ORIGINAL RESEARCH
published: 16 Oc obe 2018
doi: 10.3389/ su s.2018.00068
F on ie s in Sus ainable Food Sys ems | www. on ie sin.o g 1Oc obe 2018 | Volume 2 | A icle 68
Edi ed by:
Paula Al a enga,
Ins i u o Supe io de Ag onomia (ISA),
Po ugal
Re iewed by:
Eng acia Madejon,
Ins i u e o Na u al Resou ces and
Ag obiology o Se ille (CSIC), Spain
Raul Zo noza,
Uni e sidad Poli écnica de Ca agena,
Spain
*Co espondence:
Ma ía T. Gómez-Sagas i
[email p o ec ed]
Special y sec ion:
This a icle was submi ed o
Was e Managemen in
Ag oecosys ems,
a sec ion o he jou nal
F on ie s in Sus ainable Food Sys ems
Recei ed: 27 June 2018
Accep ed: 24 Sep embe 2018
Published: 16 Oc obe 2018
Ci a ion:
Gómez-Sagas i MT, He nández A,
A e xe U, Ga bisu C and Bece il JM
(2018) How Valuable A e O ganic
Amendmen s as Tools o he
Phy omanagemen o Deg aded
Soils? The Knowns, Known
Unknowns, and Unknowns.
F on . Sus ain. Food Sys . 2:68.
doi: 10.3389/ su s.2018.00068
How Valuable A e O ganic
Amendmen s as Tools o he
Phy omanagemen o Deg aded
Soils? The Knowns, Known
Unknowns, and Unknowns
Ma ía T. Gómez-Sagas i1*, An onio He nández1, Unai A e xe1, Ca los Ga bisu2and
José M. Bece il1
1Depa men o Plan Biology and Ecology, Uni e si y o he Basque Coun y UPV/EHU, Bilbao, Spain, 2Depa men o
Conse a ion o Na u al Resou ces, NEIKER-Tecnalia, De io, Spain
Nowadays, soil unc ionali y and p oduc i i y a e se e ely impai ed due, in g ea pa ,
o he ac ha mos o he land is being in ensi ely used o ood p oduc ion
and u baniza ion pu poses, wi h a consequen ise in he gene a ion o was es and
consump ion/deg ada ion o e ile soils. These issues can be join ly add essed by
an in eg a ed and sus ainable managemen o he soil esou ce ca ied ou in he
amewo k o wo ecen pa adigms: ci cula economy and phy omanagemen . Wi hin
he ields o esou ce conse a ion and egene a i e (u ban) land managemen , a leas
he h ee ollowing undamen al aspec s can be con empla ed: (i) he alo iza ion and sa e
eco e y o o ganic was es (e.g., compos s, g een and animal manu es, and biosolids)
as soil amendmen s ( om esidue o esou ce); (ii) he e-de elopmen and e ege a ion
o deg aded soils cha ac e ized by low o ganic ma e con en , de icien physical
s uc u e and dep essed biological s a us ( om ba e o ege a ed soil); and, inally, (iii)
he p omo ion o soil heal h in o de o suppo soil ecological p ocesses, unc ions
and concomi an ecosys em se ices (in eg a ion o ecocen ic and an h opocen ic
pe spec i es). He e, we discuss he bene i s (knowns), po en ial isks (known unknowns)
and u u e/a o dable unce ain ies (unknowns) esul ing om he applica ion o o ganic
amendmen s (OAs) o soil. T adi ionally, mos s udies ha e used physical-chemical
pa ame e s o assess soil heal h/quali y, whe eas less a en ion has been paid o soil
biological c i e ia. Thus, we highligh he ele ance o soil biological p ope ies as key
d i e s o ecological es o a ion and sui able indica o s o soil heal h. No wi hs anding,
special a en ion should be paid o “amendmen s-plan s-mic oo ganisms” in e ac ions
in di e en soils and ield condi ions. Finally, he isk o in oduc ion o eme ging
con aminan s, including o ins ance mic oplas ics and an ibio ic esis ance genes
(ARGs), h ough he applica ion o OAs o soil, is cu en ly a ma e o much conce n
ha mus u gen ly be add essed i we a e o con inue wi h such p ac ice.
Keywo ds: ci cula economy, deg aded soils, con amina ion, mic oplas ics, an ibio ic- esis ance genes, soil
heal h, soil quali y
Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
PHYTOMANAGEMENT STRATEGIES FOR
THE “SOFT RE-USE” OF SOILS:
PROMISING APPROACH INTO THE
CIRCULAR ECONOMY PARADIGM
Acco ding o global demog aphic p ojec ions, by he yea 2050
he wo ld’s popula ion will each, a leas , nine billion people.
This ac , oge he wi h he cu en scena ios o accele a ed
u baniza ion and clima e change, poin s ou o a majo challenge
o ou p esen socie y: how o inc ease ood and ene gy
p oduc ion whils p ese ing ecosys em heal h. Fo una ely,
he e is inc easing ecogni ion ha he p o ec ion o soil heal h is
c i ical o he s abili y o he en i onmen al, economic and social
sphe es (Jones e al., 2012; Glæsne e al., 2014). In pa icula , we
mus lea n how o sus ainably manage he soil esou ce so ha i
keeps on p o iding an essen ial sui e o ecosys em unc ions (e.g.,
p o isioning, egula ing, habi a , in o ma ion) and se ices (e.g.,
ood p oduc ion, o ganic ma e decomposi ion, nu ien cycling,
wa e egula ion, con ol o pes s and diseases, cul u al he i age,
e c.). He eina e , we will use he e m “soil heal h” o e e o he
con inued capaci y o soil o unc ion as a i al li ing sys em and
he closely connec ed e m “soil quali y” o indica e he i ness o
soil o a speci ic land-use, such as plan g ow h (Gómez-Sagas i
e al., 2012; Laish am e al., 2012).
The so-called “G een Re olu ion” en ailed he mode niza ion
o adi ional ag icul u e by in oducing mechaniza ion,
i iga ion, gene ically imp o ed high-yield g ain a ie ies, and
syn he ic ag ochemicals, in o de o inc ease c op p oduc i i y.
Howe e , he o e use o wa e and soil esou ces and he
indisc imina e inpu s o ag ochemicals ha e undoub edly aken
a oll on he heal h o ag icul u al soils. Wi hin his con ex ,
he egene a i e and esou ce-conse ing ag icul u e pu sues
he in eg a ion o high c op p oduc ion wi h he sus ainable
managemen o he soil esou ce (i.e., he p o ec ion o i s
physical, chemical, and biological p ope ies), while minimizing
he use o ex e nal and non- enewable inpu s.
Unde s ood as a s a egic non- enewable esou ce a human
scale, soils cons i u e dynamic, complex, and mul i- unc ional
ecosys ems ha lie a he in e ace be ween he a mosphe e,
hyd osphe e, li hosphe e and biosphe e. E osion, compac ion,
sealing, saliniza ion, con amina ion, loss o soil o biodi e si y,
loods, landslides, and decline o soil o ganic ma e (SOM) ha e
been iden i ied as he main h ea s ha lead o soil deg ada ion
(Food and Ag icul u e O ganiza ion o he Uni ed Na ions
(FAO), 2015; Ka len and Rice, 2015). I comes, he e o e, a no
su p ise ha he Eu opean Union ecognizes soil deg ada ion
as a “se ious p oblem” and emphasizes he u gen need o a
mo e holis ic app oach o soil p o ec ion (Palea i, 2017). In 2006,
he Eu opean Commission p esen ed he “Thema ic S a egy o
Soil P o ec ion” (COM(2012)46), which included a p oposal o
a Soil F amewo k Di ec i e and Impac Assessmen . Howe e ,
in 2014, such p oposal was ejec ed. Wi hou exclusi e soil
legisla ion, nowadays, he legal p o ec ion o soils is in eg a ed
in o he al eady de eloped Eu opean Di ec i es (e.g., EU
Di ec i e on En i onmen al Liabili y 2004/35/CE). The e is a
igh linkage among speci ic soil h ea s, soil mul i- unc ionali y
and ecosys em se ices (Bünemann e al., 2018), bu his
pe spec i e has a ely been implemen ed o he assessmen o
soil heal h/quali y.
In ecen yea s, soil heal h/quali y is se e ely h ea ened by he
unwa e ing changes o land-use and deple ion o SOM (Vimal
e al., 2017). In ac , app oxima ely 45% o Eu opean opsoils
(0–30 cm) a e cha ac e ized by low SOM con en (<3.5%)
(Eu opean Commission, 2006; Ma ínez-Blanco e al., 2013), and
p incipally soils o Medi e anean egions a e e y suscep ible
o i s loss, whe e nea ly 75% o soils has a low (≤2%) o e y
low (≤1%) SOM con en (Sch eude and De Visse , 2014), being
mos o hem conside ed deg aded soils. Deg aded soils a e hose
o en a isen om abandonmen o u al a eas and ag icul u al
p ac ices (Benayas e al., 2007; Rod igo-Comino e al., 2017),
as well as om u ban acan and de elic lands usually loca ed
wi hin he ci y limi s (Néme h and Langho s , 2014; Kuma and
Hundal, 2016). As hese a eas a e equen ly used as dumpsi es,
hei soils a e usually cha ac e ized by poo soil s uc u e, low
SOM (Ga cía e al., 2017) and, o en imes by low con aminan
le els. While ecen a en ion has been la gely ocused on he
eclama ion o u ban b own ields (i.e., highly con amina ed
and indus ialized si es), ew esea ches ende a en ion o he
as po en ial o u ban acan and de elic si es as a esou ce
o e-de elopmen and achie emen o economic and social
bene i s (Kim e al., 2018) by, o ins ance, he applica ion o
phy omanagemen p ac ices.
A he same ime as he sca ci y o e ile soil is sha pening, he
as economic and demog aphic g ow h is leading o a massi e
gene a ion o o ganic was es de i ed om human ac i i ies,
wi h hei subsequen en i onmen al impac s and managemen
cos s. Consequen ly, was es in gene al and o ganic ones in
pa icula a e inc easingly being iewed as po en ial esou ces. In
ac , conside ing con empo a y socie al demands and inc easing
cos o ag ochemicals (Thanga ajan e al., 2013), a sus ainable
es o a ion o unc ionali y and e ili y o such deg aded soils
can be achie ed h ough he applica ion o o ganic amendmen s
(OAs) de i ed om p ope ly ea ed o ganic was es such as
compos s, c ops esidues, animal manu es, and biosolids (Apa na
e al., 2014; Ree e e al., 2016).
The eu iliza ion o o ganic was es as soil condi ione s/ene gy
supplie s is an old bu inc easingly popula p ac ice ha no only
helps o educe ag ochemicals dependence, bu also ep esen s
an ecologically-sound, economically-a ac i e and socially-
accep able al e na i e o land ill disposal and incine a ion and,
likewise, con ibu es owa d he objec i es o he EU’s “Ze o
Was e” Policy, “End-O -Was e” Policy, and “Ci cula Economy
S a egy” (Sa eyn and Ede , 2014). To comba soil deg ada ion
in a sus ainable way, he Ci cula Economy (CE) concep
has ecen ly gained momen um in he deba es on was e and
esou ce managemen . Unlike open lineal models o p oduc ion
and consump ion (“p oduc ion-use-disposal”), CE p omo es
esou ce closed-loops, meaning ha la ge olumes o ini e
esou ces (me als and mine als, among o he s), and su plus
o ganic was es a e cap u ed and eused, educing he need
o ex ac ion o aw ma e ials (P es on, 2012). In Eu ope,
e o s a e unde way o comp ehensi e legisla i e b eak h oughs
along wi h ac ions o was e educ ion, managemen , and
F on ie s in Sus ainable Food Sys ems | www. on ie sin.o g 2Oc obe 2018 | Volume 2 | A icle 68
Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
ecycling (Zuin, 2016), wi h a iew o p o ide a mo e holis ic
app oach o sus ainabili y (Geissdoe e e al., 2017). Al hough
he applica ion o OAs o soil has a long his o y as an
economically- easible and e ec i e p ac ice (Vimal e al., 2017),
i s known (eu ophica ion, p esence o eco oxic con aminan s
and pa hogens, e c.) and eme ging isks [mic oplas ics and
dissemina ion o plasmid-con aining an ibio ic esis ance genes
(ARGs), e c.], oge he wi h he OA-plan -mic oo ganism
ipa i e in e ac ions, need o be u he in es iga ed.
In his en i onmen al scena io, he managemen and
sus ainable es o a ion o u ban acan lands and o he deg aded
a eas o en equi e a di e en app oach om ha applied o
na u al o ag icul u al soils (De Lucia e al., 2013). In his
ega d, phy omanagemen has eme ged as a new pa adigm
ha allows he e-use and e-de elopmen o deg aded and/o
con amina ed si es. Phy omanagemen is o en ou ed as a sui e
o managemen s a egies, based on gen le emedia ion op ions,
which, alongside isk managemen , place ealiza ion o o he
bene i s (including economic and social bene i s) a he co e o
si e design (Cundy e al., 2016). In phy omanagemen , plan -
based sys ems a e used as a “holding s a egy” while concu en ly
seeking o ecological (e.g., es o a ion o ecosys em unc ions
and se ices), economical (e.g., biomass and ene gy gene a ion,
si e alue upli o su oundings) and social bene i s (e.g., u ban
clima e managemen , ecosys em se ices, ameni y, and leisu e;
Cundy e al., 2016). Phy omanagemen usually encompasses a
combina ion o biomass and ene gy c ops (and hei associa ed
mic oo ganisms), and he applica ion o OAs o he eco e y o
unde u ilized lands (e.g., deg aded and/o con amina ed soils).
Thus, phy omanagemen gene a es a synch onous imp o emen
o soil biological unc ions and ecosys em se ices (i.e., c op
pe o mance) h ough an e ec i e eco e y o land p o i abili y.
Thus, he main goal o his e iew is o ou line he po en ial
p o i s and d awbacks con e ed by ecen ly used OAs o
soil es o a ion as a ou ine phy omanagemen p ac ice. This
wo k is o ganized as ollows: i s , a b ie and cu en (2013–
2018) li e a u e e iew, ha explo es he posi i es and nega i es
impac s o he applica ion o di e en OAs on he soil physico-
chemical and biological p ope ies, is p esen ed, whe eby
he mos ele an endpoin e ec s in plan and associa ed
mic oo ganisms a e summa ized. La e , g ea e a en ion is paid
o eme ging con aminan s associa ed wi h o ganic amendmen s
(conc e ely o mic oplas ics and an ibio ic- esis ance genes) and
hei su ounding unce ain ies.
WHY ARE ORGANIC AMENDMENTS
RECOGNIZED AS SUITABLE TOOLS FOR
SOIL RESTORATION AND REMEDIATION?
Soil o ganic ma e (SOM), composed o a mix u e o animal,
plan and mic obial esidues a di e en mine aliza ion and
humi ica ion s ages, is o en conside ed he mos de e minan
na u al soil componen inasmuch as i go e ns, in he
long- e m, he physical, chemical, and biological dimensions
o soil heal h (Hijbeek e al., 2017). The e is widesp ead
ecogni ion ha SOM p e en s e osion by imp o ing/s abilizing
bulk s uc u e, po osi y, and wa e holding capaci y, p o ides
essen ial nu ien s o (mic o)bio a ( ha , in u n, con e
hem o plan -a ailable/abso bable o ms; Ree e e al., 2016),
s imula es soil mic obial biomass and ac i i y (La kin, 2015),
allows high biodi e si y (Tu mel e al., 2015), inc eases na u al
supp essi eness agains soil-bo ne pa hogens, and educes
pollu an eco oxici y (Sco i e al., 2015). Co espondingly,
heal hy soils wi h a high o ganic ma e con en a e expec ed o
ha e mo e obus soil communi ies which may esul in mo e
esilien soils (La kin, 2015). In his si ua ion, plan s ecei e
be e nu i ion and p oduce be e de ense esponses, and a e in
gene al less suscep ible o in ec ion by phy opa hogens (La kin,
2015). In his ligh , he es o a ion and main enance o SOM
con en a an adequa e le el is a c i ical objec i e o sa egua d soil
ecosys em se ices (Sco i e al., 2015; Lal, 2016), as e idenced
by some Eu opean policy documen s (Eu opean Commission,
2011a,b) and in e na ional ood secu i y and clima e objec i es
(UNFCCC, 2015).
Conse a ion o SOM can be imp o ed by minimizing illage,
main aining ac i e c op g ow h (sho e allow pe iods), and
con olling e osion (La kin, 2015). O ganic ma e can be added
o soil h ough (i) in- ield sou ces like c op esidues, o a ions
and co e c ops; and (ii) o - ield sou ces such as compos s,
manu es and biosolids (La kin, 2015). Con e sely, hese la e
p ac ices need o be sho - e m balanced no only wi h economic
objec i es (i.e., p o i maximiza ion, labo use e iciency o
minimiza ion o g oss ma gin a ia ion; Hijbeek e al., 2018), bu
also wi h social and en i onmen al objec i es (i.e., soil heal h
and nu i ional secu i y), all o hem mu ually in e dependen
(Geissdoe e e al., 2017).
O e all, he basic bene i s o he di ec addi ion o o ganic
ma e o soil h ough OAs ely on: (i) he inc ease o he
soil o ganic ca bon (SOC) s ock; (ii) he acili a ion o g ow h
and di e si y o soil mic obial communi ies; and (iii) he
enhancemen o a ailable nu ien s (N, P, K, Ca, and Mg),
o en due o he sligh ly acidic pH and also ele a ed soil ca ion
exchange capaci y (CEC), which in u n allows he chela ion,
supply and s o age o essen ial nu ien s, he eby a ec ing
plan nu ien balance (Sco i e al., 2015; Ree e e al., 2016;
Al a enga e al., 2017). E en so, i mus be no iced ha ,
depending on he ype and na u e o he amendmen and
ecei ing soil, OAs could also aise soil pH and, he e o e,
dec ease he bioa ailabili y o bo h essen ial and eco oxic me als,
by shi ing hem o ac ions o low a ailabili y associa ed
wi h OM, ca bona es o me al oxides (Be nal e al., 2007;
Clemen e e al., 2015). O ganic amendmen applica ion is
also epo ed o dec ease soil c us ing and bulk densi y,
bo h essen ial p ope ies o a heal hy soil (Zhao e al., 2009;
Thanga ajan e al., 2013). Among o he p ope ies, OAs can
maximize a s able C s ock eco e y and, a he same ime,
p o ide a con inuous elease o mine al nu ien s, hus sa is ying
c op equi emen s (Sco i e al., 2015). E en hough a la ge
body o empi ical s udies ca ied ou in di e en ag icul u al
sys ems ha e demons a ed he bene i s o OAs as subs i u es
o chemical e ilize s, a numbe o s udies ha e also e idenced
po en ial en i onmen al isks associa ed o hei imp ope ly
applica ion/o e eliance.
F on ie s in Sus ainable Food Sys ems | www. on ie sin.o g 3Oc obe 2018 | Volume 2 | A icle 68
Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
Gi en he wide a ay o OAs, we b ie ly summa ize he speci ic
in luences o ou majo ca ego ies o OAs de ined he e (i.e.,
compos s, c op esidues and g een manu es, animal manu es,
and biosolids) on he physical, chemical, and/o biological
p ope ies o soils (Table 1). This classi ica ion esul s om
he modi ica ion o ha p oposed by Goss e al. (2013). In
his la e wo k, six ca ego ies o OAs we e es ablished: (1)
compos s; (2) ood esidues and was es; (3) g een manu e and
c op esidues; (4) animal manu es; (5) municipal biosolids; and
(6) was es om manu ac u ing p ocesses. We ha e g ouped hem
o ou b oade ca ego ies: (1) and (2) ca ego ies ha e been
me ged in o wha we called “compos s,” since ood esidues
and was es a e equen ly compos ed o land applica ion;
and (5) and (6) ca ego ies ha e been clus e ed in o wha
we called “biosolids” due he simila i y o hei inal sludge
ea men s.
Compos ing ep esen s he mos common op ion o eco e
ma e ial om o ganic was es (Cesa o e al., 2015). O e all,
compos s consis o s able mix u es o la gely decayed o gano-
mine al ma e ial p oduced om ood sc aps, lea es, ca le
manu es o sewage sludges (also e e ed o as “biosolid
compos s”). The egula ions and s anda ds on compos quali y
a y conside ably ac oss Eu opean Membe S a es, mainly due
o di e ences in soil policies, as poin ed ou by Cesa o e al.
(2015) and Be nal e al. (2017). Almos 50% o he o al
amoun o compos p oduced in Eu ope is applied o ag icul u al
soils (Sa eyn and Ede , 2014). Beyond inc easing he SOC
con en , compos amendmen s ha e been shown o inc ease
soil mic obial biomass and ac i i y and modi y he s uc u al
and unc ional di e si y o he na i e mic obial communi ies,
which o en a e indi ec ly in ol ed in he long- e m supp ession
o soil-bo ne plan diseases such as hose caused by Py hium,
Phy oph ho a, and Fusa ium spp. (La kin, 2015; Sco i e al.,
2015). Ne e heless, he high elec ical conduc i i y (EC) o
high C/N a ios o some compos may con ibu e o soil
salini y o can enhance ni ogen immobiliza ion, espec i ely
(Sco i e al., 2015). Addi ionally, mainly in compos ed
biosolids, hea y me als can also be inco po a ed o he soil
sys em.
Despi e o he ple ho a o esea ch ca ied ou o decades
on compos ing, nowadays, an inc eased in e es in i s use as
a sus ainable al e na i e o he biocon ol o phy opa hogens,
as compa ed o he adi ional use o syn he ic ungicides
(Megh ansi and Va ma, 2015), has eme ged. The inc ease in soil
mic obial biomass and ac i i y p o oked by compos applica ion
can lead o a gene al disease supp ession (La kin, 2015).
Gene ally, mic obios asis (inhibi ion o g ow h, ep oduc ion
and mul iplica ion o pa hogens), hype pa asi ism/p eda ion
and induc ion o sys emic esis ance in hos plan s a e
he p incipal mechanisms esponsible o he de elopmen
o soil supp essi eness (i.e., he capaci y o educe disease
incidence caused by soil-bo ne phy opa hogens; (Megh ansi
and Va ma, 2015). Suppo ing his, p e ious me a-analy ical
s udies e idenced ha jus o e hal o compos s esul ed
in signi ican disease supp ession, wi h e ec s a ying o
di e en pa hogens (Bonanomi e al., 2007; Te mo shuizen
e al., 2007). Howe e , he a ia ion and complex in e ac ions
be ween he (i) quali y, ma u i y and decomposi ion ime
o o ganic ma e , (ii) mic obial communi y composi ion,
(iii) phy osys em, and (i ) sap ophy ic abili y o pa hogen
popula ions can lead o inconsis en esul s and hinde he
iden i ica ion o speci ic indica o s o disease supp ession
(Bonanomi e al., 2010; La kin, 2015). In his sense, i is
no ewo hy ha mic obiological p ope ies (e.g., mic obial
biomass and enzyma ic ac i i ies), a he han chemical ones,
esul be e indica o s o supp essi eness (Bonanomi e al.,
2010).
Rega ding c op esidues and g een manu es (e.g., s alks and
s ubble, lea es, and seed pods), when inco po a ed by illage o
e ained on soil su ace, hey (i) enhance assimilable ni ogen
pool by he inco po a ion o eac i e ni ogen compounds; (ii)
e ain soil mois u e; (iii) deli e sizeable inpu o ca bonaceous
ma e ial, immobilizing some ino ganic N p esen in he soil;
and (i ) d ama ically a ec soil mic obial communi ies and,
subsequen ly, he de elopmen o disease-supp essi e soils
(Thanga ajan e al., 2013; La kin, 2015; Tu mel e al., 2015).
Animal manu es (mix o exc emen and u ine om domes ic
animals) and biosolids ( ea ed and s abilized solid o ganic
esidual by-p oduc s de i ed om ag o-indus ial and municipal
was ewa e ea men p ocess) ha e been ecognized as aluable
“nu ien supplie s” owing o hei con en o plan essen ial
mac o- and mic oelemen s, o m soil agg ega es, educe bulk
densi y, and inc ease po osi y and wa e in il a ion/pe cola ion
a e (Thanga ajan e al., 2013; La kin, 2015). Po en ial side-e ec s
o animal manu es and biosolids ha e been epo ed, such as: (i)
high concen a ions o N-NH+
4and N-NO−
3and ele a ed CO2
and CH4emission om ae obic and anae obic decomposi ion,
which lead o g eenhouse gas (GHG) and leacha e emissions;
(ii) inpu o me al(oid)s, like Pb, As, Cu, and Zn, o ganic
con aminan s, an ibio ics and pa hogenic mic oo ganisms; and
inally; (iii) OA applica ion also could incu in an excessi e inpu
o nu ien s (e.g., N and P un o ; Ma ínez-Blanco e al., 2013;
Thanga ajan e al., 2013; Al a enga e al., 2015; Sco i e al., 2015;
Ga cía e al., 2017).
The in ensi y and du abili y o he abo e men ioned bene i s
and isks a e egionally a iable and si e-speci ic (physico-
chemical and biological soil p ope ies) as hey depend on
(i) clima ic and socioeconomic ac o s (Tu mel e al., 2015);
(ii) ype and ea u es o OA (s abili y, ma u i y and in insic
biochemical quali y); (iii) applica ion design (dose, me hod and
equency); and (i ) c opping sys em. The combina ion o any
(o all) hese ac o s explains a iable obse a ions and p e en s
he e ie ing o uni e sal conclusions abou OA applica ion,
making a me a-analy ical app oach impe a i e. Wi hou claiming
o be exhaus i e in excess, Table 1 ga he s compelling e idences
o abo e-men ioned bene i s and po en ial isks on soil-plan
sys em. We conduc ed a li e a u e sea ch in Google Schola
(schola .google.com) da abase using he keywo ds “o ganic,”
“amendmen ,” “soil,” “plan ,” and “heal h” (mos ecen sea ch:
June 6, 2018). Only o iginal a icles published in he las 5 yea s
(2013–2018) we e conside ed. Fo each iden i ied esea ch a icle,
i s ly we e alua ed he i le and abs ac o de e mine whe he
physical o chemical and plan and/o mic obial pa ame e s
we e de e mined. Then, hose a icles ha i ed all hese
F on ie s in Sus ainable Food Sys ems | www. on ie sin.o g 4Oc obe 2018 | Volume 2 | A icle 68
Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
TABLE 1 | Po en ial bene i s and isks on he soil heal h dimensions (physical, chemical, and biological) esul ed om he cu en ly used o ganic amendmen s
(2013–2018).
Compos s C op esidues and g een
manu es
Animal manu es Biosolids
BENEFITS
Physical ⋆
(3,8,16,29,68)
⋆ ⋆
(8,11,19,29,68,70)
⋆⋆
(8,11,19,29,46,59,70)
⋆ ⋆
(3,15,19,29,32,59,60)
Chemical ⋆ ⋆ ⋆ ⋆
(3,4,5,6,7,8,9, 10,
11,12,13,14,16,19,22,24,29,36,
40,42,43,47,48,49,52,54,56,58,63,
64,66,68)
⋆ ⋆
(6,8,11,12,29,31,37,41,61,68,70)
⋆ ⋆ ⋆
(8,11,13,19,26,29,36,40,46,49,56,
59,63,70,71)
⋆ ⋆ ⋆ ⋆
(1,3,4,5,6,9,10,14,15,17,19,20,25,
26,29,32,34,35,38,39,42,44,45,49,
52,55,59,62,64,65,67)
Biological Abo e ⋆ ⋆ ⋆
(4,5,6,8,9,12,16,19,22,24,29,30,40,
42,43,47,48,57,58,63,66,69)
Below ⋆ ⋆ ⋆
(3,7,8,12,13,14,28,36,40, 43,47,
48,49,52,54,56,58,63,64,66,68)
Abo e ⋆ ⋆
(6,8,11,12,29,31,61)
Below ⋆ ⋆
(8,11,12,31,37,41,53,61,68,70)
Abo e ⋆ ⋆
(8,11,19,23,26,29,40,46,63)
Below ⋆ ⋆
(2,8,11,13,36,40,46,49,56,
63,70,71)
Abo e ⋆ ⋆ ⋆
(1,4,5,6,9,15,19,25,26,29,32,33,
34,35,38,39,42,44,45,50,55,62,65,67)
Below ⋆ ⋆ ⋆
(2,3,14,17,20,25,27,28,38,39,45,
49,52,53,64,65,67)
POTENTIAL RISKS
Chemical GHG emissions (e.g CO2, CH4)
(4,8,10)
Me als (6,24,48,49)
Salini y (12)
N inmo iliza ion (24)
B eak-down oxic compounds (30)
GHG emissions (e.g., CH4, N2O)
(8,31,37)
Me als (6,53)
Salini y (12)
GHG emissions (8)
Me als (6,49)
NO−
3leaching (23,26,59)
GHG emissions (e.g., CO2; N2O)
(4,10,50)
Me als (6,33,35,49,53,55)
NO−
3leaching (26,59)
P leaching (39)
B eak-down oxic compounds (30)
To a . 39 11 17 42
Mos o he e ised a icles de e mined a leas a couple o each ollowing indica o s: physical— ex u e, oo ing dep h, bulk densi y, in il a ion, agg ega e s abili y, and wa e -holding
capaci y–; chemical— o al and/o pa icula e o ganic ma e (o o al o ganic C and N), pH, EC, and ex ac able N, P, and K–; and biological—below-g ound (“Below”): mic obial biomass C
and N, mic obial unc ional and s uc u al di e si y, soil espi a ion and enzyme ac i i ies om C-, N-, P- and S-cycling, po en ially mine alizable N; myco hizal (AM ungal) oo coloniza ion;
meso auna/ea hwo m abundance; and abo e-g ound (“Abo e”): biomass, yield, nu i ional s a us, chlo ophyll con en –). The quan i y o s a s e lec s he numbe ange o a icles ha
e idence such bene i ⋆:≤5 a .; “⋆ ⋆”: 5-15 a .; “⋆ ⋆ ⋆”: 15-25 a .; “⋆ ⋆ ⋆ ⋆”: 25-35 a .). Numbe s co espond o he a icles lis ed in he Supplemen a y Ma e ial.
c i e ia we e examined in de ail ( o al numbe o 71 a icles;
Supplemen a y Ma e ial).
Mos o he s udies ca ied ou in he las 5 yea s we e mainly
ield s udies (wi h an a e age du a ion o 1.9 yea s) ocused on
he use o compos s and biosolids (mainly biosolid compos s)
in ag icul u al soils, wi h he main objec i e o s udying hei
e ec s on chemical p ope ies and c op p oduc ion. A la ge
body o he s udies epo ed he esponses o chemical, plan ,
and mic obial pa ame e s (81.7, 70.4, and 60.6%, espec i ely)
and only 18.3% o he examined s udies measu e physical
p ope ies. Al hough he in luence o he na i e mic obial
communi ies o he hizosphe e on plan g ow h and c op
yield is widely ecognized, plan -mic oo ganism in e ac ions a e
s ill bu dened by unce ain y, and his is ce ainly e lec ed in
he low numbe o s udies (only 32.4% o he pape s) ha
collec da a on bo h plan and mic obial p ope ies. We also
no iced ha none o he e ised a icles compiles in o ma ion
abou he po en ial dis u bances o mic obial popula ions o
OA on he biomass, ac i i y, and di e si y o he na i e soil
mic obio a.
I is gene ally assumed ha he in insic mic obial
communi ies o he OA su ende o na i e mic obial
communi ies in he ecei ing soil wi h a minimal impac
on hem (Saison e al., 2006; Bas ida e al., 2008). This is
p obably due o he sho su i al ime o amendmen -bo ne
mic oo ganisms (wi h excep ion o pa hogenics) ollowing land
applica ion (Holm e al., 2010). Howe e , changes occu ing
in soil mic obial communi y a e usually associa ed o he
chemical cha ac e is ics p o ided by he OA whe eas he
impac o OA-bo ne mic oo ganisms (bac e ia and ungi)
a e o en o e looked, as ecognized Tian e al. (2015), Ga cía
e al. (2017), and Ren e al. (2017). Indeed, OAs can in oduce
changes in he biomass, ac i i y and composi ion o he
na i e mic obial communi ies due o compe i ion o a ailable
subs a es and/o an agonisms (Ondoño e al., 2014) and he
deg ee o con aminan emo al (Ros e al., 2006; Mascianda o
e al., 2013). In his ega ds, Galende e al. (2014b) obse ed
ha na i e mic obial communi ies o Zn-Pb mine soil we e
no subs an ially a ec ed by he ollowing amendmen s:
sheep manu e, poul y li e , cow slu y, and pape mill
sludge mixed wi h poul y li e . This could be ela ed o he
na u e o he ha sh en i onmen s o mine soils showing high
le els o me als (Zn, Pb, and Cd), which would allow only
he su i al o na i e ex emophile mic oo ganisms. Tian
e al. (2015) and Llo e e al. (2016) also concluded ha he
mic oo ganisms associa ed o pig manu e based compos and
sewage sludge, espec i ely, did no signi ican ly displace he
na i e mic obio a o ag icul u al soils. In con as , Anas asi
e al. (2009), Pu nomo e al. (2010), and Lin e al. (2016)
asc ibe o compos -bo ne bac e ia and ungi a ele an ole
in go e ning he biodeg ada ion o o ganic compounds in
soils.
F on ie s in Sus ainable Food Sys ems | www. on ie sin.o g 5Oc obe 2018 | Volume 2 | A icle 68
Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
The assessmen and moni o ing o en i onmen al bene i s and
isks associa ed o o ganic managemen o deg aded lands can
be ou inely ca ied ou by a se o simple bu obus indica o s
and minimum da a se (see also Table 1). The mos commonly
used and accep ed indica o s ha ha e meaning o bo h scien is s
and land manage s include: (i) physical p ope ies as ex u e,
oo ing dep h, bulk densi y, in il a ion, agg ega e s abili y, and
wa e -holding capaci y; (ii) chemical p ope ies as o al and/o
pa icula e o ganic ma e (o o al o ganic C and N), pH, EC, and
ex ac able N, P, and K; and (iii) biological p ope ies as mic obial
biomass C and N, mic obial unc ional and s uc u al di e si y,
soil espi a ion and enzyme ac i i ies, po en ially mine alizable
N, ea hwo m popula ions and plan bioassays ( o mo e de ails
see La kin, 2015). In any case, usually he objec i e is o inc ease
c op p oduc ion and heal h.
Mos o he s udies on OA e ec s on plan s ocus on
he analysis o o al biomass p oduc ion. Howe e , o u he
unde s anding o soil heal h-plan in e ac ion, i is necessa y
o explo e o he indica o s o he po en ial phy o oxic e ec s
and physiological s a us o plan s. No wi hs anding, Table 1
e idence he knowledge gap ega ding he sho /long- e m
phy o oxici y and physiological s a us (e.g., ne pho osyn hesis,
anspi a ion, plan wa e po en ial, pho ochemical e iciency
o PSII, pigmen p o iles and seconda y me aboli e con en ,
e c.) o c ops g own in o ganically managed soils. Seed
and/o oo elonga ion plan bioassays pe o med by di ec
exposu e o soil ma ix o indi ec ly o i s leacha es a e
highly ecommended eco oxicological es s o soil phy o oxic
assessmen , being also help ul o amendmen sc eening and
selec ion p og ams. Mo eo e , bioassays using apid-cycling
plan s like dico yledonous Cucumis sa i us (cucumbe ) and
Lac uca sa i a (le uce) (OPPTS 850.4100, 1996; OPPTS
850.4200, 1996; OECD Guidelines o Tes ing o Chemicals
No. 208, 2006; ISO 11269-1, 2012; ISO 11269-2, 2012),
allow measu emen o mul iple endpoin s a biochemical (e.g.,
an ioxidan con en ) and mo phological le el (e.g., su i al and
oo elonga ion; Al a enga e al., 2017).
Meanwhile, soil mic obial p ope ies (i.e., biomass, ac i i y,
unc ional, and s uc u al di e si y) ha e a ac ed g ea
in e es as quick, in eg a i e, and sensi i e indica o s o
soil pe u ba ions (Epelde e al., 2010; Bu ges e al., 2015;
Ga aiyu ebaso e al., 2017) and can se e o iden i y he
magni ude o he imp o emen s b ough abou by managemen
in e en ions (Apa na e al., 2014). These mic obial indica o s
p o ide mo e di ec insigh in o soil heal h/quali y han
adi ional physical and chemical indica o s alone (Ge e al.,
2013). Ex ensi e esea ches showed he ecological ele ance
o mic obial communi ies o hizosphe e in he o ches a ion
o ene gy and nu ien cycling (specially, a e and a e o
mine aliza ion o mac onu ien s), he eby ac ing as bo h
nu ien sou ce and sink (Thanga ajan e al., 2013). Na i e
mic oo ganisms also di ec ly in luence plan heal h by al e ing
physiological and de elopmen p ocesses, acili a ing nu ien
and wa e up ake, and helping plan s ole a e bio ic and
abio ic s ess (Philippo e al., 2013; Ree e e al., 2016). Thus,
p og esses in he knowledge o ecological s a us o he mic obial
communi y wi hin he soil a e necessa y o de e mine he
long- e m e ec s o changing soil quali y (Su e al., 2014; Ga cía
e al., 2017).
The cu en in o ma ion on he e ec o OAs on soil
mic obial p ope ies indica es ha mic obial biomass, usually
in e ed by induced espi a ion, mic obial biomass C (MBC) and
phospholipid a y acid (PFLA) measu emen s, and soil enzymes
whose ac i i ies a e ela ed o he biochemical cycles o N (u ease
and p o ease), S (a ylsulpha ase), P (alkaline-phospha ase), and
C (β-glucosidase) a e highly in luenced by he p esence o
exogenous o ganic ma e . Func ional and s uc u al mic obial
di e si y, despi e o e ealing a g ea sensi i i y o changing soil
condi ions, is mo e di icul o assess (Ha mann e al., 2015). A
p esen , some o he p ima y publica ions deal wi h soil mic obial
di e si y (e.g., Bas ida e al., 2015, 2016; Bonanomi e al., 2016;
Daquiado e al., 2016; Fe nández e al., 2016; Cesa ano e al.,
2017; Tian e al., 2017) in pa because o mul iple “omic”
app oaches (me agenomic, me a ansc ip omic, me ap o eomic,
and me abolomic) ha , in combina ion wi h mo e adi ional
me hods like Biolog mic opla es and dena u ing g adien gel
elec opho esis (DGGE), ha e come o exceed he unce ain ies
su ounding dynamics o mic obial communi y as well as axon
le el. The inco po a ion o soil o e micompos (Wu e al.,
2013; Song e al., 2015), g een esidues (Kim e al., 2013; Aslam
e al., 2014; Tejada and Bení ez, 2014); animal manu es (Bowles
e al., 2014; Ninh e al., 2015; Blanche e al., 2016), and biosolid-
based compos s (Di Bene e al., 2013; Xue and Huang, 2013;
Bonanomi e al., 2014) inc eases signi ican ly plan g ow h and
c op yield, which is p incipally a ibu ed o an enhance o
biomass, ac i i y and di e si y o he mic obial hizosphe e
communi y. Howe e , changes in mic obial p ope ies a y
conside ably in acco dance wi h soil ype (mine al composi ion
and ex u e), na u e, dose and applica ion equency o he OA
and du a ion o he s udy (Ninh e al., 2015; Rea don and Wues ,
2016; Zo noza e al., 2016). The complex in e ac ion ne wo ks in
mic obial communi ies and echnical cons ain s make di icul
ull unde s and o he esponse o mic obial communi ies owa d
OAs (Ha mann e al., 2015).
USING A “WIN-TO-WIN” APPROACH:
ORGANIC WASTES AS AMENDMENTS
FOR AIDED PHYTOSTABILIZATION
STRATEGY IN CONTAMINATED SOILS
Many pe i-u ban acan lands a o me indus ial si es end o
ha e inc eased load o o ganic and ino ganic pollu an s ela i e
o mo e dis an u al a eas (Bas a e al., 2016; Benis on e al.,
2016). Among pollu an s, me als a e especially c i ical as hey a e
cha ac e ized by high s abili y and lack o biodeg adabili y (Zhou
e al., 2017). E en wo se, some me als a e eco oxic and exhibi
long- e m pe sis ence in soil, s ongly a ec ing he s uc u e
and unc ioning o ecosys ems and allowing hei mig a ion
and inco po a ion in o he ophic web un il, inally, endange
human heal h (Deng e al., 2015; Venegas e al., 2015; Ga cía
e al., 2017). As a consequence, and being he public awa eness
a d i ing o ce, esea che s and au ho i ies wo ldwide ha e paid
a en ion o emedia ion o me al con amina ed soils no only
F on ie s in Sus ainable Food Sys ems | www. on ie sin.o g 6Oc obe 2018 | Volume 2 | A icle 68
Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
o en i onmen al and human heal h conce ns (Madejón e al.,
2018), jus as much o he po en ial implica ions o in e na ional
( ood) ade (Pa k e al., 2011).
Soil managemen o hese pollu ed a eas aces dual challenges
o minimizing con aminan exposu e o soil inhabi an s
(including human) and es o ing and main aining soil
unc ioning/heal h by apid de elopmen o h i ing soil
mic obial communi y and plan assemblies (Bas a e al., 2016;
Ob ycki e al., 2017). Resea ch and demons a ion s udies ha e
e idenced ha he applica ion o o ganic soil amendmen s
ha e been pa icula ly e ec i e o achie e bo h managemen
goals (Bas a e al., 2016; Zhou e al., 2017), which also possess
he accep ance o public and egula o s (Ob ycki e al., 2017).
Acco ding o Käs ne and Mil ne (2016), he use o OAs is
ce ainly jus i ied o pollu ed soils in u ban a eas, whe e he
economic p essu e o hei euse is high enough o make e en
cos -in ensi e emedia ion s a egies economically easible.
Mo eo e , he use o OAs o es o e u ban and pollu ed a eas
un in ha mony wi h Eu opean pollu ion p e en ion and con ol
p oposals (Ga cía e al., 2017).
O e las yea s, phy o emedia ion echnologies such as
“aided phy os abiliza ion” ha e been success ully implemen ed
as a phy omanagemen s a egy, succeeding mi iga e he
en i onmen al impac o me al-con amina ed soils and
displaying g ea po en ial o be applied o ex ended a eas
(Venegas e al., 2015). Aided phy os abiliza ion is de ined as an
en i onmen ally iendly in si u phy o emedia ion s a egy based
on he combina ion o me al- ole an plan s (phy os abiliza ion)
and o ganic o ino ganic amendmen s (chemical s abiliza ion;
Ga aiyu ebaso e al., 2017), which simul aneously educe soil
me al mobili y/bioa ailabili y, he eby educing leaching and
hei ans e h ough ophic web, imp o ing soils mic obial
p ope ies and acili a ing plan es ablishmen ( e ege a ion;
Gómez-Sagas i e al., 2012; Clemen e e al., 2015). In he ield
o es o a ion o mining impac ed soils and me alli e ous
mine ailings, he applica ion o aided phy os abiliza ion
p og ams a e pa icula ly encou aged (Galende e al., 2014a;
Pa do e al., 2014; Madejón e al., 2018), in o de o a oid
he bu densome esou ce in es men s ha in ol ed soil
emedia ion (B own and Chaney, 2016). Comp ehensi e
o e iews o he e ec s o aided phy os abiliza ion expe iences
on physical, chemical and biological p ope ies o mining
soils a e summa ized in Clemen e e al. (2015),B own and
Chaney (2016), and mo e ecen ly, in Sha ma and Nagpal
(2017).
The me al s abiliza ion and immobiliza ion p ocesses,
including adso p ion, p ecipi a ion and/o complexa ion
(Sha ma and Nagpal, 2017), depend upon he pa icula me al
and soil ype in ol ed, deg ee o humi ica ion o he o ganic
ma e , con en o me als and sal s and he e ec s o o ganic
ma e on he edox po en ial and soil pH (Clemen e e al.,
2005; Pé ez-Es eban e al., 2014). Howe e , al hough me als
a e immobilized wi hin soil and become less bioa ailable, he
amended si es equi e long- e m and egula moni o ing and
uno con ol measu es o ensu e ha he op imal s abilizing
condi ions o me als emain unchanged (Bas a e al., 2016;
Ga aiyu ebaso e al., 2017; Khalid e al., 2017).
The e ec i eness o aided phy os abiliza ion o pollu ed
soils has been alida ed in bo h labo a o y and ield scale
expe imen s. Inc easingly, measu es o mic obial biomass,
ac i i y, and di e si y a e being used o e alua e he educ ions
in me al bioa ailabili y and he es o a ion o soil unc ioning in
amended soils in bo h in mic ocosm and ield s udies (Gómez-
Sagas i e al., 2012; Pa do e al., 2014; B own and Chaney,
2016). Animal manu e, biosolids and hei espec i e compos s
a e o en ecommended OAs o me al immobiliza ion (Khalid
e al., 2017). Fo example, Ca lson e al. (2015) epo ed ha
biosolids om sewage sludges inc eased soil enzyme ac i i ies
and ungal biomass wi hin he i s yea a e amending deg aded
indus ial soil. Simila ly, Bas a e al. (2016) e idenced ha
biosolid amendmen s inc eased soil enzyma ic ac i i ies and
g ass di e si y in u ban deg aded soil. Zhou e al. (2017) obse ed
signi ican educ ion o me al a ailable ac ion while mic obial
biomass was inc eased in u ban ag icul u al soil amended wi h
ed mud and compos . Mo e in o ma ion abou he e icacy o
amendmen s was e iewed by Ga cía e al. (2017). Conce ning
ungal communi y, Mon iel-Rozas e al. (2016) indica ed ha
biosolid compos s p omo ed a mo e phylogene ically di e se
a buscula myco hizal (AM) in me al pollu ed soils. Howe e ,
when colonizing plan species we e changed and expe imen was
ca ied ou in a longe e m, exogenous o ganic ma e addi ion
did no in luence AM ungal pa ame e s o me al plan up ake
(Mon iel-Rozas e al., 2017). Addi ionally, OAs such as g een
and biosolid compos s can also s imula e he deg ada ion and/o
mine aliza ion o o he equen soil co-pollu an s like o ganic
pollu an s because hey play a ole in supplemen ing nu ien s
and ca bon sou ce, as was e idenced by Mascianda o e al. (2013),
Bas ida e al. (2016), and Lacalle e al. (2018).
CONTAMINANTS OF EMERGING
CONCERN IN SOILS AMENDED WITH
ORGANIC WASTES AND THE ROAD
AHEAD
E e since “Silen Sp ing” (1962) by Rachel Ca son and “The
Closing Ci cle: Na u e, Man, and Technology” (1971) by Ba y
Commone we e published in ull G een Re olu ion, he popula
and poli ical conce ns owa d side-e ec s o con aminan s
in he en i onmen ha e been inc eased, and wi h i he
legisla ion and di ec i e p oposals abou app o al and use o
chemicals (Käs ne and Mil ne , 2016). T adi ionally, egula
applica ion o biosolids and animal manu es o ag icul u al
soils has been conside ed as a majo con amina ion sou ce o
me al(loid)s (Pa k e al., 2011; Clemen e e al., 2015), o ganic
con aminan s (Semblan e e al., 2015) and mos p e alen
pa hogenic mic oo ganisms such as Campylobac e , Esche ichia
coli, Salmonella, and Ye sinia (Ga cía e al., 2017). The
iden i ica ion, cha ac e iza ion, and p io i iza ion o po en ially
haza dous chemical and biological agen s o hese o ganic
was es be o e hei use as soil amendmen s is an impo an
equi emen , i no manda o y, in he amewo k o was e
managemen and en i onmen al isk assessmen . None heless,
o da e only he 29.6% o he s udies ake in o accoun
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Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
he po en ial isks o exogenous o ganic ma e applica ion
(Table 1).
In acco dance wi h his, he exis ing EU legisla ion co e ing
was e managemen , undamen ally comp ised o Was e
F amewo k Di ec i e 2008/98/EC, Haza dous Was e Di ec i e
94/31/EC ( u he speci ied by he Decision 2000/532/EC),
In eg a ed Pollu ion P e en ion and Con ol Di ec i e
96/61/EC and Di ec i e on he Land ill o Was e 99/31/EC
and complemen ed by Sewage Sludge Di ec i e 86/278/EEC
and Animal Was e Di ec i e 90/667/EEC, among o he s, seeks
o encou age p e en ion mechanisms and he es ablishmen o
indica i e maximum (limi ) concen a ions ( alues) o each
class o con aminan p esen in was es o ensu e hei sa e use
as OAs. The eupon, he ad ances in he sewage and was ewa e
ea men echnologies and imp o emen s in eed u iliza ion
in animal and poul y indus ies, ha e success ully educed he
me al con en o biosolids and animal manu es (Pa k e al.,
2011; Khalid e al., 2017). Fu he mo e, he humi ica ion o
o ganic ma e may also dec ease he bioa ailabili y o me al and
o ganic con aminan s h ough he o ma ion o pollu an -humic
complexes (Clemen e and Be nal, 2006; Mascianda o e al.,
2013). The isk o pa hogens embedded in manu es can be
signi ican ly mi iga ed h ough compos ing, which mos ly
comp ise e icien hygieniza ion, al hough i may no en i ely
p e en pa hogenic eg ow h (Mascianda o e al., 2013; Ga cía
e al., 2017). Mo e speci ic c i e ia o guidelines wi h e e ence o
compos ’ assessmen o i s use as soil amendmen in di e en
Eu opean coun ies a e p o ided by Sa eyn and Ede (2014) and
Cesa o e al. (2015).
Unlike me als and pa hogens, much less is known
abou he a e and beha io in e es ial en i onmen s o
mic o(nano)plas ics and ARGs in some o ganic was es,
including compos s, li es ock manu es, and biosolids. As such,
hese mic o- and nano-sized agen s should be conside ed
global eme ging con aminan s ha need o be immedia ely
add essed in he cu en egula o y amewo k o was es. As
shown below, hei inc easingly occu ence in soils and he
unce ain ies connec ed o hei po en ial exposu e pa hways
and unp edic able eco oxicological e ec s ende hem wo hy
o esea ch a en ion in ecen yea s.
Imme sed as we a e in he golden age o he “plas ic e a”
due he accessibili y and sp ead o ab ica ion echnology and
e sa ili y o applica ions, pe oleum-based plas ics can be
ound in each and e e y indus y (e.g., packaging, building and
cons uc ion, ae onau ics, au omo i e, elec onics, ag icul u e
and heal hca e) and, hence, hey ha e become essen ial o
he daily li e. Wi hin Eu ope, 60 million ons o plas ics we e
p oduced in 2016 (accoun ing o 18% o wo ld p oduc ion)
o co e an es ima ed o al demand o 50 million ons
(Plas icsEu ope, 2017). O icial da a also shown ha only
he 45% o p oduced plas ics in 2016 (c.a. 27 million
ons) we e hen collec ed a e use, o which a ound 31%
en e ed o ecycling s eam (Plas icsEu ope, 2017). Al hough
he ele ance o plas ics o economies and social wel a e
a e unques ionable, he o e p oduc ion and inadequa e was e
managemen ele a ed plas ics in o a majo en i onmen al
h ea . Fu he mo e, he mos commonly used polyme s (e.g.,
polye hylene, polyp opylene, poly inyl chlo ide) a e no eadily
biodeg adable, hey a e subjec ed o wea he ing and agmen ing
in o mic oplas ics and emain in he en i onmen o hund eds
o yea s (Uni ed Na ions En i onmen P og amme (UNEP),
2015; Ho on e al., 2017). Thus, Eu opean Commission
iden i ied “plas ics” as a key p io i y a ea and, p o i o ha , is
he ecen ly adop ed Eu opean Commission (2018).
Mic oplas ic (plas ic pa icles smalle han 5 mm) can occu
in he en i onmen ei he as p ima y (manu ac u ed a a
mic oscopic size and in en ionally added o pe sonal ca e
p oduc s, known as mic obeads) o indi ec ly as seconda y
mic oplas ics ( esul ing om he disin eg a ion o la ge -sized
plas ic deb is and li e by he e ec o UV adia ion o
mechanic ab asion such as hose gene a ed du ing use o
i e and syn he ic ga men s, plas ic mulching o along he
p oduc ion, supply and end-o -li e s age o plas ics; Duis and
Coo s, 2016). E en hough ag icul u al and u ban lands a e
expec ed o ep esen majo en y poin s and ese oi s o
mic oplas ics in e es ial ecosys ems, possibly comp ehensi ely
la ge han he ma ine basins, e y ew da a is a ailable
ega ding he sou ces, pa hways, and possible accumula ion
o mic oplas ics in di e en soil compa men s (Duis and
Coo s, 2016; Nizze o e al., 2016; Ho on e al., 2017;
Rillig e al., 2017; de Souza Machado e al., 2018; Hu ley
and Nizze o, 2018; Mai e al., 2018). This is in pa
due o analy ical di icul ies. Commonly employed me hods
o analyzing mic oplas ics o en in ol e il e ing, lo a ion,
isual selec ion by mic oscope ollowed by con i ma ion
me hods o py olysis gas ch oma og aphy-mass spec ome y
ha a e sui able o aqua ic en i onmen s bu p esen pa icula
limi a ions o e es ial and o he con inen al en i onmen s (de
Souza Machado e al., 2017). E o s a e cu en ly unde aken o
es ablish e ec i e and s anda dized analy ical p ocedu es, bu he
de ec ion o mic oplas ic om he e ogeneous, o ganic- ich soil
ma ices is no ye possible (Hu ley and Nizze o, 2018). In line
wi h Eu opean S a egy o Plas ics and REACH p ocedu es o
es ic ing po en ially haza dous subs ances o he en i onmen
o human heal h, Eu opean Commission eques ed scien i ic
e idences o Eu opean Chemical Agency o aking egula o y
measu es o educe he use o in en ionally-added mic oplas ics
o p oduc s.
The addi ion o biosolids collec ed om municipal was ewa e
ea men s as soil amendmen s ha e been ecen ly es ima ed
as one o he la ges sou ces o mic oplas ics o he soils
(Nizze o e al., 2016; Hu ley and Nizze o, 2018). Nizze o
e al. (2016) e en es ima e ha annually be ween 125 and
850 ons mic oplas ics pe million inhabi an s a e added o
Eu opean ag icul u al soils ei he h ough di ec applica ion
o sewage sludge o as p ocessed biosolids. As app oxima ely
99% o mic oplas ics in he was ewa e s eam a e likely o
be e ained in sludge, he e is a possibili y ha , e en a e
ea men p io land-sp eading, hey could con ain signi ican
amoun s o mic oplas ics (Mahon e al., 2017). In his sense,
se e al s udies (Ca e al., 2016; Mahon e al., 2017; Min enig
e al., 2017; Tal i ie e al., 2017; Ziajah omi e al., 2017;
La es e al., 2018) poin ed ou he u gen need o ad anced
inal-s age was ewa e ea men echnologies mo e e icien in
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Gómez-Sagas i e al. Phy omanagemen o Deg aded Lands
he emo al o mic oplas ics om was ewa e e luen s and
sludges.
In essence, mic oplas ics could be inges ed and accumula e
by bio a leading o s a a ion (physical damage), could in e ac
and concen a e pe sis en o ganic con aminan s (Rocha-San os
and Dua e, 2015) and/o adso b me als mo e han by soil
pa icles wi h equal mass (Hodson e al., 2017), due o hei la ge
su ace a ea- o- olume a io (chemical damage). Mic oplas ic-
associa ed eco oxici y could be also caused by he leaching
o endoc ine-dis up ing addi i es added du ing manu ac u ing
p ocesses o plas ics (And ady, 2015). The subsequen ans e o
such con aminan s and addi i es om mic oplas ics o ma ine
o ganisms has been con i med unde expe imen al condi ions
(Taylo e al., 2016; Galloway e al., 2017). Howe e , he e a e no
expe imen al e idences so a o ou knowledge on he ans e
and bioaccumula ion o mic o(nano)plas ics in he e es ial
bio ic ood web (Mai e al., 2018; Ng e al., 2018).
Ecological impac s o mic oplas ics on in e eb a es,
e eb a es, bi ds, and mammals o eshwa e and ma ine
en i onmen s a e cu en ly he subjec o in ense ield and
labo a o y esea ch (Anbumani and Kakka , 2018 and e e ences
he ein). Ea ly in es iga ions e idenced ha soil mic o- and
meso auna, such as mic obial communi y (Wang e al., 2016;
de Souza Machado e al., 2018; Rillig and Bonkowski, 2018);
collembolan (Maaß e al., 2017; Zhu e al., 2018), ea hwo ms
(Hue a Lwanga e al., 2016; Cao e al., 2017; Rillig e al.,
2017; Rod iguez-Seijo e al., 2017), and e es ial bi ds (Zhao
e al., 2016) migh be also suscep ible o he eco oxicological
e ec s o mic oplas ics. I should be emphasized, howe e ,
ha he exposu e concen a ions used in mos o he s udies
a e highe han hose ound in land scena io (Ng e al.,
2018). When conside ing nanoplas ics (<100 nm), i has been
obse ed ha yeas s (Miyazaki e al., 2014), ilamen ous ungi
(Nomu a e al., 2016), and mammals (Mu ua e al., 2011)
show oxici y symp oms once hey a e exposed o nanobeads.
Up ake o mic oplas ics by plan s is no expec ed, bu i has
been epo ed ha nanoplas ics could en e in o plan s due
o hei compa able densi y o mic onu ien s (Bandmann
e al., 2012). Howe e , no s udy has been ca ied ou so a on
ansloca ion and dis ibu ion o nanoplas ics in plan o gans
(Ng e al., 2018). Eco oxici y o nano- and mic oplas ics in soils
due o applica ion o OAs equi ed u he a en ion in u u e
s udies.
Simul aneously o he sp eading o mic oplas ics, he selec i e
p essu e exe ed by o e use o an ibio ics o decades has caused
an unp eceden ed p e alence and p oli e a ion o clinically
ele an an ibio ic- esis an bac e ia (ARB) and genes (ARGs) in
na u al en i onmen s. Acco ding o Wo ld Heal h O ganiza ion
(WHO) (2014, 2015) and Uni edNa ions (UN) (2016), an ibio ic
esis ance is one o he g ea es h ea s o global public heal h.
In esponse o he po en ial loss o e icacy o clinically ele an
an ibio ics, las yea Eu opean One Heal h Ac ion Plan agains
An imic obial Resis ance was published in o de o es ablish
he oad ahead o mi iga e social and economic impac s o his
eme ging isk.
Long- e m amended soils wi h biosolids esul ed om
he ea men o domes ic sewages, hospi al was ewa e s, and
d ainage om li es ock eeding ope a ions a e ho spo s o
ARB and ARGs (Mao e al., 2015; Goulas e al., 2018; U a
e al., 2018). In ac , Su e al. (2014) and Chen e al. (2016)
e ealed mo e han 130 unique ARGs and mobile gene ic
elemen s (MEGs) in sewage sludges and animal manu es ha
con e esis ance o mos used an ibio ics g oups such as β-
lac ams and e acyclines. When soils a e amended wi h manu e,
bac e ia ca ying ARGs a e also in oduced in o he soil and
pe sis o a long ime, as demons a ed he s udies conduc ed
by Joy e al. (2013), Fah en eld e al. (2014), Udiko ic-Kolic
e al. (2014), Ross and Topp (2015), Wang e al. (2015), Peng
e al. (2017), and Tien e al. (2017).Chen e al. (2017) e en
de ec a o al o 240 unique ARGs ia a high- h oughpu
quan i a i e PCR (qPCR) a ge ing almos all majo classes
o ARGs.
Po en ial isks associa ed o ARGs ha h ea en he u u e
o an ibio ic he apy include he ho izon al gene ans e by
MGEs be ween bac e ia and pa hogens esiding in soils (Ga bisu
e al., 2018), which in u n il he balance o selec ion owa d
inc eased su i al and p oli e a ion o esis an bac e ia, and
he e ical dissemina ion along he ood chain ia plan -
up ake. Ac ually, conjuga i e plasmid-media ed ho izon al gene
ans e is conside ed he mos impo an p ocess in he
dissemina ion o mul id ug esis ance genes (Ga bisu e al.,
2017). Resis ance plasmids o en ca y in eg ons. I is well
documen ed ha in eg ons (gene ic uni s ha ac as na u al
cloning sys ems and exp ession ec o s), and conc e ely he
Class 1 in eg ons, a e p obably he mos p e alen ehicles
o ARGs casse es in was ewa e ea men plan s (Di e al.,
2016), and land applied sewage sludges (Bu ch e al., 2014;
Zhang e al., 2017) and manu es (Sandbe g and LaPa a,
2016).
The consump ion o plan s and ege ables, pa icula ly hose
ha a e ea en aw o a e subjec ed o minimal p ocessing, by
humans o animals ep esen s a po en ial ou e o exposu e
o ARB and, subsequen ly, a po en ial pa hway o ARGs
ansmission owa d ood web. Recen s udies e idenced he
dissemina ion o ARGs o plan s h ough endophy ic sys em.
When abundance o ARGs in bo h amended soil and ha es ed
ege ables we e analyzed, Ma i e al. (2013, 2014) de ec ed
ARGs on oma oes, peppe s, cucumbe s, ca o s, adishes, and
le uces g own in soils amended wi h pig manu es, including oo
endophy es, lea endophy es, and phyllosphe e mic oo ganisms.
S ikingly, nume ous an ibio ic- esis ance de e minan s we e
also de ec ed in hose ege ables g own in un-manu ed soil.
None heless, hei esul s ein o ce he ad isabili y o p e-
ea ing biosolids and manu es and/o he es ablishmen o o -
se imes be ween amending and ha es ing ege ables o human
consump ion. Simila esul s we e epo ed by Wang e al.
(2015) in le uce and endi e g own in manu e-amended soils
unde con olled condi ions. Yang e al. (2014) also iden i ied
an ibio ic- esis an endophy ic bac e ia wi h high esis ance o
cephalexin in cele y, Chinese cabbages, and cucumbe s collec ed
om g eenhouse ields e ilized wi h chicken manu e. Zhu e al.
(2017) de ec ed a o al o 134 ARGs in he phyllosphe e and lea
endophy e o le uces unde con en ional and o ganic a ming
using high- h oughpu qPCR and 16sRNA Illumina sequencing
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Con lic o In e es S a emen : The au ho s decla e ha he esea ch was
conduc ed in he absence o any comme cial o inancial ela ionships ha could
be cons ued as a po en ial con lic o in e es .
Copy igh © 2018 Gómez-Sagas i, He nández, A e xe, Ga bisu and Bece il. This
is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons
A ibu ion License (CC BY). The use, dis ibu ion o ep oduc ion in o he o ums
is pe mi ed, p o ided he o iginal au ho (s) and he copy igh owne (s) a e c edi ed
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