In e na ional Jou nal o
En i onmen al Resea ch
and Public Heal h
A icle
Hea y Me al Up ake o Le uce and Ryeg ass om
U ban Was e Compos s
Remigio Pa adelo * , An ía Villada and Ma ía Te esa Ba al
CRETUS Ins i u e, Depa amen o de Eda olox
í
a e Qu
í
mica Ag
í
cola, Uni e sidade de San iago de Compos ela,
15782 San iago de Compos ela, Spain; [email p o ec ed] (A.V.); m e [email p o ec ed] (M.T.B.)
*Co espondence: [email p o ec ed]; Tel.: +34-881-815-042
Recei ed: 5 Ap il 2020; Accep ed: 20 Ap il 2020; Published: 22 Ap il 2020
Abs ac :
In e es in using u ban was e compos s as amendmen s in u ban ag icul u e is g owing
nowadays. Howe e , conce ns abou he po en ial ans e ence o pollu an s p esen in u ban was e o
he ood chain a e e y ele an when hey a e ecycled o ood o animal eed p oduc ion. Thus, o
he sa e use o u ban was e compos s, i has o be assu ed ha no isk o me al ans e ence o plan s
om compos exis s. In his wo k, he ans e ence o hea y me als om u ban was e compos s o
plan s has been s udied in an expe imen wi h le uce and I alian yeg ass, g own in subs a es based
on i e me al- ich compos s and a manu e e micompos (included o compa ison). A wo-mon h
po expe imen was pe o med unde con olled ligh and empe a u e condi ions, and plan g ow h
and up ake o Cu, Pb, Cd and Zn we e analyzed. Fo bo h species, he concen a ion o me als in
plan issue ollowed he sequence Zn >Cu >> Pb
≈
Cd, he same as he me al concen a ions in ou
ou o he i e compos s. Plan concen a ions o Zn, Cu and Cd inc eased wi h hei concen a ions in
compos , whe eas his ela ion was no obse ed o Pb. The a io be ween elemen concen a ion in
plan and compos we e much highe o Zn, Cd and Cu han o Pb, showing he lowe bioa ailabili y
o Pb wi h espec o o he me als.
Keywo ds: compos ing; u ban was e; plan ans e ence; hea y me als
1. In oduc ion
U ban was e managemen h ough compos ing is gaining a en ion wi h he wo ldwide inc ease
o u baniza ion. In a momen whe e he amoun s o municipal solid was e a e inc easing in associa ion
o he ise o u ban popula ion, compos ing allows one o manage he la ge amoun s o o ganic was e
p oduced in u ban a eas in a simple and e icien way. The e a e se e al op ions o he eu iliza ion
o he compos p oduced om u ban was es, including he amendmen o ag icul u al soils [
1
,
2
],
p oduc ion o soilless subs a es [
3
,
4
], emedia ion o deg aded lands and con amina ed soils [
5
,
6
]
and ea men o pollu ed was ewa e s [
7
,
8
]. In addi ion, he inc easing in e es in u ban ag icul u e
and ood p oduc ion in he u ban en i onmen o e s new oppo uni ies o he use o u ban was e
compos s [
9
,
10
], whe he i is pe o med on soils [
11
,
12
] o in soilless media [
13
–
15
]. In pa icula , he
p oduc ion o subs a es o g een oo s and oo op ga dens in ci ies is an applica ion ha demands
high amoun s o compos [
16
]. F om a wide pe spec i e, compos ing u ban was es and eusing he
compos wi hin he ci ies will help he ad ancemen o se e al o he UN Sus ainable De elopmen
Goals, in pa icula “Sus ainable ci ies and communi ies” (goal numbe 11), “Responsible consump ion
and p oduc ion” (goal numbe 12) and “Clima e ac ion” (goal numbe 13).
While he use o compos s has many posi i e e ec s, imp o ing soil condi ions o plan g ow h,
dec easing e osion isk, inc easing biological ac i i y o educing he mobili y o some pollu an s [
1
,
6
,
17
],
en i onmen al and sa e y conce ns also exis . This is he case specially o compos s p oduced om
u ban was es, which may be he sou ce o con aminan s such as po en ially oxic ace elemen s,
In . J. En i on. Res. Public Heal h 2020,17, 2887; doi:10.3390/ije ph17082887 www.mdpi.com/jou nal/ije ph
In . J. En i on. Res. Public Heal h 2020,17, 2887 2 o 10
o ganic pollu an s, plas ics o pa hogenic mic oo ganisms. Acco ding o mos s udies, Cu, Pb and Zn
a e o en he mos p oblema ic pollu an s in hese compos s [
1
,
18
–
22
]. These elemen s a e ound in
u ban was e compos s, due o hei p esence in ma e ials such as ba e ies, pain s, elec onic, ce amics,
p in ed pape o plas ics, as well as hei p esence in ege ables and o he human ood ma e ials [
18
,
20
].
This conce n is pa icula ly ele an when compos s a e employed o ood p oduc ion, since pollu an s
can po en ially ans e o he ood chain h ough plan s and ege ables g own in compos -amended
soils o compos -based subs a es [
18
], and also when c ops used o animal eed p oduc ion a e
in ol ed, in which case pollu an s could be ans e ed indi ec ly o humans. Thus, o he sa e use o
compos in u ban ag icul u e and g een oo cons uc ion, he isk o me al ans e ence om u ban
was e compos s o plan s mus be assessed. This is e en mo e ele an o he applica ions o compos
in u ban en i onmen s, ha in gene al in ol e he use o highe amoun s o compos han ag icul u al
applica ions. This is he case, o example, o g een oo s’ soilless subs a es, ha can be based on
high a es o compos , e en eaching 100% in some cases [16].
Howe e , s udies e alua ing he me al up ake o plan s g owing in soilless subs a es wi h high
compos a ios a e s ill sca ce and he esul s ob ained in s udies wi h compos -amended soils canno
be di ec ly ansposed o his si ua ion. In his con ex , he objec i e o his wo k was o e alua e he
possible ans e ence o hea y me als om compos s o plan s g own in soilless subs a es, as well as
hei ela ionship wi h compos composi ion. Fo his, we ca ied ou an expe imen o plan g ow h
on subs a es elabo a ed wi h se e al u ban was e compos s, all cha ac e ized by hei high me al
con en s, using wo species: I alian yeg ass and le uce.
2. Ma e ials and Me hods
2.1. Compos s
Fou municipal solid was e compos s and a manu e e micompos we e used in he expe imen
(Table 1): MSWC1 was ob ained by anae obic e men a ion o he biodeg adable ac ion o municipal
solid was e, sepa a ed be o e collec ion, ollowed by an ae obic compos ing s ep o s abilize he
incomple ely diges ed esidue. MSWC2 was ob ained by compos ing he sou ce sepa a ed o ganic
ac ion o municipal solid was e. Bo h MSWC1 and MSWC2 we e p o ided by indus ial compos ing
acili ies loca ed in Galicia (Spain). MSGW is a comme cial compos ob ained om sou ce sepa a ed
biodeg adable municipal solid was e mixed wi h g een was e, and MGSS is compos ob ained om
municipal ga den immings mixed wi h sewage sludge; hey bo h we e supplied by an indus ial
compos ing acili y loca ed in Ca alunya (Spain). Finally, a mixed manu e e micompos (MV) was
supplied by a local p oduce in Galicia (Spain); i has been used o compa ison pu poses. Compos ed
pine ba k, ob ained h ough an ae obic ans o ma ion in wind ows, was supplied by Cos iña O g
á
nica
(A Co uña, Spain), and i was employed o p epa e he blends wi h compos used as subs a es.
In . J. En i on. Res. Public Heal h 2020,17, 2887 3 o 10
Table 1.
P ope ies o he compos s used in subs a e o mula ions. MSWC1 and MSWC2: compos s
ob ained om sou ce sepa a ed o ganic ac ion o municipal solid was e; MSGW: compos ob ained
om sou ce sepa a ed o ganic ac ion o municipal solid was e mixed wi h g een was e; MGSS: compos
ob ained om municipal ga den immings mixed wi h sewage sludge; MV: manu e e micompos ;
CPB: compos ed pine ba k; EC: elec ical conduc i i y; OM: o al o ganic ma e ; nd: unde he de ec ion
limi ; (
‡
): no allowed o ma ke ing acco ding o maximum ace elemen concen a ions published in
he Spanish Fe ilize s Law o o ganic amendmen s.
Bd
(Mg m−3)pH EC
(dS m−1)
OM
(g kg−1)
To al N
(g kg−1)C/NTo al Cu
(mg kg−1)
To al Zn
(mg kg−1)
To al Pb
(mg kg−1)
To al Cd
(mg kg−1)
Class
acco ding o
Spanish
Fe ilize s Law
MSWC1 0.42 8.4 2.3 490 17 17 325 608 188 3.5 (‡)
MSWC2 0.53 8.2 2.4 397 15 15 829 1149 223 3.1 (‡)
MSGW 0.53 9.2 1.2 429 17 14 52 200 62 2.1 C
MGSS 0.47 7.3 1.4 515 18 15 688 896 180 2.7 (‡)
MV 0.59 7.9 0.7 376 10 21 144 689 33 2.0 C
CPB 0.45 5.3 0.4 914 2.8 194 120 340 72 nd C
Hea y me al limi s Spanish Fe ilize s Law 400 1000 200 3
EPA Class A Biosolids 1500 2800 300 39
2.2. Compos Analysis
Fo he analysis o he compos s, he Eu opean me hods o he cha ac e iza ion o soil
imp o e s and g owing media [
23
–
27
] we e ollowed. B ie ly, pH was de e mined in aqueous ex ac s
(subs a e/ex ac an a io: 1/5 / ) o esh samples. To al o ganic ma e (OM) was de e mined by
weigh loss on igni ion o d ied g ound samples a 450
◦
C, and o al o ganic C (TOC) calcula ed
mul iplying OM by a ac o o 0.58. To al N was measu ed by Kjeldahl diges ion o d ied g ound
samples and s eam dis illa ion. To al elemen s we e ex ac ed a e he diges ion o d ied g ound
sample wi h HCl and HNO
3
(3:1 a io), and he ex ac s we e analyzed using lame a omic abso p ion
spec ome y (Va ian Spec aAA 220FS).
2.3. G ow h Expe imen
Fi e ea men s and a con ol we e assayed in he g ow h expe imen , in h ee eplica es each.
Fo his, i e subs a es we e p epa ed by blending each o he ou u ban was e compos s (MSWC1,
MSWC2, MSGW, MGSS) and he manu e e micompos (MV) wi h he pine ba k compos (CPB) a a
50% a io, on a olume basis. Using hese speci ic compos s o subs a e p oduc ion a a es highe
han 50% is no possible because o phy o oxici y (as pe p e ious wo ks by Moldes e al. [
28
] and
Ba al e al. [3]), and he e o e hey we e no assessed alone. CPB alone was used as a con ol.
Once he g owing media p epa ed, h ee po s o 12 cm diame e and 7 cm heigh we e loosely
illed wi h 400 mL o each mix u e o he con ol. Po s we e wa e ed and a e a sho pe iod o
su plus wa e o un o , 50 seeds o I alian yeg ass (Lolium mul i lo um Lam.) o h ee seeds o le uce
(Lac uca sa i a L.) we e sown in each po . A mul i-nu ien solu ion (Welg o S anda d Plus comme cial;
Qu
í
mica Masso S.A., Ba celona, Spain) con aining 17% N, 15% K
2
O, 30% P
2
O
5
, 0.13% Fe, 0.052%
Mn, 0.06% Zn, 0.02% B and 0.005% Mo, was added ini ially o he mix u es, in o de o ob ain inal
concen a ions o 220 mg N L
−1
, 160 mg K L
−1
and 170 mg P L
−1
in he subs a es. I is impo an o
no e ha e iliza ion in ol es he addi ion o 0.8 mg Zn L
−1
, a e y low quan i y in compa ison wi h
Zn concen a ions in he compos s. The po s we e co e ed wi h a glass pla e o educe e apo a i e
wa e losses du ing he i s days, and placed in an incuba ion chambe o 60 days a 20
◦
C, wi h a
luminous s eng h o 2150 lux and a 12-h pho ope iod.
By he end o he expe imen , he numbe o plan s was eco ded and hey we e cu exac ly be ween
he oo and s alk, and he esh weigh o he shoo s was eco ded. The plan s we e hen d ied a
65
◦
C and he d y weigh was eco ded. Fo he quan i ica ion o me al ans e ence o plan , d y plan
ma e ial was g ound and diges ed wi h aqua egia (HCl and HNO
3
in 3:1 a io) and Cu, Zn, Pb and Cd
we e analyzed in he ex ac s by ICP-OES (Pe kinElme , Op ima 4300 DV, Wal ham, MA, USA).
In . J. En i on. Res. Public Heal h 2020,17, 2887 4 o 10
2.4. S a is ics
To assess he signi icance o di e ences in plan p oduc i i y in he g eenhouse expe imen ,
one-way ANOVA and Tukey’s mul iple ange es we e pe o med, using he R s a is ical package
o MacOSX [
29
] and R commande [
30
]. Be o e pe o ming ANOVA, he no mali y o da a and he
homogenei y o a iance we e checked using he Shapi o-Wilk es and he Le ene es , espec i ely.
3. Resul s and Discussion
Table 1shows a summa y o he main p ope ies o he compos s. Thei pH goes om neu al
(MGSS) o alkaline (MSGW), wi h he excep ion o pine ba k compos (CPB), ha was acidic. All he
u ban was e compos s p esen ed high concen a ions o hea y me als. Among hese, Zn and Cu we e
he mos abundan in all he compos s, ollowed by Pb and Ni, and las , Cd. These concen a ions
su passed, in some cases, he le els allowed in he Spanish egula ion o he lowes quali y o ganic
amendmen s [
31
]. Acco ding o his law, MSWC1 exceeded he limi o Cd, MSWC2 o Cu, Cd,
Pb and Zn, and MGSS o Cu, so hey could no be comme cialized. E en he compos s MV and
MSGW, which p esen ed he lowes concen a ions o ace elemen s, would be ca ego ized as class C
compos s and could no be used in ag icul u al soils a a es highe han 5 Mg d y ma e ha
−1
yea
−1
.
Mo e de ailed in o ma ion abou phy o oxici y, ma u i y and hea y me al dis ibu ion and a ailabili y
is a ailable in p e ious wo ks [22,32,33].
Table 2shows he esul s o he g ow h expe imen wi h yeg ass and le uce. Despi e he
me al con en s ha su pass egula o y h esholds in se e al compos s, in gene al hey imp o ed he
p oduc i i y o bo h species wi h espec o pine ba k alone (CPB). This is p obably ela ed o he
acid pH o he pine ba k compos , gi en ha acidi y educes nu ien a ailabili y and has a gene al
nega i e impac on plan g ow h, as well as o i s high C/N a io ha can cause N immobiliza ion.
Fo bo h species, he yields in he subs a es based on he compos s MSWC1 and MSWC2 we e
lowe han he o he compos s. This is likely due o a nega i e e ec o he high salini y o hese
wo compos s, as shown by hei elec ical conduc i i y alues (Table 1), ha exceeded he alue o
1.5 dS m
−1
, which is usually ega ded as inadequa e o he ag icul u al use o compos [
34
]. In yeg ass,
e y low ge mina ion pe cen ages (unde 50%) we e obse ed in hose wo compos s, p obably also
because o phy o oxici y p oblems. Since he mean weigh o each plan is simila o hose g own on
o he compos s, he lowe yields mus be due o his low ge mina ion pe cen age. Fo le uce, lowe
ge mina ion pe cen ages we e also obse ed in MSWC1 and MSWC2, bu he lowe yields a e also due
o wo se plan de elopmen , as shown by he lowe a e age weigh pe plan .
Table 2.
Ge mina ion and shoo weigh o he plan s g own in he mix u es o compos s wi h pine ba k
compos . Di e en le e s in each column mean s a is ically signi ican di e ences in he Tukey es a p
<0.05. MSWC1 and MSWC2: compos s ob ained om sou ce sepa a ed o ganic ac ion o municipal
solid was e; MSGW: compos ob ained om sou ce sepa a ed o ganic ac ion o municipal solid was e
mixed wi h g een was e; MGSS: compos ob ained om municipal ga den immings mixed wi h
sewage sludge; MV: manu e e micompos ; CPB: compos ed pine ba k.
Ryeg ass Numbe o Plan s F esh Weigh (g) D y Weigh (g) D y Weigh /Plan
MSWC1 20 ±3 a 8.4 ±2.5 a 1.0 ±0.3 ab 0.05
MSWC2 24 ±6 ab 9.7 ±2.8 a 1.0 ±0.3 ab 0.04
MSGW 43 ±6 c 9.9 ±1.8 a 1.4 ±0.03 bc 0.03
MGSS 38 ±3 c 17.0 ±2.5 b 1.8 ±0.2 c 0.05
MV 36 ±5 bc 16.9 ±2.4 b 1.8 ±0.3 c 0.05
CPB 24 ±5 ab 5.5 ±2.3 a 0.6 ±0.2 a 0.03
Le uce Numbe o Plan s F esh Weigh (g) D y Weigh (g) D y Weigh /Plan
MSWC1 2.3 ±1.2 a 3.8 ±1.4 a 0.19 ±0.1 a 0.08
MSWC2 2 ±0 a 5.7 ±0.9 a 0.26 ±0.04 ab 0.13
MSGW 3 ±0 a 22.6 ±2.4 c 1.1 ±0.3 d 0.37
MGSS 3 ±0 a 13.4 ±0.4 b 0.57 ±0.04 bc 0.19
MV 3 ±0 a 19.5 ±1.5 c 0.88 ±0.1 cd 0.29
CPB 2.7 ±0.3 a 2.4 ±0.7 a 0.08 ±0.01 a 0.03
In . J. En i on. Res. Public Heal h 2020,17, 2887 5 o 10
Table 3and Figu e 1show he concen a ions o Cu, Pb, Zn and Cd in le uce and yeg ass issue.
Whe eas Cu, Pb and Zn we e p esen in e y simila concen a ions in yeg ass and le uce, ans e ence
o Cd was highe o le uce han o yeg ass. In bo h species, me al concen a ions ollowed he
sequence Zn >Cu >> Pb
≥
Cd, which is he same sequence o me al concen a ions in ou ou o he
i e compos s, and is he sequence commonly obse ed o me als in plan issue o di e en species
g own in non-con amina ed soils [35], o in o ganic subs a es wi h compos [36–40]. Concen a ions
o Cu and Zn a e highe han he ypical me al con en s in plan s g own in non-con amina ed soils,
bu o e all compa able o alues ound in plan s g own in u ban was e-compos s [
36
,
37
,
39
]. Cadmium
and Pb con en s we e e y low and did no su pass he h esholds es ablished in he EU egula ions
o lea y ege ables: 0.3 mg kg−1(we weigh ) o Pb and 0.20 mg kg−1(we weigh ) o Cd [41].
Table 3.
Hea y me al concen a ions (mg kg
−1
, d y weigh ) in plan s g own in he mix u es o compos s
wi h pine ba k compos . Composi ion o le uce g own in CPB is no shown because he amoun o
sample was insu icien o analysis. Di e en le e s deno e signi ican di e ences be ween compos s
in he Tukey es a p<0.05. MSWC1 and MSWC2: compos s ob ained om sou ce sepa a ed o ganic
ac ion o municipal solid was e; MSGW: compos ob ained om sou ce sepa a ed o ganic ac ion
o municipal solid was e mixed wi h g een was e; MGSS: compos ob ained om municipal ga den
immings mixed wi h sewage sludge; MV: manu e e micompos ; CPB: compos ed pine ba k.
Ryeg ass Cu Zn Pb Cd
MSWC1 29 ±3 c 103 ±14 c 0.3 ±0.2 a 0.17 ±0.02 b
MSWC2 32 ±2 c 133 ±4 d 0.12 ±0.01 a 0.17 ±0.03 b
MSGW 19 ±2 ab 50 ±9 a 0.2 ±0.1 a 0.02 ±0.004 a
MGSS 23 ±1 b 86 ±8 bc 0.13 ±0.03 a 0.05 ±0.01 a
MV 29 ±1 c 97 ±5 c 0.13 ±0.05 a 0.03 ±0.01 a
CPB 15 ±0.6 a 67 ±1 ab 0.10 ±0.1 a 0.05 ±0.004 a
Re e ence alues [35] 5–10 25–47 0.4–5 0.1–0.6
Le uce Cu Zn Pb Cd
MSWC1 24 ±1 b 101 ±8 b 0.50 ±0.12 b 0.49 ±0.05 c
MSWC2 31 ±3 c 128 ±18 b 0.32 ±0.09 ab 0.48 ±0.05 c
MSGW 10 ±1 a 66 ±9 a 0.21 ±0.06 a 0.11 ±0.01 a
MGSS 11 ±1 a 107 ±10 b 0.19 ±0.04 a 0.33 ±0.02 b
MV 23 ±2 b 115 ±14 b 0.14 ±0.05 a 0.23 ±0.06 b
Re e ence alues [35] 6–8 44–73 0.7–3.6 0.40–0.66
Figu e 1. Compa ison o me al concen a ions (d y weigh ) ound in plan s o he wo species.
In . J. En i on. Res. Public Heal h 2020,17, 2887 6 o 10
Plan concen a ions o Zn, Cu and Cd inc eased wi h hei concen a ions in compos , whe eas
his ela ion was no obse ed o Pb (Figu e 2), ha , as men ioned ea lie , was ans e ed o a much
lowe ex en han he o he elemen s. In his sense, plan s g own in he compos MSGW p esen ed he
lowes me al concen a ions, whe eas he plan s g own in MSWC2 and MSWC1, especially he i s ,
always p esen ed he highes concen a ions. The la ge di e ences in me al con en s be ween hese
compos s (Table 1) mus be he main ac o explaining he esul s. In addi ion, he compos MSGW
p esen ed a pH which was almos one uni highe han all he o he compos s, which can also p oduce
a educ ion in me al ans e ence. The a ios be ween he concen a ion o he elemen in plan and in
compos ( ans e ac o , a e aged o all ea men s) we e ma kedly lowe o Pb (0.002 in yeg ass
and 0.003 in le uce) han o Cu (0.15 in yeg ass and 0.10 in le uce), Cd (a ound 0.05 in yeg ass and
0.15 in le uce) o Zn (0.15 in yeg ass and 0.18 in le uce), indica ing he lowe bioa ailabili y o Pb in
compos wi h espec o he o he elemen s.
Figu e 2. Rela ionships o concen a ions o me als in plan s and compos s.
This low isk o ans e ence o Pb o plan , despi e i s high o al concen a ion in some compos s,
is in ag eemen wi h he li e a u e, ha shows ha his elemen has excep ionally low mobili y and
bioa ailabili y in compos -amended soils [
20
] and low ex ac abili y in compos [
22
,
42
,
43
]. The ew
s udies whe e plan s ha e been g own di ec ly in compos gi e he same esul s [
37
,
38
,
40
]. This is
an e ec o he low mobili y o Pb a alkaline pH and i s s ong a ini y o o ganic ma e , ha can
immobilize i in poo ly soluble o ms, hus limi ing up ake and ansloca ion o plan oliage in ha m ul
amoun s. The e o e, he soil-plan ba ie p o ec s he ood chain in his case and up ake o his elemen
by edible plan s should no be a p oblem o human heal h [35].
Plan ans e ence o Cu and Zn was highe han o Pb. The high bioa ailabili y o compos
Zn and he lowe ans e ence o Cu wi h espec o Zn ha e also been consis en ly obse ed in
compos -amended soils [
20
] and in ege ables g owing in di e en compos s [
36
–
39
]. In p e ious
wo ks whe e we assessed he po en ial bioa ailabili y o me als in hese compos s using chemical
ex ac ions, we also obse ed ha Zn was he elemen wi h he highes po en ial mobili y, ei he in
he compos s [
22
] o in soils amended wi h hem [
28
]. The lowe bioa ailabili y o Cu is a ibu ed
o a s onge associa ion o Cu o soil componen s, so plan s a e able o egula e i s abso p ion mo e
In . J. En i on. Res. Public Heal h 2020,17, 2887 7 o 10
e ec i ely han in he case o Zn [
35
]. In any case, hese elemen s do no commonly ep esen a isk o
human heal h, as phy o oxici y may limi hei plan con en s in sa e le els o ch onic inges ion.
Plan Cd in his s udy emained in concen a ions ypical o non-con amina ed soils. Al hough
Cd concen a ions in he plan we e low, his elemen was ans e ed in simila a ios o Cu o Zn,
wi h espec o i s concen a ion in compos , so ha he isk associa ed o Cd would be highe han o
Pb. In addi ion, he s ong in luence o pH on he mobili y and plan up ake o his elemen mus be
kep in mind: o example, Eklind e al. [
36
] obse ed a s ong nega i e co ela ion be ween subs a e
pH and Cd concen a ions in plan s, ha inc eased exponen ially wi h dec easing pH. This esul ed in
unaccep ably high Cd le els in ansplan s g own in e y acid subs a es. In his sense, i is impo an
o emembe ha he alkaline pH o u ban was es compos s helps educe mobili y, no only o Cd, bu
o o he me als oo. O e all, e y low ans e s o hea y me als o plan issues occu in high pH
and calca eous soils [
20
], and i has been obse ed ha , in some cases, pH can be mo e impo an in
con olling plan a ailabili y han ac ual hea y me al concen a ions in compos [
36
]. In his sense,
i is in e es ing o highligh he ac ha , when we compa e ac ual plan ans e ence wi h measu es
o me al a ailabili y in he compos s (Table 4), o al concen a ions a e he bes co ela ed o plan
con en s, whe eas wa e -ex ac able ac ions a e he wo s .
Table 4.
Co ela ions be ween hea y me al concen a ions in plan s g own in he mix u es o compos s
and pine ba k compos and he esul s o chemical ex ac ions o compos s om Pa adelo e al. [
22
] o
all elemen s oge he . Signi icance o co ela ions is indica ed as ollows: ** signi ican a a p- alue o
0.01; *** signi ican a a p- alue o 0.001.
To al DTPA-Ex ac able TCLP Wa e -Ex ac able
Ryeg ass 0.83 *** 0.74 *** 0.78 *** 0.28
Le uce 0.80 *** 0.76 ** 0.70 ** 0.22
The in e p e a ion o he esul s o his wo k may di e depending on whe he compos is going
o be used as a soil amendmen o as a componen o high-compos subs a es. In his s udy, plan s
we e no g own in soil, bu in mix u es wi h high amoun s o u ban was e compos s, much highe han
wha is usual in compos -amended soils. Thus, he isk associa ed o hea y me al up ake by plan s in
soil would be e en lowe han wha we ha e ound he e. In a compos -amended soil, oo s quickly
g ow h ough he illed soil dep h, whe e he applied me als accumula e, and hen a e much less likely
o be ha med by he me als [
18
]. In u n, in po s udies, oo s a e cons ained o he compos , and i has
been obse ed ha me al concen a ions a e highe in plan s g own in po s han in he same plan s
g own in he ield [
18
]. The e o e, he esul s o his wo k a e mo e signi ican o applica ions whe e
high amoun s o compos a e used, such as soilless subs a es o ho icul u e o oo op ga dens.
Fu he mo e, he in ended use o he subs a e is decisi e o isk conside a ion: is i going o be used
o ood p oduc ion o o some o he use? Ob iously, he accumula ion o hea y me als is a much
less se ious p oblem in con aine cul u e o o namen als han whe e compos s a e used in c ops o
human o animal consump ion. And inally, i is essen ial keeping in mind he in luence o pH on
me al bioa ailabili y. Since acidi y inc eases me al up ake, he pH o compos s and subs a es mus be
con olled ca e ully in applica ions in ol ing ood p oduc ion.
4. Conclusions
G owing le uce and yeg ass on subs a es based on u ban was es compos has shown ha me al
up ake in bo h species ollowed, in all cases, he sequence Zn >Cu >> Pb
≥
Cd, which is he same
sequence as he o al concen a ions in ou ou o he i e compos s. Plan concen a ions o Zn, Cu
and Cd inc eased wi h hei concen a ions in compos , whe eas his ela ion was no obse ed o Pb.
The a ios be ween elemen concen a ion in plan and compos we e much highe o Zn, Cd and Cu
han o Pb, showing he lowe bioa ailabili y o Pb wi h espec o o he me als. The ans e ence o
Cu, Pb and Zn o plan ollowed simila ends in bo h species, bu Cd was mo e ans e ed o le uce
In . J. En i on. Res. Public Heal h 2020,17, 2887 8 o 10
han o yeg ass. We ound highe Cu and Zn con en s in plan s o ha which is e e enced in he
li e a u e as no mal o plan s g own in non-con amina ed soils, and simila o lowe o Pb and Cd,
and, in any case, a om he EU h esholds o ood secu i y p o ec ion. In summa y, he isk o plan
ans e ence o hea y me als in amoun s ha ep esen a conce n o he ood chain is low, e en when
g owing ege ables di ec ly on compos wi h high concen a ions o hese elemen s.
Au ho Con ibu ions:
Au ho con ibu ions we e as ollows: concep ualiza ion, R.P. and M.T.B.; me hodology,
M.T.B., R.P. and A.V.; alida ion, A.V. and R.P.; o mal analysis, R.P. and A.V.; in es iga ion, R.P. and A.V.; esou ces,
M.T.B.; da a cu a ion, R.P. and A.V.; w i ing—O iginal d a p epa a ion, R.P.; w i ing—Re iew and edi ing, R.P.
and M.T.B.; isualiza ion, R.P.; supe ision, M.T.B. and R.P.; p ojec adminis a ion, M.T.B. and R.P.; unding
acquisi ion, M.T.B. and R.P. All au ho s ha e ead and ag eed o he published e sion o he manusc ip .
Funding:
This esea ch was unded by he Spanish Minis y o Economy and Compe i i eness (MINECO),
h ough a “Ramón y Cajal” ellowship, g an numbe RYC-2016-19286.
Con lic s o In e es :
The au ho s decla e no con lic o in e es . The unde s had no ole in he design o he
s udy; in he collec ion, analyses, o in e p e a ion o da a; in he w i ing o he manusc ip , o in he decision o
publish he esul s.
Re e ences
1.
Ha g ea es, J.C.; Adl, M.S.; Wa man, P.R. A e iew o he use o compos ed municipal solid was e in
ag icul u e. Ag ic. Ecosys. En i on. 2008,123, 1–14. [C ossRe ]
2.
S i as a a, V.; de A aujo, A.S.F.; Vaish, B.; Ba el -Hun , S.; Singh, P.; Singh, R.P. Biological esponse o using
municipal solid was e compos in ag icul u e as e ilize supplemen . Re . En i on. Sci. Bio echnol.
2016
,15,
677–696. [C ossRe ] [PubMed]
3.
Ba al, M.T.; Moldes, A.B.; Cend
ó
n, Y.; D
í
az-Fie os, F. Assessmen o municipal solid was e compos quali y
using s anda dized me hods be o e p epa a ion o plan g ow h media. Was e Manag. Res.
2007
,25, 99–108.
[C ossRe ]
4.
He e a, F.; Cas illo, J.E.; Chica, A.F.; L
ó
pez Bellido, L. Use o municipal solid was e compos (MSWC) as a
g owing medium in he nu se y p oduc ion o oma o plan s. Bio esou . Technol.
2008
,99, 287–296. [C ossRe ]
5.
Fa ell, M.; Jones, D.L. C i ical e alua ion o municipal solid was e compos ing and po en ial compos
ma ke s. Bio esou . Technol. 2009,100, 4301–4310. [C ossRe ]
6.
Pa k, J.H.; Lamb, D.; Panee sel am, P.; Choppala, G.; Bolan, N.; Chung, J.-W. Role o o ganic amendmen s
on enhanced bio emedia ion o hea y me al (loid) con amina ed soils. J. Haza d. Ma e .
2011
,185, 549–574.
[C ossRe ]
7.
Sil e i, M.; Demu as, D.; Ga au, G.; Deiana, S.; Cas aldi, P. So p ion o Pb, Cu, Cd, and Zn by municipal
solid was e compos s: Me al e en ion and deso p ion mechanisms. Clean Soil Ai Wa e
2017
,45, 1600253.
[C ossRe ]
8.
Pa adelo, R.; Vecino, X.; Moldes, A.B.; Ba al, M.T. Po en ial use o compos s and e micompos s as low-cos
adso ben s o dye emo al: An o e looked applica ion. En i on. Sci. Pollu . Res.
2019
,26, 21085–21097.
[C ossRe ]
9.
Cogge , C.G. Po en ial compos bene i s o es o a ion o soils dis u bed by u ban de elopmen . Compos
Sci. U il. 2005,13, 243–251. [C ossRe ]
10.
Heyman, H.; Bassuk, N.; Bonho al, J.; Wal e , T. Compos quali y ecommenda ions o emedia ing u ban
soils. In . J. En i on. Res. Public Heal h 2019,16, 3191. [C ossRe ]
11.
So amenou, J.; Pa o , L. Sus ainable u ban ag icul u e and he adop ion o compos s in Came oon. In . J.
Ag ic. Sus ain. 2013,11, 282–295. [C ossRe ]
12.
Ulm, F.; A ela , D.; Hobson, P.; Penha-Lopes, G.; Dias, T.; M
á
guas, C.; C uz, C. Sus ainable u ban ag icul u e
using compos and an open-pollina ed maize a ie y. J. Clean. P od. 2019,212, 622–629. [C ossRe ]
13.
G a d, B.J.-P.; Bel, N.; Ma chal, N.; Mad e, F.; Cas ell, J.-F.; Cambie , P.; Houo , S.; Manoucheh i, N.;
Besancon, S.; Michel, J.-C.; e al. Recycling u ban was e as possible use o oo op ege able ga den.
Fu u e Food J. Food. Ag ic. Soc. 2015,3, 21–34.
14.
Ma lock, J.M.; Rowe, D.B. Does compos selec ion impac g een oo subs a e pe o mance? Measu ing
physical p ope ies, plan de elopmen , and uno wa e quali y. Compos Sci. U il.
2017
,25, 231–241.
[C ossRe ]
In . J. En i on. Res. Public Heal h 2020,17, 2887 9 o 10
15.
Pa adelo, R.; Basan a, R.; Ba al, M.T. Wa e -holding capaci y and plan g ow h in compos -based subs a es
modi ied wi h polyac ylamide, gua gum o ben oni e. Sci. Ho ic. Ams . 2019,243, 344–349. [C ossRe ]
16.
Eksi, M.; Rowe, D.B.; Fe n
á
ndez-Cañe o, R.; C egg, B.M. E ec o subs a e compos pe cen age on g een
oo ege able p oduc ion. U ban Fo . U ban G een. 2015,14, 315–322. [C ossRe ]
17.
Diacono, M.; Mon emu o, F. Long- e m e ec s o o ganic amendmen s on soil e ili y. A e iew. Ag on.
Sus ain. De . 2010,30, 410–422. [C ossRe ]
18.
Chaney, R.L.; B own, S.L.; Malik, M.; Siebielec, G.; Kukie , U.; Ryan, J.A.; Angle, J.S. Hea y me al aspec s
o compos use. In Compos U iliza ion in Ho icul u al C opping Sys ems; S o ella, P.J., Kahn, B.A., Eds.;
CRC P ess: Boca Ra on, FL, USA, 2001; pp. 323–359.
19.
Ti a elli, F.; Pe uzelli, G.; Pezza ossa, B.; Ci ilini, M.; Benede i, A.; Sequi, P. Quali y and ag onomic use o
compos . In Compos Science and Technology; D
í
az, L.F., de Be oldi, M., Bidlingmaie , W., S en i o d, E., Eds.;
Else ie : Ams e dam, The Ne he lands, 2007; pp. 119–157.
20.
Smi h, S.R. A c i ical e iew o he bioa ailabili y and impac s o hea y me als in municipal solid was e
compos s compa ed o sewage sludge. En i on. In . 2009,35, 142–156. [C ossRe ]
21.
Lopes, C.; He a, M.; F anco-U
í
a, A.; Roca, E. In en o y o hea y me al con en in o ganic was e applied as
e ilize in ag icul u e: E alua ing he isk o ans e in o he ood chain. En i on. Sci. Pollu . Res.
2011
,18,
918–939. [C ossRe ]
22. Pa adelo, R.; Villada, A.; De esa-Rey, R.; Moldes, A.B.; Domínguez, M.; Pa iño, J.; Ba al, M.T. Dis ibu ion
and a ailabili y o ace elemen s in municipal solid was e compos s. J. En i on. Moni o .
2011
,13, 201–211.
[C ossRe ]
23.
AENOR (Asociaci
ó
n Española de No malizaci
ó
n y Ce i icaci
ó
n). Soil Imp o e s and G owing Media.
De e mina ion o Ph; AENOR: Mad id, Spain, 2001.
24.
AENOR (Asociaci
ó
n Española de No malizaci
ó
n y Ce i icaci
ó
n). Soil Imp o e s and G owing Media.
De e mina ion o Elec ical Conduc i i y No ma Española UNE-EN 13038; AENOR: Mad id, Spain, 2001.
25.
AENOR (Asociaci
ó
n Española de No malizaci
ó
n y Ce i icaci
ó
n). Soil Imp o e s and G owing Media—
De e mina ion o O ganic Ma e Con en and Ash; AENOR: Mad id, Spain, 2001.
26.
AENOR (Asociaci
ó
n Española de No malizaci
ó
n y Ce i icaci
ó
n). Soil Imp o e s and G owing Media—Ex ac ion
o Aqua Regia Soluble Elemen s; AENOR: Mad id, Spain, 2002.
27.
AENOR (Asociaci
ó
n Española de No malizaci
ó
n y Ce i icaci
ó
n). Soil Imp o e s and G owing
Media—De e mina ion o Ni ogen—Pa 1: Modi ied Kjeldahl Me hod; AENOR: Mad id, Spain, 2002.
28.
Moldes, A.; Cend
ó
n, Y.; L
ó
pez, E.; Ba al, M.T. Biological quali y o po ing media based on MSW compos s:
A compa a i e s udy. Compos Sci. U il. 2006,14, 296–302. [C ossRe ]
29.
R Co e Team. R: A Language and En i onmen o S a is ical Compu ing; R Founda ion o S a is ical Compu ing:
Vienna, Aus ia, 2018; A ailable online: h p://www.R-p ojec (accessed on 1 Janua y 2018).
30.
Fox, J.; Bouche -Vala , M. Rcmd : R Commande . R Package Ve sion 2.6-1. A ailable online: h p://socse .
socsci.mcmas e .ca/j ox/Misc/Rcmd /(accessed on 1 Janua y 2018).
31.
Minis e io de Ag icul u a. Real Dec e o 506/2013, de 28 de junio, sob e p oduc os e ilizan es. B.O.E.
2013
,
164, 51119–51207.
32.
Pa adelo, R.; Moldes, A.B.; P ie o, B.; Sandu, R.-G.; Ba al, M.T. Can s abili y and ma u i y be e alua ed in
inished compos s om di e en sou ces? Compos Sci. U il. 2010,18, 22–31. [C ossRe ]
33.
Pa adelo, R.; Villada, A.; Ba al, M.T. Chemical ac iona ion o ace elemen s in a me al- ich amphiboli e
soil amended wi h municipal solid was e compos s. Was e Biomass Valo iz. 2018,9, 1935–1943. [C ossRe ]
34.
Masague , A.; Beni o, M. E aluaci
ó
n de la calidad del compos . In Compos aje; Mo eno, J., Mo al, R., Eds.;
Mundi-P ensa: Mad id, Spain, 2008; pp. 285–304.
35. Kaba a-Pendias, A.; Pendias, H. T ace Elemen s in Soils and Plan s; CRC P ess: Boca Ra on, FL, USA, 1984.
36.
Eklind, Y.; Räme , B.; Wi s ad, M. E alua ion o g owing media con aining a mya d manu e compos ,
household was e compos o chicken manu e o he p opaga ion o le uce (Lac uca sa i a L.) ansplan s.
Biol. Ag ic. Ho ic. 2001,19, 157–181. [C ossRe ]
37.
Zubillaga, M.S.; La ado, R.S. Hea y me al con en in le uce plan s g own in biosolids compos . Compos
Sci. U il. 2002,10, 363–367. [C ossRe ]
38.
In awongse, M.; Dean, J.R. Up ake o hea y me als by ege able plan s g own on con amina ed soil and
hei bioa ailabili y in he human gas oin es inal ac . Food Addi . Con am. 2006,23, 36–48. [C ossRe ]