Anaerobic digestion and microfiltration of the liquid fraction of pig slurry: N Mineralization, C-CO2 emissions and agricultural value of the products

Vol.:(0123456789)
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Was e and Biomass Valo iza ion
h ps://doi.o g/10.1007/s12649-022-01963-y
ORIGINAL PAPER
Anae obic Diges ion andMic o il a ion o  heLiquid F ac ion o Pig
Slu y: N Mine aliza ion, C‑CO2 Emissions andAg icul u al Value
o  heP oduc s
MiguelFe nández‑Lab ada1 · Ma íaEl i aLópez‑Mosque a2 · Adol oLópez‑Fabal1
Recei ed: 22 May 2022 / Accep ed: 23 Oc obe 2022
© The Au ho (s) 2022
Abs ac
Pig slu y con ains aluable nu ien s and o ganic ma e , al hough i s high wa e con en makes i s managemen and use as
a e ilize mo e expensi e. I is also an in e es ing bioene gy esou ce o biogas p oduc ion. We p opose a ea men ha
consis s o solid–liquid sepa a ion ollowed by he anae obic diges ion o liquid ac ion o slu y (LFS) while a mic o il‑
a ion memb ane module concen a es he solids in he diges e and emo es a liquid ac ion o he diges a e (LFD). The
aims o he wo k we e o e alua e he e ilize alue o he LFS, diges a e and concen a ed diges a e and he possibili y o
eusing he LFD in ag icul u e. The LFS con ained 72% less d y ma e han he slu y. The solid–liquid sepa a ion mainly
emo ed N and P. Thanks o mic o il a ion, he emaining solids we e pa ially eci cula ed o he diges e , concen a ing
he e. To do his, he memb ane module con inuously emo ed he LFD, which was made up o 99% wa e wi h dissol ed
elemen s, mainly C, N, K and Na. The concen a ed diges a e con ained less K, simila amoun s o N and P, and mo e d y
ma e and C han he ini ial LFS. The en i e slu y ea men a ec ed he mine aliza ion dynamics by inc easing ecalci an
C and dec easing labile C wi hou modi ying N elease. The p oposed p ocess allowed aking ad an age o he nu ien s and
s abilized o ganic ma e con ained in he LFS, p oducing a concen a ed diges a e. LFD did no mee he eclaimed wa e
equi emen s. Howe e , i could be use ul as a e i iga ion solu ion and a pos ea men could be enough o comply wi h
he egula ions.
G aphical Abs ac
Keywo ds Modelling· Reclaimed wa e · Solid–liquid sepa a ion· Diges a e· Labile ca bon· Recalci an ca bon
* Adol o López‑Fabal
adol [email p o ec ed]
Ex ended au ho in o ma ion a ailable on he las page o he a icle
Was e and Biomass Valo iza ion
1 3
S a emen o No el y
A new pilo plan o diges he liquid ac ion o slu y was
s udied. Mic o il a ion was used o emo e he wa e om
he diges e and eci cula e he solids. The main no el y o
his s udy lies in he p ocessing o he slu y. While solid‑
liquid sepa a ion is widely s udied, he p oposed ea men
o he liquid ac ion is unusual. This a icle s udies ex en‑
si ely how his new ea men a ec s he adi ional use
o slu y as a e ilize . The amoun , balance and nu ien
elease a e o he p oduced ac ions we e measu ed. Fu ‑
he mo e, i is e alua ed how he p ocess could a ec he C
s ock in he soil. Following he ci cula economy p oduc‑
ion model, he possibili y o using he liquid ac ion o
he diges a e as eclaimed wa e is conside ed.
In oduc ion
Po k mea is la gely p oduced on in ensi e a ms which
gene a e la ge amoun s o pig slu y ha is usually eused
as an o ganic e ilize [1, 2] on he g ounds o i s high
con en s in nu ien s and o ganic ma e . Fo easie han‑
dling, and mo e economical anspo and use, he slu y
is o en spli in o a solid phase and a liquid phase [3]
ha di e in ag onomical alue. Thus, he solid ac ion
con ains mos o he ca bon and nu ien s —in o ganic
o m—, and hence li le mois u e [4], which acili a es
inexpensi e ans e o nu ien s om slu y‑ ich a eas o
nu ien ‑de icien a eas [5]. On he o he hand, he liquid
ac ion consis s mainly o wa e bu addi ionally con ains
subs an ial amoun s o dissol ed elemen s such as N and
K. These cha ac e is ics imp o e he e iciency o he
nu ien s since hey a e p o ided di ec ly in o ms ha can
be assimila ed by he c ops and, u he mo e, by apidly
in il a ing he soil, N losses o he a mosphe e a e educed
[6, 7]. Because o i s high mois u e con en , howe e , he
liquid ac ion o slu y is expensi e o anspo and
apply, which somehow es ic s i s use as a e ilize [8].
The liquid ac ion o slu y can be alo ized by anae o‑
bic diges ion o ob ain biogas and a by‑p oduc (diges a e)
wi h dis inc ag onomic p ope ies. Anae obic diges ion
con e s he mos labile ac ions o o ganic ma e o
CO2 and CH4, he eby inc easing he biological s abili y
o he diges a e and educing i s con en s in o al C and
d y ma e . Du ing he p ocess, N is pa ially mine alized
and accumula es as N‑NH4+, which dec eases he C/N
a io [9–12]. By using only he liquid ac ion, hyd au‑
lic e en ion ime is educed, C emo al is imp o ed, and
he e a e ewe ope a ional p oblems [13–16]. Anae obic
diges ion p o ides addi ional ad an ages such as educing
o ‑odou s [17], pa hogens [11] and g eenhouse gas emis‑
sions [18]; howe e , he esul ing diges a e s ill consis s
mainly o wa e .
One e icien way o concen a ing nu ien s p esen
in slu y diges a es is by il a ion ac oss memb anes and
mic o il a ion is he mos ecommended gi en ha e ain
mos o he nu ien s, a e sca cely p one o clogging, ha e
a high h oughpu and a e ope a ionally inexpensi e [19,
20]. In ac , mic o il a ion can educe biochemical oxygen
demand (BOD) by 76–89%, o al N by 12–38.5%, o al P
by 44.6–75% and o al solids by up o 37% [20, 21]. The
ea men p o ides a concen a ed e luen con aining he
nu ien s in addi ion o was e wa e ha can be used o i i‑
ga ion, indus ial use ( e ige a ion, dus con ol) o u ban
main enance pu poses (ga den i iga ion, s ee hosing) [22].
The eci cula ion o he solid ac ion o he diges a e
has been es ed as a me hod o imp o e he e iciency o he
anae obic diges ion p ocess [23, 24]. Howe e , in no case
ha we know o , he implica ions his p ocess may ha e in
he subsequen euse o he diges a e as e ilize a e s ud‑
ied. Bo h he sepa a ion p ocess and he anae obic diges ion
ea men al e he o al amoun s o C and N, hei a io and
hei chemical dis ibu ion, he eby po en ially modi ying
hei dynamics in soil and hei e ilizing capaci y [25–27].
In ac , he soil dynamics o C and N is in luenced by he
con en s o he wo elemen s and hei a io. Thus, supplying
soil wi h la ge amoun s o labile, easily deg aded C causes
an exponen ial inc ease in mic obial ac i i y. Also, he C/N
a io dic a es whe he N will be p e e en ially mine alized
o immobilized du ing mic obial g ow h [7].
The p ima y aim o his wo k was o iden i y he changes
in composi ion and p ope ies go e ning he po en ial o he
liquid ac ion o pig slu y, and he elemen s o i s anae o‑
bic diges ion and mic o il a ion, as e ilize s. Because
bo h ea men s we e expec ed o al e he composi ion and
C/N a io, we also examined and modelled he mine aliza‑
ion dynamics o he wo elemen s in soil. In addi ion, we e
cha ac e ized he liquid ac ion o he diges a e o assess
i s po en ial use as ecycled wa e (speci ically, i iga ion
wa e ).
Ma e ial andMe hods
Slu y P ocessing Plan
I was used an anae obic diges ion pilo plan loca ed in Cos‑
pei o, Lugo (Galicia, no h‑eas e n Spain). In his wo k, he
plan was exclusi ely used o p ocess he slu y liquid ac‑
ion, which was concen a ed by using a memb ane module
du ing and a e diges ion. The plan comp ised a slu y
ank, a o a ing‑sie e solid–liquid sepa a o o 1mm mesh
(TAGA ATR) and a 4.5 m3 anae obic diges e equipped
Was e and Biomass Valo iza ion
1 3
wi h an helical s i e (TIMSA HRT‑03 17L01) and hea ing
wi es o main ain a cons an empe a u e. The diges e was
ollowed by a mic o il a ion module o syn he ic polyme
memb anes (0.1µm po e size, 6.25 m2 su ace a ea, −15
o −35kPa ansmemb ane p essu e) (TAGA MBR07).
Mic o il a ion was ca ied ou in sequences o 10min o
wo k and 3min o es . Du ing es , a mic obubble di use
sys em used he biogas o c ea e an ai cu en ha d agged
he laye s ha co e he memb anes. This allowed he same
memb ane o be used h oughou he p ocess. A e he mod‑
ule o mic o il a ion, wo anks we e placed o collec he
esul ing ac ions.
Slu y T ea men andF ac ions Ob ained
The slu y (S) was ob ained om a con en ional pig a ‑
ening a m in he icini y o he plan ( he main cha ‑
ac e is ics a e desc ibed in Table2). As equi ed i was
subjec ed o solid–liquid sepa a ion, he esul ing liquid
ac ion (SLF) being ed o an anae obic diges e a a a e
o 0.15–0.40 m3 day−1. The diges e was ope a ed in he
mesophilic ange (37°C), using a hyd aulic e en ion ime
o 10–20days. On an in e mi en basis, a po ion o diges‑
a e (D) in he diges e was ed o he memb ane module o
mic o il a ion se e al imes a day. This ope a ion p o ided
a liquid ac ion (DLF) ha was s o ed in a ank and a con‑
cen a ed ac ion (DCF) ha was ecycled o he diges e
in o de o ensu e a con inuous o ganic load, as chemical
oxygen demand, o 2–4kg·m−3. I he o ganic load was
adequa e, he DCF was sen o a s o age ank.
Cha ac e iza ion o F ac ions
Wi h he plan ope a ing unde i s usual egime, samples
o he di e en ac ions we e ob ained o e a pe iod o
4weeks. By excep ion, only a single sample o slu y (S)
was aken om he s o age ank since i was homogeneous
and no changed h oughou he sampling pe iod. SLF, D
and DCF we e sampled on a weekly basis h ough s opcocks
inse ed in he p ocessing line. Unlike he p e ious ac ions,
DLF was sampled wice a week a he poin o discha ge.
Samples we e s o ed e ige a ed a 4°C un il analysis.
DLF Analysis
F esh samples we e analysed o (a) pH and elec ical con‑
duc i i y; (b) u bidi y wi h a D . LANGE LTP4 u bidim‑
e e ; (c) NO3– and NH4+ wi h ion‑selec i e elec odes; (d)
suspended solids by acuum il a ion h ough a mic o‑ ib e‑
glass il e o 0.45μm po e size; (e) o al solids by e apo‑
a ion a 105°C; ( ) C and N simul aneously on a LECO
T uSpec combus ion analyse ; and (g) P, K, Ca, Mg, Na,
Cd, Cu, C , Hg, Ni, Pb, Zn, As, B, Co, Mn, Mo, Se and
V by induc i ely coupled plasma mass spec ome y (ICP‑
MS). The las esul s we e used o calcula e he Sodium
Adso p ion Ra io (SAR) aco dingEq.1, whe e [Na+],
[Ca2+] and [Mg2+] a e he concen a ion o he espec i e
ions(mmol(+) L–1)
S, SLF, D andDCF analysis
F esh samples we e used o measu e pH, elec ical con‑
duc i i y and d y ma e . An aliquo each o S, SLF, D and
DCF ha was p e iously ozen and eeze‑d ied was used o
de e mine C and N on he LECO au oanalyse ; N–NO3− and
N‑NH4+ wi h ion‑selec i e elec odes in a 1:25 (w/w) esus‑
pension a e hyd a ion wi h e hanol; and P, K, Ca, Mg, Na,
Cd, Cu, C , Hg, Ni, Pb and Zn by ICP‑MS ollowing mic o‑
wa e‑assis ed diges ion in ni ic acid [28].
Incuba ion Tes s
The mine aliza ion dynamics o C and N we e s udied
o S, SLF, D and DCF upon hei applica ion o soil.
A labo a o y es was pe o med using he su ace laye
(0–20cm) o an ex ensi e c opland in he icini y o he
pilo plan . Samples we e ai ‑d ied and sie ed h ough
2mm mesh p io o incuba ion. The soil was sandy loam
in ex u e, had pH 6.34 in a 1:2.5 wa e suspension, and
an elec ical conduc i i y o 0.121dS·m−1 in a 1:5 suspen‑
sion; also, i con ained 5.40% o ganic ma e and 0.247%
o al N (d y combus ion); 21.3mgN–NO3− kg–1 and
16.8mgN–NH4+ kg−1 (as desc ibed below) and 32.6mg
Olsen P kg–1. The ca ion con en s ex ac ed by 1N NH4Cl
and analyzed in ICP‑AES we e 7.65 (Ca2+), 1.53 (Mg2+),
0.13 (Na+), 1.09 (K+) and 0.05 (Al3+), all in cmol(+) kg–1.
(1)
SAR
=
[
Na+
]
√
[Ca2+]+[Mg2+]
2
Table 1 Amoun s o esh and d y ma e , wa e , N and C supplied by
each p oduc o he soil in he incuba ion es s
S slu y; SLF slu y liquid ac ion; D diges a e; DCF diges a e con‑
cen a ed ac ion; FM esh ma e ; DM d y ma e
*Sum o N–NH4+ and N–NO3−
Componen S SLF D DCF
FM (g kg−1 soil) 46.64 111.08 96.87 117.16
DM (g kg−1 soil) 2.85 0.13 2.13 6.20
H2O (mL kg−1 soil) 67.17 0.00 16.22 0.00
Mine al N (mg kg−1soil) * 60.15 2.53 69.68 59.66
To al N (mg kg−1 soil) 156.99 4.13 107.61 229.32
C (mg kg−1 soil) 1455.67 41.84 798.21 2557.40
Was e and Biomass Valo iza ion
1 3
In o de o a oid an ini ial inc ease in mic obial ac i i y by
e ec o he a ou able empe a u e and mois u e condi‑
ions, he soil was p e iously mois ened and incuba ed in
he absence o e ilize o 2weeks.
Ni ogen mine aliza ion was quan i ied by incuba ing
an amoun equi alen o 600g o d y soil wi h he p opo ‑
ional dose o e ilize s (Table1) in 1L he me ic plas ic
boxes, which we e ae a ed a leas once a week. Pe iodi‑
cally, samples o 25g o esh soil we e aken and supplied
wi h 75mL o 2M KCl and passed h ough Wha man no.
42 il e pape a e s i ing o 1h. The esul ing ex ac
was analysed o ammonium ion wi h he Indophenol Blue
colo ime ic me hod [29], and also o ni a e ion by col‑
o ime ic measu emen a e educ ion o ni i e ion wi h
hyd azine sulpha e [30].
Ca bon mine aliza ion was e alua ed by incuba ing an
amoun equi alen o 50g o d y soil wi h he p opo ‑
ional dose o e ilize (Table1). The soil was placed in
igh ‑closed con aine s also holding a ial con aining an
alkaline solu ion (1N NaOH) o ap CO2 and ano he
con aining wa e o a oid desicca ion. A each sampling
ime, he NaOH ial was i a ed wi h 0.5N HCl ollow‑
ing p ecipi a ion o ca bona e ion wi h BaCl2 [31] and
eplaced wi h ano he con aining esh NaOH solu ion.
In bo h incuba ions he same dose o each e ilize was
added o he soil. An amoun o S, D, and DCF equi alen
o app oxima ely 60mg mine al N·kg–1 d y soil (Table1)
was applied, adding wa e la e o achie e 60% ield capac‑
i y. No simila amoun o SLF could be used because his
p oduc had a e y high mois u e con en ha limi ed he
o al amoun o e ilize i supplied. Fou eplica es we e
pe o med o each ea men and he con ol (no e i‑
lize ), so each es had 20 expe imen al uni s.
Bo h incuba ion es s we e conduc ed simul aneously a
25°C in he same chambe o 16weeks. Samplings we e
done simul aneously a a a iable equency on he days
2, 6, 10, 14, 21, 28, 35, 42, 56, 70, 91 and 112.
Modelling o Mine aliza ion Cu es
The esul s o he C and N mine aliza ion es s we e mod‑
elled in wo di e en ways:
(a) Wi h he single‑ ac ion i s ‑o de kine ic model o
S an o d and Smi h (1972), based on Eqs.2 and 3:
whe e Ni is he amoun o soil ino ganic ni ogen p esen
a ime , Ni0 he ini ial amoun o ino ganic N, N0 ha o
po en ially mine alizable N, k he N mine aliza ion a e con‑
s an (day–1) and ime (days) in eq.2; and Ci is he amoun
o C eleased a ime , C0 ha o po en ially mine alizable
C, k he C mine aliza ion a e cons an (day–1) and ime
(days) in eq.3.
(b) Wi h he wo‑ ac ion i s ‑o de kine ic model o
Molina e al. (1980), based on Eqs.4 and 5:
(2)
Ni
=Ni0+N0×
[
1−e
(−k× )]
(3)
Ci
=C
0
×
[
1−e
(−k× )]
Table 2 Gene al p ope ies o he s a ing slu y and he ac ions ob ained om i s p ocessing
S, slu y; SLF, slu y liquid ac ion; D, diges a e; DCF, diges a e concen a ed ac ion; FM, esh ma e ; DM, d y ma e
*Sum o N‑NH4+ and N‑NO3−
P ope y S SLF D DCF
Mean SD Mean SD Mean SD
pH 7.04 7.84 ± 0.51 b 7.75 ± 0.25 ab 7.61 ± 0.17 a
EC (dS m−1) 18.54 8.24 ± 0.87 a 12.95 ± 0.51 c 11.85 ± 0.63 b
DM (g kg−1) 35.55 7.86 ± 1.43 a 19.90 ± 4.36 b 56.92 ± 9.43 c
C (g·kg−1d.m.) 321.52 331.43 ± 109.23 ab 378.11 ± 6.32 a 410.93 ± 3.78 b
N (g·kg−1d.m.) 85.28 41.62 ± 7.99 a 43.82 ± 9.30 a 36.25 ± 4.44 a
C/N 3.77 7.96 ± 1.67 a 8.63 ± 1.94 a 11.34 ± 1.58 a
N–NO3− (g kg−1d.m.) n.d 16.26 ± 5.35 b 14.31 ± 14.31 b 4.82 ± 1.90 a
N–NH4+ (g kg−1d.m.) n.d 18.93 ± 4.86 b 13.14 ± 13.14 b 6.14 ± 0.71 a
P (g kg−1d.m.) 8.56 6.56 ± 2.77 ab 7.51 ± 0.32 a 8.66 ± 0.50 b
K (g kg−1d.m.) 127.27 110.52 ± 13.11 c 60.48 ± 5.21 b 26.58 ± 4.11 a
Ca (g kg−1d.m.) 36.85 24.69 ± 10.89 a 30.01 ± 1.32 a 27.71 ± 1.96 a
Mg (g kg−1d.m.) 8.46 7.34 ± 2.62 ab 8.83 ± 0.32 b 7.82 ± 0.30 a
Na (g kg−1d.m.) 33.15 28.83 ± 3.10 c 13.75 ± 1.28 b 5.96 ± 1.17 a
Was e and Biomass Valo iza ion
1 3
whe e Ni is he amoun o soil ino ganic ni ogen a
ime ; Ni0 is he ini ial amoun o ino ganic N; N1 and
N2 a e he amoun s o he wo ac ions o po en ially
mine alizable N; k1 and k2 he mine aliza ion a e con‑
s an o N1 and N2, espec i ely (days–1); and is ime
(days) in eq.4; and Ci is he amoun o C eleased a
ime ; C1 and C2 a e he amoun s o po en ially min‑
e alizable C in he wo ac ions; k1 and k2 he espec‑
i e mine aliza ion a e cons an s (day–1); and is ime
(days) in eq.5.
The modelled esul s we e used o es ima e mine alizable N
(Ni ) and he ac ions o ca bon (mine alized and ecalci an ).
S a is ical Analysis
The esul s we e analysed s a is ically by using he so wa e
SPSS S a is ics . 25 om IBM Co p. (A monk, NY, USA).
Da a we e checked o no mali y wi h he Shapi o–Wilk es ,
ailu e o which led us o adjus hem o a no mal dis ibu ion
by app op ia e ans o ma ion. Va iances we e checked o
homoscedas ici y by using Le ene’s es . The signi ican ea ‑
men s we e compa ed h ough Tukey’s HSD mul iple ange
es (p < 0.05) o T3 Dunne ’s es (p < 0.05) i he a iables
did no ul il he homoscedas ici y c i e ion.
The e ec o each ea men was assessed om he a ia‑
ion a e o he concen a ion o each elemen and d y ma e
as ollows:
The dynamics o C and N mine aliza ion we e modelled
wi h he speci ic choice bes i ing he expe imen al esul s.
Signi ican di e ences be ween cu es we e iden i ied by
p ocessing he esul s o each ea men indi idually (whole
model) and all in combina ion o in pai s ( educed models).
The whole model was compa ed wi h he educed models ia
an F‑ es :
whe e SSE and SSE a e he sums o squa es o he educed
and whole model, espec i ely, and d and d a e he co ‑
esponding deg ees o eedom. A educed model was
deemed inapplicable, and di e ences be ween ea men s
(4)
Ni
=Ni
0
+N
1
×
[
1−e
(−k1× )]
+N
2
×
[
1−e
(−k2× )]
(5)
Ci
=C
1
×
[
1−e
(−k1× )]
+C
2
×
[
1−e
(−k2× )]
Va ia ion a e
=concen a ion a e
(
w
∕
w
)−
concen a ion be o e
(
w
∕
w
)
concen a ion be o e
(
w
∕
w
)
F
=
(
SSE −SSE
)
∕
(
d −d
)
(
SSE
−d
)
we e assumed o be signi ican as a esul , when i s di e ‑
ence om he whole model led o p < 0.001.
Resul s andDiscussion
Cha ac e iza ion o F ac ions
Slu y Liquid F ac ion
The o a ing sie e used o sepa a e he SLF o he slu y
e ained pa icles la ge han 1mm, he eby educing he d y
ma e (DM) con en o he slu y by 78% (Table2). This
sepa a ion e iciency is g ea e han p e iously epo ed al‑
ues [34], especially i one conside s ha he s a ing slu y
had a ela i ely low DM con en [35]. Also, he sepa a ion
e iciency o slu y componen s is known o be widely a i‑
able (11–87%) [3]. Solid–liquid sepa a ion has p o ed an
e ec i e choice o en iching he solid ac ion wi h mos o
he d y ma e , N and P p esen in pig slu y [36, 37]. In his
wo k, he N con en o he SLF was educed by no less han
51%; also, because he C con en was sca cely al e ed, he
C/N a io was nea ly doubled as a esul . This was a conse‑
quence o a subs an ial p opo ion o o al N (and, especially,
o ganic N) in pig slu y being p esen in la ge pa icles [25]
—in ac , 85% o all N in SLF was ino ganic. Al hough he
esul s sugges ed a educ ion in P con en by e ec o solid
ac ion o slu y being emo ed, no clea ‑cu conclusion
can be d awn in his espec because he da a we e a he
a iable. On he o he hand, he K, Ca, Mg and Na con en s
di e ed li le be ween he slu y (S) and i s liquid ac ion
SLF, which sugges s ha hese elemen s emained la gely
in he o me —some hing ha was o be expec ed since he
p e ious elemen s a e mos ly p esen in soluble o ms bound
o pa icles 0.45–50µm in size [38].
Diges a e
Th ough diges ion, a ac ion o o ganic ma e is mine al‑
ized o simple compounds, ca bon dioxide and me hane
[39]. This usually inc eases he p opo ion o soluble nu i‑
en s, and dec eases ha o ca bon and d y ma e , in he
esul ing diges a e [40]. In his wo k, howe e , we obse ed
he opposi e end. Thus, diges ion dec eased N–NO3−,
N–NH4+, K and Na le els by 12, 31, 45 and 52%, espec‑
i ely, while DM inc eased by 153% (Table2). This was
he likely esul o he diges a e being con inuously il e ed

Was e and Biomass Valo iza ion
1 3
h ough he memb ane module and he concen a ed ac ion
being ecycled while he liquid ac ion DLF was emo ed
oge he wi h dissol ed sal s (i.e., o a washing e ec ). On
he o he hand, he Ca and Mg le els we e inc eased by
abou 20%. These elemen s we e no in soluble o m bu
a he bound o pa icles 0.45–50μm in size [38], which p e‑
en ed hem om c ossing he memb anes and, as a esul ,
emaining in he DCF and being e u ned o he diges e in
concen a ed o m.
Ca bon le els should also ha e been educed by e ec
o he o ma ion o CH4 and CO2 [41]. Howe e , ecycling
caused all C bound o he la ge pa icles o be e u ned o
he diges e while o he soluble elemen s we e washed o ,
C le els inc easing by 14% as a esul . Thus, despi e he low
OM con en o he SLF, he diges e main ained an adequa e
o ganic load by e ec o excess wa e and soluble sal s being
emo ed, and he esidence ime o lignocellulosic ma e i‑
als —which a e slowe o hyd olyse— being expanded [42].
Diges a e Concen a ed F ac ion
Mic o il a ion o he diges a e led o mos d y ma e in i
passing in o he DCF, which in ac con ained an amoun o
solids 2.86 imes g ea e han ha o he D i sel and 7.24
imes mo e so han he SLF (Table2). Mic o il a ion also
inc eased he con en in P (by up o 15%), which was p esen
mos ly in he solid ac ion [36].
As s a ed abo e, mic o il a ion emo ed sal s ha we e
ans e ed o he DLF. This e lec ed in a dec ease in
elec ical conduc i i y in he DCF ela i e o he D i sel .
The sal s exhibi ing dec eased le els by e ec o mic o il‑
a ion included hose o N. Thus, ni a e and ammonium
ion le els we e educed by 66 and 53%, espec i ely. This
led o a sligh dec ease in o al N which, howe e , was no
signi ican , and especially, o he ino ganic ac ion o N
being mo e han hal ed ( om 63 o 30%) —which had
s ong implica ions on i s po en ial as a e ilize . The e was
also a dec ease in he con en s o K and Na, which we e
sen la gely o DLF as a esul o hei being mos ly (mo e
han 90%) in dissol ed o m o bound o pa icles less han
0.45µm in size [38].
Waege e al. (2010) p e iously epo ed a educ ion
o 60% (w/w) in ammonium ion le els in addi ion o an
inc ease in C and P le els (69 and 60%, espec i ely) by
e ec o slu y diges a e being concen a ed h ough mic o‑
il a ion. Chiumen i e al. [43] ob ained simila esul s by
passing he liquid ac ion o a diges a e h ough a memb ane
o 0.1µm po e size; he le els o soluble ions such as K+ and
N–NH4+ we e dec eased by 19 and 13% (w/w), espec i ely,
whe eas P was la gely e ained in he solid ac ion, wi h an
inc ease by 68%. The mo e ma ked educ ions in soluble
ions (K+ and N–NH4+) and educed P e en ion capaci y
obse ed he e may ha e esul ed om ecycling allowing
mos elemen s e ained in o ganic o exchangeable o ms
being con e ed in o soluble o ms. Hea y ecycling o DCF
was equi ed in o de o main ain an adequa e o ganic load
in he diges e —one highe han ha o SLF, wi h which
i was ed— bu would be unnecessa y o much less o a
equi emen i he whole slu y (S) we e ea ed. The e o e,
h ough he combined diges ion‑mic o il a ion p ocess, he
main disad an age o diges ing he liquid ac ion is o e ‑
come; a low o ganic load ha implies less biogas p oduc ion
pe olume uni [14]. In addi ion, he main ad an ages o
using only he liquid ac ion a e main ained; sho e hyd au‑
lic e en ion ime [14], highe biogas p oduc ion pe uni
o d y ma e [13, 14], ewe pumping, mixing o clogging
p oblems [15, 16].
The elemen s bound o he la ge pa icles (Ca, Mg)
should ha e been e u ned o he diges e and hei concen‑
a ions in DCF been e y simila o hose in he in luen
(D). This was in ac he case wi h Ca, which emained a
s eady le els h oughou , bu no wi h Mg, whose le els
we e educed by up o 10%.
Al hough he solid ac ion o slu y was emo ed a he
s a , he p ope ies o he esul ing DCF showed simila i ies
o hose o he s a ing slu y (S). Such was he case wi h
he Ca, Mg and P con en s, bu no wi h he d y ma e and
C con en s, which we e 60 and 28% highe , espec i ely, in
DCF. On he o he hand, he le els o N and K we e educed
by 57 and 80%, espec i ely, as a esul o hei washing o
DLF. These changes inc eased he C/N a io om 3.77 in S
o 11.34 in DCF and mus ha e in luenced he soil dynam‑
ics o C and N [44, 45]. Nu ien balances o N/K we e also
al e ed. Thus, he N/K a io, which is known o in luence
e ilize pe o mance [46], inc eased om 0.67 in S o 1.36
in DCF. The e o e, he N:K a io would no be as sui able o
some K‑demanding c ops such as po a oes (N:K a io 0.6)
[47] o suga cane (N:K a io 0.5) [48]. Howe e , i could be
used in N‑demanding c ops such as co n (N:K a io 1) [49]
o yeg ass (N:K a io 0.8) [50] and in op‑d essing whe e i
is sough o p o ide mainly ni ogen.
Diges a e Liquid F ac ion
Mic o il a ion p o ed e ec i e o emo e mois u e om
he D, which was 99% wa e (Table3). This was also he
case wi h suspended solids, which accoun ed o only 3% o
all solids. E en so, he le els o suspended solids exceeded
exis ing ecommenda ions and could cause clogging o i i‑
ga ion sys ems. Mos o he elemen s c ossing he mem‑
b anes we e in soluble o m and inc eased he elec ical
conduc i i y (EC) o he solu ion as a esul . The solu es
consis ed mainly o C (57%), K (22%), N (14%, la gely as
ammonium ion, which accoun ed o 93% o all N) and Na
(6%). P e ious expe imen s wi h mic o il e ed diges a es and
slu ies p o ided esul s simila o ou s [21, 51]. The high
Was e and Biomass Valo iza ion
1 3
Na le els, and low Ca and Mg le els, ound he e esul ed in a
e y high Sodium Adso p ion Ra io (SAR) ha could cause
s uc u al damage in i iga ed soil. In p e ious mic o il a‑
ion expe imen s, he pe mea e swep la ge amoun s o solu‑
ble ions such as Na+, N–NH4+ and K+, he eby aising EC o
19dS m−1 [43] and SAR o ex eme le els (86meq L−1)1/2
[52].
By e ec o sal s being swep , DLF con ained subs an ial
amoun s o nu ien s such as N and K bu low le els o P.
These esul s a e consis en wi h p e ious epo s. The nu i‑
en s p esen in DLF could be exploi ed by using i as e iga‑
ion wa e . In ac , p e ious expe imen s on pas u e, co n o ,
in dilu ed o m, hyd oponic c ops, p o ided simila o e en
be e esul s wi h his ype o p oduc han wi h mine al
e ilize s [53–55]. Some c ops o managemen echniques
equi e addi ionally using supplemen s o mac onu ien s
such as P o Mg [54, 56].
Ano he possible use o he wa e and he nu ien s dis‑
sol ed in DLF is as wa e o i iga ion. In o de o use i , i
mus comply wi h he eclaimed wa e egula ions o his
use. O e all, DLF would ul il he equi emen s as ega ds
suspended solids, EC, N–NO3−, o al N and SAR, he la e
wo o which a e he mos es ic i ely egula ed (Table3).
Dilu ing DLF may be e ec i e o comply wi h exis ing
egula o y s anda ds. Thus, 1:35 dilu ion would p o ide
eclaimed wa e accep able o use in mos coun ies. Al e ‑
na i ely, e e se osmosis would e ain mo e han 95% o all
Na, K and N‑NH4+ p esen [57].
As ega ds hea y me als and ace elemen s, which a e
mo e uni o mly egula ed among coun ies, DLF only
exceeded he limi s o B and Mo, which a e in ac plan
Table 3 P ope ies o he diges a e liquid ac ion (DLF) and maximum alues ecommended by in e na ional bodies o egula ed by na ional
au ho i ies o eclaimed i iga ion wa e
TS o al solids; SS suspended solids; WHO Wo ld Heal h O ganiza ion[78]; USEPA Uni ed S a es En i onmen al P o ec ion Agency[79];
Spain, limi se by Royal Dec ee 1620/2007[80]; Po ugal VRM, Maximum Recommended Value (VRM) acco ding o Republic Dia y no.
176/1998[81]; I aly, maximum limi acco ding o Minis e ial Dec ee no. 185/2003[82]; (EC), elec ical conduc i i y unc ion
1 I iga ion wi h wa e in con ac wi h esh ood o consump ion
2 I iga ion o ood o be indus ially p ocessed o no in ended o human consump ion
P ope y Mean SD Max Min WHO USEPA Spain Po ugal VMR I aly
Tu bidi y (NTU) 99 88 207 0.67 101
TS (mg L−1) 6424 667 7099 5386
SS (mg L–1) 199 166 411 31 100 30 201/35260 10
pH 7.56 0.16 7.86 7.41 6.5–8.0 6.5–9.0 6.5–8.4 6.0–9.5
EC (dS m−1) 12.5 1.2 13.8 10.6 3 31.2 1 3
To al C (mg L−1) 4168 143 4372 3943
To al N (mg L−1) 1027 98.4 1120 859 30 15
N–NO3– (mg L−1) 104.2 39.4 174.8 61.0 50
N–NH4+ (mg L−1) 957.7 251.0 1260.8 644.4 2.58
P (mg L−1) 6.63 1.18 7.75 4.34 2
K (mg L−1) 1596.0 192.9 1747.9 1232.2
Ca (mg L−1) 48.7 10.8 66.9 37.6
Mg (mg L−1) 0.117 0.01 0.132 0.101
Na (mg L−1) 442.5 39.6 495.7 380.6
SAR [(meq L−1)1/2] 17.7 2.8 20.3 13.7 (EC) 61.2 ‑
B (μg L−1) 988 60 1089 938 750 5001.2 300 1000
As (μg L−1) 57 6 63 46 100 100 1001.2 100 20
Cd (μg L−1) 0 0 1 0 10 10 101.2 10 5
Co (μg L−1) 30 9 37 13 50 50 501.2 50 50
C (μg L−1) 17 3 19 11 100 100 1001.2 100 100
Cu (μg L−1) 16 13 39 7 200 200 2001.2 200 1000
Mn (μg L−1) 6 3 13 4 200 200 2001.2 200 200
Mo (μg L−1) 12 13 40 6 10 10 101.2 5
Ni (μg L−1) 110 11 123 92 200 200 2001.2 500 200
Se (μg L−1) 17 6 24 10 20 20 201.2 20 10
V (μg·L−1) 10 1 11 7 100 100 1001.2 100 100
Was e and Biomass Valo iza ion
1 3
mic onu ien s and whose po en ial haza ds can be a oided
simply by 1:1 dilu ion.
Hea y Me als
Mos hea y me als p esen in slu ies and hei diges a es a e
in solid o m, bound o o ganic ma e , p esen as ca bon‑
a e p ecipi a es, bound o Fe and Mn oxides o in esidual
ac ions [58]. Possibly as a esul , emo ing he solid phase
om he slu y educed he con en s in hea y me als ela i e
o he s a ing ma e ial (Table4). Con e sely, subsequen ly
emo ing he liquid ac ion om he diges a e, DLF, and
concen a ing he solids in he D and DCF inc eased such
con en s ela i e o SLF (Table4). E en so, hea y me al le ‑
els emained below he h esholds se in EU Regula ion (EC)
2019/1009 o di e en ac ions. I espec i e o ea men ,
he inal DCF had hea y me al con en s simila o hose o
he s a ing slu y and also o he ypical alues o in ensi e
pig a ening a ms [35]. By excep ion, he Zn con en was
well below a e age, possibly as esul o i s being supplied
in smalle amoun s h ough he die . Pig slu y ypically con‑
ains high le els o Cu and Zn by e ec o he wo me als
being p esen in eed supplemen s [60]. Such high le els
can esul in accumula ion o he me als in soil con inuously
ecei ing pig slu y o diges a e [61–63].
Al hough he concen a ions o hea y me als changed
h oughou , he ela i e weigh o each me al emained con‑
s an and dec eased in he ollowing sequence, consis en
wi h p e ious epo s o pig slu ies and diges a es [35, 61,
64]: Zn > Cu > Ni > C > Pb > Cd > Hg.
Ca bon Mine aliza ion
The con en s in mine alized C exceeded hose o he con ol
soil wi h all ea men s. This led us o sub ac he amoun
o C mine alized in he con ol soil (i.e., ne mine aliza ion)
om hose ob ained wi h all o he ea men s. The cu e o
ne mine alized C was i ed by using a single‑pool model
and a wo‑pool model. As can be seen om Table5, he SLF
cu e was closely i ed wi h bo h ypes o model. In ac ,
he wo‑pool model o SLF epo s wo ac ions o equal
magni ude ha mine alize a he same a e, so i is eally a
one‑pool. This in ol ed assuming ha mine alizable C was
p esen in labile o ms and con e ed in o mine al o ms a a
high a e (0.13 day−1). On he o he hand, he esul s o C in
S, D and DCF we e mo e closely i ed by a wo‑pool model,
which assumes mine alizable o ganic ma e o consis o
wo di e en ac ions being mine alized a a di e en a e
and a non mine alizable ac ion. Thus, he e was a labile
ac ion accoun ing o 68, 84 and 65% o all mine alizable
C in S, D and DCF, espec i ely, ha was mine alized a a
high a e (0.838, 1.335 and 1.175 day−1, espec i ely) and
comple ely deg aded wi hin 48h. The emaining mine al‑
izable C was bound o a mo e esis an ac ion ha was
deg aded a a conside ably lowe a e (< 0.1 day−1).
The o al amoun o C mine alized a he end o he es s
(day 112) was 32, 116, 215 and 246mg C‑CO2·kg soil–1
wi h SLF, D, DCF and S espec i ely. These esul s we e
s ongly in luenced by he o al amoun o C supplied o he
soil, which di e ed among ea men s (Table1).
In o de o be e unde s and he ne C mine aliza ion
esul s, hey we e plo ed as pe cen ages ela i e o he o al
amoun o C applied (Fig.1). Again i is obse ed ha , C
in SLF was mine alized especially apidly, wi h i ually all
mine alizable ca bon (73% o o al ca bon) being con e ed
wi hin 30days. The e o e, his ac ion sca cely helped
main ain C le els —and hence o ganic ma e le els— in
he soil. The as mine aliza ion o mos C can be asc ibed o
he mos ecalci an ac ion o OM being emo ed as la ge
pa icles oge he wi h he solid ac ion, he mos labile
po ion (soluble OM and suspended ine pa icles) emain‑
ing in he liquid ac ion SLF. Howe e , he labile o ganic
po ion o SLF, which consis ed la gely o a y acids, was
hea ily deg aded by anae obic diges ion being educed in
he diges a e o only 14% o he o al ca bon. Al hough he
diges a e has less mine alizable ca bon, i is e y labile and
Table 4 Hea y me al con en s o he s a ing slu y and i s ac ions
UE limi , highes alue allowed by Regula ion (EU) 2019/1009. S, slu y; SLF slu y liquid ac ion; D diges a e; DCF diges a e concen a ed
ac ion; Spanish limi , highes alue allowed by Royal Dec ee 506/2013 o class B e ilize s[83]; d.m., d y ma e . Di e en le e s in he same
ow deno e signi ican di e ences a p < 0.05
Me al concen a ion S SLF D DCF UE limi Spanish limi
C (mg kg−1 d.m.) 7.91 3.61 ± 0.95 a 6.08 ± 0.45 a 12.39 ± 1.46 a – 250
Ni (mg kg−1 d.m.) 10.60 6.42 ± 0.72 a 6.51 ± 0.26 a 7.70 ± 0.21 a 50 90
Cu (mg kg−1 d.m.) 187.85 115.68 ± 8.31 a 202.66 ± 8.93 b 228.50 ± 28.18 b 300 300
Zn (mg kg−1 d.m.) 606.88 433.23 ± 104.99 a 462.08 ± 19.05 a 517.63 ± 57.63 a 800 500
Cd (mg kg−1 d.m.) 0.44 0.28 ± 0.11 a 0.22 ± 0.01 a 0.23 ± 0.04 a 1.5 2
Hg (mg kg−1 d.m.) 0.31 0.17 ± 0.15 a 0.21 ± 0.11 a 0.22 ± 0.13 a 1 1.5
Pb (mg kg−1 d.m.) 5.41 1.28 ± 1.01 a 1.96 ± 0.09 a 2.44 ± 0.26 a 120 150
Was e and Biomass Valo iza ion
1 3
Table 5 Typical pa ame e alues o he modelled equa ions o one o wo ca bon and ni ogen ac ions
S slu y; SLF slu y liquid ac ion; D diges a e; DCF diges a e concen a ed ac ion. Di e en le e s in each column o a model deno e signi ican di e ences a p ≤ 0.001
Ci
=C0×
[
1−e(−k× )
]
C0k R
S 231.84 0.376 0.978
SLF 30.56 0.130 0.989
D 111.80 0.845 0.994
DCF 202.83 0.450 0.976
Ci
=C1×
[
1−e(−k1× )
]
+C2×
[
1−e(−k2× )
]
C1k1C2k2R
S 165.67 0.838 79.062 0.062 0.999 d
SLF 15.26 0.130 15.263 0.130 0.989 a
D 95.69 1.335 18.745 0.088 1.000 b
DCF 138.64 1.175 74.135 0.078 0.999 c
Ni
=Ni0+N0×
[
1−e(
−k×
)
]
Ni0N0k R
S 80.35 90.04 0.015 0.822 b
SLF 4.91 7.02 0.175 0.707 a
D 129.37 73.99 0.019 0.754 b
DCF 131.62 104.23 0.020 0.892 b
Ni
=Ni0+N
1
×
[
1−e
(−k
1
× )]
+N2×
[
1−e
(−k
2
× )]
Ni0N1k1N2k2R
S 80.35 41.26 0.015 48.78 0.015 0.822
SLF 4.91 3.51 0.175 3.51 0.175 0.707
D 129.37 20.69 0.019 53.29 0.019 0.754
DCF 131.62 0 2.314 104.23 0.020 0.892