Content uploaded by Claudia Kammann
Author content
All content in this area was uploaded by Claudia Kammann on Oct 11, 2017
Content may be subject to copyright.
Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=teel20
Download by: [Universitaetsbibliothek Giessen] Date: 29 June 2017, At: 11:59
Journal of Environmental Engineering and Landscape
Management
ISSN: 1648-6897 (Print) 1822-4199 (Online) Journal homepage: http://www.tandfonline.com/loi/teel20
Biochar as a tool to reduce the agricultural
greenhouse-gas burden – knowns, unknowns and
future research needs
Claudia Kammann, Jim Ippolito, Nikolas Hagemann, Nils Borchard, Maria
Luz Cayuela, José M. Estavillo, Teresa Fuertes-Mendizabal, Simon Jeffery,
Jürgen Kern , Jeff Novak, Daniel Rasse, Sanna Saarnio, Hans-Peter Schmidt,
Kurt Spokas & Nicole Wrage-Mönnig
To cite this article: Claudia Kammann, Jim Ippolito, Nikolas Hagemann, Nils Borchard, Maria
Luz Cayuela, José M. Estavillo, Teresa Fuertes-Mendizabal, Simon Jeffery, Jürgen Kern , Jeff
Novak, Daniel Rasse, Sanna Saarnio, Hans-Peter Schmidt, Kurt Spokas & Nicole Wrage-Mönnig
(2017) Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns
and future research needs, Journal of Environmental Engineering and Landscape Management,
25:2, 114-139, DOI: 10.3846/16486897.2017.1319375
To link to this article: http://dx.doi.org/10.3846/16486897.2017.1319375
© 2017 The Author(s) Published by VGTU
Press and Informa UK Limited, [trading as
Taylor & Francis Group].
Published online: 28 Jun 2017.
Submit your article to this journal View related articles
View Crossmark data Citing articles: 1 View citing articles
MICROBIAL COMMUNITY CHANGES IN TNT SPIKED SOIL BIOREMEDIATION
TRIAL USING BIOSTIMULATION, PHYTOREMEDIATION AND
BIOAUGMENTATION
Hiie No
˜lvak
1
, Jaak Truu
2
, Baiba Limane
3
, Marika Truu
4
,
Guntis Cepurnieks
5
, Vadims Bartkevicˇs
6
, Jaanis Juhanson
7
, Olga Muter
8
1, 7
Institute of Molecular and Cell Biology, Faculty of Science and Technology, University of Tartu,
23 Riia str., 51010 Tartu, Estonia
1, 2, 4
Institute of Ecology and Earth Sciences, Faculty of Science and Technology, University of Tartu,
46 Vanemuise str., 51014 Tartu, Estonia
3, 8
Institute of Microbiology and Biotechnology, University of Latvia, 4 Kronvalda blvd.,
LV-1586 Riga, Latvia
4, 5, 6
Institute of Food Safety, Animal Health and Environment (BIOR), 3 Lejupes str.,
LV-1076 Riga, Latvia
Submitted 6 Mar. 2012; accepted 14 Aug. 2012
Abstract. Trinitrotoluene (TNT), a commonly used explosive for military and industrial applications, can cause
serious environmental pollution. 28-day laboratory pot experiment was carried out applying bioaugmentation using
laboratory selected bacterial strains as inoculum, biostimulation with molasses and cabbage leaf extract, and
phytoremediation using rye and blue fenugreek to study the effect of these treatments on TNT removal and changes
in soil microbial community responsible for contaminant degradation. Chemical analyses revealed significant
decreases in TNT concentrations, including reduction of some of the TNT to its amino derivates during the 28-day
tests. The combination of bioaugmentation-biostimulation approach coupled with rye cultivation had the most
profound effect on TNT degradation. Although plants enhanced the total microbial community abundance, blue
fenugreek cultivation did not significantly affect the TNT degradation rate. The results from molecular analyses
suggested the survival and elevation of the introduced bacterial strains throughout the experiment.
Keywords: TNT, bioaugmentation, biostimulation, phytoremediation, microbial community.
Reference to this paper should be made as follows: No
˜lvak, H.; Truu, J.; Limane, B.; Truu, M.; Cepurnieks, G.;
Bartkevicˇs, V.; Juhanson, J.; Muter, O. 2013. Microbial community changes in TNT spiked soil bioremediation trial
using biostimulation, phytoremediation and bioaugmentation, Journal of Environmental Engineering and Landscape
Management 21(3): 153162. http://dx.doi.org/10.3846/16486897.2012.721784
Introduction
The nitroaromatic explosive, 2,4,6-trinitrotoluene (TNT),
has been extensively used for over 100 years, and this
persistent toxic organic compound has resulted in soil
contamination and environmental problems at many
former explosives and ammunition plants, as well as
military areas (Stenuit, Agathos 2010). TNT has been
reported to have mutagenic and carcinogenic potential
in studies with several organisms, including bacteria
(Lachance et al. 1999), which has led environmental
agencies to declare a high priority for its removal from
soils (van Dillewijn et al. 2007).
Both bacteria and fungi have been shown to
possess the capacity to degrade TNT (Kalderis et al.
2011). Bacteria may degrade TNT under aerobic or
anaerobic conditions directly (TNT is source of carbon
and/or nitrogen) or via co-metabolism where addi-
tional substrates are needed (Rylott et al. 2011). Fungi
degrade TNT via the actions of nonspecific extracel-
lular enzymes and for production of these enzymes
growth substrates (cellulose, lignin) are needed. Con-
trary to bioremediation technologies using bacteria or
bioaugmentation, fungal bioremediation requires
an ex situ approach instead of in situ treatment (i.e.
soil is excavated, homogenised and supplemented
with nutrients) (Baldrian 2008). This limits applicabil-
ity of bioremediation of TNT by fungiin situ at a field
scale.
Corresponding author: Jaak Truu
E-mail: jaak.truu@ut.ee
JOURNAL OF ENVIRONMENTAL ENGINEERING AND LANDSCAPE MANAGEMENT
ISSN 1648-6897 print/ISSN 1822-4199 online
2013 Volume 21(3): 153162
doi:10.3846/16486897.2012.721784
Copyright ª2013 Vilnius Gediminas Technical University (VGTU) Press
www.tandfonline.com/teel
© 2017 The Author(s) Published by VGTU Press and Informa UK Limited,
[trading as Taylor & Francis Group].
This is an Open Access article distributed under the terms of the Creative Commons Attribution-Non-
commercial-No Derivatives Licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits
non-commercial re-use, distribution, and reproduction in any medium, provided the original work is
properly cited, and is not altered, transformed, or built upon in any way.
The special issue on
Biochar as an Option for Sustainable Resource Management
Corresponding author: Claudia Kammann
E-mail: claudia.kammann@hs-gm.de
JOURNAL OF ENVIRONMENTAL ENGINEERING AND LANDSCAPE MANAGEMENT
ISSN 1648–6897 / eISSN 1822-4199
2017 Volume 25(02): 114–139
https://doi.org/10.3846/16486897.2017.1319375
Review article
BIOCHAR AS A TOOL TO REDUCE THE AGRICULTURAL GREENHOUSE
GAS BURDEN KNOWNS, UNKNOWNS AND FUTURE RESEARCH NEEDS
Claudia KAMMANNa, Jim IPPOLITOb, Nikolas HAGEMANNc, Nils BORCHARDd, Maria Luz CAYUELAe,
José M. ESTAVILLOf, Teresa FUERTES-MENDIZABALf, Simon JEFFERYg, Jürgen KERNh, Je NOVAKi,
Daniel RASSEj, Sanna SAARNIOk, Hans-Peter SCHMIDTl, Kurt SPOKASm, Nicole WRAGE-MÖNNIGn
aDepartment of Soil Science and Plant Nutrition, WG Climate Change Research for Special Crops,
Hochschule Geisenheim University, Von-Lade Str. 1, 65366 Geisenheim, Germany
bDepartment of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523-1170, USA
cGeomicrobiology, Center for Applied Geosciences, University Tübingen, Hölderlinstr. 12, 72074 Tübingen, Germany
dCenter for International Forestry Research, Jalan CIFOR, Situ Gede, Sindang Barang, Bogor 16115, Indonesia
eDepartment of Soil and Water Conservation and Waste Management, CEBAS-CSIC,
Campus Universitario de Espinardo, 30100 Murcia, Spain
fDepartment of Plant Biology and Ecology, University of the Basque Country (UPV/EHU),
Apdo. 644, E-48080 Bilbao, Spain
gCrop and Environment Sciences Department, Harper Adams University, Newport, Shropshire,
TF10 8NB, United Kingdom
hDepartment of Bioengineering, Leibniz Institute for Agricultural Engineering and Bioeconomy,
Max-Eyth-Allee 100, 14469 Potsdam, Germany
iUnited States Department of Agriculture, Agricultural Research Service (USDA-ARS),
Water and Plant Conservation Research, 2611 W Lucas street, Florence, South Carolina 295011242, USA
jDepartment of Soil Quality and Climate Change, Norwegian Institute of Bioeconomy Research,
Høgskoleveien 7, 1430 Aas, Norway
kDepartment of Environmental and Biological Sciences, University of Eastern Finland,
P.O. Box 111, 80101 Joensuu, Finland
lIthaka Institute for Carbon Strategies, Ancienne Eglise 9, CH-1974 Arbaz, Switzerland
mUnited States Department of Agriculture, Agricultural Research Service (USDA-ARS) and University of
Minnesota, Department of Soil, Water, and Climate, 1529 Gortner Ave., St. Paul, MN 55108, USA
nGrassland and Fodder Sciences, Faculty of Agriculture and the Environment, University of Rostock,
Justus-von-Liebig-Weg 6, 18051 Rostock, Germany
Submitted 7 Jan. 2017; accepted 11 Apr. 2017
Abstract. Agriculture and land use change has signicantly increased atmospheric emissions of the non-CO2 green-
house gases (GHG) nitrous oxide (N2O) and methane (CH4). Since human nutritional and bioenergy needs continue
to increase, at a shrinking global land area for production, novel land management strategies are required that reduce
the GHG footprint per unit of yield. Here we review the potential of biochar to reduce N2O and CH4 emissions from
agricultural practices including potential mechanisms behind observed eects. Furthermore, we investigate alterna-
tive uses of biochar in agricultural land management that may signicantly reduce the GHG-emissions-per-unit-of-
product footprint, such as (i) pyrolysis of manures as hygienic alternative to direct soil application, (ii) using biochar
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 115
Introduction: Human impact on global N2O and CH4
budgets and atmospheric concentrations
Human population now approaches 7.5 billion people
on earth. e land area that serves human nutrition and
bioenergy demands is not only limited, but declining due
to soil degradation in various forms (Lal 2014; Konuma
2016; FAO 2015). e dawning perception that “fertile
soils” are a nite global resource is stressed by recent land
grabbing practices where wealthier countries with large
populations and/or a lack of soil resources buy arable land
in poorer countries. is has mostly occurred in Africa
(Rulli etal. 2013), causing land use change to increase
crop productivity, likely with consequences in terms of
increasing GHG production. In fact, excessive human
land use change over the past decades has contributed to the
rapid, on-going increase in the atmospheric concentration of
non-CO2 greenhouse gases nitrous oxide (N2O) and methane
(CH4) from preindustrial levels of 270–280 ppbv to 324 ppbv
(N2O) and from ~700 ppbv to 1834 ppbv (CH4) (Myhre etal.
2013; Saunois etal. 2016).
e steep increase in atmospheric N2O concentra-
tions dominantly since the 1950s is clearly the result of
an increasing use of the Haber-Bosch process to gener-
ate reactive N forms from atmospheric N, plus the higher
proportion of legumes on farmland compared to natural
ecosystems; many important crop or fodder plants are N2-
xing legumes (e.g. soy, pea, lentils, beans, groundnuts,
clover). Global reactive-N use is now annually more than
double the amount introduced by natural processes (Gal-
loway etal. 2008); with increasing N fertilizer use comes
the increasing likelihood of N2O formation and atmo-
spheric accumulation. us, as stated by Ravishankara
etal. (2009), as the impact of uorinated halocarbons
decreases, N2O will likely become the dominant O3-de-
pleting substance within the agricultural sector over the
course of the 21st century.
Methane (CH4) emissions have also increased, by
150% since 1750 (Myhre etal. 2013) to 1834 ppb in 2015
(Dlugokencky etal. 1994; Saunois etal. 2016). Human
activities directly and indirectly contribute to the in-
creased atmospheric CH4 concentration by several path-
ways such as (i) expanding rice agriculture, ruminant
animal husbandry and landlling with unmanaged CH4
emissions, (ii) thawing permafrost areas and thermocast
lakes (Koven etal. 2011; Walter etal. 2006) and warming-
induced changes in plant community composition e.g.
expanding aerenchymal plant cover (Christensen etal.
2004), and (iii) “automatic” feedback eects such as rising
CH4 production under elevated, rising atmospheric CO2
concentrations from wetlands and agricultural lands due
to higher net biomass production as labile substrates for
methanogenesis (Van Groenigen etal. 2011).
To our knowledge, the last assessment of the human
impact of land-use changes and fertilizer use on global
CH4 consumption was made 20 years ago (Ojima etal.
1993). e authors estimated that human activities have
already reduced the global net CH4 sink capacity by 30%.
Hypotheses for explaining the reduction encompass hu-
man impact on (i) soil moisture changes, (ii) reduced soil
aeration via compaction / increased bulk density (both
impact gas diusivity and hence CH4 and O2 supply, (Cas-
tro etal. 1994; Hiltbrunner etal. 2012), and (iii) inhibition
by NH4+ (N fertilization or reduced nitrication in acidic
soils (Schnell, King 1995; Steudler etal. 1989). Also, (iv)
shis in the microbial community composition are hy-
pothesized, but without conclusive evidence (Gulledge
etal. 1997).
Over the last decades, the rising use of mineral N fer-
tilizer (Galloway etal. 2008), soil degradation and forest
clear-cutting, and a rising frequency of weather extremes
(Hansen, Sato 2016) creating “too wet” or “too dry” soil
conditions (Dijkstra etal. 2011) will likely further reduce
the global methanotrophic CH4 sink, and increase CH4
and N2O emissions. erefore, any positive contribution
that science and material use may provide agricultural
soils for reducing N2O emissions per unit yield, and in
reducing either the CH4 production and surface emis-
sions from soils or ruminant guts (see sections 3 and 4),
or by strengthening the soil CH4 oxidation capacity (sec-
tion 3.2) and its biolter function (section 3.1), needs to
be explored. Agricultural practices that utilize biochar
for meeting these needs appears promising, and should
be explored and developed to help lower the greenhouse
gas (GHG) footprint per unit yield or bioenergy produced
(also termed GHG intensity) (Wollenberg etal. 2016).
A reduction of N2O and CH4 within agroecosystems
can be achieved by either increasing the per-hectare yield
at unchanged GHG emission rates, by lowering the per-
hectare N2O and/or CH4 emissions/increasing CH4 up-
take, or ideally by both. Currently literature suggests that
biochar may play a role in reducing both of these GHGs;
biochar can aect GHG emissions directly following its
application to soils, and indirectly by adding carbonized
instead of non-carbonised residue or manures which usu-
ally have higher emissions following application. us, the
aim of this paper is to explore our current understanding
as fertilizer carrier matrix for underfoot fertilization, biochar use (iii) as composting additive or (iv) as feed additive in
animal husbandry or for manure treatment. We conclude that the largest future research needs lay in conducting life-
cycle GHG assessments when using biochar as an on-farm management tool for nutrient-rich biomass waste streams.
Keywords: biochar, greenhouse gases (GHG), nitrous oxide (N2O), methane (CH4), soil aeration, nitrate, soil N trans-
formations, GHG intensity.
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
116
and knowledge gaps of biochar use as a tool to reduce N2O
and CH4 emissions from agricultural land use. To this
end, the biogeochemical mechanisms of formation and
consumption of N2O and CH4 in soils and their emission
to the atmosphere are presented and discussed. e topic
of build-up of the soil organic carbon stocks by biochar
amendment, or by reduced soil organic carbon decompo-
sition (negative priming) is not explored here, only some
rough assessments are made to illustrate potentials (e.g.
for using biochar as animal feed additive).
1. Eects of biochar application to soils on N2O
emissions
1.1. Mechanisms of N2O formation in soils and release
to the atmosphere
Soils are a prominent source of N2O emissions, especial-
ly when fertilised with organic or mineral N fertilisers.
A wide range of microbial and chemical processes and
pathways are responsible for these emissions (see Fig. 1),
with knowledge on these pathways continuously improv-
ing. e classical view was that bacterial denitrication,
the reduction of nitrate and nitrite in several steps to N2,
is the main source of N2O from most soils, especially at
intermediate water contents (Bateman, Baggs 2005). Vari-
ous bacteria that are phylogenetically unrelated are ca-
pable of denitrication, with many not having the full set
of enzymes for the complete pathway (Zum 1997). is
leads to the escape of intermediates, including N2O. Un-
der certain circumstances such as low pH and high NO3/
Corg ratios, the production of N2O is favoured compared to
the nal production of N2. e reduction of N2O to N2 is
performed by the enzyme nitrous oxide reductase, which
is encoded by the nosZ gene in denitrifying bacteria. In a
laboratory study, lower N2O emissions were inversely cor-
related to the nosZ gene expression (Harter etal. 2014).
Meanwhile, we know that bacterial nitriers may
dominate N2O emission from some soils, e.g. by the path-
way nitrier denitrication (Kool etal. 2011a). Bacterial
nitriers use ammonia as a substrate and reduce interme-
diately produced nitrite in a comparable way as in denitri-
cation. Nitriers have been found to be also able to use
nitrite provided exogenously in incubation studies under
aerobic conditions (Shaw etal. 2006). Fungi may play a
dominant role for N2O production from soils, either by
codenitrication or by fungal denitrication (Laughlin,
Stevens 2002; Rohe etal. 2014). e role of archaea for
N2O production from soils is still unknown, but there is
evidence of potentially signicant archaeal contributions
(Jung etal. 2014), although the responsible pathways are
yet unresolved (Jung etal. 2014; Stieglmeier etal. 2014).
As these processes may take place simultaneously in
dierent soil microsites, it is not straightforward to distin-
guish among them. Several methods have recently been
developed that try to unravel the sources of N2O, including
stable isotopes (Sutka etal. 2006; Kool etal. 2011b; Rohe
etal. 2014; Lewicka-Szczebak etal. 2016) and molecular
or modelling approaches (Rütting, Müller 2007; Kozlowski
etal. 2014; Perez-Garcia etal. 2014; Snider etal. 2015).
So far, no single method has oered a complete picture of
the diverse N2O producing pathways and a combination of
methods seems most promising.
1.2. Impact of biochar on soil N2O emissions: frequent
observations and assumed mechanisms
One of the rst biochar experiments reporting reduced
N2O emissions was presented in the 3rd USDA Symposium
on greenhouse gases and carbon sequestration in agricul-
ture and forestry (Rondon etal. 2005). A signicant de-
crease in N2O emissions was observed in pots planted with
soybean and grass in a greenhouse experiment. However,
Fig. 1. a) Processes and b) pathways of N conversions associated with N2O emissions in soils in relation to N transformations (A)
and N and C substrates (B). (Figure credit: N. Wrage-Mönnig)
a) b)
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 117
this nding went unnoticed for several years and only aer
the pioneering studies by Yanai etal. (2007), Spokas etal.
(2009) and van Zwieten etal. (2009), the number of pub-
lications on this topic started to rise. Hence, a new eld
of research was established, exploring a potential win-win
situation: biochar not only sequestered carbon but also
had the potential to decrease non-CO2 GHG emissions.
To date, the hypotheses for biochar’s impact in char-
soil mixtures on N2O emissions has been linked to bio-
char properties, the soil and the environmental conditions
such as temperature and precipitation (Spokas, Reicoscoky
2009; Dicke etal. 2015). Studies have mostly been carried
out in the lab using sieved/disturbed soil samples wetted
either to the same gravimetric moisture, or to the same
water-lled pore space, water holding capacity or water
potential. Other investigations in combination with plant
growth in the greenhouse or under less controlled con-
ditions in the eld have also shown that biochar may af-
fect the soil N2O emissions (e.g. Taghizadeh-Toosi etal.
2011; Schimmelpfennig etal. 2014; Kammann etal. 2012;
Deng etal. 2015; Hüppi etal. 2015). In the presence of
N2O-producing earthworms (soil fauna interactions), N2O
emissions were also reduced by biochar application (Au-
gustenborg etal. 2012; Bamminger etal. 2014). However,
in some studies no dierence between biochar and con-
trol treatments was observed (Scheer etal. 2011; Sánchez-
García etal. 2016) or N2O emissions were increased from
biochar amended soils (e.g. Spokas, Reicoscoky 2009;
Clough etal. 2010; Saarnio etal. 2013; Troy etal. 2013).
However, laboratory results cannot be generalised to eld
expectations. In eld trials, oen no statistical dierences
are observed between biochar and control treatments fol-
lowing eld application of biochar (Castaldi etal. 2011;
Jones et al. 2012; Karhu etal. 2011; Scheer et al. 2011;
Schimmelpfennig etal. 2014; Suddick, Six 2013; Dicke
etal. 2015). One potential reason for no signicant bio-
char eects on N2O emissions may be the application
dose, less homogeneous particle distribution and greater
soil (and plant) heterogeneity in elds resulting in high
variability in N2O uxes (large error bars, e.g. Hüppi etal.
2015).
Nevertheless, overall, meta-analyses conrmed that
N2O emissions are reduced with biochar application rates
of 1–2% by weight (van Zwieten etal. 2015; Cayuela etal.
2014). In spite of the extensive literature published during
the past several years on the topic, knowing if a biochar
will be eective in mitigating N2O emissions in a certain
agricultural eld is still highly unpredictable. us, most
research eorts are now directed towards achieving the
largest N2O emission reductions (what type of biochar to
use in what soils) by analysing the mechanisms involved.
Many studies have shown that biochar N2O mitigation
capacity will depend not only on the characteristics of
the biochar, but also on the type of soil and predominant
environmental conditions (Cayuela etal. 2013; Malghani
etal. 2013; Nelissen etal. 2014). A remarkable nding was
that, under identical environmental conditions, the same
biochar could increase emissions in one soil and decrease
emissions in another (Yoo, Kang 2012; Sánchez-García
etal. 2014). is fact seems to be linked to diverse N2O
formation mechanisms operating in dierent soils, of
which biochar might be aecting dierently. In this sense,
knowing how biochar interacts with the key microbial
pathways regulating N2O formation and consumption in
soil is crucial for developing and implementing eective
mitigation strategies. However, the number of studies
looking at specic N2O formation pathways is still very
limited and the mechanisms mediating N2O suppression
are still unresolved.
To date, most N2O-biochar studies selected certain
environmental conditions and assumed or speculated the
predominant N2O formation mechanisms. For instance,
studies at high water-lled pore space anticipated that the
main N2O formation pathway would be heterotrophic de-
nitrication. However, this reasoning has frequently been
shown to be incorrect. In complex soil environments,
ammonia oxidation and nitrier denitrication generally
coexist with heterotrophic denitrication (Hu etal. 2015)
and the proportion of N2O produced in each pathway de-
pends on many factors, not just water-lled pore space
(Wrage etal. 2001; Butterbach-Bahl etal. 2013). ere-
fore, studies that really dierentiate among N2O produced
by dierent sources aer addition of biochars are still ur-
gently needed.
1.2.1. What do we know about the impact of biochar on
denitrication N2O?
Denitrication is classically the most well-known mecha-
nism leading to N2O emissions and to date, also the most
investigated in biochar studies. Biochar might interact with
denitrication in dierent ways. Biochar might directly
stimulate or suppress total denitrication, i.e. the amount
of N that goes to gaseous form (N2 + N2O + NO). e
impact of biochar on total denitrication has been barely
studied and the results are inconclusive. For instance, us-
ing stable isotope enrichment, Cayuela etal. (2013) ana-
lyzed the ux of total N denitried (N2 + N2O) at the peak
of N2O emissions and found that biochar decreased the
total denitricatory N eux in 9 out of 15 soils, but sig-
nicantly increased the ux in two soils. Obia etal. (2015)
measured NO, N2O and N2 by high resolution gas kinet-
ics under strictly anaerobic conditions and calculated the
maximum induced denitrication rate, which was found
to increase with one type of biochar (cacao shell), but not
with another biochar (rice husk) in an acidic soil. By using
the acetylene inhibition technique, Ameloot etal. (2016)
found a general decrease in total denitried N (N2 + N2O)
with biochar in a neutral soil. Biochar might therefore
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
118
decrease or increase total denitrication depending on the
type of soil. More studies are needed to understand the
mechanisms behind these observations.
A decrease in total denitrication was initially at-
tributed to improved soil aeration following biochar ad-
dition (Zhang etal. 2010), a hypothesis that has been
rebutted by Case etal. (2012) who demonstrated that
soil aeration played a minimal role in N2O mitigation.
Furthermore, several studies used adjusted water con-
tents to account for increased water holding capacities
that oen arise when biochar is mixed into the soil (e.g.
light-weight porous biochars in sandy soils), to render
simple aeration eects unlikely (e.g. Kammann etal.
2012); still these studies observed signicant N2O emis-
sion reductions. Another hypothesis suggested a gen-
eral decrease in soil microbial activity as a consequence
of toxic compounds present in biochar. For example,
phenolic compounds and PAHs have been observed to
contribute to the reduction in N2O release from agricul-
tural soils (Wang etal. 2013a). However, Alburquerque
etal. (2015) demonstrated that this hypothesis was un-
founded, since the presence of PAHs at typical biochar
concentrations did stimulate, rather than inhibit, N2O
emissions. Moreover, even if PAH containing biochars
would reduce N2O emissions, they will denitely never
be used in soils under any countries’ soil and fertilizer
regulations. In addition, numerous studies used clean
biochars with hardly detectable traces of even the most
abundant PAH (naphthalene) and these studies still
showed reduced N2O emissions (study compilations in
Cayuela etal. (2014) and van Zwieten etal. (2015)).
Several studies pointed out that microbial or
physical or plant immobilization of NO3– in soil fol-
lowing biochar addition could signicantly contribute
to the reduction of soil N2O emissions (compilation of
N2O-biochar studies in van Zwieten etal. 2015). is
hypothesis is reinforced by recent research showing
that biochar is able to capture considerable amounts of
nitrate, which is only partly detectable with standard
methods and largely protected against leaching (Kam-
mann etal. 2015; Haider etal. 2016). Nitrate capture
may physically separate nitrate from denitriers and
thus reduce nitrate availability.
On the other hand, biochar might interact with the
denitrication process by modifying the ratio of denitri-
cation products (N2O/N2). us, biochar may decrease
the N2O/N2 ratio (Cayuela etal. 2013; Harter etal. 2014;
Obia etal. 2015), but many questions arise from this
nding. For instance, Obia etal. (2015) related this phe-
nomenon to the alkalinizing eect of biochar in soil.
However, the decrease in the N2O/N2 ratio has also been
found in alkaline soils (Cayuela etal. 2013), where an
increase in pH did not occur aer biochar amendment.
Harter etal. (2016) found that biochar addition led to
the development of functional traits capable of N2O
reduction, containing typical and atypical nosZ genes.
Following a dierent line of research, several recent ar-
ticles highlight the importance of biochar redox prop-
erties, which may have a bigger impact on soil biogeo-
chemical processes than previously thought (Prévoteau
etal. 2016). In this line, Quin etal. (2015) measured
N2O reduction by injecting 15N-N2O in sterilized soil
columns and demonstrated that biochar took part in
abiotic redox reactions reducing N2O to dinitrogen (N2),
in addition to adsorption of N2O. Despite the current
knowledge about the impact of biochar on denitrica-
tion, additional studies are highly needed to explore the
detailed response mechanisms of denitriers to biochar
amendment.
1.2.2. What do we know about the impact of biochar on
N2O from nitrication and other processes?
It has been described that gross nitrication rates could
be increased aer biochar amendment because of high-
er substrate availability for nitrifying bacteria (Nelissen
etal. 2012), and several studies have analysed the impact
of biochar on gross and net nitrication (Prommer etal.
2014). ere is also a potential that biochar addition may
increase nitrication (and with it, N2O formation via ni-
trication pathways; Figure 1 in systems (such as needle-
rich raw humus soils) due to the sorption of phenolic
compounds; the latter can block or reduce nitrication. A
signicant increase in nitrication was seen in boreal for-
ests aer biochar addition (DeLuca etal. 2006; Ball etal.
2010) where sorption of phenols on biochar was respon-
sible for increased nitrication rates. However, only a cou-
ple of studies distinguished among N2O emissions from
nitrication pathways (via ammonia oxidation or nitrier
denitrication) and other sources by using isotopic signa-
tures of N2O, inhibition techniques or molecular methods.
In a laboratory incubation, Sánchez-García etal. (2014)
found that the addition of biochar increased N2O emis-
sions from a calcareous soil and concluded that the N2O
formation pathway operating in the soil was nitrication
(probably nitrier-denitrication). In another study, Wells
and Baggs (2014) showed that the biochar inuence came
primarily via ammonia oxidation, not N2O reduction or
production by denitriers, and increased N2O emissions
by 27%.
Dedicated studies of biochar eects on other soil
sources of N2O are largely missing. At low soil pH values,
it has been observed that fungi produced N2O instead of
N2 through codenitrication in presence of other nitro-
gen compounds, such as azide, salicylhydroxamic acid,
nitrite and ammonium (Liiri etal. 2002). Since biochar
can contain azide as well as other compounds, biochar
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 119
additions could theoretically enhance these fungal code-
nitrication processes. ere are limited studies examin-
ing the functionality of the N2O suppression through use
of selective microbial inhibitors, and data did support
the role of a particular microbial group in the N2O sup-
pression (bacteria or fungal, Lin etal. 2014). However, a
soil pH increase caused by biochar addition could also
reduce N2O production from fungal codenitrication,
thus the net outcome is unknown. Microbial community
composition will likely play a role: Using an identical
biochar in laboratory incubations across a series of 10
dierent soils, omazini etal. (2015) observed a trend
for the biochar suppression that could be correlated to
the total soil microbial biomass in the original soil. e
knowledge of eects of biochar additions on various
microbial sources of N2O are still little understood and
partly contradictory. Clearly, more research is needed
to be able to design biochars for the purpose of N2O
emission reduction not only in soils, but also when us-
ing biochar in the management of N-rich agricultural
(fertilizer) materials such as manures or composts (see
sections 3.1 and 3.3).
1.2.3. Long-term eects of biochar addition and in old
charcoal-rich soils: what do we know?
It is also still unclear how long N2O emission reductions
may persist following biochar addition to soil; or if old,
black-carbon rich soils that undergo a change in their
physico-chemical properties (such as Amazonian or Af-
rican Dark Earths) will have a lower or higher potential
for mitigating N2O emissions compared to soils without
biochar. While a lab study reported that aged biochar
particles increased N2O emissions (Spokas 2013), the op-
posite was observed in an experiment with >100 year-old
charcoal particles from a kiln site (Kömpf 2013). Hage-
mann etal. (2016) reported that biochar still signicantly
suppressed N2O emissions in the third season in the eld
compared to the corresponding control eld site without
biochar. More data are slowly emerging on old charcoal-
rich soils (e.g. from historic kiln sites, Borchard etal.
2014a; Hardy etal. 2016, 2017), and more Dark Earth
sites besides those in the Amazon basin have now been
identied (e.g. in Liberia and Ghana, Solomon etal. 2016).
However, to our knowledge no experiments on N2O emis-
sions and soil N transformations have yet been carried out
on these long-term analogues compared to their adjacent
native, non-black-carbon soils. For the overall question if
using biochar does oer long-term benets regarding N2O
emission suppression, exploring long-term eects is likely
of great importance, since reducing peak emissions in the
rst years will only be a small part over the long-term.
Particularly, these longer- and long-term eects are com-
pletely underexplored, and deserve much more research
attention in the near future.
2. Eects of biochar application on soil CH4 uxes
2.1. Mechanisms of CH4 uxes: production and
consumption in soils and net release to the atmosphere
e two biotic processes that determine the net methane
(CH4) exchange between soils/ecosystems and the at-
mosphere are methane production by strictly anaerobic
methanogenic Archaea (Methanogens) and methane con-
sumption by methanotrophic bacteria (Methanothrophs).
Methane production takes place in all anoxic environ-
ments where organic carbon is microbially degraded
(Conrad 2007a, 2007b; Whalen 2005), for example in
peatlands, lake sediments, ooded rice elds, in landlls,
in the guts of ruminant animals, termites or Scarabaeidae
larvae (Hackstein, Stumm 1994; Kammann etal. 2009).
Methanogens derive their energy from H2 and carbon di-
oxide (CO2) or acetate, formate, methanol or other pri-
mary and secondary alcohols and methylated compounds
(Brasseur, Chateld 1991; Conrad 1999). Methanogenesis
is thermodynamically the least ecient process i.e. other
reduction processes outcompete CH4 production, if the
concentration of alternative electron acceptors, such as
nitrate (NO3-), sulphate (SO42-), iron (Fe(III)) and manga-
nese (Mn(IV)), is high in relation to the input of organic
substrates (Lovley, Phillips 1987; Oremland 1988; Conrad
1989). Spatial and temporal variation in CH4 can be large
(e.g. Saarnio etal. 1997; Juutinen etal. 2003): Spatial vari-
ation in CH4 ux within dierent microsites of the same
ecosystem (e.g. Saarnio etal. 1997) and between dier-
ent ecosystem types (e.g. Saarnio etal. 2009). Water table
and temperature are dominant controls on CH4 eux in
bogs and swamps whereas the eect of aquatic vascular
plants (aerenchyma “ventilation”) was the most important
in fens or rice paddies (Turetsky etal. 2014). Besides the
aerenchyma transport, CH4 can also be transported with
the transpiration water stream in swamp tree species as
shown by Terazawa etal. (2007). Many 14CO2 experiments
have shown that recently xed C is rapidly delivered from
plants to methanogens (e.g. Megonigal etal. 1999) but the
amount of exuded carbon is many times lower than that
delivered via litter formation (Saarnio etal. 2004).
Methane consumption in soils is also ubiquitous in
all terrestrial environments (Hütsch 2001; Seiler etal.
1984), and human land-use changes such as deforesta-
tion, ploughing and N fertilization reduce the soil CH4
sink (Powlson etal. 1997). Net CH4 consumption is due
to the activity of methanotrophic α- and γ-proteobacteria.
Most methanotrophs use CH4 as the sole carbon source
and need oxygen to be active (Conrad 2007a). In upland
soils, methane oxidation is largely determined by the soil
diusivity for CH4 and O2 (Castro etal. 1994, 1995). Ac-
cording to their CH4-oxidation kinetics, categories of
“high-affinity” and “low-affinity” methanotrophs are
oen dened (Duneld 2007). e rst group occurs
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
120
dominantly in upland soils and can consume atmospheric
and sub-atmospheric CH4 concentrations (<1800 ppb),
while low-anity groups are found in anoxic environ-
ments (e.g. rice paddy soils) in the aerobic centimeters or
millimeters of topsoil or in the oxygenated plant rhizo-
spheres; these methanotrophs need higher CH4 concentra-
tions. CH4 consumption can provide a “biolter function”
for environments with high CH4 production (rice paddies,
landll cover soils etc.).
2.2. Biochar eects on CH4 production and release in
net CH4-source soils
e interactions between biochar application to soil and
CH4 uxes are not well understood, with disparate litera-
ture results (Jeery etal. 2016; Song etal. 2016). Biochar
application to paddy or ooded soils have been shown to
increase (Yu etal. 2013; Zhang etal. 2012), decrease (Feng
etal. 2012; Khan etal. 2013b; Lin etal. 2015; Qian etal.
2014), or have no signicant eect on CH4 emissions (Xie
etal. 2013). In anaerobic environments, the labile C pool
of biochar may theoretically function as methanogenic
substrate, promoting CH4 production (Zhang etal. 2010).
However, the labile C pool of root exudates and root lit-
ter is by far larger, thus labile biochar C may only play a
role (i) initially, (ii) when the biochar has been produced
at low temperature (i.e., greater labile C fraction), (iii)
in bare/fallow soils without root carbon supply, and (iv)
when the biochar amount added is great (>40 t/ha) (Saar-
nio 2016). As an example, Zhang etal. (2012) did not ob-
serve increased soil CO2 eux over two consecutive rice
cropping years with 10–40 t ha-1 biochar amendments,
but signicantly reduced N2O emissions at increased CH4
emissions; thus labile biochar-C is an unlikely explanation.
Biochar was reported to also promote methanotrophic
CH4 consumption at oxic/anoxic interfaces in anoxic envi-
ronments. is lowered the net CH4 emissions by the “bio-
lter” function of bacterial (low-anity) CH4 oxidation
before it escaped to the atmosphere. When methanotro-
phic organisms increasingly oxidise CH4 in the presence
of biochar at the oxic/anoxic root interface, they lower the
amount of CH4 that can enter into the plants’ aerenchyma
to escape (Feng etal. 2012).
In a greenhouse mesocosm study with sewage sludge
biochar (high application rates of 5% and 10%), rice yield
increased while the paddy soil turned from a net CH4
source to a net CH4 sink; this occurred in both rice-plant-
ed and bare paddy soil. ese results may have been due
to the addition of electron-accepting ash substances or ni-
trate with the sewage sludge biochar. In biochar-amended
landll cover soil, an increased CH4 oxidation activity was
responsible for decreasing CH4 eux from greater landll
depths (Sadasivam, Reddy 2015; Reddy etal. 2014). Here,
the physico-chemical properties including air conductivity
were considerably increased by biochar, i.e. the biochar ef-
fect might have been to improve the O2 supply to meth-
ane oxidizers. A recent meta-analysis (Song etal. 2016) of
CH4 emissions reported that biochar application caused
no pronounced change in CH4 emissions overall but
that there was signicant increase in methane emissions
(+19%). In another recent meta-study including papers
up to December 2015, Jeery etal. (2016) reported that
biochar amendment to ooded and/or acidic soils had the
potential to signicantly reduce CH4 emissions. ese two
meta-studies dier in their conclusions, which may be due
to a dierent database and meta-analytical approach.
Biochar impacts on natural net-methanogenic en-
vironments such as salt ats and wetlands are even less
well understood. Owing to the longevity of biochar and its
potential mobility and migration from anthropogenic sys-
tems, it will likely migrate to coastal areas over the long-
term (as recently shown for dissolved pyrogenic organic
carbon, Jaé etal. 2013). Lin etal. (2015) investigated bio-
char application to saline costal soils where soybean and
wheat was grown. ey did not nd any signicant eect
of biochar application to such soils on the (overall low)
CH4 emissions, but they observed a yield increase of 24
and 28% in soy and wheat, respectively. In rice eld stud-
ies, reductions in CH4 and/or N2O emissions were also of-
ten accompanied with increases in crop yields by between
10 and 20% (Dong etal. 2015; Khan etal. 2013a; Zhang
etal. 2012), resulting in a reduced greenhouse gas inten-
sity per kg of rice grain.
Biochar implementation may also reduce the GHG
intensity per unit of agricultural product by reducing
N-fertilizer and labile-C inputs at unaltered or increased
yields. Qian etal. (2014) reported that the use of 4 dif-
ferent biochar-compound fertilizers made of chemical
fertilizers, biochar and bentonite, at rates of well below
1t biochar ha–1, signicantly improved the GHG intensity
of a rice crop (by 36–56%) by: 1) the biochar-compound
fertilizer increasing grain yields by 10–31%; and 2) re-
ducing CH4 emissions by 25–50% and N2O emissions by
17–39%. ese results coincided with a reduced overall
N fertilizer input, from 210 kg N to 168 kg N ha–1, and
without taking the CO2-equivalents of reduced fertilizer
production and use into account (Qian etal. 2014). us,
there is a considerable potential for reducing the GHG
intensity of rice crop production, particularly in acidic
soils (Jeery etal. 2016), and that this potential extends
beyond the C-sequestration potential. Large amounts of
biochar do not need to be used at once since improve-
ments were found at biochar rates <1 t ha–1 (Qian etal.
2014). erefore, three central research topics emerge
here: (1) More research is needed on mechanisms of CH4
(and N2O) emission reductions with biochar use from
paddy and anaerobic soils including the eects on the
“methanotrophic biolter”; (2) Dedicated research on
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 121
biochar-eect-mechanism systematics to design biochars
with desired properties (omazini etal. 2015); and per-
haps most importantly (3) Research on biochar compound
fertilizers or underfoot fertilizers (Schmidt etal. 2015), to
achieve higher yields at reduced GHG emissions and re-
duced N fertilizer use.
2.3. Biochar eects on net CH4 consumption in oxic
upland soils
Well-aerated upland soils are characterised by CH4 con-
sumption, mediated by methanotrophic bacteria. Forest,
grassland and arable land have been described as CH4
sinks with ux rates of up to 65 µg CH4 m–2 hr–1 (Dalal
etal. 2008; Kern etal. 2012; Wang etal. 2005). As out-
lined above, in oxic/anoxic soil interfaces with a consid-
erable CH4 source strength, where the methane oxidiser
community is dominated by low-anity methanotrophs,
signicant increases in methanotrophic abundance and/or
activity have been reported following biochar amendment
(Feng etal. 2012; Reddy etal. 2014; Sadasivam, Reddy
2015). However, upland soils mostly host high-anity
methanotrophs, capable of consuming atmospheric meth-
ane. Species composition and biology is dierent to that
from anoxic soils (Duneld 2007), and the CH4-consum-
ing activity is quite easily hampered by human “activities”
such as land conversion (particularly deforestation), N
fertilization and ploughing. e number of studies using
upland soils and measuring CH4 consumption with/with-
out biochar is currently not large. Kollah etal. (2015) ob-
served signicantly increased CH4 consumption rates in a
lab study with tropical soil amended with biochar (with or
without organic amendments), as did Karhu etal. (2011)
in in-eld boreal, ploughed grassland soil. Karhu etal.
(2011) assumed that the observed doubling of the CH4
consumption in the ploughed grassland soil was due to
altered gas diusivity and water holding capacity (which
increased by 11%). However, the eects may also be con-
nected to increased N mineralization which usually occurs
aer ploughing, and where biochar may have prevented
N (NH4+) inhibition by sorbing NH4+ (Taghizadeh-Toosi
etal. 2012). Schimmelpfennig etal. (2014) observed in-
creased CH4 consumption in clay loam soil under labora-
tory condition; however, in the eld this was only present
in tendency. Similarly, Scheer etal. (2011) did not observe
increased soil CH4 consumption in a subtropical pasture
that had been amended by 10 t ha–1 manure biochar in
Australia.
In their meta-analysis, Song etal. (2016) reported
high levels of uncertainty for CH4 oxidation in upland
soils, while Jeery etal. (2016) concluded that biochar
addition may reduce the CH4 sink in neutral to alkaline
upland soils. Over all data sets, biochar had a CH4 sink-
increasing (or source-decreasing) eect in soils fertilized
at rates <120 kg N ha–1. Translated to upland soils this
indicates that, when true high-anity methanotrophic
activity is present, it may be increased by biochar applica-
tion. However, when high N application rates are used this
was not the case (Jeery etal. 2016); with high N fertiliza-
tion the CH4-oxidising activity of an agricultural soil is of-
ten considerably reduced or completely shut down, likely
due to nitriers replacing methanotrophs. In this case, the
methanotrophic population would not be supported or
improved. Taken together, the eects of biochar amend-
ment on soil CH4 consumption are not well understood.
Here, mechanistic studies are missing in particular, and
thus should be a focus for future research.
3. GHG emission reduction in animal husbandry and
waste management using biochar
Aer nearly a decade of research where biochar was
solely added to soil to assess GHG uxes, there is a shi-
ing perception, that biochar may also be used as a tool
to achieve GHG emission reductions during the handling
and management of organic nutrient-rich materials such
as manures. is section focuses on the use of biochar in
animal husbandry and in composting or plant-substrate
production (the topic of peat replacement is addressed
by Kern etal. 2017, this issue). In Germany, Austria and
Switzerland about 90% of the traded biochar is used in
animal husbandry, mainly as feed additive (in the way ac-
tivated carbon is used). However, to date, this topic has
been nearly neglected in biochar research.
3.1. Biochar as additive for feed and manure treatment
in animal farming to reduce the emission of GHG
Charcoal has been used to treat digestive disorder in
animals for several thousand years. Cato the Elder
(234–149 BC) mentioned it in his classic On Agriculture:
“If you have reason to fear sickness, give the oxen before
they get sick the following remedy: 3 grains of salt, 3 lau-
rel leaves, […], 3 pieces of charcoal, and 3 pints of wine.”
(Cato 1935, §70; O’Toole etal. 2016). At the end of 19th to
beginning of the 20th century, charcoal was increasingly
used on a regular base to increase animal performance and
health (PSAC 1905; Day 1906; Savage 1917; Totusek, Bee-
son 1953; Volkmann 1935). Later during the last century,
veterinarian research focused on activated charcoal trials
mostly in the form of time-restricted medications against
intoxication and bacteriological as well as viral diseases
(Toth, Dou 2016; Schmidt etal. 2016). Only since about
2010 has biochar increasingly been used as regular feed
additive in animal farming (O’Toole etal. 2016), usually
mixed with standard feed at approximately 1% of the daily
feed intake. While scientists and farmers gained most of
the results and experience in cattle and chicken farming,
biochar is also administered to sheep, goats, pigs, horses,
rabbits, cats, dogs and extensively in sh farming (Toth,
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
122
Dou 2016; Schmidt etal. 2016). In a German review pa-
per, Schmidt etal. (2016) evaluated more than 100 scien-
tic papers on feeding biochar to various animal groups.
Most of the studies showed for all investigated livestock
species, positive (but not always signicant) eects on pa-
rameters such as toxin adsorption, digestion, blood val-
ues, feed-use eciency, cell numbers in milk and livestock
weight gain; the latter may result from the pH-increasing
eect of various biochars since these are mostly alkaline
in nature (see 3.3). Buering the pH in the rumen could
likely prevent acidosis which is known to impact livestock
weight gain. However, only a small number of researchers
measured GHG emissions.
While chicken, pigs, sh and other omnivore ani-
mals provoke GHG emissions (mainly CH4, N2O; and
NH3) when their liquid and solid excretions decompose
anaerobically, ruminants cause direct methane emissions
through atulence and burps (eructation). is is espe-
cially the case for cattle that emit daily 500 to 600 l gas
with an average methane content between 6 and 8%. e
earliest evidence that feeding of biochar might reduce
cattle methane emissions came in a 2012 Vietnam study
(Leng etal. 2012a). In-vitro studies revealed signicant
methane reductions of 10 to 12.7% when biochar was fed
at rates between 0.5 and 1%. If biochar was blended with
nitrate, methane emissions were reduced by up to 49%.
Nitrate becomes a strong electron acceptor in the anaero-
bic rumen, keeping the hydrogen potential low, and thus
replacing a function of methane producing microorgan-
isms. Vongsamphanh etal. (2015) also found in in-vitro
tests with 1% biochar, while using cassava in rumen uid,
a 7% reduction of methane emissions within 24 h. In-vivo
trials of Leng etal. (2012b) revealed a reduction of enteric
methane of cattle by 20% with feeding 0.6% biochar and
by 40% with feeding 0.6% biochar blended to 6% potas-
sium nitrate, leading to a highly signicant animal weight
increase of 25% over 98 days. is is by far the most spec-
tacular result in reducing enteric cattle methane, but it has
unfortunately not yet been supported by other in-vivo or
in-vitro trials. Hansen etal. (2012) published the results of
an in-vitro trial with various non-characterized biochars
and their eect on methane production in rumen liq-
uids. All tested biochars showed a trend to reduce meth-
ane emissions between 11% and 17%. Other groups have
not repeated Leng and colleagues’ promising results. e
reason could be that Leng and colleagues used high tem-
perature gasier biochars made from rice husk, resulting
usually in carbonaceous materials with high electric con-
ductivity and electron buering capacity (Yu etal. 2015)
which may have had a stronger inuence on the digestion
reactions electrochemically than woody biochar. Using
biochar feeding to reduce ruminant methane emissions is
currently only an interesting perspective that needs more
systematic research.
Methane adsorption capacity by biochar is typically
the most investigated pathway for explaining eects when
fed to animals, but adsorption cannot explain all observa-
tions. Another decisive complementary function of bio-
char is its electro-biochemical interaction with biological
active systems, with research only recently beginning. Bio-
chars that are produced at temperatures above 700 °C are
not only good electrical conductors (Yu etal. 2015; Mo-
chidzuki etal. 2003) but can take part in biotic and abiotic
redox-reactions as an electron mediator (Husson 2013;
Kluepfel etal. 2014; Joseph etal. 2015a; Liu etal. 2012;
Shi etal. 2016; Van der Zee, Cervantes 2009; Yu etal.
2015; Kappler etal. 2014). A well balanced animal feed
regime contains multiple electron mediating substances,
however, in the high energetic diets of intensive livestock
farming these compounds are oen not contained in suf-
cient amounts (Sophal etal. 2013). If in these cases inert
or other non-toxic electron mediators like biochar, wood
vinegar or humic substances are added to the feed, many
redox reactions may take place more smoothly and e-
ciently which could increase energy conversion eciency
and thus feed eciency (Liu etal. 2012; Leng etal. 2013),
and eventually decrease enteric and post digestive GHG
production. Particularly, lowering CH4 emissions (which
are always a sign of energy loss) may be aided by the elec-
tron shuttling abilities of biochar. Moreover, it might be
assumed that the buering of the redox-potential as well
as the eect of electron shuttling between various micro-
bial species has a selective, milieu forming eect which
facilitates and accelerates the formation of functional mi-
crobial consortia and syntrophic species (Kalachniuk etal.
1994). e latter could explain why several studies found
a strong increase of Lactobacilli or a decrease of gram-
negative bacteria (Naka etal. 2001; Choi etal. 2009) which
seems to improve animal health. us, it may be hypoth-
esized that direct electron transfers between dierent spe-
cies of bacteria or microbial consortia (Chen etal. 2014)
via a biochar mediator may aid in a more energy ecient
digestion and thus higher feed eciency and eventually
result in lower GHG emissions (Leng etal. 2012a, 2012b).
When animals receive charcoal feed additives com-
bined with Lactobacilli spraying (i.e. microbial milieu
management in the stable), it is interesting to note that
antibiotic use may be reduced and in some cases down
to zero. Farmers in Germany who use this practice fre-
quently report reduced veterinarian costs (Kammann,
pers. comm.) that “pay” for the use of biochar and Lacto-
bacilli solution. Reduced antibiotics may also reduce CH4
emissions from ruminant husbandry. Recently, Hammer
etal. (2016) showed that application of broad-spectrum
antibiotics enhanced CH4 emissions from cattle manure,
and altered the gut microora from dung beetles feeding
on the manure from cows treated with broad-spectrum
antibiotics. As Choi etal. (2009) and Islam etal. (2014)
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 123
showed that feeding 0.3 to 1% biochar could replace anti-
biotic treatment in chicken and ducks, respectively, feed-
ing biochar plus administering Lactobacilli could have
an indirect eect on GHG emissions when it is able to
replace regular antibiotic “feeding”. Furthermore, Joseph
etal. (2015b) demonstrated that feeding biochar to graz-
ing cows had positive secondary eects on soil fertility
and fertilizer eciency, reducing mineral N-fertilizing re-
quirements which could be construed as another indirect
biochar GHG mitigation eect. us, enabling farmers to
stop or reduce administering antibiotics by using biochar
and Lactobacilli may be promising, not only for animal
health, but also for reducing methane emissions from ani-
mal husbandry operations (Hammer etal. 2016).
3.2. Calculating CO2-equivalent balances of biochar
use in animal husbandry: rst considerations
Besides the possible eects of biochar feeding on ruminant
CH4 emissions, it is not unlikely that microbial decom-
position of manure containing digested biochar produces
less ammonia, less CH4 and thus retains more nitrogen.
is has been observed between manure composted with
and without biochar (section 3.3; e.g., Sonoki etal. 2013;
Steiner etal. 2010; Troy etal. 2013; Wang etal. 2013b) and
may also occur when biochar is used as bedding or ma-
nure treatment additive. Ghezzehei etal. (2014) estimated
that using biochar for liquid manure treatment could save
57,000 t NH4 and 4,600 t P2O5 fertilizer per year in Califor-
nia alone, though this estimate is only based on laboratory
adsorption tests and not on eld trials. However, it cannot
be excluded that digested biochar will not have the same
eect on microbial decomposition, GHG emissions and
plant nutrient retention as when production-fresh biochar
is applied to the bedding or manure pit. To our knowl-
edge, there are no published data on GHG-emissions in
animal housing and of manure pits aer feeding animals
with biochar.
Easier to calculate is the C-sequestration potential of
biochar that is rst fed to livestock and eventually applied
to soil with the manure. Assuming an average C-content
of fed biochar of 80%, as required by the EBC feed certi-
cate (EBC 2012) and produced at recommended tempera-
tures above 500°C resulting in H/Corg ratios below 0.4, at
least 56% of the dry weight of the fed and manure-applied
biochar will persist as stable carbon in soil for at least
100years (Lehmann etal. 2015). If the global livestock
would, just theoretically and for the sake of a “back-of-the
envelope” assessment to explore magnitudes, receive 1%
of their feed in form of such a biochar, about 400 Mio.t
of CO2eq or 1.2% of the global CO2 emissions could be
compensated (Table 1).
While the feeding of “vegetal carbon” (biochar) is
permitted in the EU (EU 2011), it certainly cannot be
recommended yet as in a generalized biochar-livestock
feeding regime, since feed-grade certication of biochar
is currently not established in most countries and since
long-term eects are not suciently investigated. How-
ever, the potential for improving animal health and nu-
trient eciency, for reducing enteric methane emissions
as well as GHG emissions from manure management,
and for sequestering carbon while improving soil fertility
improvements, calls for increasing the scientic eort to
investigate, measure and optimize the GHG reduction po-
tential of biochar use in animal farming systems. e use
of biochar in animal husbandry is one of the largest unex-
plored research topics within the biochar research realm.
Although many unknowns and open questions exist, bio-
char use in animal operations appears promising from a
GHG reduction standpoint and thus future research could
focus eorts towards this area.
Table 1. Carbon sequestration potential of biochar fed to livestock (globally) with subsequent manure application to soil. Numbers
of total livestock follow FAO statistics obtained for 2014 (FAO 2016). An intake dosage of 1% of the daily feed weight was assumed.
e C sequestration potential was calculated with the assumption of 80% C in biochar, and 70% C persistence over 100 years
(Lehmann etal. 2015; Camps-Arbestain etal. 2015)
Animal Global number of
individual animals Daily intake dosage*
(g bc animal–1 d–1)Annual intake dosage
(kg bc animal–1 yr–1)Total biochar
(Mio. t yr–1)Total C seq.
(Mio. t yr–1)Total C O2eq
(Mio. t yr–1)
Cattle 1,482,144,415 120 43.8 64.9 36.4 133.3
Bualoes 195,098,316 120 43.8 8.5 4.8 17.5
Sheep 1,209,908,142 50 18.25 22.1 12.4 45.3
Goats 1,006,785,725 50 18.25 18.4 10.3 37.7
Pigs 986,648,755 80 29.2 28.8 16.1 59.2
Horses 58,913,957 120 43.8 2.6 1.4 5.3
Chickens 21,321,834,000 6 2.19 46.7 26.1 95.9
Turkeys 461,453,000 6 2.19 1.0 0.6 2.1
Total 193.0 108.1 396.3
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
124
3.3. Biochar as composting additive
Composting is the aerobic biotic oxidation of organic res-
idue, manure and waste for producing organic fertilizer
and occasionally waste management. Labile organic car-
bon is transformed into humic like substances and CO2,
with N2O and CH4 as non-desired by-products. Emission
rates of N2O and CH4 depend on compost management,
and increase with increasing degrees of anoxia during
composting. During a perfect aerobic quality compost-
ing procedure, N2O and CH4 emissions are usually low
(Amlinger etal. 2003, 2008; Bernal etal. 2009). However,
aerobic conditions cannot always be perfectly maintained,
particularly when manure-rich waste is composted; here
larger N2O and CH4 emissions are common (Li etal. 2016;
Wang etal. 2013b). us, it is desirable to develop strate-
gies to reduce GHG emissions during composting, par-
ticularly of nutrient-rich wet materials.
With regard to biochar, “co-composting” refers to the
addition of biochar to the initial composting feedstock.
During co-composting, biochar can sorb compost liquids
rich in nutrients, particularly nitrate (Prost etal. 2013;
Kammann etal. 2015). Furthermore, some studies report
an accelerated thermophilic phase with higher compost
temperatures (Kammann etal. 2016; Vandecasteele etal.
2016). CO2 emissions are an obligate result of compost-
ing due to the decomposition of labile organic matter. is
loss during composting ranges from ~40% (Vandecasteele
etal. 2016) to ~80% (Sánchez-García etal. 2015) depend-
ing on the compost feedstock and composting conditions.
Some studies show no eect of biochar on CO2 emissions
or increases of emission rates (Steiner etal. 2011; López-
Cano etal. 2016). However, Malinska etal. (2014) and
Vandecasteele etal. (2016) reported a reduction of CO2
emissions. Vandecasteele etal. (2016) argue that pristine
biochar used in their experiments might have physically
adsorbed CO2 (Creamer etal. 2014; Fornes etal. 2015)
and thus reduced CO2 emissions, although actual CO2
production probably increased (e.g., increase of decom-
position, higher temperatures). However, a faster rate of
C loss does not necessarily mean that, overall, biochar will
reduce the long-term storage of non-pyrolyzed feedstock
in soils; it just means that a process that happens other-
wise over longer periods is accelerated.
CH4 and N2O emissions from compost are non-de-
sired side eects and can be reduced by adequate man-
agement of the composting process with regard to oxygen
supply, including windrows not exceeding certain sizes,
optimized water content and forced or mechanical aera-
tion (Fukumoto etal. 2003; Amlinger etal. 2008). Howev-
er, these management strategies can be costly. Recent stud-
ies indicate that biochar addition during the composting
process can indeed reduce emissions of both CH4 and N2O
probably due to enhanced access of oxygen mediated by
biochar. Methane emissions are oen drastically reduced
by biochar addition, with reported reduction rates of 55%
for chicken manure compost with biochar added at 20%
w/w (Jia etal. 2016), >70% for organic waste compost with
biochar added at 10% rate (Sonoki etal. 2011), and >80%
for municipal solid waste compost with biochar added at
10% w/w (Vandecasteele etal. 2016). However, at low bio-
char additions (e.g. 3%), Sánchez-García etal. (2015) ob-
served no signicant eect on CH4 emissions during the
composting process, suggesting that a certain biochar rate
during composting is necessary to reach desired reduc-
tions in CH4 emissions.
Gaseous N losses also oen decrease when biochar is
used as an additive during the composting process since
the pH of composts does usually stay below or around
Fig. 2. Mean GHG ux rates of compost (comp), biochar-compost (BC-comp) and compost with later addition of fresh biochar
(comp + BC), n = 5 + standard deviation; GHG ux measurements with 400 g substrate per 1-L Weck® jar as described in
Kammann etal. (2012); Material properties and composting procedure described in Schmidt etal. (2014) and Kammann etal.
(2015). Substrates were adjusted to 60% of their respective water-holding capacity one week before measurement. Letters indicate
signicant dierences by one-way ANOVA (n = 5, p < 0.05)
CO2 efux (mg CO2 kg–1
h–1)
N2O emission (ng N2O kg–1
h–1)
CH4 ux (mg CH4 kg–1
h–1)
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 125
pH 7.5. However, care has to be taken to prevent a strong
pH increase due to (large amounts of) biochar addition
in composting, with animal bedding, manure treatment
or elsewhere. If values above a pH of 8 are reached, NH3
losses may result which was systematically investigated
by Chen etal. (2013) with biochar additions up to 20%
by weight to bauxite processing sands in a pH-adjusted
set-up of pH values ranging from 5 to 9. e authors re-
ported that at low and high pH values, NH3 losses were
increased by biochar additions (at low pH when the ad-
dition of biochar was suciently large to provoke a pH
increase), while at a high pH NH3 losses were high any-
way. However at a more neutral pH, the NH4+ adsorption
capacity of biochar dominated which decreased N losses
(Chen etal. 2013). However, the rst available results are
contradictory: While Schimmelpfennig etal. (2014) found
a reduction of NH3 emissions when slurry was added to a
loam soil (pH 6.0) amended with biochar when compared
to the same soil amended with (less alkaline) straw, Subedi
etal. (2015) reported an increase in the NH3 emissions
from slurry when both, an alkaline biochar and an acidic
hydrochar were added to the slurry. It is possible that the
overall “evaporation surface” which may increase by add-
ing a bulky material to soil or slurry may also play a role
for increasing NH3 losses. Nevertheless, the biochar-dose-
to-pH-increase relationship should always be taken into
account.
Studies conducted with relatively low dosages of bio-
char (e.g. 3–4%) showed either a reduction in N2O emission
(Wang etal. 2013a; Li etal. 2016) or no eect (Sánchez-Gar-
cía etal. 2015; López-Cano etal. 2016). When reductions in
N2O emissions were observed, they were pronounced but
happened only during a portion of the composting process.
For example, Li etal. (2016) reported that 3% biochar ad-
dition during composting reduced N2O emission by 54%,
which was entirely attributable to N2O-peak suppression for
only one of the eight measurement dates. is eect was
further attributed to a marked reduction in the abundance
of the nirK gene of denitrifying bacteria when biochar was
co-composted (Li etal. 2016).
Ammonia (NH3) is not a greenhouse gas, but a rele-
vant atmospheric precursor of N2O (shown in section1.2),
and its volatilization during composting is a relevant path-
way for N loss. Biochar amendment was shown to reduce
NH3 volatilization particularly in N-rich materials such as
sludge or manures, probably due to NH4+ sorption (Chen
etal. 2010; Hua etal. 2009; Steiner etal. 2010; Malins-
ka etal. 2014). Increased N content in the compost, in
the form of NH4+, is a desired property for compost use
as an organic fertilizer. When applied to soil, the larger
quantity of N and labile C retained in the composted bio-
char particles (or in the biochar-compost product) may
theoretically lead to higher N2O emissions as compared to
pure, non-composted biochar (Prost etal. 2013; Borchard
etal. 2014b). is was, however, not observed in a plant-
ing study using co-composted (nitrate-enriched) biochar
as soil amendment (Kammann etal. 2015), or when the
compost itself was tested (Fig. 2).
At the moment, results are just snapshots of rst
composting experiments with biochar, and studies in-
clude a wide range of experiments from 150 g mixtures in
jars (Jia etal. 2016), 45 L composting reactors (Malinska
etal. 2014), 1 m³ gardening compost boxes (Prost etal.
2013) to 60×3×2 m windrows with forced aeration and
automated mechanical turning (Vandecasteele etal. 2016)
or daily machine turning (Schmidt etal. 2014; Kammann
et al. 2015) at varying time scales (few weeks to sev-
eral months). Generally, the value of composting studies
would be increased if the resulting compost quality is sub-
sequently evaluated by plant germination and growth tests
(e.g. Hua etal. 2012, soil faunal tests, e.g. Fig. 3) and eld
application trials.
Biochar is a promising tool to optimize composting,
improve compost quality and charge biochar with plant-
available nutrients and reduce non-CO2 GHG emissions
during composting. However, the longer-term eects of
biochar-composts in soils are largely unexplored. More
systematic studies with dierent combinations of N-rich
and N-poor feedstock and dierent well-characterized
biochars under comparable, praxis-relevant conditions are
needed, and subsequently product quality and its eects
on soil GHG emissions aer soil amendment should be
investigated.
Fig. 3. Results of earthworm avoidance tests (method: ISO
17512-1:2008; Busch etal. 2012) with the compost (comp),
biochar-compost (bc-comp) and compost with later addition of
fresh biochar (comp+bc), material properties and composting
described in Schmidt etal. (2014) and Kammann etal. (2015).
“Comp vs. comp” is the control and did not result in an eect
(as needed); boric acid (BA) was the “positive control” where
avoidance behaviour conrmed that the test was valid. Bars
give means of n = 5 repetitions per treatment (50 worms),
shown as preference or avoidance of the respective substrate
(Fishers exact test, (*) p < 0.1, * p < 0.05, ** p < 0.01, n.s. not
signicant)
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
126
4. Novel approaches of using biochar for GHG
emission reductions in agriculture
GHG emission reductions with biochar use may not nec-
essarily be direct; rather, reductions may result from al-
ternative waste stream management involving pyrolysis.
Another option is to use biochar as a fertilizer carrier to
match plant demands more closely, enabling the reduced
use of common mineral fertilizers and hence associated
N2O emissions (see 3.1, Qian etal. 2014). is section ad-
dresses novel biochar concepts for reducing the overall
GHG intensity of agricultural production, including those
from unwanted NO3- and NH3 losses and deposition, caus-
ing N2O emissions elsewhere (Turner etal. 2015).
4.1. Biochar as carrier for (organic) underfoot
fertilizers
e use of large biochar amounts (e.g. 10–20 tons) being
ploughed into soils does usually not increase crop yields
suciently to justify the costs (Jeery etal. 2015; Bieder-
man, Harpole 2013; Ruysschaert etal. 2016). Here, the
economy of biochar use may be better for special crops
as long as yield increases without negative eects on crop
quality can be realized, as observed by Baronti etal. (2014)
and Genesio etal. (2015) for grapevine cultures. However,
grapevines are low-N cultures with low N2O emissions
(Marras etal. 2015) compared to higher N-fertilizer de-
manding vegetable crops such as radish, carrot, spinach
or potato. ese receive much higher N fertilizer amounts,
oen with several cropping cycles per year, resulting in
high N2O emissions (Ruser etal. 1998; Min etal. 2016). In
highly fertilized vegetable crops, biochar amendment may
play a role in signicantly reducing the greenhouse gas in-
tensity per unit of crop, likely by reducing N2O emissions
and partly by yield increases (Jia etal. 2012; Li etal. 2015).
However, use of biochar in these situations, as with others,
comes with a cost.
In order to reduce costs, it is desirable to maximize
the eect of biochar per unit applied, suggesting that op-
timum application rates might be fairly low especially if
the product can be concentrated around the root zone.
Indeed, root zone application of only 2–4 t ha–1, together
with fertilizer in conservation farming systems, has been
reported to improve yields in acidic sandy soils (Cornelis-
sen etal. 2013). In addition, using biochar as an ingredi-
ent of, or carrier matrix for, mineral or organic fertilizer
blends (“fertichars”) has recently been investigated as a
promising strategy to reduce the need for large biochar
amounts while improving crop yields and/or reduce N
use (Joseph etal. 2013). Supporting this contention, Qian
etal. (2014) showed that biochar organo-mineral fertil-
izer blends reduced the GHG-intensity of rice crop pro-
duction even at reduced N fertilization rates and at very
low amounts of biochar (<1 t ha–1).
In practice, the on-farm availability of clean, inex-
pensive, and amounts required will decide whether bio-
char will be used, particularly in rural areas in developing
countries (Cornelissen etal. 2013). In Nepal, a self-made
organic “fertichar” was used as underfoot fertilizer in 8
dierent farmer sites (fertile loamy soils) and compared
to the same nutrient additions without biochar. Here,
pumpkin yields were consistently increased by 400% with
the urine-loaded biochar applied as underfoot fertilizer,
and multiple eld trials on dierent soils, crops and bio-
char consistently showed a growth-promoting eect of
the organic biochar-root zone fertilizer (Schmidt etal.
2015). It has not yet been tested if these biochar-fertil-
izer blends will reduce GHG emissions compared to an
equal or greater amount of standard fertilizer. However,
we argue that GHG emission reductions (namely those
of N2O) per unit of crop yield may be achieved for the
following reasons: (1) e fertichar blends mean a com-
paratively high amount of biochar concentrated together
with the nutrients, i.e. within the “biochar concentration
range” found to reduce N2O emissions in soils consider-
ably in meta-studies (Cayuela etal. 2014); (2) By stimu-
lating plant growth, N uptake increases, which reduces
the availability of N for nitrication / denitrication and
hence N2O formation; (3) When applied underfoot, the
total land area that receives N fertilizer and is able to pro-
duce N2O emissions is smaller; (4) By using root-zone fer-
tichars, the overall amount of N fertilizer that needs to be
applied, per unit of crop produced, can likely be reduced
(Joseph etal. 2013; Qian etal. 2014). is may automati-
cally reduce the GHG emissions (as a percentage of the
applied fertilizer); and (5) Biochar will reduce the soil bulk
density (e.g. Obia etal. 2016) and increase soil air capac-
ity, which has been shown to reduce N2O production due
to improved oxygen supply in upland soils. However, it is
simply unknown if this type of application will reduce the
GHG intensity of crop production and if this will occur on
dierent soils and climatic zones alike. Further research
is needed on fertilizer-biochars, either as broadcast gran-
ules (Qian etal. 2014) or as underfoot fertilizers (Schmidt
etal. 2015), since these techniques may oer a win-win
in terms of reducing GHG emissions concomitantly with
improved yields.
4.2. Pyrolysis as alternative waste stream management
technique
Over the past twenty years, localization of conned ani-
mal feeding operations (CAFOs) in the USA has brought
about a massive production of animal manures (Gollehon
etal. 2001). Traditional management practices have ap-
plied manure to crops as a fertilizer, yet long-term manure
applications have caused nutrient imbalances in soils far
in excess of what crops can assimilate (Barker, Zublena
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 127
1995; Kellogg etal. 2000). e situation is so severe that
CAFO producers must have nutrient management plans
(e.g., MDE 2016; ISDA 2016) or manure application can
be restricted if soils contain excess N and/or P. A clear
need exists for alternate animal waste management and
recycling methods.
ermal processing of animal manures using gasi-
cation and pyrolysis technology is gaining considerable
interest as an alternate treatment option because of the
energy quantity generated (Cantrell etal. 2007, 2008).
Manure gasication is a popular conversion process, yet
the higher temperatures (>900 °C) required for conver-
sion into gases, along with impurities in the feedstocks
(e.g. salts, silicates, etc.), oentimes limits the conversion
eciency (Lv etal. 2010) and can corrode downstream
metal surfaces (Demirbas 2005). us, pyrolysis is more
oen regarded as the eective method of processing bio-
mass to produce a combination of non-condensable gases,
bio-oil, and biochar (Antal, Grønli 2003). Manures can be
pyrolyzed at various temperatures (e.g. 300 to 750°C) to
create biochars. Aerwards, the energy content (as MJ/kg)
contained within biochar identies the quantity of energy
generated per equivalent dry weight and serves as a con-
venient energy index relative to coal (Table 2). Globally,
animal waste pyrolysis is performed to create a thermal
energy source, to generate heat for animal connement
stables, for the production of bio-oil, and to produce bio-
char, a nutrient-enriched end-product to be used as a soil
amendment (Laird etal. 2009; Lee etal. 2013) or fertilizer
replacement.
Table 2. Net thermal energy in various manures, and their
biochars pyrolyzed at various temperatures, as compared to
hard/so coals, gasoline and methane. na = not available
Feedstock ermal
tempe ra-
ture (°C)
Energy
content
(MJ/kg) Source
Poultry litter 0 15 Novak etal. (2013)
700 14.2 Novak etal. (2013)
Dairy manure
0 17.6 Cantrell etal.
(2012)
350–700 19.0–20.9 Cantrell etal.
(2012)
Swine Solids
0 19.4 Cantrell etal.
(2012)
350–700 15.1–21.1 Cantrell etal.
(2012)
Human Feces 300–750 13.8–25.6 Ward etal. (2014)
Hard/so coal na 29.3–33.5 Euronuclear (2016)
Gasoline na 43–47 Energynumbers
(2005)
Methane na 55.5 Energynumbers
(2005)
Following manure pyrolysis, it has been shown by
Gaskin etal. (2008) that nutrient availability may be de-
creased in the biochar, which may make manure-based
biochar use attractive in terms of land areas where nu-
trient management plans are necessary; biochars may
be able to supply a more balanced quantity of essential
plant nutrients without degradation in environmental
quality due to nutrient over-application. Furthermore,
an additional benet similar to previously mentioned
underfoot fertilizer-biochars, manure-based biochar
may significantly reduce overall farm-management
based GHG emissions simply by reducing mineral fer-
tilizer use (Cayuela etal. 2014; Nguyen etal. 2014).
e production of animal manure biochar via py-
rolysis, and the subsequent partial or complete replace-
ment of standard mineral NPK fertilization by manure-
biochar, oers the following pathways to N2O emissions
reduction: (1) Reduced N use which reduces the overall
environmental burden by limiting N2O formation both
from direct manure application as well as emissions
originating from o-site N pollution (e.g. NH3 emis-
sions, N export via overland ow, N leaching to ground-
water, Turner etal. (2015); (2) e use of manure-based
biochar may reduce N2O emissions compared to using
the same amount of N in the mineral or manure form.
Cayuela etal. (2014) examined 107 articles related to
manure-based biochar land application, showing a –46
to +39% change in N2O emissions, with average N2O
emission changes close to 0%. us, changes or reduc-
tions in N2O emissions is likely process dependent,
something that was not examined by Cayuela et al.
(2014). However, Subedi etal. (2016) added poultry lit-
ter or swine manure biochar to two dierent soils. e
authors showed that poultry litter or swine manure bio-
chars pyrolyzed at 400 °C produced the same N2O emis-
sion factor (i.e., N2O emitted as a percentage of the total
N supplied) as control soils. When pyrolyzed at 600 °C,
the N2O emission factor decreased for both biochars as
compared to controls. Higher temperatures during pro-
duction will result in manure-based biochars containing
lesser quantities of easily degradable C compounds (e.g.,
volatile compounds) that are available for denitriers,
leading to less likelihood of anaerobic soil conditions
(e.g., Liu etal. 2014) and thus lower N2O emissions. Ob-
viously, in order to reduce N2O emissions when apply-
ing manure-based biochars, easily degradable C sources
needs to be at a minimum; and (3) e use of pyrolysis
for heat generation in animal housing, and/or the use of
manure biochar for energy production, can be imple-
mented to reduce GHG emissions when it replaces the
use of fossil fuels for the same purpose (see energy con-
tent comparison in Table2).
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
128
Conclusions: promising options for GHG emission
reduction and future research needs
After a decade of intense biochar research, it has be-
come clear that biochar soil amendments are able to
reduce N2O emissions (i.e. emission peaks). Biochar
can also reduce CH4 emissions, particularly in flooded
soils, and when N fertilization rates are not too high.
However, great uncertainty still exists with respect to
biochar use and its GHG reducing effect as associated
with different biochars and soil types/conditions. This
is due to the lack of understanding of mechanistic bio-
char effects. Good “candidate” mechanisms that might
explain N2O emission reductions are pH increases (lim-
ing effect) and changes in microbial community com-
position, particularly changes in the denitrifier gene
expression and abundance, and N (mostly nitrate) cap-
ture in biochar particles. It is likely that these mecha-
nisms work in concert under field conditions. Good
“candidate” mechanisms that might explain CH4 emis-
sion reductions are the stimulation of methanotrophic
low-affinity communities at the anoxic/oxic interface in
reduced environments as well as the electron shuttling
and redox activity of biochars (e.g. rice paddies and ru-
minant guts).
Biochar use in animal husbandry is economically
promising and the dominant route of biochar use in
central Europe; however, research on GHG emission
reductions is largely lacking. Studies dealing with the
medical use of charcoal/biochar in animal feeding near-
ly never characterize char properties. Biochar shows a
strong potential for reducing GHG and NH3 emissions
in the composting of wet nutrient-rich materials, par-
ticularly when composts are not so frequently turned
(aerated, i.e. “lazy composting”). Yet, more detailed
studies on the dynamics of this effect along the com-
posting process are needed, as well as a cost-benefit
evaluation for potential implementation.
One new promising option of using biochar for
improving the GHG-intensity (yield-to-GHG emission
ratio), via both increasing yields plus reduced GHG
emissions, may be the use of designed (organic) “Fer-
tiChars” (biochar as fertilizer carrier) administered as
concentrated root zone fertilizers. Here the biochar-
to-N ratio may certainly be in the range where biochar
should have an effect as well as effectively and envi-
ronmentally deliver optimal nutrient concentrations to
plants. However, to date, GHG flux measurements of
this implementation pathway are lacking and strongly
call for future research. We conclude that the use of
biochar in agriculture provides a unique opportunity to
reduce the non-CO2 greenhouse gas “cost” per unit of
yield produced, yet future research is required to maxi-
mize its benefits.
Acknowledgements
We thank the participants of the ANS & EU-COST Bio-
char Symposium 2015 in Geisenheim for their active and
lively discussions in section 6 “Biochar and GHG emis-
sions”. C. Kammann and H.-P. Schmidt thank Matthias
Schröder for his work during the composting trials in Ar-
baz, Switzerland and later in the lab at Gießen University.
Contribution
CK developed the structure, wrote sections, contributed to
sections and coordinated writing. JI and NH helped stream-
lining and nalizing the manuscript in addition to section
contributions. All other authors contributed equally by re-
viewing the literature within their particular eld of exper-
tise and writing sections of the manuscript. (erefore, all
authors besides authors 1–3 are listed in alphabetical order.)
Funding
e COST Action TD1107, “Biochar for sustainable en-
vironmental management”, provided nancial support for
the EU-COST biochar symposium in 2015; the German
BLE and FACCE-JPI funded the German participants
of the “DesignerChar4Food” (D4F) project (CK: Project
No.2814ERA01A; NW-M: Project No. 2814ERA02A),
the Spanish colleagues (JME and TFM) were funded by
FACCE-CSA nº 276610/MIT04-DESIGN-UPVASC and
IT-932-16, and US colleagues (JN, JI and KS) were funded
by e USDA-National Institute of Food and Agricul-
ture (Project # 2014-35615-21971), USDA-ARS CHAR-
net and GRACENet programs – D4F greatly stimulated
discussions. We also gratefully acknowledge the follow-
ing individual grants that enabled authors to contribute
to this work: Claudia Kammann: German Science Foun-
dation (DFG) grant [KA3442/1-1]; ML Cayuela thanks
Fundación Séneca (Grant number 19281/PI/14); Nils
Borchard was placed as integrated expert into the Center
for International Forestry Research (CIFOR) by the Cen-
tre for International Migration and Development (CIM).
CIM is a joint operation of the Deutsche Gesellscha für
Internationale Zusammenarbeit (GIZ) GmbH and the In-
ternational Placement Services (ZAV) of the German Fed-
eral Employment Agency (BA).
Disclosure statement
None of the authors do have any competing nancial, pro-
fessional, or personal interests from other parties.
References
Alburquerque, J. A.; Sánchez-Monedero, M. A.; Roig, A.;
Cayuela, M. L. 2015. High concentrations of polycyclic
aromatic hydrocarbons (naphthalene, phenanthrene and
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 129
pyrene) failed to explain biochar’s capacity to reduce soil nit-
rous oxide emissions, Environmental Pollution 196: 72–77.
https://doi.org/10.1016/j.envpol.2014.09.014
Ameloot, N.; Maenhout, P.; De Neve, S.; Sleutel, S. 2016. Biochar-
induced N2O emission reductions aer eld incorporation in
a loam soil, Geoderma 267: 10–16.
https://doi.org/10.1016/j.geoderma.2015.12.016
Amlinger, F.; Götz, B.; Dreher, P.; Geszti, J.; Weissteiner, C. 2003.
Nitrogen in biowaste and yard waste compost: dynamics of
mobilisation and availability – a review, European Journal of
Soil Biology 39(3): 107–116.
https://doi.org/10.1016/S1164-5563(03)00026-8
Amlinger, F.; Peyr, S.; Cuhls, C. 2008. Green house gas emissions
from composting and mechanical biological treatment, Waste
Management & Research 26(1): 47–60.
https://doi.org/10.1177/0734242X07088432
Antal, M. J.; Grønli, M. 2003. e art, science, and technology of
charcoal production, Industrial & Engineering Chemistry Re-
search 42(8): 1619–1640. https://doi.org/10.1021/ie0207919
Augustenborg, C. A.; Hepp, S.; Kammann, C.; Hagan, D.;
Schmidt, O.; Müller, C. 2012. Biochar and earthworm eects
on soil nitrous oxide and carbon dioxide emissions, Journal
of Environmental Quality 41(4): 1203–1209.
https://doi.org/10.2134/jeq2011.0119
Ball, P.; Mackenzie, M.; DeLuca, T.; Montana, W. 2010. Wildre
and charcoal enhance nitrication and ammonium-oxidizing
bacterial abundance in dry montane forest soils, Journal of
Environmental Quality 39(4): 1243–1253.
https://doi.org/10.2134/jeq2009.0082
Bamminger, C.; Marschner, B.; Juschke, E. 2014. An incubation
study on the stability and biological eects of pyrogenic and
hydrothermal biochar in two soils, European Journal of Soil
Science 65(1): 72–82. https://doi.org/10.1111/ejss.12074
Barker, J. C.; Zublena, J. P. 1995. Livestock manure nutrient as-
sessment in North Carolina. Final Report. Raleigh, NC: North
Carolina Agricultural Extension Service, North Carolina
State University [online], [cited 28 December 2016]. Avail-
able from the Internet: https://pdfs.semanticscholar.org/3bab
/336a20fc9d6710092faac2e3cbc8189495cc.pdf
Baronti, S.; Vaccari, F. P.; Miglietta, F.; Calzolari, C.; Lugato, E.;
Orlandini, S.; Pini, R.; Zulian, C.; Genesio, L. 2014. Impact of
biochar application on plant water relations in Vitis vinifera
(L.), European Journal of Agronomy 53: 38–44.
https://doi.org/10.1016/j.eja.2013.11.003
Bateman, E. J.; Baggs, E. M. 2005. Contributions of nitrication
and denitrication to N2O emissions from soils at dierent
water-lled pore space, Biology and Fertility of Soils 41(6):
379–388. https://doi.org/10.1007/s00374-005-0858-3
Bernal, M. P.; Alburquerque, J. A.; Moral, R. 2009. Composting
of animal manures and chemical criteria for compost matu-
rity assessment. A review, Bioresource Technology 100(22):
5444–5453. https://doi.org/10.1016/j.biortech.2008.11.027
Biederman, L. A.; Harpole, W. S. 2013. Biochar and its eects on
plant productivity and nutrient cycling: a meta‐analysis, GCB
Bioenergy 5(2): 202–214. https://doi.org/10.1111/gcbb.12037
Borchard, N.; Ladd, B.; Eschemann, S.; Hegenberg, D.; Mose-
ler,B.M.; Amelung, W. 2014a. Black carbon and soil proper-
ties at historical charcoal production sites in Germany, Geo-
derma 232: 236–242.
https://doi.org/10.1016/j.geoderma.2014.05.007
Borchard, N.; Spokas, K.; Prost, K.; Siemens, J. 2014b. Green-
house gas production in mixtures of soil with composted
and noncomposted biochars ss governed by char-associated
organic compounds, Journal of Environmental Quality 43(3):
971–979. https://doi.org/10.2134/jeq2013.07.0290
Brasseur, G. P.; Chateld, R. B. 1991. e fate of biogenic trace
gases in the atmosphere, in T. Sharkey, E. Holland. (Eds.).
Trace gas emissions by plants. Cambridge MA: Academic
Press. https://doi.org/10.1016/B978-0-12-639010-0.50006-6
Busch, D.; Kammann, C.; Grünhage, L.; Müller, C. 2012. Simple
biotoxicity tests for evaluation of carbonaceous soil additives:
establishment and reproducibility of four test procedures,
Journal of Environmental Quality 41(4): 1023–1032.
https://doi.org/10.2134/jeq2011.0122
Butterbach-Bahl, K.; Baggs, E. M.; Dannenmann, M.; Kiese, R.;
Zechmeister-Boltenstern, S. 2013. Nitrous oxide emissions
from soils: how well do we understand the processes and
their controls?, Philosophical Transactions of the Royal So-
cietyB: Biological Sciences 368(1621): 20130122.
https://doi.org/10.1098/rstb.2013.0122
Camps-Arbestain, M.; Amonette, J. E.; Singh, B.; Wang, T.;
Schmidt, H. P. 2015. A biochar classication system and as-
sociated test methods, in J. Lehmann, J. Stephen (Eds.) Bio-
char for Environmental Management: Science, Technology and
Implementation. 2nd ed. London: Routledge.
Cantrell, K.; Ro, K.; Mahajan, D.; Anjom, M.; Hunt, P. G. 2007.
Role of thermochemical conversion in livestock waste-
to-energy treatments: obstacles and opportunities, Indus-
trial & Engineering Chemistry Research 46(26): 8918–8927.
https://doi.org/10.1021/ie0616895
Cantrell, K. B.; Ducey, T.; Ro, K. S.; Hunt, P. G. 2008. Livestock
waste-to-bioenergy generation opportunities, Bioresource
Techn ol ogy 99(17): 7941–7953.
https://doi.org/10.1016/j.biortech.2008.02.061
Cantrell, K. B.; Hunt, P. G.; Uchimiya, M.; Novak, J. M.; Ro, K. S.
2012. Impact of pyrolysis temperature and manure source on
physicochemical characteristics of biochar, Bioresource Tech-
nology 107: 419–428.
https://doi.org/10.1016/j.biortech.2011.11.084
Case, S. D. C.; Mcnamara, N. P.; Reay, D. S.; Whitaker, J. 2012.
e eect of biochar addition on N2O and CO2 emissions
from a sandy loam soil – e role of soil aeration, Soil Biol-
ogy & Biochemistry 51: 125–134.
https://doi.org/10.1016/j.soilbio.2012.03.017
Castaldi, S.; Riondino, M.; Baronti, S.; Esposito, F. R.; Marzaio-
li,R.; Rutigliano, F. A.; Vaccari, F. P.; Miglietta, F. 2011. Im-
pact of biochar application to a Mediterranean wheat crop
on soil microbial activity and greenhouse gas uxes, Chemo-
sphere 85(9): 1464–1471.
https://doi.org/10.1016/j.chemosphere.2011.08.031
Castro, M. S.; Melillo, J. M.; Steudler, P. A.; Chapman, J. W. 1994.
Soil moisture as a predictor of methane uptake by temper-
ate forest soils, Canadian Journal of Forest Research 24(9):
1805–1810. https://doi.org/10.1139/x94-233
Castro, M. S.; Steudler, P. A.; Melillo, J. M.; Aber, J. D.; Bow-
den,R.D. 1995. Factors controlling atmospheric methane
consumption by temperate forest soils, Global Biogeochemical
Cycles 9(1): 1–10. https://doi.org/10.1029/94GB02651
Cato, M. P. 1935. On agiculture. London.
Cayuela, M. L.; Sanchez-Monedero, M. A.; Roig, A.; Hanley, K.;
Enders, A.; Lehmann, J. 2013. Biochar and denitrication in
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
130
soils: when, how much and why does biochar reduce N2O
emissions?, Scientic Reports 3(1732).
Cayuela, M. L.; Van Zwieten, L.; Singh, B. P.; Jeery, S.; Roig,A.;
Sánchez-Monedero, M. A. 2014. Biochar’s role in mitigating
soil nitrous oxide emissions: a review and meta-analysis, Ag-
riculture, Ecosystems & Environment 191: 5–16.
https://doi.org/10.1016/j.agee.2013.10.009
Chen, S.; Rotaru, A.-E.; Shrestha, P. M.; Malvankar, N. S.; Liu, F.;
Fan, W.; Nevin, K. P.; Lovley, D. R. 2014. Promoting interspe-
cies electron transfer with biochar, Scientic Reports 4: 5019.
https://doi.org/10.1038/srep05019
Chen, C. R.; Phillips, I. R.; Condron, L. M.; Goloran, J.; Xu, Z. H.;
Chan, K. Y. 2013. Impacts of greenwaste biochar on ammo-
nia volatilisation from bauxite processing residue sand, Plant
and Soil 367(1–2): 301–312.
https://doi.org/10.1007/s11104-012-1468-0
Chen, Y.-X.; Huang, X.-D.; Han, Z.-Y.; Huang, X.; Hu, B.;
Shi, D.-Z.; Wu, W.-X. 2010. Eects of bamboo charcoal and
bamboo vinegar on nitrogen conservation and heavy met-
als immobility during pig manure composting, Chemosphere
78(9): 1177–1181.
https://doi.org/10.1016/j.chemosphere.2009.12.029
Choi, J.; Shinde, P.; Kwon, I.; Song, Y.; Chae, B. 2009. Eect of
wood vinegar on the performance, nutrient digestibility and
intestinal microora in weanling pigs, Asian-Australian Jour-
nal of Animal Science 22(2): 267–274.
https://doi.org/10.5713/ajas.2009.80355
Christensen, T. R.; Johansson, T.; Åkerman, H. J.; Mastepa-
nov,M.; Malmer, N.; Friborg, T.; Crill, P.; Svensson, B. H.
2004. Thawing sub-arctic permafrost: effects on vegeta-
tion and methane emissions, Geophysical Research Letters
31(L04501). https://doi.org/10.1029/2003gl018680
Clough, T. J.; Bertram, J. E.; Ray, J. L.; Condron, L. M.;
O’callaghan, M.; Sherlock, R. R.; Wells, N. S. 2010. Unweath-
ered wood biochar impact on nitrous oxide emissions from
a bovine-urine-amended pasture soil, Soil Science Society of
America Journal 74(3): 852–860.
https://doi.org/10.2136/sssaj2009.0185
Conrad, R. 1989. Control of methane production in terrestrial
ecosystems, in M. Andreae, D. Schimel (Eds.). Exchange of
trace gases between terrestrial ecosystems and the atmosphere.
New York: Wiley.
Conrad, R. 1999. Contribution of hydrogen to methane produc-
tion and control of hydrogen concentrations in methano-
genic soils and sediments, FEMS Microbiology Ecology 28(3):
193–202. https://doi.org/10.1111/j.1574-6941.1999.tb00575.x
Conrad, R. 2007a. Microbial ecology of methanogens and meth-
anotrophs, Advances in Agronomy 96: 1–63.
https://doi.org/10.1016/S0065-2113(07)96005-8
Conrad, R. 2007b. Soil microbial communities and global cli-
mate change-methanotrophic and methanogenic communi-
ties as paradigms, in J. Van Elsas, J. Jansson, J. Trevors. (Eds.).
Modern soil microbiology. 2nd ed. Boca Raton: CRC Press.
Cornelissen, G.; Martinsen, V.; Shitumbanuma, V.; Alling, V.;
Breedveld, G. D.; Rutherford, D. W.; Sparrevik, M.; Hale,S.E.;
Obia, A.; Mulder, J. 2013. Biochar eect on maize yield and
soil characteristics in ve conservation farming sites in Zam-
bia, Agronomy 3(2): 256–274.
https://doi.org/10.3390/agronomy3020256
Creamer, A. E.; Gao, B.; Zhang, M. 2014. Carbon dioxide cap-
ture using biochar produced from sugarcane bagasse and
hickory wood, Chemical Engineering Journal 249: 174–179.
https://doi.org/10.1016/j.cej.2014.03.105
Dalal, R.; Allen, D.; Livesley, S.; Richards, G. 2008. Magnitude
and biophysical regulators of methane emission and con-
sumption in the Australian agricultural, forest, and sub-
merged landscapes: a review, Plant and Soil 309(1–2): 43–76.
https://doi.org/10.1007/s11104-007-9446-7
Day, G. E. 1906. Swine: a book for students and farmers. Ithaca,
NY: Cornell University Library.
https://doi.org/10.5962/bhl.title.56553
DeLuca, T. H.; Mackenzie, M. D.; Gundale, M. J.; Holben, W. E.
2006. Wildre-produced charcoal directly inuences nitro-
gen cycling in ponderosa pine forests, Soil Science Society of
America Journal 70(2): 448–453.
https://doi.org/10.2136/sssaj2005.0096
Demirbas, A. 2005. Potential applications of renewable energy
sources, biomass combustion problems in boiler power
systems and combustion related environmental issues,
Progress in Energy and Combustion Science 31(2): 171–192.
https://doi.org/10.1016/j.pecs.2005.02.002
Deng, Q.; Hui, D. F.; Wang, J. M.; Iwuozo, S.; Yu, C. L.; Jima, T.;
Smart, D.; Reddy, C.; Dennis, S. 2015. Corn yield and soil ni-
trous oxide emission under dierent fertilizer and soil man-
agement: a three-year eld experiment in Middle Tennessee,
PLoS ONE 10(4): 14.
https://doi.org/10.1371/journal.pone.0125406
Dicke, C.; Andert, J.; Ammon, C.; Kern, J.; Meyer-Aurich, A.;
Kaupenjohann, M. 2015. Eects of dierent biochars and
digestate on N2O fluxes under field conditions, Science
of the Total Environment 524–525: 310–318. https://doi.
org/10.1016/j.scitotenv.2015.04.005
Dijkstra, J.; Oenema, O.; Bannink, A. 2011. Dietary strategies to
reducing N excretion from cattle: implications for methane
emissions, Current Opinion in Environmental Sustainability
3(5): 414–422. https://doi.org/10.1016/j.cosust.2011.07.008
Dlugokencky, E. J.; Steele, L. P.; Lang, P. M.; Masarie, K. A. 1994.
e growth rate and distribution of atmospheric methane,
Journal of Geophysical Research: Atmospheres 99(D8): 17021–
17043. https://doi.org/10.1029/94JD01245
Dong, D.; Feng, Q. B.; Mcgrouther, K.; Yang, M.; Wang, H.L.;
Wu, W. X. 2015. Eects of biochar amendment on rice
growth and nitrogen retention in a waterlogged paddy eld,
Journal of Soils and Sediments 15(1): 153–162.
https://doi.org/10.1007/s11368-014-0984-3
Duneld, P. F. 2007. 10 e soil methane sink, in D. S. Reay,
C.N.Hewitt, K. A. Smith, J. Grace (Eds.). Greenhouse gas
sinks. Wallingford and Cambridge MA: CABI.
https://doi.org/10.1079/9781845931896.0152
EBC. 2012. European Biochar Foundation – European Biochar
Certicate – Guidelines for a Sustainable Production of Bio-
char, Version 6.1 of June 19, 2015. European Biochar Founda-
tion (EBC), Arbaz, Switzerland.
Energynumbers. 2005. Energy in natural processes and human
consumption – Energy content of fuels [online], [cited 28 De-
cember 2016]. Available from Internet: http://www.ocean.
washington.edu/courses/envir215/energynumbers.pdf
EU. 2011. Commission Regulation (EU) No 575/2011 of 16 June
2011 on the Catalogue of feed materials, Ocial Journal of
the European Union L159, 54: 25–114.
Euronuclear. 2016. Fuel comparison – coal equivalent [online],
[cited 28 December 2016]. Available from Internet: http://
www.euronuclear.org/info/encyclopedia/coalequivalent.htm.
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 131
FAO. 2015. Statistical pocketbook – world food and agriculture. Food
and Agriculture Organization of the United Nations, Rome.
FAO. 2016. Live animals [online]. Food and Agriculture Or-
ganization of the United Nations [cited 28 December
2016]. Available from Internet: http://www.fao.org/faostat/
en/?#data/QA
Feng, Y.; Xu, Y.; Yu, Y.; Xie, Z.; Lin, X. 2012. Mechanisms
of biochar decreasing methane emission from Chinese
paddy soils, Soil Biology and Biochemistry 46: 80–88.
https://doi.org/10.1016/j.soilbio.2011.11.016
Fornes, F.; Belda, R. M.; Lidón, A. 2015. Analysis of two bio-
chars and one hydrochar from different feedstock: fo-
cus set on environmental, nutritional and horticultural
considerations, Journal of Cleaner Production 86: 40–48.
https://doi.org/10.1016/j.jclepro.2014.08.057
Fukumoto, Y.; Osada, T.; Hanajima, D.; Haga, K. 2003. Pat-
terns and quantities of NH3, N2O and CH4 emissions during
swine manure composting without forced aeration – eect
of compost pile scale, Bioresource Technology 89(2): 109–114.
https://doi.org/10.1016/S0960-8524(03)00060-9
Galloway, J. N.; Townsend, A. R.; Erisman, J. W.; Bekunda, M.;
Cai, Z.; Freney, J. R.; Martinelli, L. A.; Seitzinger, S. P.; Sut-
ton, M. A. 2008. Transformation of the nitrogen cycle: Recent
trends, questions, and potential solutions, Science 320(5878):
889–892. https://doi.org/10.1126/science.1136674
Gaskin, J.; Steiner, C.; Harris, K.; Das, K.; Bibens, B. 2008. Eect
of low-temperature pyrolysis conditions on biochar for agri-
cultural use, Transactions of the American Society of Agricul-
tural and Biological Engineers 51(6): 2061–2069.
Genesio, L.; Miglietta, F.; Baronti, S.; Vaccari, F. P. 2015. Bio-
char increases vineyard productivity without aecting grape
quality: Results from a four years eld experiment in Tus-
cany, Agriculture, Ecosystems & Environment 201: 20–25.
https://doi.org/10.1016/j.agee.2014.11.021
Ghezzehei, T.; Sarkhot, D.; Berhe, A. 2014. Biochar can be used
to recapture essential nutrients from dairy wastewater and
improve soil quality, Solid Earth Discussions 6: 1101–1125.
https://doi.org/10.5194/sed-6-1101-2014
Gollehon, N.; Caswell, M.; Ribaudo, M.; Kellogg, R.; Lander, C.;
Letson, D. 2001. Conned animal production and manure
nutrients [online]. Resource Economics Division, Economic
Research Service, U.S. Department of Agriculture. Agricul-
ture Information Bulletin No. 771 [cited 28 December 2016].
Available from the Internet: https://www.ers.usda.gov/web-
docs/publications/aib771/17786_aib771_1_.pdf.
Gulledge, J.; Doyle, A. P.; Schimel, J. P. 1997. Dierent NH4+-in-
hibition patterns of soil CH4 consumption: a result of distinct
CH4-oxidizer populations across sites?, Soil Biology and Bio-
chemistry 29(1): 13–21.
https://doi.org/10.1016/S0038-0717(96)00265-9
Hackstein, J.; Stumm, C. K. 1994. Methane production in ter-
restrial arthropods, Proceedings of the National Academy of
Sciences 91(12): 5441–5445.
https://doi.org/10.1073/pnas.91.12.5441
Hagemann, N.; Harter, J.; Kaldamukova, R.; Guzman-Busta-
mante, I.; Ruser, R.; Grae, S.; Kappler, A.; Behrens, S.
2016. Does soil aging aect the N2O mitigation potential
of biochar? A combined microcosm and eld study, GCB
Bioenergy 12390: 1–12.
Haider, G.; Steens, D.; Müller, C.; Kammann, C. I. 2016. Stan-
dard extraction methods may underestimate nitrate stocks
captured by eld-aged biochar, Journal of Environmental
Quality 45(4): 1196–1204.
https://doi.org/10.2134/jeq2015.10.0529
Hammer, T. J.; Fierer, N.; Hardwick, B.; Simojoki, A.; Slade, E.;
Taponen, J.; Viljanen, H.; Roslin, T. 2016. Treating cattle with
antibiotics aects greenhouse gas emissions, and microbiota
in dung and dung beetles, Proceedings of the Royal Society B:
Biological Sciences 283(20160150).
https://doi.org/10.1098/rspb.2016.0150
Hansen, H. H.; Storm, I. M. L. D.; Sell, A. M. 2012. Eect of
biochar on in vitro rumen methane production, Acta Ag-
riculturae Scandinavica, Section A – Animal Science 62(4):
305–309.
Hansen, J.; Sato, M. 2016. Regional climate change and na-
tional responsibilities, Environmental Research Letters 11(3):
034009. https://doi.org/10.1088/1748-9326/11/3/034009
Hardy, B.; Cornelis, J. T.; Houben, D.; Lambert, R.; Dufey, J. 2016.
e eect of pre‐industrial charcoal kilns on chemical proper-
ties of forest soil of Wallonia, Belgium, European Journal of Soil
Science 67(2): 206–216. https://doi.org/10.1111/ejss.12324
Hardy, B.; Cornelis, J. T.; Houben, D.; Leifeld, J.; Lambert, R.;
Dufey, J. E. 2017. Evaluation of the long-term eect of bio-
char on properties of temperate agricultural soil at pre-in-
dustrial charcoal kiln sites in Wallonia, Belgium, European
Journal of Soil Science 68(1): 80–89.
https://doi.org/10.1111/ejss.12395
Harter, J.; Krause, H. M.; Schuettler, S.; Ruser, R.; Fromme, M.;
Scholten, T.; Kappler, A.; Behrens, S. 2014. Linking N2O
emissions from biochar-amended soil to the structure and
function of the N-cycling microbial community, ISME Jour-
nal 8(3): 660–674. https://doi.org/10.1038/ismej.2013.160
Harter, J.; Weigold, P.; El-Hadidi, M.; Huson, D. H.; Kappler, A.;
Behrens, S. 2016. Soil biochar amendment shapes the com-
position of N2O-reducing microbial communities, Science of
e Total Environment 562: 379–390.
https://doi.org/10.1016/j.scitotenv.2016.03.220
Hiltbrunner, D.; Zimmermann, S.; Karbin, S.; Hagedorn, F.; Ni-
klaus, P. A. 2012. Increasing soil methane sink along a 120-
year aorestation chronosequence is driven by soil moisture,
Global Change Biology 18(12): 3664–3671.
https://doi.org/10.1111/j.1365-2486.2012.02798.x
Hu, H.-W.; Chen, D.; He, J.-Z. 2015. Microbial regulation of ter-
restrial nitrous oxide formation: understanding the biological
pathways for prediction of emission rates, FEMS Microbiology
Reviews 39(5): 729–749. https://doi.org/10.1093/femsre/fuv021
Hua, L.; Chen, Y.; Wu, W. 2012. Impacts upon soil quality and
plant growth of bamboo charcoal addition to composted
sludge, Environmental Technology 33(1): 61–68.
https://doi.org/10.1080/09593330.2010.549845
Hua, L.; Wu, W.; Liu, Y.; Mcbride, M. B.; Chen, Y. 2009. Reduc-
tion of nitrogen loss and Cu and Zn mobility during sludge
composting with bamboo charcoal amendment, Environmen-
tal Science and Pollution Research 16(1): 1–9.
https://doi.org/10.1007/s11356-008-0041-0
Hüppi, R.; Felber, R.; Neel, A.; Six, J.; Leifeld, J. 2015. Eect
of biochar and liming on soil nitrous oxide emissions from
a temperate maize cropping system, SOIL 1(2): 707–717.
https://doi.org/10.5194/soil-1-707-2015
Husson, O. 2013. Redox potential (Eh) and pH as drivers of soil/
plant/microorganism systems: a transdisciplinary overview
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
132
pointing to integrative opportunities for agronomy, Plant and
Soil 362(1–2): 389–417.
https://doi.org/10.1007/s11104-012-1429-7
Hütsch, B. W. 2001. Methane oxidation in non-ooded soils as
aected by crop production – invited paper, European Jour-
nal of Agronomy 14(4): 237–260.
https://doi.org/10.1016/S1161-0301(01)00110-1
ISDA. 2016. e State of Idaho and USDA: Idaho OnePlan Nutrient
Management Plan [online], [cited 28 December 2016]. Avail-
able from Internet: http://www.oneplan.org/NMPlan.asp
Islam, M. M.; Ahmed, S. T.; Kim, Y. J.; Mun, H. S.; Kim, Y. J.;
Yang, C. J. 2014. Eect of sea tangle (Laminaria japonica)
and charcoal supplementation as alternatives to antibiotics
on growth performance and meat quality of ducks, Asian-
Australasian Journal of Animal Sciences 27(2): 217–224.
https://doi.org/10.5713/ajas.2013.13314
ISO 17512-1:2008. Soil quality – Avoidance test for determining
the quality of soils and eects of chemicals on behaviour–
Part1: Test with earthworms (Eisenia fetida and Eisenia an-
drei). International Organization for Standardization.
Jaé, R.; Ding, Y.; Niggemann, J.; Vähätalo, A. V.; Stubbins,A.;
Spencer, R. G.; Campbell, J.; Dittmar, T. 2013. Global char-
coal mobilization from soils via dissolution and river-
ine transport to the oceans, Science 340(6130): 345–347.
https://doi.org/10.1126/science.1231476
Jeery, S.; Abalos, D.; Spokas, K.; Verheijen, F. G. A. 2015. Bio-
char eects on crop yield, in J. Lehmann, S. D. Joseph. (Eds.).
Biochar for environmental management: science, technology
and implementation. 2nd ed. Florence, KY, USA: Taylor and
Francis.
Jeery, S.; Verheijen, F. G.; Kammann, C.; Abalos, D. 2016. Bio-
char eects on methane emissions from soils: a meta-analy-
sis, Soil Biology and Biochemistry 101: 251–258.
https://doi.org/10.1016/j.soilbio.2016.07.021
Jia, J.; Li, B.; Chen, Z.; Xie, Z.; Xiong, Z. 2012. Eects of biochar
application on vegetable production and emissions of N2O
and CH4, Soil Science and Plant Nutrition 58(4): 503–509.
https://doi.org/10.1080/00380768.2012.686436
Jia, X. Y.; Wang, M.; Yuan, W. Q.; Ju, X. T.; Yang, B. Z. 2016. the
inuence of biochar addition on chicken manure compost-
ing and associated methane and carbon dioxide emissions,
Bioresources 11(2): 5255–5264.
https://doi.org/10.15376/biores.11.2.5255-5264
Jones, D. L.; Rousk, J.; Edwards-Jones, G.; Deluca, T. H.; Mur-
phy, D. V. 2012. Biochar-mediated changes in soil quality and
plant growth in a three year eld trial, Soil Biology and Bio-
chemistry 45: 113–124.
https://doi.org/10.1016/j.soilbio.2011.10.012
Joseph, S.; Graber, E. R.; Chia, C.; Munroe, P.; Donne, S.;
omas, T.; Nielsen, S.; Marjo, C.; Rutlidge, H.; Pan, G. X.;
Li, L.; Taylor, P.; Rawal, A.; Hook, J. 2013. Shiing paradigms:
development of high-eciency biochar fertilizers based on
nano-structures and soluble components, Carbon Manage-
ment 4(3): 323–343. https://doi.org/10.4155/cmt.13.23
Joseph, S.; Husson, O.; Graber, E. R.; Van Zwieten, L.; Tahery-
moosavi, S.; omas, T.; Nielsen, S.; Ye, J.; Pan, G.; Chia,C.
2015a. e electrochemical properties of biochars and how
they aect soil redox properties and processes, Agronomy
5(3): 322–340. https://doi.org/10.3390/agronomy5030322
Joseph, S.; Pow, D.; Dawson, K.; Mitchell, D. R. G.; Rawal,A.;
Hook, J.; Taherymoosavi, S.; Van Zwieten, L.; Rust, J.;
Donne,S.; Munroe, P.; Pace, B.; Graber, E.; omas, T.;
Nielsen, S.; Ye, J.; Lin, Y.; Pan, G.; Li, L.; Solaiman, Z. M.
2015b. Feeding biochar to cows: an innovative solution for
improving soil fertility and farm productivity, Pedosphere
25(5): 666–679.
https://doi.org/10.1016/S1002-0160(15)30047-3
Jung, M.-Y.; Well, R.; Min, D.; Giesemann, A.; Park, S.-J.;
Kim,J.-G.; Kim, S.-J.; Rhee, S.-K. 2014. Isotopic signatures
of N2O produced by ammonia-oxidizing archaea from soils,
ISME Journal 8(5): 1115–1125.
https://doi.org/10.1038/ismej.2013.205
Juutinen, S.; Alm, J.; Larmola, T.; Huttunen, J. T.; Morero, M.;
Saarnio, S.; Martikainen, P. J.; Silvola, J. 2003. Methane (CH4)
release from littoral wetlands of boreal lakes during an ex-
tended ooding period, Global Change Biology 9(3): 413–424.
https://doi.org/10.1046/j.1365-2486.2003.00595.x
Kalachniuk, H. I.; Marounek, M.; Kalachniuk, L. H.; Savka, O. H.
1994. Rumen bacterial metabolism as aected by extracellu-
lar redox potential, Ukrainskii biokhimicheskii zhurnal (1978)
66(1): 30–40.
Kammann, C.; Hepp, S.; Lenhart, K.; Müller, C. 2009. Stimula-
tion of methane consumption by endogenous CH4 produc-
tion in aerobic grassland soil, Soil Biology and Biochemistry
41(3): 622–629. https://doi.org/10.1016/j.soilbio.2008.12.025
Kammann, C.; Ratering, S.; Eckhard, C.; Muller, C. 2012. Biochar
and hydrochar eects on greenhouse gas (carbon dioxide, ni-
trous oxide, and methane) uxes from soils, Journal of Envi-
ronmental Quality 41(4): 1052–1066.
https://doi.org/10.2134/jeq2011.0132
Kammann, C. I.; Glaser, B.; Schmidt, H.-P. 2016. Combining bio-
char and organic amendments, in S. Shackley, G. Ruysscha-
ert, K. Zwart, B. Glaser (Eds.). Biochar in European soils and
agriculture: science and practice. London: Routledge.
Kammann, C. I.; Schmidt, H. P.; Messerschmidt, N.; Linsel, S.;
Steens, D.; Muller, C.; Koyro, H. W.; Conte, P.; Stephen, J.
2015. Plant growth improvement mediated by nitrate cap-
ture in co-composted biochar, Scientic Reports 5(11080).
https://doi.org/10.1038/srep11080
Kappler, A.; Wuestner, M. L.; Ruecker, A.; Harter, J.; Halama, M.;
Behrens, S. 2014. Biochar as an electron shuttle between bac-
teria and Fe(III) minerals, Environmental Science & Technol-
ogy Letters 1(8): 339–344. https://doi.org/10.1021/ez5002209
Karhu, K.; Mattila, T.; Bergström, I.; Regina, K. 2011. Biochar
addition to agricultural soil increased CH4 uptake and water
holding capacity – Results from a short-term pilot eld study,
Agriculture, Ecosystems & Environment 140(1–2): 309–313.
https://doi.org/10.1016/j.agee.2010.12.005
Kellogg, R. L.; Lander, C. H.; Mott, D. C.; Gollehon, N. 2000.
Manure nutrients relative to the capacity of cropland and
pastureland to assimilate nutrients: spatial and temporal
trends for the United States, Proceedings of the Water Envi-
ronment Federation 2000(16): 18–157.
https://doi.org/10.2175/193864700784994812
Kern, J.; Hellebrand, H. J.; Gömmel, M.; Ammon, C.; Berg, W.
2012. Eects of climatic factors and soil management on
the methane ux in soils from annual and perennial energy
crops, Biology and Fertility of Soils 48(1): 1–8.
https://doi.org/10.1007/s00374-011-0603-z
Kern, J.; Tammeorg, P.; Shanskiy, M.; Sakrabani, R.; Knicker,H.;
Kammann, C. I.; Tuhkanen, E.-M.; Smidt, G.; Prasad, M.;
Kari, T.; Sohi, S.; Gascó, G.; Steiner, C.; Glaser, G. 2017.
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 133
Synergistic use of peat and charred material in growing media–
an option to reduce the pressure on peatlands?, Journal of Envi-
ronmental Engineering and Landscape Management (this issue).
Khan, S.; Chao, C.; Waqas, M.; Arp, H. P.; Zhu, Y. G. 2013a. Sew-
age sludge biochar inuence upon rice (Oryza sativa L) yield,
metal bioaccumulation and greenhouse gas emissions from
acidic paddy soil, Environmental Science & Technolog y 47:
8624–8632. https://doi.org/10.1021/es400554x
Khan, S.; Chao, C.; Waqas, M.; Arp, H. P. H.; Zhu, Y. G. 2013b.
Sewage sludge biochar inuence upon rice (Oryza sativa L)
yield, metal bioaccumulation and greenhouse gas emissions
from acidic paddy soil, Environmental Science & Technology
47(15): 8624–8632. https://doi.org/10.1021/es400554x
Kluepfel, L.; Keiluweit, M.; Kleber, M.; Sander, M. 2014. Redox
properties of plant biomass-derived black carbon (biochar),
Environmental Science & Technolog y 48(10): 5601–5611.
https://doi.org/10.1021/es500906d
Kollah, B.; Dubey, G.; Parasai, P.; Saha, J. K.; Gangil, S.; Mohan-
ty, S. R. 2015. Interactive eect of biochar size and organic
amendments on methane consumption in a tropical vertisol,
Soil Use and Management 31(1): 52–59.
https://doi.org/10.1111/sum.12168
Kömpf, K. 2013. Consequences of aging of pyrogenous biochar re-
garding the potential to reduce nitrous oxide from soil: Bach-
elor esis. Justus-Liebig-University, Giessen. 61 p. (in Ger-
man).
Konuma, H. 2016. Status of world food security and its future
outlook, and role of agricultural research and education,
Journal of Developments in Sustainable Agriculture 10(2):
69–75.
Kool, D. M.; Dolng, J.; Wrage, N.; Van Groenigen, J. W. 2011a.
Nitrier denitrication as a distinct and signicant source of
nitrous oxide from soil, Soil Biology and Biochemistry 43(1):
174–178. https://doi.org/10.1016/j.soilbio.2010.09.030
Kool, D. M.; Van Groenigen, J. W. Wrage, N. 2011b. Source de-
termination of nitrous oxide based on nitrogen and oxygen
isotope tracing: dealing with oxygen exchange, Chapter 6, in
G. K. Martin, Y. S. Lisa. (Eds.). Methods in enzymology. Aca-
demic Press.
https://doi.org/10.1016/b978-0-12-386489-5.00006-3
Koven, C. D.; Ringeval, B.; Friedlingstein, P.; Ciais, P.; Cadule,P.;
Khvorostyanov, D.; Krinner, G.; Tarnocai, C. 2011. Perma-
frost carbon-climate feedbacks accelerate global warming,
Proceedings of the National Academy of Sciences 108(36):
14769–14774. https://doi.org/10.1073/pnas.1103910108
Kozlowski, J. A.; Price, J.; Stein, L. Y. 2014. Revision of N2O-Pro-
ducing pathways in the ammonia-oxidizing bacterium Nitro-
somonas europaea ATCC 19718, Applied and Environmental
Microbiology 80(16): 4930–4935.
https://doi.org/10.1128/AEM.01061-14
Laird, D. A.; Brown, R. C.; Amonette, J. E.; Lehmann, J. 2009.
Review of the pyrolysis platform for coproducing bio‐oil and
biochar, Biofuels, Bioproducts and Biorening 3(5): 547–562.
https://doi.org/10.1002/bbb.169
Lal, R. 2014. Desertication and soil erosion, in B. Freedman
(Ed.). Global environmental change. Dordrecht: Springer
Netherlands. https://doi.org/10.1007/978-94-007-5784-4_7
Laughlin, R. J.; Stevens, R. J. 2002. Evidence for fungal domi-
nance of denitrication and codenitrication in a grassland
Soil, Soil Science Society of America Journal 66(5): 1540–1548.
https://doi.org/10.2136/sssaj2002.1540
Lee, J. W.; Hawkins, B.; Li, X.; Day, D. M. 2013. Biochar fertilizer
for soil amendment and carbon sequestration, in J. W.Lee
(Ed.). Advanced biofuels and bioproducts. New York, NY:
Springer New York.
https://doi.org/10.1007/978-1-4614-3348-4_6
Lehmann, J.; Abiven, S.; Kleber, M.; Pan, G.; Singh, B. P.;
Sohi, S. P.; Zimmerman, A. R.; Lehmann, J.; Joseph, S. 2015.
Persistence of biochar in soil, in J. Lehmann, J. Stephen
(Eds.). Biochar for environmental management: science, tech-
nology and implementation. 2nd ed. London: Routledge.
Leng, R. A.; Inthapanya, S.; Preston, T. R. 2012a. Biochar lowers
net methane production from rumen uid in vitro. Livestock
Research for Rural Development 24(103) [online], [cited 28
December 2016]. Available from Internet: http://www.lrrd.
org/lrrd24/6/sang24103.htm
Leng, R.; Preston, T.; Inthapanya, S. 2012b. Biochar reduces
enteric methane and improves growth and feed conversion
in local “Yellow” cattle fed cassava root chips and fresh cas-
sava foliage, Livestock Research for Rural Development 24(11)
[online], [cited 28 December 2016]. Available from Internet:
http://www.lrrd.org/lrrd24/11/leng24199.htm
Leng, R. A.; Inthapanya, S.; Preston, T. R. 2013. All biochars are
not equal in lowering methane production in in vitro rumen
incubations, Livestock Research for Rural Development 25(6)
[online], [cited 28 December 2016]. Available from Internet:
http://www.lrrd.org/lrrd25/6/leng25106.htm
Lewicka-Szczebak, D.; Dyckmans, J.; Kaiser, J.; Marca, A.; Au-
gustin, J.; Well, R. 2016. Oxygen isotope fractionation dur-
ing N2O production by soil denitrication, Biogeosciences 13:
1129–1144. https://doi.org/10.5194/bg-13-1129-2016
Li, B.; Fan, C.; Zhang, H.; Chen, Z.; Sun, L.; Xiong, Z. 2015.
Combined eects of nitrogen fertilization and biochar on the
net global warming potential, greenhouse gas intensity and
net ecosystem economic budget in intensive vegetable agri-
culture in southeastern China, Atmospheric Environment 100:
10–19. https://doi.org/10.1016/j.atmosenv.2014.10.034
Li, S. Q.; Song, L. N.; Jin, Y. G.; Liu, S. W.; Shen, Q. R.; Zou, J. W.
2016. Linking N2O emission from biochar-amended com-
posting process to the abundance of denitrify (nirK and
nosZ) bacteria community, Amb Express 6(37): 1–9.
https://doi.org/10.1186/s13568-016-0208-x
Liiri, M.; Setälä, H.; Haimi, J.; Pennanen, T.; Fritze, H. 2002. Soil
processes are not inuenced by the functional complexity of
soil decomposer food webs under disturbance, Soil Biology
and Biochemistry 34(7): 1009–1020.
https://doi.org/10.1016/S0038-0717(02)00034-2
Lin, X.; Spokas, K. A.; Venterea, R. T.; Zhang, R.; Baker, J. M.;
Feyereisen, G. W. 2014. Assessing microbial contributions
to N2O impacts following biochar additions, Agronomy 4(4):
478–496. https://doi.org/10.3390/agronomy4040478
Lin, X.; Xie, Z.; Zheng, J.; Liu, Q.; Bei, Q. Zhu, J. 2015. Eects of
biochar application on greenhouse gas emissions, carbon se-
questration and crop growth in coastal saline soil, European
Journal of Soil Science 66(2): 329–338.
https://doi.org/10.1111/ejss.12225
Liu, F.; Rotaru, A.-E.; Shrestha, P. M.; Malvankar, N. S.;
Nevin, K. P.; Lovley, D. R. 2012. Promoting direct interspe-
cies electron transfer with activated carbon, Energy & Envi-
ronmental Science 5(10): 8982–8989.
https://doi.org/10.1039/c2ee22459c
Liu, L.; Shen, G.; Sun, M.; Cao, X.; Shang, G.; Chen, P. 2014. Ef-
fect of biochar on nitrous oxide emission and its potential
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
134
mechanisms, Journal of the Air & Waste Management Asso-
ciation 64: 894–902.
https://doi.org/10.1080/10962247.2014.899937
López-Cano, I.; Roig, A.; Cayuela, M. L.; Alburquerque, J. A.;
Sánchez-Monedero, M. A. 2016. Biochar improves N cycling
during composting of olive mill wastes and sheep manure,
Waste Management 49: 553–559.
https://doi.org/10.1016/j.wasman.2015.12.031
Lovley, D. R.; Phillips, E. J. 1987. Competitive mechanisms for
inhibition of sulfate reduction and methane production in
the zone of ferric iron reduction in sediments, Applied and
Environmental Microbiology 53(11): 2636–2641.
Lv, D.; Xu, M.; Liu, X.; Zhan, Z.; Li, Z.; Yao, H. 2010. Eect of
cellulose, lignin, alkali and alkaline earth metallic species on
biomass pyrolysis and gasication, Fuel Processing Technology
91(8): 903–909. https://doi.org/10.1016/j.fuproc.2009.09.014
Malghani, S.; Gleixner, G.; Trumbore, S. E. 2013. Chars produced
by slow pyrolysis and hydrothermal carbonization vary in
carbon sequestration potential and greenhouse gases emis-
sions, Soil Biology and Biochemistry 62: 137–146.
https://doi.org/10.1016/j.soilbio.2013.03.013
Malinska, K.; Zabochnicka-Swiatek, M.; Dach, J. 2014. Eects
of biochar amendment on ammonia emission during com-
posting of sewage sludge, Ecological Engineering 71: 474–478.
https://doi.org/10.1016/j.ecoleng.2014.07.012
Marras, S.; Masia, S.; Duce, P.; Spano, D.; Sirca, C. 2015. Carbon
footprint assessment on a mature vineyard, Agricultural and
Forest Meteorology 214: 350–356.
https://doi.org/10.1016/j.agrformet.2015.08.270
MDE. 2016. AFO (CAFO/MAFO) information page [online].
Maryland Department of the Environment [cited 28 Decem-
ber 2016]. Available from the Internet: http://www.mde.state.
md.us/programs/Land/RecyclingandOperationsprogram/
AFO/Pages/index.aspx
Megonigal, J.; Whalen, S. C.; Tissue, D.; Bovard, B.; Allen, A.;
Albert, D. 1999. A plant-soil-atmosphere microcosm for trac-
ing radiocarbon from photosynthesis through methanogen-
esis, Soil Science Society of America Journal 63(3): 665–671.
https://doi.org/10.2136/sssaj1999.03615995006300030033x
Min, J.; Lu, K.; Sun, H.; Xia, L.; Zhang, H.; Shi, W. 2016. Global
warming potential in an intensive vegetable cropping system
as aected by crop rotation and nitrogen rate, CLEAN– Soil,
Air, Water 44(7): 766–774.
https://doi.org/10.1002/clen.201400785
Mochidzuki, K.; Soutric, F.; Tadokoro, K.; Antal, M. J.; Tóth, M.;
Zelei, B.; Várhegyi, G. 2003. Electrical and physical properties
of carbonized charcoals, Industrial & Engineering Chemistry
Research 42(21): 5140–5151.
https://doi.org/10.1021/ie030358e
Myhre, G.; Shindell, D.; Bréon, F. M.; Collins, W.; Fuglestvedt,J.;
Huang, J.; Koch, D.; Lamarque, J. F.; Lee, D.; Mendoza,B.;
Nakajima, T.; Robock, A.; Stephens, G.; Takemura, T.;
Zhang,H. 2013. Anthropogenic and natural radiative forcing,
in T. F. Stocker, D. Qin, G. K. Plattner, M. Tignor, S.K.Allen,
J.Boschung, A. Nauels, Y. Xia, V. Bex, P. M. Midgley (Eds.)
Climate change 2013: the physical science basis. Contribution
of working group I to the h assessment report of the inter-
governmental panel on climate change. Cambridge and New
York, NY: Cambridge University Press.
Naka, K.; Watarai, S.; Tana; Inoue, K.; Kodama, Y.; Oguma, K.;
Yasuda, T.; Kodama, H. 2001. Adsorption eect of activated
charcoal on enterohemorrhagic Escherichia coli, Journal of
Veterinary Medical Science 63(3): 281–285.
https://doi.org/10.1292/jvms.63.281
Nelissen, V.; Rütting, T.; Huygens, D.; Staelens, J.; Ruysscha-
ert,G.; Boeckx, P. 2012. Maize biochars accelerate short-term
soil nitrogen dynamics in a loamy sand soil, Soil Bio logy&
Biochemistry 55: 20–27.
https://doi.org/10.1016/j.soilbio.2012.05.019
Nelissen, V.; Saha, B. K.; Ruysschaert, G.; Boeckx, P. 2014. Eect
of dierent biochar and fertilizer types on N2O and NO emis-
sions, Soil Biology & Biochemistry 70: 244–255.
https://doi.org/10.1016/j.soilbio.2013.12.026
Nguyen, D. H.; Biala, J.; Grace, P. R.; Scheer, C.; Rowlings, D. W.
2014. Greenhouse gas emissions from sub-tropical agricul-
tural soils aer addition of organic by-products, Springerplus
3(491): 14. https://doi.org/10.1186/2193-1801-3-491
Novak, J.; Cantrell, K.; Watts, D. 2013. Compositional and ther-
mal evaluation of lignocellulosic and poultry litter chars via
high and low temperature pyrolysis, Bioenergy Research 6(1):
114–130. https://doi.org/10.1007/s12155-012-9228-9
O’Toole, A.; Andersson, D.; Gerlach, A.; Glaser, B.; Kam-
mann, C. I.; Kern, J.; Kuoppamäki, K.; Mumme, J.;
Schmidt,H. P.; Schulze, M.; Srocke, F.; Stenrød, M.; Sten-
ström, J. 2016. Current and future applications for biochar, in
S.Shackley, G. Ruysschaert, K. Zwart, B. Glaser (Eds.). Bio-
char in European soils and agriculture: science and practice.
London: Routledge.
Obia, A.; Cornelissen, G.; Mulder, J.; Dörsch, P. 2015. Eect of
soil pH increase by biochar on NO, N2O and N2 produc-
tion during denitrication in acid soils, PLoS ONE 10(9):
e0138781. https://doi.org/10.1371/journal.pone.0138781
Obia, A.; Mulder, J.; Martinsen, V.; Cornelissen, G.; Børresen,T.
2016. In situ eects of biochar on aggregation, water reten-
tion and porosity in light-textured tropical soils, Soil and Till-
age Research 155: 35–44.
https://doi.org/10.1016/j.still.2015.08.002
Ojima, D. S.; Valentine, D. W.; Mosier, A. R.; Parton, W. J.;
Schimel, D. S. 1993. Eect of land use change on methane ox-
idation in temperate forest and grassland soils, Chemosphere
26(1): 675–685. https://doi.org/10.1016/0045-6535(93)90452-B
Oremland, R. S. 1988. Biogeochemistry of methanogenic bacte-
ria, in A. J. B. Zehnder (Ed.). Biology of anaerobic microor-
ganisms. New York: John Wiley and Sons.
Perez-Garcia, O.; Villas-Boas, S. G.; Swi, S.; Chandran, K.; Sing-
hal, N. 2014. Clarifying the regulation of NO/N2O produc-
tion in Nitrosomonas europaea during anoxic–oxic transition
via ux balance analysis of a metabolic network model, Water
Research 60: 267–277.
https://doi.org/10.1016/j.watres.2014.04.049
Powlson, D.; Goulding, K.; Willison, T. Webster, C.; Hütsch, B.
1997. e eect of agriculture on methane oxidation in soil,
Nutrient Cycling in Agroecosystems 49(1–3): 59–70.
https://doi.org/10.1023/A:1009704226554
Prévoteau, A.; Ronsse, F.; Cid, I.; Boeckx, P.; Rabaey, K. 2016. e
electron donating capacity of biochar is dramatically under-
estimated, Scientic Reports 6(32870).
https://doi.org/10.1038/srep32870
Prommer, J.; Wanek, W.; Hoansl, F.; Trojan, D.; Ore, P.;
Urich,T.; Schleper, C.; Sassmann, S.; Kitzler, B.; Soja, G.;
Hood-Nowotny, R. C. 2014. Biochar decelerates soil organic
nitrogen cycling but stimulates soil nitrication in a temper-
ate arable eld trial, PLoS ONE 9(1): e86388.
https://doi.org/10.1371/journal.pone.0086388
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 135
Prost, K.; Borchard, N.; Siemens, J.; Kautz, T.; Séquaris, J.-M.;
Möller, A.; Amelung, W. 2013. Biochar aected by compost-
ing with farmyard manure, Journal of Environmental Quality
42(1): 164–172. https://doi.org/10.2134/jeq2012.0064
PSAC. 1905. Annual report of the Pennsylvania Agricultural Ex-
periment Station. State College, PA, Pennsylvania State Agri-
cultural College.
Qian, L.; Chen, L.; Joseph, S.; Pan, G.; Li, L.; Zheng, J.; Zhang, X.;
Zheng, J.; Yu, X.; Wang, J. 2014. Biochar compound fertilizer
as an option to reach high productivity but low carbon inten-
sity in rice agriculture of China, Carbon Management 5(2):
145–154. https://doi.org/10.1080/17583004.2014.912866
Quin, P.; Joseph, S.; Husson, O.; Donne, S.; Mitchell, D.; Mun-
roe, P.; Phelan, D.; Cowie, A.; Van Zwieten, L. 2015. Low-
ering N2O emissions from soils using eucalypt biochar: the
importance of redox reactions, Scientic Reports 5(16773).
https://doi.org/10.1038/srep16773
Ravishankara, A. R.; Daniel, J. S.; Portmann, R. W. 2009. Ni-
trous oxide (N2O): e dominant ozone-depleting substance
emitted in the 21st century, Science 326(5949): 123–125.
https://doi.org/10.1126/science.1176985
Reddy, K. R.; Yargicoglu, E. N.; Yue, D.; Yaghoubi, P. 2014. En-
hanced microbial methane oxidation in landll cover soil
amended with biochar, Journal of Geotechnical and Geoenvi-
ronmental Engineering 140(9): 04014047.
https://doi.org/10.1061/(ASCE)GT.1943-5606.0001148
Rohe, L.; Anderson, T.-H.; Braker, G.; Flessa, H.; Giesemann,A.;
Lewicka-Szczebak, D.; Wrage-Mönnig, N.; Well, R. 2014.
Dual isotope and isotopomer signatures of nitrous oxide
from fungal denitrication – a pure culture study, Rapid
Communications in Mass Spectrometry 28(17): 1893–1903.
https://doi.org/10.1002/rcm.6975
Rondon, M.; Ramirez, J.; Lehmann, J. 2005. Greenhouse gas
emissions decrease with charcoal additions to tropical soils,
in Proceedings of the 3rd USDA Symposium on Greenhouse
Gases and Carbon Sequestration, 2005, Baltimore, USA.
Rulli, M. C.; Saviori, A.; D’odorico, P. 2013. Global land and wa-
ter grabbing, Proceedings of the National Academy of Sciences
110(3): 892–897. https://doi.org/10.1073/pnas.1213163110
Ruser, R.; Schilling, R.; Steindl, H.; Flessa, H.; Beese, F. 1998.
Soil compaction and fertilization eects on nitrous oxide and
methane uxes in potato elds, Soil Science Society of Ameri-
ca Journal 62(6): 1587–1595.
https://doi.org/10.2136/sssaj1998.03615995006200060016x
Rütting, T.; Müller, C. 2007. 15N tracing models with a Monte
Carlo optimization procedure provide new insights on gross
N transformations in soils, Soil Biology and Biochemistry
39(9): 2351–2361.
https://doi.org/10.1016/j.soilbio.2007.04.006
Ruysschaert, G.; Nelissen, V.; Postma, R.; Bruun, E.; O’toole,A.;
Hammond, J.; Rödger, J.-M.; Ylander, L.; Kihlberg, T.;
Zwart,K.; Hauggaard-Nielsen, H.; Shackley, S. 2016. Field ap-
plications of pure biochar in the North Sea region and across
Europe, in S. Shackley, G. Ruysschaert, K. Zwart, B.Glaser
(Eds.). Biochar in European soils and agriculture: science and
practice. London: Routledge.
Saarnio, S. 2016. Impacts of biochar amendment on greenhouse
gas emissions from agricultural soils, Chapter 9 in M. Guo,
Z.He, M. Uchimiya (Eds.). Agricultural and environmental
applications of biochar: advances and barriers. 63 ed. Madi-
son, WI.: Soil Science Society of America.
https://doi.org/10.2136/sssaspecpub63.2014.0045
Saarnio, S.; Alm, J.; Silvola, J.; Lohila, A.; Nykänen, H.; Marti-
kainen, P. J. 1997. Seasonal variation in CH4 emissions and
production and oxidation potentials at microsites on an oli-
gotrophic pine fen, Oecologia 110(3): 414–422.
https://doi.org/10.1007/s004420050176
Saarnio, S.; Heimonen, K.; Kettunen, R. 2013. Biochar addi-
tion indirectly aects N2O emissions via soil moisture and
plant N uptake, Soil Biology & Biochemistry 58: 99–106.
https://doi.org/10.1016/j.soilbio.2012.10.035
Saarnio, S.; Winiwarter, W.; Leitao, J. 2009. Methane release from
wetlands and watercourses in Europe, Atmospheric Environ-
ment 43(7): 1421–1429.
https://doi.org/10.1016/j.atmosenv.2008.04.007
Saarnio, S.; Wittenmayer, L.; Merbach, W. 2004. Rhizospheric
exudation of Eriophorum vaginatum L. – potential link
to methanogenesis, Plant and Soil 267(1–2): 343–355.
https://doi.org/10.1007/s11104-005-0140-3
Sadasivam, B. Y.; Reddy, K. R. 2015. Adsorption and transport
of methane in landll cover soil amended with waste-wood
biochars, Journal of Environmental Management 158: 11–23.
https://doi.org/10.1016/j.jenvman.2015.04.032
Sánchez-García, M.; Alburquerque, J. A.; Sánchez-Monede-
ro,M.A.; Roig, A.; Cayuela, M. L. 2015. Biochar accelerates
organic matter degradation and enhances N mineralisation
during composting of poultry manure without a relevant im-
pact on gas emissions, Bioresource Technology 192: 272–279.
https://doi.org/10.1016/j.biortech.2015.05.003
Sánchez-García, M.; Roig, A.; Sanchez-Monedero, M. A.;
Cayuela, M. L. 2014. Biochar increases soil N2O emissions
produced by nitrication-mediated pathways, Frontiers in
Environmental Science 2(25): 1–10.
Sánchez-García, M.; Sánchez-Monedero, M. A.; Roig, A.; López-
Cano, I.; Moreno, B.; Benitez, E.; Cayuela, M. L. 2016. Com-
post vs biochar amendment: a two-year eld study evaluating
soil C build-up and N dynamics in an organically managed
olive crop, Plant and Soil 408(1): 1–14.
https://doi.org/10.1007/s11104-016-2794-4
Saunois, M.; Jackson, R. B.; Bousquet, P.; Poulter, B.; Cana-
dell,J.G. 2016. e growing role of methane in anthropo-
genic climate change, Environmental Research Letters 11(12):
120207. https://doi.org/10.1088/1748-9326/11/12/120207
Savage, E. S. 1917. Feeding dairy cattle, Holstein-Friesian World
1(47).
Scheer, C.; Grace, P. R.; Rowlings, D. W.; Kimber, S.; Van Zwie-
ten, L. 2011. Eect of biochar amendment on the soil-at-
mosphere exchange of greenhouse gases from an intensive
subtropical pasture in northern New South Wales, Australia,
Plant and Soil 345(1–2): 47–58.
https://doi.org/10.1007/s11104-011-0759-1
Schimmelpfennig, S.; Müller, C.; Grünhage, L.; Koch, C.; Kam-
mann, C. 2014. Biochar, hydrochar and uncarbonized
feedstock application to permanent grassland – Eects on
greenhouse gas emissions and plant growth, Agriculture,
Ecosystems & Environment 191: 39–52.
https://doi.org/10.1016/j.agee.2014.03.027
Schmidt, H.-P.; Pandit, B.; Martinsen, V.; Cornelissen, G.;
Conte,P.; Kammann, C. 2015. Fourfold increase in pump-
kin yield in response to low-dosage root zone application of
urine-enhanced biochar to a fertile tropical soil, Agriculture
5(3): 23. https://doi.org/10.3390/agriculture5030723
Schmidt, H. P.; Kammann, C.; Niggli, C.; Evangelou, M. W. H.;
Mackie, K. A.; Abiven, S. 2014. Biochar and biochar-compost
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
136
as soil amendments to a vineyard soil: Inuences on plant
growth, nutrient uptake, plant health and grape quality, Agri-
culture Ecosystems & Environment 191: 117–123.
https://doi.org/10.1016/j.agee.2014.04.001
Schmidt, H. P.; Kammann, C. I.; Gerlach, A.; Gerlach, H. 2016.
Der Einsatz von Panzenkohle in der Tierfütterung, Ithaka-
Journal 95: 364–394.
Schnell, S.; King, G. M. 1995. Stability of methane oxidation ca-
pacity to variations in methane and nutrient concentrations,
FEMS Microbiology Ecology 17(4): 285–294.
https://doi.org/10.1111/j.1574-6941.1995.tb00153.x
Seiler, W.; Conrad, R.; Schare, D. 1984. Field studies of methane
emission from termite nests into the atmosphere and mea-
surements of methane uptake by tropical soils, Journal of At-
mospheric Chemistry 1(2): 171–186.
https://doi.org/10.1007/BF00053839
Shaw, L. J.; Nicol, G. W.; Smith, Z.; Fear, J.; Prosser, J. I.;
Baggs, E. M. 2006. Nitrosospira spp. can produce nitrous
oxide via a nitrier denitrication pathway, Environmental
Microbiology 8(2): 214–222.
https://doi.org/10.1111/j.1462-2920.2005.00882.x
Shi, L.; Dong, H.; Reguera, G.; Beyenal, H.; Lu, A.; Liu, J.;
Yu, H.-Q.; Fredrickson, J. K. 2016. Extracellular electron
transfer mechanisms between microorganisms and minerals,
Nature Reviews Microbiology 14: 651–662.
https://doi.org/10.1038/nrmicro.2016.93
Snider, D.; ompson, K.; Wagner-Riddle, C.; Spoelstra, J.; Dun-
eld, K. 2015. Molecular techniques and stable isotope ratios
at natural abundance give complementary inferences about
N2O production pathways in an agricultural soil following
a rainfall event, Soil Biology and Biochemistry 88: 197–213.
https://doi.org/10.1016/j.soilbio.2015.05.021
Solomon, D.; Lehmann, J.; Fraser, J. A.; Leach, M.; Amanor, K.;
Frausin, V.; Kristiansen, S. M.; Millimouno, D.; Fairhead,J.
2016. Indigenous African soil enrichment as a climate-
smart sustainable agriculture alternative, Frontiers in Ecol-
ogy and the Environment 14(2): 71–76.
https://doi.org/10.1002/fee.1226
Song, X.; Pan, G.; Zhang, C.; Zhang, L.; Wang, H. 2016. Eects
of biochar application on uxes of three biogenic greenhouse
gases: a meta-analysis, Ecosystem Health and Sustainability
2(2): e01202. https://doi.org/10.1002/ehs2.1202
Sonoki, T.; Furukawa, T.; Jindo, K.; Suto, K.; Aoyama, M.;
Sanchez-Monedero, M. A. 2013. Inuence of biochar addi-
tion on methane metabolism during thermophilic phase of
composting, Journal of Basic Microbiology 53(7): 617–621.
https://doi.org/10.1002/jobm.201200096
Sonoki, T.; Furukawa, T.; Mizumoto, H.; Jindo, K.; Aoyama, M.;
Sanchez-Monedero, M. 2011. Impacts of biochar addition on
methane and carbon dioxide emissions during composting of
cattle manure, in Asia Pacic Biochar Conference Kyoto, 2011,
15–18 September 2011, Kyoto, Japan.
Sophal, C.; Khang, D. N.; Preston, T.; Leng, R. 2013. Nitrate
replacing urea as a fermentable N source decreases enteric
methane production and increases the eciency of feed uti-
lization in Yellow cattle, Livestock Research for Rural Devel-
opment 25(7) [online], [cited 28 December 2016]. Available
from Internet: http://www.lrrd.org/lrrd25/7/soph25113.htm
Spokas, K. A. 2013. Impact of biochar eld aging on laboratory
greenhouse gas production potentials, Global Change Biology
Bioenergy 5(2): 165–176.
https://doi.org/10.1111/gcbb.12005
Spokas, K. A.; Koskinen, W. C.; Baker, J. M.; Reicosky, D. C.
2009. Impacts of woodchip biochar additions on greenhouse
gas production and sorption/degradation of two herbicides
in a Minnesota soil, Chemosphere 77(4): 574–581.
https://doi.org/10.1016/j.chemosphere.2009.06.053
Spokas, K. A.; Reicoscoky, D. A. 2009. Impacts of sixteen dif-
ferent biochars on soil greenhouse gas production, Annals of
Environmental Science 3(4): 179–193.
Steiner, C.; Das, K. C.; Melear, N.; Lakly, D. 2010. Reducing ni-
trogen loss during poultry litter composting using biochar,
Journal of Environmental Quality 39(4): 1236–1242.
https://doi.org/10.2134/jeq2009.0337
Steiner, C.; Melear, N.; Harris, K.; Das, K. C. 2011. Biochar as
bulking agent for poultry litter composting, Carbon Manage-
ment 2(3): 227–230. https://doi.org/10.4155/cmt.11.15
Steudler, P.; Bowden, R.; Melillo, J.; Aber, J. 1989. Inuence of
nitrogen fertilization on methane uptake in temperate forest
soils, Nature 341: 314–316. https://doi.org/10.1038/341314a0
Stieglmeier, M.; Mooshammer, M.; Kitzler, B.; Wanek, W.; Zech-
meister-Boltenstern, S.; Richter, A. Schleper, C. 2014. Aero-
bic nitrous oxide production through N-nitrosating hybrid
formation in ammonia-oxidizing archaea, ISME Journal 8(5):
1135–1146. https://doi.org/10.1038/ismej.2013.220
Subedi, R.; Kammann, C.; Pelissetti, S.; Taupe, N.; Bertora, C.;
Monaco, S.; Grignani, C. 2015. Does soil amended with bio-
char and hydrochar reduce ammonia emissions following the
application of pig slurry?, European Journal of Soil Science
66(6): 1044–1053. https://doi.org/10.1111/ejss.12302
Subedi, R.; Taupe, N.; Pelissetti, S.; Petruzzelli, L.; Bertora, C.;
Leahy, J. J.; Grignani, C. 2016. Greenhouse gas emissions and
soil properties following amendment with manure-derived
biochars: Inuence of pyrolysis temperature and feedstock
type, Journal of Environmental Management 166: 73–83.
https://doi.org/10.1016/j.jenvman.2015.10.007
Suddick, E. C.; Six, J. 2013. An estimation of annual nitrous oxide
emissions and soil quality following the amendment of high
temperature walnut shell biochar and compost to a small
scale vegetable crop rotation, Science of the Total Environment
465: 298–307. https://doi.org/10.1016/j.scitotenv.2013.01.094
Sutka, R. L.; Ostrom, N. E.; Ostrom, P. H.; Breznak, J. A.; Gan-
dhi,H.; Pitt, A. J.; Li, F. 2006. Distinguishing nitrous oxide pro-
duction from nitrication and denitrication on the basis of iso-
topomer abundances, Applied and Environmental Microbiology
72(1): 638–644. https://doi.org/10.1128/AEM.72.1.638-644.2006
Taghizadeh-Toosi, A.; Clough, T.; Sherlock, R.; Condron, L.
2012. Biochar adsorbed ammonia is bioavailable, Plant and
Soil 350(1–2): 57–69.
https://doi.org/10.1007/s11104-011-0870-3
Taghizadeh-Toosi, A.; Clough, T. J.; Condron, L. M. Sher-
lock,R.R.; Anderson, C. R.; Craigie, R. A. 2011. Biochar in-
corporation into pasture soil suppresses in situ nitrous oxide
emissions from ruminant urine patches, Journal of Environ-
mental Quality 40(2): 468–476.
https://doi.org/10.2134/jeq2010.0419
Terazawa, K.; Ishizuka, S.; Sakata, T.; Yamada, K.; Takahashi, M.
2007. Methane emissions from stems of Fraxinus mandsh-
urica var. japonica trees in a oodplain forest, Soil Biology
and Biochemistry 39(10): 2689–2692.
https://doi.org/10.1016/j.soilbio.2007.05.013
omazini, A.; Spokas, K.; Hall, K.; Ippolito, J.; Lentz, R.; No-
vak, J. 2015. GHG impacts of biochar: Predictability for the
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 137
same biochar, Agriculture, Ecosystems & Environment 207:
183–191. https://doi.org/10.1016/j.agee.2015.04.012
Toth, J. D.; Dou, Z. 2016. Use and impact of biochar and char-
coal in animal production systems, in M. Guo, Z. He, S. M.
Uchimiya. (Eds.). Agricultural and environmental applications
of biochar: advances and barriers. Madison, WI: Soil Science
Society of America, Inc.
https://doi.org/10.2136/sssaspecpub63.2014.0043.5
Totusek, R.; Beeson, W. 1953. e nutritive value of wood char-
coal for pigs, Journal of Animal Science 12(2): 271–281.
https://doi.org/10.2527/jas1953.122271x
Troy, S. M.; Lawlor, P. G.; O’ Flynn, C. J.; Healy, M. G. 2013. Im-
pact of biochar addition to soil on greenhouse gas emissions
following pig manure application, Soil Biology and Biochemis-
try 60: 173–181. https://doi.org/10.1016/j.soilbio.2013.01.019
Turetsky, M. R.; Kotowska, A.; Bubier, J.; Dise, N. B.; Crill,P.;
Hornibrook, E. R.; Minkkinen, K.; Moore, T. R.; Myers‐
Smith, I. H.; Nykänen, H. 2014. A synthesis of methane
emissions from 71 northern, temperate, and subtropi-
cal wetlands, Global Change Biology 20(7): 2183–2197.
https://doi.org/10.1111/gcb.12580
Turner, P. A.; Gris, T. J.; Lee, X.; Baker, J. M.; Venterea, R. T.;
Wood, J. D. 2015. Indirect nitrous oxide emissions from
streams within the US Corn Belt scale with stream order,
Proceedings of the National Academy of Sciences 112(32):
9839–9843. https://doi.org/10.1073/pnas.1503598112
Van Der Zee, F. P.; Cervantes, F. J. 2009. Impact and application
of electron shuttles on the redox (bio) transformation of con-
taminants: a review, Biotechnology Advances 27(3): 256–277.
https://doi.org/10.1016/j.biotechadv.2009.01.004
Van Groenigen, K. J.; Osenberg, C. W.; Hungate, B. A. 2011.
Increased soil emissions of potent greenhouse gases under
increased atmospheric CO2, Nature 475(7355): 214–216.
https://doi.org/10.1038/nature10176
Van Zwieten, L.; Kammann, C. I.; Cayuela, M. L.; Singh, B. P.; Jo-
seph, S.; Kimber, S.; Donne, S.; Clough, T. J.; Spokas, K. 2015.
Biochar eects on nitrous oxide and methane emissions from
soil, in J. Lehmann, S. Joseph (Eds.). Biochar for environmen-
tal management – science, technology and implementation.
2ed. New York: Routledge.
Van Zwieten, L.; Singh, B.; Joseph, S. D.; Kimber, S.; Cowie, A.;
Chan, K. Y. 2009. Biochar and the emissions of non-CO2
greenhouse gases from soil, in J. Lehmann, S. Joseph (Eds.).
Biochar for environmental management, science and technol-
ogy. London: Earthscan.
Vandecasteele, B.; Sinicco, T.; D’hose, T.; Vanden Nest, T.; Mon-
dini, C. 2016. Biochar amendment before or aer compost-
ing aects compost quality and N losses, but not P plant
uptake, Journal of Environmental Management 168: 200–209.
https://doi.org/10.1016/j.jenvman.2015.11.045
Volkmann, A. 1935. Behandlungsversuche der Kaninchen-bzw.
Katzencoccidiose mit Viscojod und Carbo medicinalis “Merck”:
Doctoral esis. University of Leipzig.
Vongsamphanh, P.; Napasirth, V.; Inthapanya, S.; Preston, T.
2015. Eect of biochar and leaves from sweet or bitter cas-
sava on gas and methane production in an in vitro rumen
incubation using cassava root pulp as source of energy, Live-
stock Research for Rural Development 27(04) [online], [cited
28 December 2016]. Available from Internet: http://www.lrrd.
org/lrrd27/4/phan27072.html
Walter, K. M.; Zimov, S. A.; Chanton, J. P.; Verbyla, D.;
Chapin, F. S. 2006. Methane bubbling from Siberian thaw
lakes as a positive feedback to climate warming, Nature
443(7107): 71–75. https://doi.org/10.1038/nature05040
Wang, Z.; Zheng, H.; Luo, Y.; Deng, X.; Herbert, S.; Xing, B.
2013a. Characterization and inuence of biochars on ni-
trous oxide emission from agricultural soil, Environmen-
tal Pollution 174: 289–296. https://doi.org/10.1016/j.en-
vpol.2012.12.003
Wang, C.; Lu, H.; Dong, D.; Deng, H.; Strong, P. J.; Wang, H.;
Wu, W. 2013b. Insight into the eects of biochar on manure
composting: evidence supporting the relationship between
N2O emission and denitrifying community, Environmental
Science & Technolog y 47(13): 7341–7349.
https://doi.org/10.1021/es305293h
Wang, Y.; Xue, M.; Zheng, X.; Ji, B.; Du, R.; Wang, Y. 2005. Ef-
fects of environmental factors on N2O emission from and
CH4 uptake by the typical grasslands in the Inner Mongolia,
Chemosphere 58(2): 205–215.
https://doi.org/10.1016/j.chemosphere.2004.04.043
Ward, B. J.; Yacob, T. W.; Montoya, L. D. 2014. Evaluation of solid
fuel char briquettes from human waste, Environmental Sci-
ence and Technology 48(16): 9852–9858.
https://doi.org/10.1021/es500197h
Wells, N. S.; Baggs, E. M. 2014. Char amendments impact
soil nitrous oxide production during ammonia oxidation,
Soil Science Society of America Journal 78(5): 1656–1660.
https://doi.org/10.2136/sssaj2013.11.0468n
Whalen, S. C. 2005. Biogeochemistry of methane exchange be-
tween natural wetlands and the atmosphere, Environmental
Engineering Science 22(1): 73–94.
https://doi.org/10.1089/ees.2005.22.73
Wollenberg, E.; Richards, M.; Smith, P.; Havlík, P.; Oberstein-
er,M.; Tubiello, F. N.; Herold, M.; Gerber, P.; Carter, S.;
Reisinger, A.; Van Vuuren, D. P.; Dickie, A.; Neufeldt, H.;
Sander,B.O.; Wassmann, R.; Sommer, R.; Amonette, J. E.;
Falcucci, A.; Herrero, M.; Opio, C.; Roman-Cuesta, R. M.;
Stehfest, E.; Westhoek, H.; Ortiz-Monasterio, I.; Sapkota,T.;
Runo, M. C.; ornton, P. K.; Verchot, L.; West, P. C.; Sous-
sana, J.-F.; Baedeker, T. Sadler, M.; Vermeulen, S.; Camp-
bell,B. M. 2016. Reducing emissions from agriculture to
meet the 2°C target, Global Change Biology 22(12): 3859–
3864. https://doi.org/10.1111/gcb.13340
Wrage, N.; Velthof, G. L.; Van Beusichem, M. L. Oenema, O.
2001. Role of nitrier denitrication in the production of ni-
trous oxide, Soil Biology and Biochemistry 33(12–13): 1723–
1732. https://doi.org/10.1016/S0038-0717(01)00096-7
Xie, Z.; Xu, Y.; Liu, G.; Liu, Q.; Zhu, J.; Tu, C.; Amonette, J. E.;
Cadisch, G.; Yong, J. W.; Hu, S. 2013. Impact of biochar ap-
plication on nitrogen nutrition of rice, greenhouse-gas emis-
sions and soil organic carbon dynamics in two paddy soils of
China, Plant and Soil 370(1–2): 527–540.
https://doi.org/10.1007/s11104-013-1636-x
Yanai, Y.; Toyota, K.; Okazaki, M. 2007. Eects of charcoal addi-
tion on N2O emissions from soil resulting from rewetting air-
dried soil in short-term laboratory experiments, Soil Science
and Plant Nutrition 53(2): 181–188.
https://doi.org/10.1111/j.1747-0765.2007.00123.x
Yoo, G.; Kang, H. 2012. Eects of biochar addition on green-
house gas emissions and microbial responses in a short-term
laboratory experiment, Journal of Environmental Quality
41(4): 1193–1202. https://doi.org/10.2134/jeq2011.0157
C. Kammann et al. Biochar as a tool to reduce the agricultural greenhouse-gas burden – knowns, unknowns...
138
Yu, L.; Yuan, Y.; Tang, J.; Wang, Y.; Zhou, S. 2015. Biochar as
an electron shuttle for reductive dechlorination of penta-
chlorophenol by Geobacter sulfurreducens, Scientic Reports
5(16221). https://doi.org/10.1038/srep16221
Yu, L. Q.; Tang, J.; Zhang, R. D.; Wu, Q. H.; Gong, M. M. 2013.
Eects of biochar application on soil methane emission at
dierent soil moisture levels, Biology and Fertility of Soils
49(2): 119–128.
https://doi.org/10.1007/s00374-012-0703-4
Zhang, A.; Bian, R.; Pan, G.; Cui, L.; Hussain, Q.; Li, L.; Zheng,J.;
Zheng, J.; Zhang, X.; Han, X.; Yu, X. 2012. Eects of biochar
amendment on soil quality, crop yield and greenhouse gas
emission in a Chinese rice paddy: a eld study of 2 consecu-
tive rice growing cycles, Field Crops Research 127: 153–160.
https://doi.org/10.1016/j.fcr.2011.11.020
Zhang, A.; Cui, L.; Pan, G.; Li, L.; Hussain, Q.; Zhang, X.;
Zheng,J.; Crowley, D. 2010. Eect of biochar amendment on
yield and methane and nitrous oxide emissions from a rice
paddy from Tai Lake plain, China, Agriculture, Ecosystems&
Environment 139(4): 469–475. https://doi.org/10.1016/j.
agee.2010.09.003
Zum, W. G. 1997. Cell biology and molecular basis of denitri-
cation, Microbiology and Molecular Biology Reviews 61(4):
533–616.
Claudia KAMMANN. PhD, Professor for Climate Change Research for Special Crops, Institute for Soil Science and Plant
Nutrition, Hochschule Geisenheim University, Geisenheim, Germany, 58 peer-reviewed articles in scientic journals, 7
book chapters, 2453 citations, h-index 27 (Google Scholar).
Jim IPPOLITO. PhD, Associate Professor in the Department of Soil and Crop Sciences, Colorado State University, Fort
Collins, CO, USA. 170 publications in peer reviewed scientic publications, book chapters, conference reports, and experi-
ment station technical reports and bulletins. 2099 citations, h-index 24 (Google Scholar).
Nikolas HAGEMANN. PhD, Nikolas Hagemann, PhD. Researcher at University of Tuebingen, Germany. 2 peer-reviewed
articles, 5 book chapters, 16 citations, h-index 3 (Google Scholar).
Nils BORCHARD. PhD, Soil Science Expert at the Center for International Forestry Research (CIFOR), Jalan CIFOR,
16115 Bogor Barat, Indonesia and at the Deprtament of Soil Science and Soil Ecology, Institute of Geography, Ruhr-
University of Bochum, Universitätsstr. 150, 44801 Bochum, Germany. 15 peer reviewed publications, 3 non-peer reviewed
publication, 156 citations, h-index 7 (WoS).
Maria Luz CAYUELA. PhD, is a researcher at the National Research Council in Spain. She has published 40 articles in
peer- reviewed journals and 6 book chapters. 2046 citations, h-index 24. (Google Scholar)
José M. ESTAVILLO. PhD, Professor of Plant Physiology, Faculty of Science and Technology, University of the Basque
Country/EHU, Spain, 40 peer-reviewed articles in scientic journals, 783 citations, h-index 15 (WoS).
Teresa FUERTES-MENDIZABAL. PhD, Researcher, Faculty of Science and Technology, University of the Basque Coun-
try/EHU, Spain, 9 peer-reviewed articles in scientic journals, 71 citations, h-index 5 (WoS).
Simon JEFFERY. PhD, Senior Lecturer in Sustainable Technology. Crop and Environment Sciences Department, Harper
Adams University, Newport, Shropshire, TF10 8NB. United Kingdom. 24 peer reviewed articles in scientic journals, 3
policy reports to the European Commission. Editor of two atlases (including lead editor of one), 3 book chapters. 1768
citations, h-index 15 (Google Scholar).
Jürgen KERN. PhD, Senior Scientist of Biogeochemistry, Leibniz Institute for Agricultural Engineering Potsdam-Bornim,
Germany, 1211 citations, h-index 16 (Google Scholar).
Je NOVAK. PhD, Research Soil Scientist, in the United States Department of Agriculture, Agriculture Research Service-
Coastal Plains Research Center, Florence, South Carolina, USA. 150 publications in peer reviewed scientic publications,
book chapters, and conference reports. 4130 citations; h-index 26 (Scopus).
Daniel RASSE. PhD, Senior Scientist and Head of the Department for Soil Quality and Climate Change at the Norwegian
Institute of Bioeconomy Research, Aas, Norway, 55 peer-reviewed articles in scientic journals, 2948 citations, h-index
25 (Scopus).
Sanna SAARNIO. PhD, Lecturer in the Department of Environmental and Biological Sciences, University of Eastern
Finland, Finland, 52 peer-reviewed articles in scientic journals or books, 1400 citations, h-index 20 (WoS).
Journal of Environmental Engineering and Landscape Management, 2017, 25(2): 114–139 139
Hans-Peter SCHMIDT. Director of Ithaka Institute for Carbon Strategies, Arbaz, Switzerland, 16 peer-reviewed articles,
9 book chapters, 259 citations, h-index 9 (google scholar).
Kurt SPOKAS. PhD, Research Soil Scientist with the United States Department of Agriculture-Agricultural Research
Service, Soil and Water Management Laboratory, 1991 Upper Buford Circle, St. Paul, MN 55108. He has produced over
200 scientic publications in peer reviewed journals, book chapters, conference proceedings, and bulletins. 4904 citations;
h-index 31 (google scholar).
Nicole WRAGE-MÖNNIG. PhD, Professor of Grassland and Forage Sciences, Faculty of Agricultural and Environmental
Sciences, University of Rostock, Germany, 45 peer-reviewed articles in scientic journals, 6 monographs and book chap-
ters, 1968 citations, h-index 18 (WoS).
