Agriculture,
Ecosystems
and
Environment
160 (2012) 15–
22
Contents
lists
available
at
ScienceDirect
Agriculture,
Ecosystems
and
Environment
j o
u r
n
a l
h o m e p a g e :
w w w . e l s e v i e r . c o m / l o
c a t e / a g e e
Chemical
properties
of
anaerobic
digestates
affecting
C
and
N
dynamics
in
amended
soils
José
Antonio
Alburquerque
∗
,
Carlos
de
la
Fuente,
María
Pilar
Bernal
Department
of
Soil
and
Water
Conservation
and
Organic
Waste
Management,
Centro
de
Edafología
y
Biología
Aplicada
del
Segura,
CSIC,
P.O.
Box
164,
30100
Murcia,
Spain
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
11
October
2010
Received
in
revised
form
1
March
2011
Accepted
14
March
2011
Available online 8 April 2011
Keywords:
Anaerobic
digestion
Animal
slurries
Organic
matter
mineralisation
Biodegradability
Nitrogen
immobilisation
a
b
s
t
r
a
c
t
The
optimisation
of
digestate
recycling
as
fertilisers,
based
on
both
environmental
and
agricultural
crite-
ria,
requires
an
evaluation
of
the
effects
on
C
and
N
dynamics
in
soil.
In
the
present
paper,
six
digestates
from
several
anaerobic
co-digestion
experiments,
using
pig
or
cattle
slurry
as
the
main
substrate,
were
evaluated
in
short-term
incubations
in
soil.
Digestate
properties
such
as
dissolved
organic-C
(DOC),
biochemical
oxygen
demand
(BOD)
and
digestate
organic-C
mineralised
in
the
soil
during
the
first
7
days
represented
properly
the
digestate
biodegradability.
These,
together
with
their
ratios
with
respect
to
the
total
nitrogen
(TN)
concentration
in
the
digestate,
were
reliable
parameters
with
respect
to
defining
the
C
and
N
dynamics
in
the
soil
and
hence
the
N-fertiliser
potential
of
the
digested
materials.
Therefore,
highly
biodegradable
digested
materials,
represented
in
the
present
study
by
digestates
from
cattle
slurry–glycerine
mixtures
were
not
suitable
for
agricultural
use
as
they
caused
a
high
CO
2
–C
production
and
led
to
N-immobilisation
and/or
denitrification
after
their
application
to
soil.
Contrastingly,
for
less
biodegradable
digested
mate-
rials
(BOD
5
d
<
6.0
g
O
2
L
−1
fresh
weight,
DOC
<
5.5
g
L
−1
fresh
weight
and
DOC/TN
<
1.5),
less
CO
2
–C
was
evolved
and
ammonium
was
rapidly
nitrified
in
soil—being
an
available
N
source
for
crops.
© 2011 Elsevier B.V. All rights reserved.
1.
Introduction
Nowadays,
there
is
increasing
interest
in
Europe
in
the
imple-
mentation
of
anaerobic
digestion
in
productive
sectors
such
as
livestock
and
agroindustry,
where
vast
amounts
of
biodegradable
wastes
(animal
manure
and
slurries,
agricultural
and
food
industry
wastes,
etc.)
must
be
adequately
managed,
due
to
the
demand
for
renewable
energy.
Co-digestion
can
enhance
the
energy
produc-
tion
from
animal
manure
and
slurries,
as
co-digestible
materials
such
as
slaughterhouse
wastes,
glycerine
and
energy
crops
or
silage
can
increase
the
amount
of
biodegradable
organic
matter,
dilute
potential
toxic
compounds,
improve
the
nutrient
balance
and
favour
synergistic
effects
of
microorganisms,
thereby
raising
biogas
production
(
Álvarez
et
al.,
2010;
Holm-Nielsen
et
al.,
2009;
Pesta,
2007
).
However,
the
sustainability
of
biogas
production
also
depends
on
an
appropriate
end-use
of
the
digested
material
(digestate)—which
should
be
treated,
disposed
of
or
re-used
in
a
proper
way,
avoiding
any
negative
environmental
impact.
The
use
of
digestates
as
organic
fertilisers
in
agricultural
sys-
tems
seems
the
best
option
for
their
recycling
since
they
contain
considerable
amounts
of
residual
organic-C
and
plant
nutrients.
∗ Corresponding
author.
Tel.:
+34
968
396200;
fax:
+34
968
396213.
E-mail
addresses:
jalburquerque@cebas.csic.es
,
jalburquerquemendez@yahoo.es
(J.A.
Alburquerque).
Digestates
also
present
advantages
in
comparison
with
untreated
waste,
such
as
greater
microbial
stability
and
hygiene
and
a
higher
amount
of
N
present
as
ammonium
(
Al
Seadi,
2002;
Holm-Nielsen
et
al.,
2009
).
So,
land
spreading
of
digestate
can
lead
to
benefits
if
integrated
into
good
agricultural
practices,
by
controlling
the
N
application
rate
and
heavy
metal
load,
and
by
securing
digestate
hygiene
(
Al
Seadi,
2002;
Fuchs
et
al.,
2008;
Holm-Nielsen
et
al.,
2009
).
Nevertheless,
the
biodegradability
of
these
materials,
which
determines
organic
matter
(OM)
mineralisation
and
thus
nutrient
turnover
in
soil,
is
not
well
characterised.
The
complete
exhaustion
of
the
most
labile
organic
fraction
during
the
anaerobic
process,
in
order
to
obtain
digestates
with
a
high
stability
degree,
is
not
easy
to
achieve
at
the
industrial
level,
the
main
objective
of
the
anaerobic
co-digestion
being
the
pro-
duction
of
a
high
rate
of
biogas,
rich
in
methane.
This
process
is
conditioned
mainly
by
the
composition
of
the
raw
materials
and
the
development
of
the
anaerobic
process,
leading
in
some
cases
to
the
production
of
unstable
digested
materials
which
may
exert
negative
impacts
on
the
plant–soil
system
(
Abdullahi
et
al.,
2008;
Salminen
et
al.,
2001
).
In
this
context,
aerobic
respiration
indices
based
on
oxygen
uptake
are
considered
the
most
suitable
param-
eters
for
assessing
the
biodegradability
of
organic
amendments
(
Barrena
et
al.,
2006;
Copperband
et
al.,
2003
).
In
wastewaters
and
animal
slurries
the
biochemical
oxygen
demand
(BOD)
test
is
a
reliable
and
commonly
used
method
to
determine
readily
biodegradable
OM
(
APHA,
2005;
Brookman,
1997;
Williams,
1983
).
0167-8809/$
–
see
front
matter ©
2011 Elsevier B.V. All rights reserved.
doi:
10.1016/j.agee.2011.03.007
16
J.A.
Alburquerque
et
al.
/
Agriculture,
Ecosystems
and
Environment
160 (2012) 15–
22
Although
there
is
no
threshold
value
established
as
a
stability
and
quality
criterion
for
the
agricultural
use
of
waste
materials
based
on
BOD
data,
it
is
possible
with
some
caution
to
compare
it
with
the
limits
established
in
the
solid
waste
field
based
on
oxygen
uptake
rate
and/or
cumulative
oxygen
consumption
indices.
Dif-
ferent
methodologies
for
characterising
the
biological
stability
of
organic
materials
have
been
used,
such
as
SOUR
(specific
oxygen
uptake
rate
as
the
maximum
rate
of
oxygen
consumption),
OD
20
h
(cumulative
oxygen
demand
for
the
first
20
h
of
the
test;
Lasaridi
and
Stentiford,
1998
)
and
DRI
24
h
(dynamic
respiration
index,
which
is
the
average
oxygen
uptake
rate
at
24
h
of
maximum
biological
activity;
Adani
et
al.,
2004
).
Also,
little
information
is
available
about
the
degree
of
stabil-
ity
of
digestates
and
their
C
and
N
dynamics
in
amended
soils
(
Sánchez
et
al.,
2008;
Tambone
et
al.,
2009
).
The
information
gained
from
decomposition
studies
in
digestate-treated
soil
(OM
mineral-
isation,
N
mineralisation–immobilisation,
etc.)
may
be
useful
for
assessing
N
availability,
and
for
optimising
the
digestate
applica-
tion
rate
to
agricultural
soils.
Thus,
defining
the
main
digestate
properties
affecting
such
C
and
N
dynamics
in
soil
can
help
achieve
the
sustainable
use
of
digestates
as
fertilisers
in
soil–plant
system,
which
will
have
both
agricultural
and
environmental
benefits.
The
present
paper
evaluates
the
dynamics
of
C-mineralisation
and
inorganic-N
in
soil
amended
with
six
digestates
produced
from
representative
anaerobic
co-digestion
processes
in
Spain.
These
effects
were
investigated
in
aerobic
incubation
experiments,
an
appropriate
tool
to
evaluate
the
feasibility
of
the
use
of
organic
amendments
in
agricultural
soils
(
Qiu
et
al.,
2008;
Trinsoutrot
et
al.,
2000
).
Based
on
these
considerations,
the
main
objective
of
this
paper
is
to
identify
the
most
relevant
parameters
related
to
digestate
composition
for
assessing
the
maximum
benefits
of
these
materials
as
fertilisers.
2.
Materials
and
methods
2.1.
Incubation
experiments
in
soil
Six
digestates
were
collected
as
representative
samples
from
anaerobic
co-digestion
experiments
based
on
cattle
or
pig
slurry
mixed
with
agro-industrial
wastes
(co-digestion
mixtures):
cat-
tle
slurry
+
4%
glycerine
(CG4),
cattle
slurry
+
6%
glycerine
(CG6),
cattle
slurry
+
4.3%
cattle
manure
+
11.6%
maize–oat
silage
(CMS),
cattle
slurry
+
5%
orange
peel
waste
(CO),
pig
slurry
+
1.0%
sludge
from
a
slaughterhouse
wastewater
treatment
plant
+
6.5%
biodiesel
wastewaters
(PSB),
and
pig
slurry
+
0.6%
pasteurised
slaughter-
house
waste
(PS).
Digestates
were
sampled
directly
after
anaerobic
digestion
(without
post-treatments),
stored
at
a
temperature
<4
◦
C
and
processed
quickly
to
prevent
any
chemical
or
biological
alter-
ation.
Their
main
characteristics
and
the
specifications
of
anaerobic
co-digestion
performance
are
shown
in
Table
1
.
CMS
and
PSB
sam-
ples
came
from
industrial-scale
co-digestion
processes,
while
the
rest
of
the
samples
came
from
laboratory-scale
experiments,
run
mainly
to
optimise
the
production
of
biogas
through
anaerobic
co-digestion.
From
an
agricultural
soil
at
La
Alberca
(Murcia,
Spain),
soil
was
taken
from
the
top
20
cm,
air-dried
and
sieved
to
2
mm
before
use.
Its
main
characteristics
were:
24%
CaCO
3
,
pH
7.5
and
electrical
conductivity
(EC)
1.72
dS
m
−1
(both
saturated
paste,
with
water),
24.3
g
kg
−1
OM,
14.1
g
kg
−1
total
organic-C
(TOC)
and
1.85
g
kg
−1
total
nitrogen
(TN),
with
14.8%
clay,
22.3%
silt
and
62.9%
sand.
The
digested
materials
were
mixed
thoroughly
with
the
soil
in
a
proportion
of
4
g
of
fresh
digestate
per
100
g
of
dry
soil
(equiva-
lent
to
a
field
application
of
96
m
3
ha
−1
).
This
application
rate
was
selected
in
order
to
avoid
excessively
low
inputs
of
organic-C
to
the
soil
with
some
digestate
samples,
which
could
limit
the
accu-
racy
of
the
C-mineralisation
study,
while
keeping
the
N
addition
(140–380
kg
N
ha
−1
)
realistic
for
the
requirements
of
agricultural
crops
(
MARM,
2010
).
The
digestate-soil
mixtures
were
incubated
in
darkness
under
aerobic
conditions,
at
26
±
1
◦
C
for
56
days.
Each
treatment
was
run
in
triplicate,
and
soil
without
digestate
was
used
as
the
control.
Soil
moisture
was
maintained
at
60%
of
the
water-holding
capac-
ity
during
incubation,
with
deionised
water.
To
follow
N
dynamics,
a
set
of
destructive
samples
of
the
digestate-soil
mixtures
were
placed
in
50-mL
tubes
without
drainage
holes;
then,
they
were
closed
with
parafilm
–
which
allows
gas
exchange
–
to
retain
soil
moisture
and
avoid
anaerobic
conditions
(
de
la
Fuente
et
al.,
2010
).
Periodically,
three
replicates
per
treatment
were
removed
from
the
incubator
(at
0,
2,
7,
14,
28,
42
and
56
days)
for
analysis
of
inorganic-
N
(NH
4
–N
and
NO
3
–N).
Since
the
digestate
samples
were
mixed
homogeneously
with
the
soil
at
the
time
of
application
and
there
was
no
airflow
at
the
soil
surface
during
incubation,
N-loss
through
volatilisation
was
negligible—as
demonstrated
by
de
la
Fuente
et
al.
(2010)
.
Net
organic-N
mineralisation
was
evaluated
by
the
accu-
Table
1
Main
characteristics
of
the
digestate
samples
(mean
value
±standard
deviation,
data
expressed
on
a
fresh
weight
basis).
Parameter
CG4
CG6
CMS
CO
PSB
PS
BOD
24
h
(g
L
−1
)
7.5
±
1.5
35.0
±
3.0
1.6
±
0.2
0.5
±
0.1
0.7
±
0.1
1.1
±
0.1
BOD
5
d
(g
L
−1
)
37.5
±
3.5
52.5
±
3.5
5.9
±
0.7
1.3
±
0.1
2.2
±
0.2
2.3
±
0.2
pH
5.64
±
0.01
7.35
±
0.03
7.50
±
0.01
7.86
±
0.01
8.20
±
0.02
7.95
±
0.03
EC
(dS
m
−1
)
14.5
±
0.3
11.7
±
0.2
25.7
±
0.8
8.7
±
0.2
30.3
±
0.9
21.1
±
0.1
DM
(g
L
−l
)
38.3
±
0.5
72.9
±
5.8
90.1
±
0.2
24.4
±
0.3
19.5
±
0.1
21.0
±
2.4
OM
(g
L
−l
)
26.4
±
0.1
56.4
±
0.9
66.4
±
0.2
18.0
±
0.1
8.5
±
0.1
11.4
±
0.2
TOC
(g
L
−l
)
17.8
±
0.1
42.8
±
0.1
33.7
±
0.5
9.4
±
0.1
5.9
±
0.1
5.8
±
0.1
DOC
(g
L
−l
)
10.6
±
0.3
27.6
±
0.9
5.4
±
0.1
1.2
±
0.1
2.4
±
0.1
1.2
±
0.1
TN
(g
L
−l
)
1.88
±
0.02
2.32
±
0.07
3.97
±
0.02
1.44
±
0.01
3.96
±
0.03
2.89
±
0.02
NH
4
–N
(g
L
−l
)
0.97
±
0.03
0.89
±
0.01
2.43
±
0.01
0.76
±
0.01
3.46
±
0.04
2.21
±
0.01
TOC/TN
ratio
9.5
±
0.1
18.5
±
0.5
8.5
±
0.1
6.6
±
0.1
1.5
±
0.1
2.0
±
0.1
Anaerobic
co-digestion
performance
Operation
Discont
Discont
Cont
Discont
Cont
Cont
Scale
L
L
I
L
I
L
Temperature
(
◦
C)
35
35
38.5
38
37
35
HRT
(days)
40
40
25
28
21
20
BOD
24
h
and
BOD
5
d
:
24-h
and
5-d
biochemical
oxygen
demand,
respectively.
EC:
electrical
conductivity,
DM:
dry
matter,
OM:
total
organic
matter,
TOC:
total
organic-C,
DOC:
dissolved
organic-C
and
TN:
total
nitrogen.
Discont:
discontinuous
operation,
Cont:
continuous
operation,
L:
laboratory-scale
(2–6
L
digester),
I:
industrial-scale
(3000
m
3
digester)
and
HRT:
hydraulic
residence
time
CG4:
cattle
slurry
+
4%
glycerine,
CG6:
cattle
slurry
+
6%
glycerine,
CMS:
cattle
slurry
+
4.3%
cattle
manure
+
11.6%
maize–oat
silage,
CO:
cattle
slurry
+
5%
orange
peel
waste,
PSB:
pig
slurry
+
1.0%
sludge
from
a
slaughterhouse
wastewater
treatment
plant
+
6.5%
biodiesel
wastewaters,
and
PS:
pig
slurry
+
0.6%
pasteurised
slaughterhouse
waste.
J.A.
Alburquerque
et
al.
/
Agriculture,
Ecosystems
and
Environment
160 (2012) 15–
22
21
ages
of
TN
as
NH
4
–N
(>50%),
which
improve
the
soil
N
balance
(44
and
59%
of
added
TN
for
CO
and
PS,
respectively,
was
converted
into
nitrate
with
low
N-immobilisation),
representing
an
available
N
source
for
plants.
Based
on
the
characteristics
of
such
diges-
tates,
DOC
<
1.5
g
L
−1
(<25%
of
TOC),
BOD
5
d
<
2.5
g
L
−1
,
C
m
<
35%
and
DOC/TN
<
1
can
be
used
to
define
a
high
quality
digestate
appropri-
ate
for
use
as
a
fertiliser.
The
characteristics
of
the
PSB
and
CMS
digestates
showed
a
higher
similarity
to
CO
and
PS
(stable
digested
materials)
than
to
the
CG
samples
(highly
unstable).
The
PSB
sample
showed
a
relatively
low
BOD
5
d
value,
in
accordance
with
its
low
TOC
content
(5.9
g
L
−1
fresh
weight);
however,
it
was
highly
labile
(41%
of
TOC
as
DOC)
and
had
the
highest
percentage
of
TN
as
NH
4
–N
(87%).
This,
combined
with
its
low
DOC/TN
ratio
(0.6),
could
explain
the
observed
priming
effect
on
C-mineralisation
when
PSB
was
added
to
soil;
however,
negative
effects
on
the
soil
N
dynamic
were
not
seen.
Finally,
the
CMS
sample
showed
an
acceptable
degree
of
stability
considering
its
much
higher
organic
load
relative
to
CO
and
PS
(33.7
g
TOC
L
−1
fresh
weight,
only
16%
as
DOC);
however,
it
showed
a
relatively
high
CO
2
–C
production
at
the
end
of
the
incubation,
similar
to
that
resulting
from
CG4
addition
to
soil.
The
CMS
sample
had
a
DOC/TN
ratio
of
1.4
with
61%
of
its
TN
as
NH
4
–N,
leading
to
a
percentage
conversion
of
TN
into
nitrate
of
about
50%.
Therefore,
digestate
properties
such
as
DOC
<
5.5
g
L
−1
(<45%
of
TOC),
BOD
5
d
<
6.0
g
L
−1
and
DOC/TN
<
1.5
can
be
established
as
less
restrictive
quality
cri-
teria
compared
with
those
defined
previously
for
stable
digested
materials.
The
suitable
land
application
of
these
digestates
may
require
some
precautions
depending
on
the
land
use
and
manage-
ment.
A
curing
or
maturation
period
may
be
necessary
in
order
to
increase
digestate
stability
or
to
allow
digestates
to
stabilise
in
soil
before
sowing.
4.
Conclusions
Our
results
demonstrate
that
digestate
composition
and
stabil-
ity
degree
can
vary
greatly
depending
on
the
raw
materials
used
for
co-digestion
and
process
characteristics.
Therefore,
the
anaerobic
co-digestion,
including
the
selection
of
co-substrates,
must
guaran-
tee
that
a
certain
degree
of
OM
stability
of
the
digested
material
is
reached
in
order
to
avoid
detrimental
effects
on
the
plant–soil
sys-
tem.
These
are
mainly
conditioned
by
the
biodegradability
of
the
digested
material
obtained,
which
determines
whether
the
diges-
tate
can
be
used
directly
(highly
stable),
after
a
curing/maturation
period
(moderately
stable)
or
after
aerobic
post-treatments
to
achieve
stabilisation
(highly
unstable).
In
this
context,
the
biochemical
oxygen
demand
(BOD
24
h
or
BOD
5
d
),
dissolved
organic-C
(DOC)
together
with
the
DOC/TN
can
be
considered
the
most
reliable
parameters
to
describe
digestate
biodegradability
and
hence
provide
a
quick
estimation
of
the
main
effects
on
C
and
N
turnover
produced
by
digestate
addition
to
soil.
Highly
unstable
and
easily
biodegradable
materials,
represented
in
our
study
by
digestate
from
cattle
slurry–glycerine
mixtures
(BOD
5
d
>
37
g
O
2
L
−1
fresh
weight,
DOC
>
10
g
L
−1
fresh
weight
and
DOC/TN
>
5),
gave
rise
to
a
strong
CO
2
–C
production
and
a
loss
of
N-fertiliser
value
through
N-immobilisation
in
soil.
These
materials
need
more
extensive
biological
treatment,
such
as
aerobic
stabilisa-
tion,
in
order
to
reduce
potential
detrimental
impacts.
In
contrast,
ammonium
in
the
more
stable
digested
materials
was
oxidised
by
nitrifiers
in
the
very
short
term.
These
less
biodegradable
digested
materials
(BOD
5
d
<
6.0
g
O
2
L
−1
fresh
weight,
DOC
<
5.5
g
L
−1
fresh
weight
and
DOC/TN
<
1.5)
showed
a
scaled
degree
of
stability,
from
highly
stabilised
materials,
which
can
be
used
directly
in
soils
as
fertilisers,
to
moderately
stabilised
materials,
which
may
need
a
curing/maturation
period
or
stabilisation
in
the
soil
before
sowing.
Acknowledgements
This
research
was
funded
by
the
“Ministerio
de
Ciencia
e
Inno-
vación,
Plan
Nacional
I+D+I
2008-2011”
and
FEDER
Funds
“Fondo
Europeo
de
Desarrollo
Regional,
una
manera
de
hacer
Europa”,
in
the
framework
of
the
project
“singular
estratégico
PROBIOGAS”:
sub-project
3
Agronomical
evaluation
of
digestates;
and
subproject
8,
Co-digestion
of
citric
and
farm
residues
(Refs.:
PSS-120000-2008-58;
PSS-120000-2008-62).
The
authors
thank
all
the
research
groups
involved
in
the
project
PROBIOGAS
(
http://www.probiogas.es
),
especially
the
GIRO
and
AINIA
Technological
Centres,
the
Univer-
sity
of
Oviedo,
San
Ramón
Group
and
Treatments
of
Juneda
Society
(Tracjusa)
for
providing
the
digested
materials
used
in
this
work.
The
authors
wish
to
thank
Dr.
D.J.
Walker
for
the
English
revision.
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