systems with high tree density. This could partially explain the very high estimation of soil C storage found in Kim et al. (2016)
compared to other papers. Organic amendments do not include biochar. The control used for comparison with organic amendments is an
experiment managed with inorganic fertilizers. For cover crops meta-analysis, Vicente-Vicente et al. (2016) only consider Mediterranean
woody crops (olive, almond and vineyards), which could also explain the large soil C rates estimated. Uncertainty is given as standard error
(SE) for every paper. If it was provided as a confidence interval (CI) or standard deviation (SD) it has been adequately transformed to unify
the units. (*Reviews; **For these meta-analysis the values reported in the graph have been recalculated as the weighted mean across all
experiments, from the database provided by the authors, because the values coming from the papers could not be used as they were
reported as a percentage only) (Abdalla et al., 2019; Du et al., 2017; Skinner et al., 2014; Vicente-Vicente et al., 2016)

of terracing on erosion depends on the terrace structure and main- the field scale. Since erosion control aims to avoid lateral losses of
tenance, crop type, soil conditions, crop management practices or soil material (containing various forms of N) ending up in rivers or in
agricultural machinery. To maximize its positive effects, terracing floodplains, it is necessary to combine measurements in the terraced
needs to be combined with other soil conservation measures such or unterraced fields with measurements and modelling on the fate of
as cover crops, agroforestry, organic amendments or no-till (Chen eroded N in floodplains and rivers.
et al., 2017; McLauchlan, 2006). Furthermore, terraces need to be
sustained, otherwise abandoned terraces can become sources of
substantial land degradation due to gully formation. This is the case 3.4 | Cover crops
in the Mediterranean region where over 50% of the terraces have
been abandoned (Tarolli et al., 2014; Wei et al., 2016). Planting cover crops is an effective management practice to increase
The N2O emissions associated with terracing are still poorly SOC content. According to a recent meta-analysis, it leads to SOC
known. Terracing decreases the aggregate breakdown and trans- accumulation rates in the order of 1.18 t CO2-eq. ha−1 year−1 over
port of soil by erosion, which would lead to reduced N2O emissions. 50 years (Poeplau & Don, 2015) in the topsoil, with a positive ef-
However, as stated previously, N2O emissions may increase with fect independent of tillage method, climatic zone or plant type (le-
increased SOC. In addition, terracing tends to change the soil C:N guminous vs. non-leguminous). The impact of cover crops on SOC
ratio (Wei et al., 2016) and this may change the N availability for ni- will depend on their duration and the frequency with which they
trifying/denitrifying bacteria and thus affect N2O emissions. Finally, are included in a crop rotation, and this information is sometimes
to fully estimate the effect of erosion control on N2O budgets, it is unclear in published reports of field trials (Poeplau & Don, 2015).
important to measure emissions at the catchment scale not only at It is also necessary to interpret reviews of SOC data from cover
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244 GUENET et al.

crop experiments with caution because annual rates of increase are a biogeochemistry model framework at European scale, estimated
greatest in the early years following their introduction, so it is incor- that systematic planting of N-fixing cover crops may lead to a
rect to assume that these rates can be sustained over long periods. N surplus of about 0.04 t N ha−1 year−1, compared to the use of
As the majority of experiments reported in Figure 2 are short term non-legumes as cover crop (Lugato, et al., 2018). In this scenario,
(e.g. often only 2 years in Abdalla et al., 2019), all the average values the cumulative climate change mitigation effect of SOC sequestra-
shown for SOC increases from cover crops are likely to be overes- tion was, on average, totally offset after 50 years since the adop-
timates. In addition the large rates shown by Vicente-Vicente et al. tion of cover crops, due to enhanced N2O emissions. While cover
(2016) are for situations where cover crops were grown between crops may induce higher N2O emissions, in particular if leguminous
rows of woody perennial crops; in this situation cover crops cover crops are extensively used, they can also reduce nitrate leaching,
a larger area than in arable agriculture with annual crops and may by about 56% on average (Thapa et al., 2018). This is beneficial for
be present permanently. The main driver of SOC storage seems to water quality and would be expected to lead to decreased indirect
be the extra C input, as suggested by the high correlation between N2O emission through denitrification of nitrate entering surface
rates of SOC stock change and the amounts of C returned to the water. Finally, another indirect effect of leguminous cover crops
soil by cover crop biomass (Soane et al., 2012). However, there are on N2O emissions will strongly depend on whether or not mineral
limitations to the use of cover crops depending on cropping systems N fertilization rates are reduced to take account of N provided by
and climate conditions. For example, in temperate regions they can biological fixation. The meta-analyses we compiled here indicate
be readily utilized during the winter period prior to sowing a spring- that, on average, additional N2O emissions decrease the SOC stor-
sown crop, when the soil would otherwise be bare. But if only age benefit of cover crops, but do not fully offset it (Figure 2). But,
autumn-sown crops are grown, there is very limited time between as discussed above, the overall effects may be highly site specific.
harvesting and the sowing of the subsequent crop.
The effects of cover crops on N2O emissions are more vari-
able and contrasted than those on SOC changes (Table 1). Many 3.5 | Agroforestry
factors influence the magnitude of N2O emissions, such as
the C:N ratio of cover crop residues, their rate of decomposi- Agroforestry systems include a diversity of practices ranging
tion, the extra inputs of fertilizer N sometimes applied to cover from complex associations found in homegardens, multistrata
crops, whether the residues are ploughed or left to decay on the systems or agroforests to simpler systems such as alley crops, sil-
soil surface. Current evidence points to a negative relationship vopastoral systems, riparian plantings, shelterbelts, windbreaks
between N2O emissions and the C:N ratio of residues (Chen or hedgerows (Nair, 1985). Despite this broad diversity, recent
et al., 2013). A low C:N ratio will increase the availability of soil reviews and meta-analyses consistently suggest that the conver-
N for microbial transformations (e.g. nitrification and denitrifi- sion of arable land to agroforestry systems increases SOC stocks
cation), whereas larger ratios will result in N immobilization and (Feliciano et al., 2018; Kim et al., 2016; Lorenz & Lal, 2014). In
deplete the soil inorganic N pool (Gentile et al., 2008). Additional temperate regions, SOC accumulation rates are usually around
C inputs from cover crops may stimulate the activity of denitrifier 0.92 t CO2-eq. ha−1 year−1 in the topsoil (0–30 cm; Cardinael, et al.,
bacteria, which use these organic compounds as a source of en- 2015; Cardinael et al., 2017). They are highly dependent on local
ergy (Mitchell et al., 2013). A meta-analysis (Basche et al., 2014) pedoclimatic conditions and on the type and design of agrofor-
reported a significant increase in N2O emission when leguminous estry systems (tree density, tree species, pruning management,
cover crops were introduced. However, another review (Han etc), but rarely exceed 3.67 t CO2-eq. ha−1 year−1 (Cardinael, et al.,
et al., 2017) found out that the incorporation of either legume 2018; Corbeels et al., 2019). However, the spatial distribution of
and non-legume cover crops tended to increase N2O emissions SOC stocks in agroforestry systems is usually very heterogene-
but the magnitude of the effect was not significant due to the ous, with higher stocks under the tree canopy or along tree rows
high variability of data. The small average increase in N2O emis- (Bambrick et al., 2010; Cardinael, et al., 2015). Several mecha-
sion shown by Abdalla et al. (2019) in figure 2 is somewhat mis- nisms contribute to explain SOC sequestration in agroforestry
leading as there was a considerable range in emissions in the data systems. The main one is probably being linked to higher organic
they summariszd, including both increases and decreases. The inputs to the soil compared to treeless agricultural land (Cardinael,
effect of cover crops on N2O emissions is therefore not yet fully et al., 2018), including litterfall, pruning residues and root inputs
understood and may well be highly site specific. (Germon et al., 2016).
One of the key points controlling cover crop effect on N2O A recent synthesis of N2O emissions under agroforestry com-
emissions is how often leguminous crops are integrated within the pared to adjacent agricultural lands only found minor differences
crop rotation. Leguminous cover crops generally have a lower C:N in net emissions, with no clear overall direction of change (Kim
ratio than non-leguminous crops, and can fix substantial amounts et al., 2016). However, several authors found increased N2O emis-
of atmospheric N, reaching up to 0.1–0.2 t N ha−1 year−1 (Anglade sions in agroforestry, related to a greater N supply through N2-
et al., 2015). These rates may lead to an N surplus if all the legu- fixing trees (Chikowo et al., 2004; Dick et al., 2006; Hall et al., 2006;
minous cover crop biomass is incorporated. A recent study, using Hergoualc'h et al., 2008) or to the incorporation of tree residues
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GUENET et al. 245

(Baggs et al., 2006; Millar & Baggs, 2004). By contrast, N2O emis- consensus that organic amendments lead, on average, to a relative
sions are often reduced in silvoarable systems and in riparian buf- increase of SOC stocks in the top soils (roughly 20–30 cm) of about
fers (Kim et al., 2016). Some authors suggest that concerns over 25% on a 20 year time frame (or three times the ‘4 per mil’ target).
N2O emissions from N2-fixing trees are unwarranted since fluxes In one example (Poulton et al., 2018) where manure was applied an-
from soils planted with N2-fixing trees are similar to those fertil- nually at a high rate compared to what is usual in agrosystems, the
ized with mineral N (Rosenstock et al., 2014). Furthermore, the annual rate of SOC accumulation averaged 18‰ per year in the first
yield of crops in tropical agroforestry systems may be boosted as 20 years, then declined to 6‰ per year after 40–60 years, and to
a result of higher N inputs from trees. In temperate regions where only 2‰ per year after 80–100 years. However, from the perspec-
agroforestry systems are generally planted with non-legume trees, tive of mitigating climate change, it is arguable whether any increase
N2O emissions are often reduced (Kim et al., 2016), with several in SOC stocks resulting from applications of manure or similar mate-
processes contributing to the trend. Increased nitrogen utiliza- rials can be considered as C mitigation in the sense of either a trans-
tion at the plot scale may be due to the presence of deep-rooted fer of C from atmosphere to land or an avoided emission. Manure is
trees (Cardinael, et al., 2015), which are capable of taking up ni- generated in agricultural systems and is almost always used in some
trate-N that has leached below crop rooting depth (Andrianarisoa way by application to soils, though often quite inefficiently. Thus,
et al., 2016; Bergeron et al., 2011; Tully et al., 2012). This process an increase in SOC stocks at a given location mainly represents a
can potentially reduce the amount of N available for nitrification transfer of C from one site to another as opposed to a net removal of
and denitrification, and thus reduce indirect N2O emissions. Soil atmospheric carbon (Poulton et al., 2018). Local additional SOC stor-
water content is often lower in agroforestry than in treeless plots age may not represent a CO2 sink, that is, a net transfer of carbon
(Zhu et al., 2019), due to a higher daily water consumption by from the atmosphere to the soil at the landscape scale.
trees and crops (Sarmiento-Soler et al., 2019). A drier soil profile Because organic amendments such as manures contain read-
in agroforestry systems could therefore lower N2O emissions. In ily decomposable N-rich compounds, there is a significant risk that
temperate silvoarable systems, tree rows are usually uncropped they may enhance N2O emissions (Cayuela et al., 2010; Laville
and unfertilized. This reduction in the fertilized cropping area et al., 2014; Obriot et al., 2016). Conversely, their use permits de-
indirectly leads to lower N2O emissions per hectare. An obvious creased use of mineral N fertilizers, thereby saving N2O emission
consequence of agroforestry, especially as tends to be practiced from this source and fossil energy and the associated GHG emis-
in temperate regions, is that a smaller area of land is devoted to sions from fertilizer manufacture. A further complicating factor in
the agricultural crop being grown. So the impact of decreased N2O assessing the overall impact of manure use is that indirect emis-
emissions may be different if expressed on an area basis compared sions due to storage or management are not negligible (Venterea
to per unit of production. et al., 2011). There are few reports in the literature of long-term
monitoring of N2O emissions compared to data on SOC stock
changes, primarily because the former are much more difficult to
3.6 | Non-pyrogenic organic amendments measure. However, the effects of multiple types of organic amend-
ments on SOC storage and N2O emissions have been evaluated in
A literature review (Diacono & Montemurro, 2011) reported in- short-term experiments for various soil types, climates, soil incor-
creases in SOC (sometimes expressed as stocks and sometimes as poration practices and amendments types including crop residues,
concentration) after prolonged large applications of organic amend- manure, composts of various origin and maturation stages and sew-
ments under several different agroclimatic conditions. These in- age sludge. A meta-analysis (Charles et al., 2017) concluded that
creases ranged from 20% to 90% of the initial total SOC after few the N2O emission factors (EFs) related to N inputs were mainly con-
years (3–60 years), compared to unfertilized controls or treatments trolled by the C:N ratios of the added material, but that many other
receiving only synthetic mineral N fertilizers, with most being in factors influenced emission, such as soil properties (texture, drain-
the range of 20%–45%. A meta-analysis (Maillard & Angers, 2014) age, SOC and N content), and climatic factors. For instance, the
based on 130 observations worldwide quantified the response of authors observed that the EFs were on average 2.8 times greater
SOC stocks to manure application over periods ranging from 3 to in fine-textured soils compared to coarse-textured, consistent with
82 years. The mean manure-C retention coefficient defined as the a previous meta-analysis (Chen et al., 2013). However, we should
average proportion of manure-C remaining in the soil was estimated mention that the value of meta-analyses is often limited due to nu-
at 12% for an average study duration of 18 years. The authors finally merous controlling factors that are not always correctly reported
estimated a relative SOC stock change factor of 26% which was also in the papers reviewed, and the general paucity of organic amend-
related to cumulative manure inputs. Concerning Mediterranean ments' characterization in the literature. For instance, the two
cropping systems, and shorter durations, a meta-analysis (Aguilera meta-analyses mentioned in this paragraph only involved 28–38
et al., 2013) reported that the application of organic amendments individual journal articles (Charles et al., 2017; Chen et al., 2013).
increased SOC stocks by 23.5% with an average SOC storage rate Another approach is to compare organically managed soils with
of 4.81 t CO2-eq. ha−1 year−1 calculated for an average duration those managed without organic amendments (Skinner et al., 2014).
of 7.9 years. From these meta-analyses, it seems that there is a Results from such a comparison seem to indicate reduced N2O
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246 GUENET et al.

emissions compared to situations relying totally on mineral fertil- (positive priming), decrease (negative priming) or have no effect on
izers, as shown in Figure 2. It should be noted that there is limited the mineralization of native SOM. The biochar effect on the mag-
data from long-term studies on N2O emissions associated with ad- nitude and direction of priming is influenced by the incubation pe-
ditions of organic amendments; the data cover only a limited di- riod and pyrolysis temperature (Fang et al., 2014; Kerré et al., 2016;
versity of pedoclimatic conditions, and especially the range of soil Zimmerman et al., 2011). Positive priming, which would cause desta-
water filled pore space values explored. bilization of SOM, thus offseting part of the increased SOC storage,
could result from the biochar affecting microbial biomass activity
and enzyme production (Lehmann et al., 2011) through changes in
3.7 | Biochar amendments availability of organic substrates and nutrients, and modification of
microorganism habitat associated with the great porosity and large
Biochar (pyrolyzed organic matter amended to the soil) technology specific surface area of charcoal particles (Lehmann et al., 2011).
is considered by some authors to be one of the methods with the Conversely, some studies showed that biochar-induced negative
highest potential to sequester carbon in soils compared to natural priming, leading to further SOC storage in addition to direct bio-
C cycle without biochar production step (Paustian et al., 2016). The char-C inputs, resulted from the enhancement of organo-mineral
aim of biochar production from biomass pyrolysis is to produce re- interactions and soil aggregation with biochar (Pituello et al., 2018;
calcitrant organic matter (i.e. charcoal and biomass-derived black Singh & Cowie, 2014), and a greater adsorption of dissolved organic
C) which is then added to the soil. For this reason, biochar can be carbon onto biochar particles (Hernandez-Soriano et al., 2016). In
considered as a negative emission technology different from other addition, biochar amendments have been shown to increase soil
soil C sequestration methods (Smith et al., 2016). Biochar properties water holding capacity, the availability of some nutrients (Ca2+,
and effects on SOC stabilization strongly depend on the feedstock Mg2+ in particular) and to increase soil pH. All of these mecha-
material and pyrolysis conditions (e.g.. maximum temperature, heat- nisms could further enhance crop productivity and biomass inputs
ing rates; Baveye, 2014; Fang et al., 2014; Singh et al., 2012; Weldon into soil (Atkinson et al., 2010; Biederman & Harpole, 2013; Hardy
et al., 2019; Zimmerman et al., 2011), as well as biochar ageing and et al., 2017; Jeffery et al., 2011), with clearer effects on crop yields
soil properties (Luo et al., 2011; Paetsch et al., 2018). in highly weathered tropical soils (Crane-Droesch et al., 2013).
The efficiency of biochar for C sequestration is twofold as com- Nevertheless, to process biomass into biochar, transport it
pared to simply relying on soil stabilization processes. First, slow and incorporate it to the soil, some energy is needed (possibly
pyrolysis for biochar production results in a much higher proportion produced by pyrolysis) and the related GHG emissions associated
of the feedstock C bound in persistent molecular structures than with this process must be accounted for to calculate a full GHG
through in situ stabilization by addition of unprocessed organic balance for biochar. Life cycle assessments (LCA) have shown that
matter to soil (Lehmann et al., 2006). With a slow pyrolysis at about a positive balance can be obtained, illustrated by GHG reductions
500°C, approximately 50% of the carbon contained in a feedstock up to 2.74 t CO2 equivalent per ton of biochar amended on vol-
of Miscanthus or maize cobs ended up within the biochar and can canic soils from Southern Chile (Muñoz et al., 2017). The balance
therefore be assumed to be more stable than carbon in the raw bio- can also significantly increase when plant biomass production is
mass (Budai et al., 2014). This compares with only 8%–12% of straw accompanied by an efficient use of the bioenergy produced during
residue returned to the field being transformed into longer-lived the pyrolysis process in order to maximize climate benefits from
SOM forms (Bolinder et al., 1999; Fujisaki et al., 2018). Thus, py- biochar production followed by addition to soil, as shown by an
rolysis is about four times more efficient than SOM-formation pro- LCA performed in Spain (Peters et al., 2015); implementation costs
cesses to produce persistent C in soils. Second, field studies show were also decreased. One simulation study suggests that the max-
that biochar has a longer mean residence time in soils than SOM, imum sustainable technical potential of biochar to mitigate climate
that is, >100 years (Rasse et al., 2017) versus about 50 years for the change, involving the widespread use of biochars, without threat-
latter (Schmidt et al., 2011). Combining effects of the higher per- ening food security and landscapes, could be a mitigation of 12%
sistent C yield with that of the longer mean residence time, biochar of current anthropogenic CO2 emissions (1.8 Pg CO2-C equivalent
appears at least eight times more efficient at storing SOC than the per year; Woolf et al., 2010). The C:N ratio of SOM approximates
return of non-pyrolysed residues. In meta-analyses, biochar amend- 14 (Cleveland & Liptzin, 2007) while that of biochar is generally
ment tends to increase the SOC stocks by 40% but the studies used higher than that of its feedstock, that is, generally >50 for straw
were generally short term (no more than 4 years; Liu et al., 2016). biochar and >100 for wood biochar. It takes therefore at least five
Nevertheless, this result must be considered with due care since times less N to stabilize organic C in the form of biochar than in
it is not straightforward to measure the effect of biochar, which is the form of SOM. Beyond this critical observation, biochar has
mainly C, on native SOC but one published study suggests that bio- other important interactions with the N cycle, notably: (a) vol-
char amendment increases total SOC including non-biochar C (Liang atilization and immobilization of N during the pyrolysis process
et al., 2010). (Mandal et al., 2016), (b) reduction of N2O emissions after appli-
In addition to the direct inputs of pyrolyzed biomass to the soil, cation to arable fields (Borchard et al., 2019), (c) reduction of NO3
recent studies showed that biochar amendments could increase and NH4 leaching (Lehmann et al., 2003). Emissions of N2O from
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GUENET et al. 247

soils are in most cases substantially reduced by biochar addition: a in CO2 equivalents, using a global warming potential value inte-
recent meta-analysis reported an average decrease of 38% across grated over 100 years and including global warming potential
studies (Borchard et al., 2019). However, most measurements are (GWP) of 298 for N2O as recommend by last IPCC report (Myhre
short term, the majority in this meta-analysis being <30 days; the et al., 2013). GWP is the time-integrated radiative forcing induced
impact over an entire growing season under field conditions has by a pulse emission of a given component (here N2O), relative to a
rarely been measured. This effect appears consistent when bio- pulse emission of an equal mass of CO2 (Myhre et al., 2013). The
char is produced at over ~450°C, so that the product has both a data in Figure 2 were taken from several meta-analyses and re-
high pH and a high surface area while containing very little labile C view papers. Here we did not re-analyse the data gathered by such
(Weldon et al., 2019). The contribution of N2O emissions attenua- meta-analysis, but rather presented the mean effect size from each
tion with biochar was shown to be negligible in the LCA performed study converted in CO2 equivalents. When results were given for
in Southern Chile, compared to the climate change mitigation asso- the whole experiment duration, we divided by the duration of the
ciated to C storage (Muñoz et al., 2017). Furthermore, reductions experiment to obtain the mean annual SOC storage/N2O emis-
in N2O emission with biochar appears only significant for the first sions (see Supporting Information for detailed methods). The data
year after application, which suggests that frequent applications in Figure 2 are based on over 700 measurements of SOC change
are necessary to maintain such an effect. In view of the large quan- and 200 measurements of N2O. Even allowing for some papers
tities of biochar usually applied in such studies, this may greatly being cited in more than one meta-analysis, this is a large body of
limit the practical and/or economical potential for using biochar as data and, to our knowledge, has not previously been assembled in
a method for decreasing N2O emissions. this way. At first sight it appears that SOC increases produced by
One approach to capitalizing on the positive interactions be- the four sets of treatments varied widely from −0.52 ± 0.46 to −6.
tween biochar properties and the N cycle is through the devel- 74 ± 1.21 t CO2-eq. ha−1 year−1, the negative sign representing ac-
opment of biochar-based fertilizers made by mixing biochar with cumulation of SOC that is; transfer of C from atmosphere to soil.
mineral or organic sources of nutrients (Hagemann et al., 2017). This However, this wide range is somewhat deceptive as the two larg-
method aims at reducing nitrate losses and N2O emissions, and at in- est values are from very specific situations. The value of −6.74 ± 1
creasing N use efficiency. Moreover, biochar tends to adsorb mineral .21 t CO2-eq. ha−1 year−1 for agroforestry (Kim et al., 2016) is from
N and the mixing with a nutrient-rich material prevents potential N 34 sets of data for systems with a particularly high tree density
deficiency created by field application of large amounts of raw bio- (see legend to Figure 2); the other two meta-analyses for agrofor-
char. Some biochar structures have been successfully loaded with ni- estry, based on >200 data sets, give values of less than half this
trate ions through co-composting, which could greatly increases the at around −3 t CO2-eq. ha−1 year−1. For cover crops the majority of
fertilization value of the product (Kammann et al., 2015). Producing data, based on 186 data sets, lead to mean rates of C accumulation
biochar fertilizers requires the development of appropriate technol- in the range of −1.2 to −2.0 t CO2-eq. ha−1 year−1. The highest value
ogies. For example, mixing raw biochar—a high pH product—with observed for cover crop was 3.67 t CO2-eq. ha−1 year−1 but it spe-
manure and slurries can result in large amounts of NH3 being vol- cifically refers to cover crops included between the wide rows of
atilized. Therefore, biochar acidification is generally required when Mediterranean woody crops (olive, almond and vineyards) where
making biochar fertilizers from organic feedstocks. However, bio- the soil would otherwise be bare (Vicente-Vicente et al., 2016).
char is also a strong sorbent for NH3 (Taghizadeh-Toosi et al., 2012), This is clearly an important management change within this en-
which may be captured from the atmosphere during the pyrolysis vironment but represents a much greater input of plant material
process and made available to plants later. This is a promising tech- than, say, cover crops grown during winter within temperate ar-
nology to abate anthropogenic emissions of NH3 (Taghizadeh-Toosi able cropping systems. For both agroforestry and cover crops, and
et al., 2012) as well as directly reduce NH3 volatilization from soils even ignoring the two sets of data for SOC increases that are es-
(Mandal et al., 2016). In conclusion, pending proper technology, bio- pecially large, it appears from the summarized data in Figure 2 that
char may be intimately mixed with N sources and applied each year SOC increases resulting from these two changes in management
as a fertilizer to maximize reductions in both N2O emissions and ni- considerably outweigh increased N2O emissions when both are
trate leaching, while sequestering C in a structure requiring little N. expressed on a CO2-eq basis and these management changes can
However, further studies are needed to validate the scant results be expected to beneficial for climate change mitigation. However,
currently available. the annual rates of SOC increase shown in Figure 2, especially for
cover crops, are probably overestimates because they are based
on short-term measurements, in some cases only 2 years; over
3.8 | Overview of the current evidence longer periods the annual rate will decline as SOC moves towards
a new equilibrium value. For no-tillage the situation is different:
Figure 2 summarizes published data on rates of change in SOC the relatively small rates of SOC accumulation are approximately
and rates of emission of N2O resulting from four prominent sets equal to the increases in N2O emission when both are expressed
of practices designed to increase SOC, namely agroforestry, cover on a CO2-eq basis, so there appears to be no overall climate
crops, no-tillage and organic amendment. All fluxes are expressed change benefit. For organic amendments the results indicate that
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248 GUENET et al.

N2O emissions are decreased and thus reinforce the SOC benefit, be produced in order to make the approach realistic at large scale,
though this is based on a very limited amount of data and also, as in addition to the ongoing debate regarding the actual impacts of
discussed earlier, it is questionable whether SOC increases from biochar on soils and crops and the mechanisms involved.
addition of organic amendments can be fully regarded as climate To be deployed at large scale and to enter emission trading
change mitigation. It should be noted that most of the studies are systems, the GHG fluxes of each change in agricultural practices
performed over a few years and assessment of GHG balance in the should be estimated precisely. Various models may be used to ac-
long term, especially for N2O, are still missing (Lugato, et al., 2018). count for scale or leakage effects such as indirect land-use changes
Some practices were too little documented or with not enough (Qin et al., 2016). The methods currently available include data-­
information to be compared with the others (e.g. biochar or ero- driven approaches based on worldwide measurement networks
sion control). (Shang et al., 2019), statistical or empirical flux-upscaling models
(Shang et al., 2019; Wang et al., 2019), process-based models and,
lastly, integrated assessment models (IAM; Zomer et al., 2016).
4 | D I S CU S S I O N A N D O U TLO O K Process-based models include a representation of N cycling pro-
cesses, which are an essential tool in assessing and predicting the
Overall, the meta-analysis we gathered here (Figure 2) suggest terrestrial N cycle and N2O fluxes in response to multi-factor global
that, with the exception of reduced tillage practices, increased changes. Such models have been used to estimate N2O emissions
N2O emissions are not sufficient to invalidate the GHG abate- from natural and agricultural soils at various scales, from field to
ment potential achieved by SOC sequestration strategies. Some global level via the integration of a prognostic N cycle into differ-
sequestration strategies (e.g. biochar or non-pyrogenic organic ent land surface models (Tian, et al., 2018). As an example, Figure 3
amendment application) may even generate win–win situations shows the results of simulations by various models at global scale.
through a decrease in N2O emissions, although the experimental Most of N2O emissions from cropland are due to the use of min-
evidences are still scant. This N2O emissions reduction is more eral fertilizers (Figure 3a) and are mainly located in United States,
and more scrutinized (Assémien et al., 2019; Buchen et al., 2019; Europe, India and China. They may be used to quantify carbon se-
Conthe et al., 2019; Shurpali et al., 2016) and some win–win prac- questration in soil minus the N2O emission trade-off at global scale,
tices may emerge in the near future from increasing SOC to reduce based on ensemble runs as was initiated in the global N2O Model
N2O emissions. For instance, biochar application known to im- Inter-Comparison Project (Tian, et al., 2018).
prove SOC storage (Lehmann et al., 2006) may also be associated Integrated assessment models focus on the interactions be-
with an N2O emissions reduction by decreasing labile N availabil- tween the economic activities and earth system responses and
ity, N-cycling enzymatic activity and nitrification/denitrification are vital for estimating what socio-economic changes would be
rates (Song et al., 2019). In addition, the economic impacts and needed to reduce GHG emissions across sectors and increase
large-scale effects of the options examined here warrant further biospheric C sinks (IPCC, 2014). Until recently, most IAMs did
assessment. Some practices may affect crop yields or farmers' in- not explicitly take into account SOC restoration practices (Smith
come, depending on pedoclimatic conditions and the details and et al., 2016). A recent study that did include them found that soils
practicalities of the cropping systems. For instance, conservation could be a sink of 3.5 Gt CO2-eq/year by 2050 under a carbon
practices, and especially no-till may slightly decrease crop yields price of 190 USD/tCO2 (Frank et al., 2017). This carbon mitiga-
under temperate climates but be beneficial in drier conditions tion option, if achievable in practice, would reduce the burden
(Pittelkow et al., 2015). Similarly, the yield of arable crops is usu- of climate stabilization for all sectors of the economy, including
ally reduced in agroforestry systems in temperate regions (Pardon agriculture. In addition, SOC increases are often correlated with
et al., 2018) but in more arid climates, crops perform better (Bright higher crop yields and contribute to a range of other environ-
et al., 2017). Nevertheless, for agroforestry, trees produce timber, mental benefits and increased sustainability of agricultural sys-
firewood, honey, fruits, etc. that are also a source of incomes for tems. Practices designed to increase SOC can offer a win–win
the farmers and may lead to greater overall sustainability. Beyond solution vis a vis food security, by mitigating food calorie losses
yield impacts, some socio-cultural or economic factors come into resulting from the application of emission reduction targets (e.g.
play that may hinder the adoption of carbon sequestration prac- through decreased applications of mineral fertilizers) and reduc-
tices. For example, in the United States, the cost of carbon cap- ing undernourishment.
ture through Natural Resources Conservation Service programs is Finally, many of the practices reviewed (Table 1) here may be
estimated at US $32–442 per tonne of CO2, with an average of combined on a given field: for example, no-till can be combined with
US $183 (Biardeau et al., 2016). A carbon price much higher than cover crops, organic amendments or agroforestry. Such combina-
the present value (around US $10 as a global average; Ramstein tions have been little tested in practice and in particular synergetic
et al., 2019) would be necessary to promote carbon sequestration effects between them have not been evaluated in depth (Autret
practices, as well as a regulation to direct the financial flow of in- et al., 2016, 2019). Conversely, they may come with trade-off, an-
dustrial and energy emitters to the agricultural sector. For biochar, tagonistic or synergistic effects regarding SOC storage rates, as well
there are still questions about whether a sufficient quantity could as N2O emissions or other impacts and these needs to be identified
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GUENET et al. 249

F I G U R E 3 Spatial and latitudinal patterns of contributions of fertilizer (a) and manure (b) on cropland soil N2O emissions obtained during
the global N2O Model Intercomparison Project (Tian, et al., 2018). Average over the 2006–2015 period

and quantified. Furthermore, proper assessment of carbon seques- or integrated assessment models could be a prime target to assess
tration measures raises classical GHG accounting issues, such as their impacts at global scale.
double counting, improper setting of system boundaries and coun-
terfactual scenarios (Smith et al., 2016). Although further research is AC K N OW L E D G E M E N T S
still needed to quantify the potential of SOC sequestration options This paper stemmed from a workshop ‘Emerging challenges in large
on a local to regional basis, it appears that their potential to miti- scale soil carbon sequestration’ held in Paris on 8–10 October 2018.
gate climate change, even when factoring in N2O emissions is still The workshop was financially supported by the French government
significant and that they deserve further consideration in climate under the ANR ‘Investissements d'avenir’ program with the reference
stabilization scenarios. Including the state-of-the-art knowledge re- CLAND ANR-16-CONV-0003. F.Z. acknowledges support from the
viewed here on the effectiveness of such measures in land system National Natural Science Foundation of China (grant no. 41671464).
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250 GUENET et al.

D.A. is coordinator of the research consortium GLADSOILMAP sup- to increase soil organic carbon storage? Results from a 16 year field
experiment. Agriculture, Ecosystems & Environment, 232, 150–164.
ported by LE STUDIUM Loire Valley Institute for Advanced Research
https://doi.org/10.1016/j.agee.2016.07.008
Studies. The authors acknowledge John Bazire for all the help to organ- Baggs, E. M., Chebii, J., & Ndufa, J. K. (2006). A short-term investiga-
ize the workshop and Chris Van Kessel for data sharing. This study is tion of trace gas emissions following tillage and no-tillage of agrofor-
dedicated to the memory of Jérôme Balesdent, a great scientist and a estry residues in western Kenya. Soil and Tillage Research, 90, 69–76.
https://doi.org/10.1016/j.still.2005.08.006
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Songchao Chen https://orcid.org/0000-0003-1245-0482
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