Jou nal o Haza dous Ma e ials 459 (2023) 132216
A ailable online 3 Augus 2023
0304-3894/© 2023 The Au ho (s). Published by Else ie B.V. This is an open access a icle unde he CC BY-NC license (h p://c ea i ecommons.o g/licenses/by-
nc/4.0/).
Wha dead seaweeds can ell us abou me al up ake and hei applica ion o
con ol ma ine pollu ion
An ´
on V´
azquez-A ias
*
, Jesús R. Aboal, J. ´
Angel Fe n´
andez
CRETUS Ins i u e, Ecology A ea, Depa men o Func ional Biology, Facul y o Biology, Uni e sidade de San iago de Compos ela, San iago de Compos ela 15782, Spain
HIGHLIGHTS GRAPHICAL ABSTRACT
•We compa ed he elemen al up ake by
esh and de i alized seaweed
ansplan s.
•Mos o he ma e ial in de i alized
ansplan s was los du ing he exposu e
pe iod.
•De i alized samples had highe
elemen al up ake o mos ace
elemen s.
•Physicochemical changes on he sea-
weeds’ su ace con ibu e o he
inc eased up ake.
•Ex acellula chemical binding and
physical adso p ion a e ele an up ake
pa hways.
ARTICLE INFO
Edi o : Wagne L. A aújo
Keywo ds:
Biomoni o ing
Hea y me al
Wa e pollu ion
Ma ine pollu ion
Mac oalgae
ABSTRACT
The mechanisms o ace elemen up ake by seaweeds a e s ill unknown, despi e being key o unde s and he
impac o pollu ion in coas al en i onmen s. This knowledge gap, in addi ion o he lack o s anda diza ion, ha e
also hinde ed he use o seaweeds o moni o seawa e pollu ion. To add ess hese sho comings, we es ed he
use o de i aliza ion as a p e-exposu e ea men o b own seaweed ansplan s, and we compa ed de i alized
and esh ansplan s o gain some insigh s in o he mechanisms o elemen up ake. We exposed ou ypes o
Fucus esiculosus ansplan s in 6 si es o 4, 8 and 20 days: esh and de i alized (d ied o boiled) algal segmen s
held in mesh bags, and whole algal halli imi a ing na u al condi ions. We hen de e mined he concen a ions o
11 ace elemen s in he algal issues. The elemen concen a ions we e highes in he de i alized ansplan s, bu
he ma e ial los consis ency and weigh h oughou he exposu e pe iod, limi ing hei use o sho pe iods. We
p oposed se e al ac o s ha may con ibu e o he di e en accumula ion pa e ns be ween ea men s, and
examined he implica ions o he up ake mechanisms, e ealing ha wo o he mos impo an a e su ace
adso p ion o sedimen pa icles and chemical bounds o ex acellula componen s.
1. In oduc ion
Pollu ion is one o he main ways by which human ac i i ies damage
he en i onmen [6] and is also ha m ul o human heal h, being
esponsible o up o 9 million dea hs a yea [29]. Many coun ies and
o ganiza ions ha e egula o y agencies and legisla ion in ended o
* Co esponding au ho .
E-mail add ess: [email p o ec ed] (A. V´
azquez-A ias).
Con en s lis s a ailable a ScienceDi ec
Jou nal o Haza dous Ma e ials
jou nal homepage: www.else ie .com/loca e/jhazma
h ps://doi.o g/10.1016/j.jhazma .2023.132216
Recei ed 17 Ap il 2023; Recei ed in e ised o m 22 July 2023; Accep ed 2 Augus 2023
Jou nal o Haza dous Ma e ials 459 (2023) 132216
2
con ol pollu ion le els and p e en he impac o pollu an s on eco-
sys ems and human heal h. Aqua ic en i onmen s a e pa icula ly sen-
si i e o pollu ion [23] and con amina ion is s ic ly egula ed by
legisla ion wo ldwide, such as he Clean Wa e Ac in he Uni ed S a es
[40], he Eu opean Wa e F amewo k Di ec i e [13] and he Ma ine
En i onmen P o ec ion Law in China [34]. The egula ions apply o
coas al wa e s, which a e impo an o ood p oduc ion, and also o
ma ine ecosys ems in gene al, owing o hei impo ance in p ima y
p oduc ion and as nu se ies [37]. None heless, aqua ic en i onmen s
a e se e ely a ec ed by human ac i i ies, as wa e has been his o ically
used o was e disposal, and pe sis en pollu an s such as po en ially
oxic elemen s (PTEs) equen ly each coas al en i onmen s [4,42].
The i s s ep in con olling pollu ion is o ob ain eliable in o ma ion
abou pollu an le els. The classical app oach o measu ing he con-
cen a ion o pollu an s di ec ly in seawa e has some disad an ages: he
analy ical de e mina ions can be di icul and cos ly [28]; he e is no
empo al ep esen a i eness, owing o he apid a e o eplacemen o
coas al wa e ; and he measu emen s do no e lec he impac o he
pollu an s on o ganisms, which may depend on he chemical species
in ol ed. Biomoni o ing is an al e na i e app oach ha sol es hese
p oblems by measu ing he concen a ions o pollu an s in o ganisms
exposed o he wa e a he han di ec ly in he wa e . This app oach is
use ul o p o iding in o ma ion abou he en i onmen whe e he o -
ganisms li e and abou he o ganisms hemsel es, which may make i
especially aluable o en i onmen al impac assessmen s. Howe e ,
his echnique also has some disad an ages, such as he lack o compa-
abili y o di e en s udies owing o he use o di e en o ganisms and
me hods [15,17].
To s anda dize he o ganism used o such s udies, he axonomic
g oup ha has a ac ed he mos a en ion is seaweed. They ha e been
widely used in he pas in coas al biomoni o ing because hey a e
abundan in mos egions h oughou he yea [17]. No only his, bu
measu ing he concen a ion o pollu an s in seaweed issues is also
in e es ing due o hei g ea impo ance; in coas al ecosys ems hey
play a ole as ecosys em enginee s [39], and p o ide ood and shel e o
many o he o ganisms; and di ec ly o socie y as we ex ac coun less
p oduc s om hem, including ood, bio uels, and subs ances used in he
ood and pha maceu ical indus ies [5,31]. Thus, unde s anding how
seaweed in e ac wi h PTEs in he en i onmen is key o p edic ing how
pollu ion will a ec hei ecosys em unc ions, he p ope ies o
seaweed-de i ed p oduc s, and o in e p e ing he esul s o bio-
moni o ing s udies. Howe e , he accumula ion mechanisms and ac o s
a ec ing i a e ba ely unde s ood.
This knowledge gap, in addi ion o he lack o s anda dized p o ocols
hinde he applica ion o seaweed o biomoni o ing. Some ad ances
ha e al eady been made; F. esiculosus has been ecommended o he
A lan ic egion, bu he p o ocol o using his species as a biomoni o is
a om being op imized. The ac i e biomoni o ing echnique, which
has p o ed success ul in o he c yp ogams such as e es ial mosses [2]
and eshwa e mosses [10], has been ecommended o use wi h sea-
weeds [15]. This app oach in ol es cul u ing o ob aining he plan
ma e ial om an unpollu ed si e and ans e ing i o he es a ea o
exposu e. The echnique allows he use o p e-exposu e ea men s,
including de i aliza ion. De i aliza ion consis s o killing an o ganism in
a way ha p ese es he ele an p ope ies o biomoni o ing. This
me hod has p oduced mo e s able esul s wi h o he c yp ogams [11,2,
20], and i has simpli ied he logis ics o he moni o ing me hod, making
i possible o p ese e he ma e ial o longe imes. Thus, he p esen
s udy has wo objec i es: o compa e he loss o ma e ial and he abili y
o accumula e PTEs o li e and de i alized ansplan s o he seaweed
F. esiculosus; and o analyze hei physicochemical p ope ies and
accumula ion capabili ies o examine he possible up ake mechanisms.
2. Ma e ial and me hods
2.1. Sampling and p e-exposu e ea men s
Thalli o he b own algae Fucus esiculosus L. we e collec ed om an
unpollu ed coas al a ea (a ound SS1, Table 1) in NW Spain. S ones o
app oxima e size 30 ×30×20 cm we e also collec ed in he same si e.
The halli we e insed b ie ly in seawa e and anspo ed o he labo-
a o y in polye hylene bags, along wi h he s ones. Some o he halli
samples (25%) we e p ese ed whole in seawa e ; he o he halli we e
p ocessed by emo ing heal hy apical segmen s using glass equipmen .
The h ee mos apical dicho omies we e selec ed om each hallus, o
p oduce simila ly-aged, homogeneous es ma e ial [16].
The selec ed apices we e di ided in o h ee equal po ions (each
comp ising 25% o he o iginal ma e ial collec ed) and each was sub-
jec ed o a di e en ea men : one po ion was le un ouched; ano he
was o en-d ied (a 50 ◦C o 8 h, 80 ◦C o 8 h, and 100 ◦C o 8 h), and
he inal po ion was boiled o 5 min in a 2 L glass beake hea ed on a
ho pla e.
2.2. P epa a ion and exposu e o he ansplan s
The ansplan s we e p epa ed by placing he esh o boiled ma e ial
(11 g) o he d ied ma e ial (1.8 g) ( he ma e ial los app oxima ely 5/6
o i s weigh du ing d ying) in 9 ×9 cm la ibe glass mesh bags (2 mm
mesh size). The whole halli we e a ached o he s ones by gluing he
basal pa o he s one su ace wi h wa e p oo silicone sealan . To
p e en loss o ma e ial bu wi hou hampe ing wa e low, he s ones
wi h a ached seaweeds we e co e ed wi h 2 cm mesh size polye hylene
ne s. These ansplan s imi a ed na u al condi ions.
A o al o 5 s ones each wi h 15 whole halli a ached we e ans-
po ed o each s udy si e. A o al o 45 bag ansplan s we e also exposed
in each si e, 15 o each ype, dis ibu ed in 15 s ings ha we e a ached
o he meshes used o w ap he s ones. In addi ion, 5 ansplan s o each
ype we e anspo ed o he s udy si e bu we e no exposed in he
wa e , as a ime ze o con ol (T0).
This was done in 6 s udy si es (SS) in he in e io o ias on he NW
coas o Spain (Table 1): 5 o he si es we e po en ially pollu ed due o
hei p oximi y o ci ies o o cu en o p e ious indus ial a eas, and
he o he was he same si e whe e he seaweeds we e collec ed.
2.3. Sample collec ion and p ocessing
In each SS, samples we e collec ed a e exposu e o 4, 8, and 20
Table 1
Lis o s udy si es. The coo dina es a e in WGS 84 wi h a web Me ca o
p ojec ion.
S udy
si e
S a
da e
End
da e
Coo dina es Pollu ion sou ce
SS1 31/
10/
2019
20/
12/
2019
42.22391, −
8.75815
Nex o an indus ial ci y o
300,000 inhabi an s
SS2 14/
11/
2019
04/
12/
2019
42.34626, −
8.61331
Nex o an old ce amics ac o y,
known o discha ge Pb- ich
was e in o he wa e
SS3 28/
11/
2019
18/
12/
2019
43.49986, −
8.17095
Close o an indus ial ci y o
65,000 inhabi an s, in a ia wi h
a low wa e enewal a e
SS4 06/
02/
2020
26/
02/
2020
42.94528, −
9.17639
Nex o an ac i e me allu gic
indus y
SS5 20/
02/
2020
11/
03/
2020
42.40816, −
8.6812
Nex o a closed chlo -alkali
plan , known o discha ge Hg-
ich was e in o he wa e
SS6 05/
03/
2020
25/
03/
2020
42.79022, −
8.91764
No exposed o any known
sou ce o me al pollu ion
A. V´
azquez-A ias e al.
Jou nal o Haza dous Ma e ials 459 (2023) 132216
3
days. The leng h o he exposu e pe iod was selec ed o allow s abili-
za ion o elemen concen a ions [41]. A each sampling ime, ans-
plan s a he end o each s ing we e collec ed, and he mesh en elopes
we e opened and 5 halli emo ed. Thus, 5 samples o whole esh
seaweed a ached o s ones and 5 bag ansplan s subjec ed o each
de i aliza ion ea men we e collec ed each ime (i.e. 20 samples each
ime). The samples we e b ie ly insed in he su ounding seawa e ,
s o ed in polye hylene bags and anspo ed o he labo a o y. In addi-
ion, on day 20 o he exposu e pe iod, a sedimen sample (uppe 2 mm)
was ob ained in each SS. In he labo a o y, he mesh bags we e opened,
and he h ee apical dicho omies we e cu om he halli a ached o
s ones, so ha hese con ol samples we e compa able o he bag
ansplan s. The samples we e hen o en d ied a 40 ◦C un il cons an
weigh , weighed, and homogenized in a angen ial mill wi h zi conium
oxide g inding essels (Re sch ZM400). The ma e ial was s o ed in
he me ically sealed ials in da kness un il chemical analysis.
2.4. Chemical analysis
P io o analysis, he samples we e d ied again a 40 ◦C in a o ced ai
o en. The samples (1 g d.w.) we e mine alized in Te lon essels in a
mic owa e o en (Miles one E hos-1), in 3 successi e s eps (10 min a
100 ◦C, 7 min a 150 ◦C, 25 min a 190 ◦C), by adding 10 mL o HNO
3
(65%), 2 mL o H
2
O
2
(30%) and 2 mL o MilliQ wa e . The concen a-
ions o Al, V, Mn, Fe, Ni, Cu, Zn, Cd, Ba, and Pb we e de e mined by
induc i ely coupled plasma mass spec ome y (ICP–MS) (Agilen
7700x) by he Uni e si y Resea ch Suppo Se ices Uni (Uni e sidade
de San iago de Compos ela). The concen a ions o Hg we e de e mined
in an elemen al analyze (DMA 80 Miles one) in he Ecology Uni o he
same uni e si y.
The quali y o he samples was ensu ed by analyzing ce i ied
e e ence ma e ials (CRMs) and analy ical eplica es e e y 15 samples,
in addi ion o blanks. The CRMs used we e ERM-CD200 (F. esiculosus),
BCR-279 (Ul a lac uca) and BCR-277R o he sedimen s. All h ee ma-
e ials a e ce i ied by he Join Resea ch Cen e o he Eu opean Union.
The limi o de ec ion (LOD) was calcula ed as he mean blank alue plus
3 imes he s anda d de ia ion, and he limi o quan i ica ion (LOQ) as
he mean alue plus 10 imes he s anda d de ia ion.
In o de o in es iga e he causes o he di e ences in elemen al
accumula ion, s o ed seaweed samples p ocessed using he same p o-
ocol as desc ibe abo e we e analyzed in an FTIR-ATR spec ome e
(Agilen Ca y 630), in he 400 cm
−1
o 4000 cm
−1
egion wi h a eso-
lu ion o 4 cm
−1
. A o al o 14 samples we e analyzed, 2 esh and 2 d ied
unexposed (T0) seaweed samples, and 5 esh and 5 d ied samples
exposed o 14 days.
2.5. S a is ical analysis
All analyses we e pe o med wi h R so wa e [36]. The no mali y o
he samples was checked using he Shapi o es . The da a we e no
no mally dis ibu ed ei he be o e o a e loga i hmic ans o ma ion.
Due o he lack o no mali y, he di e ences in he elemen al concen-
a ions o di e en ea men s we e analyzed by he K uskal-Wallis es
and ad-hoc Dunn es s.
The ends in he elemen al concen a ions o e ime we e es ed by
i ing linea models o he un ans o med and ans o med (loga i hmic
ans o ma ion) da a. This was applied o he espec i e da a o each SS
and ea men o which ma e ial emained a e 20 days. The quo ien
o he sigma alues ( he sum o he esiduals o each model) o he linea
and loga i hmic model o each da a se was calcula ed, p oducing a
alue ha indica es whe he he end i ed bes o a linea ( alues <1)
o loga i hmic (>1) model.
The ac ion o he elemen al concen a ions o he ansplan s o
which he sedimen pa icles a ached o he su ace a e esponsible was
calcula ed using Fo mula 1.
y=[Al]Sw
[X]Sw /[Al]Sed
[X]Sed
Fo mula 1. Calcula ion o he pe cen age o he elemen al concen-
a ions a ibu ed o he sedimen , whe e ‘y
′
is he po ion o he
elemen X a ibu ed o he sedimen , [Al]
Sw
and [Al]
Sed
a e he con-
cen a ions o aluminum in seaweed and sedimen samples, and [X]
Sw
and [X]
Sed
a e he concen a ions o he s udied elemen .
This was done unde he assump ion ha all he Al in he seaweed
samples was de i ed om he sedimen , so ha he concen a ion o any
elemen p esen in he sedimen pa icles associa ed wi h he seaweed
samples should hus be p opo ional o he concen a ion o Al in he
sedimen samples. Thus, alues <1 imply ha o he ac o s a e
inc easing he concen a ion o ha elemen in he sample.
The FTIR esul s we e analyzed and isualized using he ChemoSpec
package o R [25], including he p incipal componen analysis (PCA).
The da a we e no malized wi h a p obabilis ic quo ien no maliza ion o
emo e any possible sys ema ic de ia ion.
3. Resul s
The d y weigh s o he T0 ansplan s we e simila (al hough
weighing he ma e ial in di e en s a es such as d ied o esh o make
he asnplan s led o di e ences). Thus, o T0, he a e age d y weigh
in g ams o he apical segmen s o he whole algae a ached o s ones,
exp essed as mean ±sd, was 1.29 ±0.34; o he esh ansplan s, i
was 1.53 ±0.17, o he d ied ansplan s, 1.65 ±0.20, and o he
boiled ansplan s, 1.05 ±0.11. Howe e , loss o ma e ial du ing he
exposu e pe iod led o he inal weigh s being e y di e en (Fig. 1).
The weigh o he whole algae a ached o s ones and he ansplan s
o esh ma e ial did no dec ease h oughou he expe imen ; all o mos
o he de i alized ma e ial was los , in some SS wi hin a week. The low
emaining weigh o some samples om de i alized ansplan s made i
impossible o pe o m all chemical analyses, and he concen a ion o Hg
was no de e mined in hese cases.
Rega ding he elemen al de e mina ions, he esul s o he quali y
con ol we e gene ally sa is ac o y: he a e age pe cen age eco e y o
he algal CRMs o he ce i ied elemen s (Cu, Zn, Cd, and Pb) was 84.6%
o ERM-CD200 and 86.5% o BCR-279, and in all cases i was highe
han 75%. The pe cen age eco e y om sedimen s was below 40% o
all elemen s excep Ni: his was expec ed as he diges ion me hod used is
no designed o ex ac elemen s con ained in silica es. The global e o
was below 10% o mos elemen s, excep Ni, Zn, Cd, and Pb, o which i
was below 14%. Fo Mn, Fe, Ni, Cu, Zn, Ba, and Hg, he concen a ions in
all samples we e abo e he LOQ. Fo some elemen s, he concen a ions
in all samples we e abo e he LOD, bu a ew we e below LOQ: 3% o
Al, 5% o V, and 0.5% o Cd. Finally, he only elemen o which he
esul s we e no sa is ac o y was Pb. In his case, he concen a ions in
34% o he samples we e below LOQ, and in 6% hey we e unde LOD,
all non-exposed ansplan s.
The ini ial concen a ions o elemen s in he ansplan s
(Figu e 1SM) a ied sligh ly depending on he ea men applied; e.g.,
he boiled ansplan s consis en ly had he lowes concen a ions o el-
emen s like V, Fe, and Ni. Some di e ences in he concen a ions in he
T0 ansplan s in di e en SS e lec ed empo al a ia ions in he ma-
e ial collec ed. Howe e , he di e ences we e no la ge enough o ha e
a no able impac on he en ichmen esul s, excep o Ba in SS4, as he
ini ial high concen a ions explain he loss o Ba du ing he exposu e
pe iod in he SS.
The ne elemen al up ake o he ansplan s, de ined as he concen-
a ion o each ansplan minus he mean concen a ion o he T0
ansplan s o he same ea men in he same SS, is shown in Fig. 2 (and
Figu e 2SM o he emaining elemen s). Al hough he inal
A. V´
azquez-A ias e al.
Jou nal o Haza dous Ma e ials 459 (2023) 132216
4
concen a ions a ied widely depending on he SS, some consis en
pa e ns o each elemen and ea men we e obse ed. In mos cases,
he ea men s wi h li e seaweed ollowed he same end, whe eas he
de i alized ansplan s ollowed a di e en end. Fo Al, V, Fe, Ni, Cu,
Hg, and Pb, he concen a ions in esh ansplan s emained cons an o
inc eased sligh ly du ing he exposu e pe iod, whe eas he concen a-
ions in de i alized ansplan s inc eased sha ply. Fo Mn, he concen-
a ions in esh algae emained cons an , bu he concen a ions in
de i alized ansplan s dec eased du ing he 4 i s days, be o e hen
s abilizing. Fo he o he elemen s (Zn, Cd, and Ba), he pa e ns we e
less clea and a ied ac oss SSs.
Fo mos elemen s and SSs, he concen a ions di e ed signi ican ly
depending on he ea men conside ed. The cases o which he K uskal-
Wallis es e ealed di e ences be ween ea men s a e shown in Fig. S3;
Dunn es e ealed be ween g oup di e ences (indica ed by a compac
le e display in he same Figu e). In mos cases, he e we e no signi i-
can di e ences be ween he ea men s wi h esh algae, no be ween
he de i aliza ion ea men s; signi ican di e ences we e only obse ed
be ween he li e and de i alized ansplan s.
To e alua e whe he he ends in he elemen al concen a ions
du ing he s udy pe iod s abilized a a speci ic alue o inc eased line-
a ly, bo h linea and loga i hmic models we e i ed o each elemen ,
SS, and ea men o which da a o he 20-day exposu e was a ailable
(Table 1SM). Fo a ound hal o he ea men s, he linea eg ession
p o ided he bes i and o he o he hal he loga i hmic eg ession
model p o ided he bes i . The ea men s o which he loga i hmic
model gene ally yielded he bes i s we e he de i alized ansplan s in
SS2 and SS3. Howe e , linea models p o ided he bes i s o he
de i alized ansplan s in SS6. Loga i hmic models p o ided he bes i s
o he concen a ions o Mn and Cd in de i alized ansplan s, owing o
he apid loss o hese elemen s du ing he i s 4 days and subsequen
s abiliza ion.
The p opo ion o he concen a ion o each elemen de i ed om
he sedimen pa icles on he su ace o he seaweed, which was
calcula ed by compa ing he concen a ions no malized wi h Al in he
samples and he sedimen s, is shown in Fig. S4. Al hough i was assumed
ha all o he Al in he samples was de i ed om he sedimen , some o
he alues we e highe han 1, indica ing ha he concen a ion o hose
elemen s in he samples was lowe han wha he sedimen pa icles
would con ibu e in ha case. Fo mos elemen s, he p opo ion was
simila among sampling poin s o each elemen , and highe in de i-
alized samples han in esh samples. The elemen o which he con-
cen a ions we e highes was Mn, which is consis en wi h he obse ed
loss o he elemen du ing he exposu e pe iod. Fo V and Fe, he a ios
we e simila among ea men s in all SSs excep SS4, in which he
concen a ions o hese elemen s we e much highe in he de i alized
samples han in he esh samples (> han 1).
The FTIR spec a o esh and d ied ansplan s a e shown in Fig. 3.
Di e ences be ween esh samples, d ied samples, and he espec i e
con ols we e obse ed. The comple e spec a om 400 o 4000 cm
−1
and he g ouping o he samples by PCA a e ep esen ed in Figs. S5 and
S6.
4. Discussion
De i aliza ion o F. esiculosus samples led o apid loss o ma e ial
du ing he exposu e pe iod. This does no occu in moss, in which he
de i aliza ion by boiling and o en-d ying wi h a empe a u e amp
causes a sligh , s able loss o ma e ial, e en when exposed in i e s [11].
In he p esen s udy, almos all he ma e ial o de i alized ansplan s
collec ed a e exposu e o 20 days exposu e was los , and in some cases
he e was li le o no ma e ial emaining a e 8 days (Fig. 1). Thus,
de i alizing he seaweed is no sui able o ansplan s in ended o be
exposed du ing long pe iods. Fo he 4-day exposu e, only in a boiled
ansplan los all he ma e ial, and all d ied seaweed ansplan s had
enough ma e ial o elemen al analysis. Thus, d ied ansplan s could be
used o sho exposu e pe iods, and would be p e e able o boiling as a
de i aliza ion ea men as sligh ly less ma e ial was los and he d ied
Fig. 1. Weigh o he F. esiculosus ansplan s collec ed du ing he exposu e pe iod. The poin s ep esen he a e age alues, and he e ical ba s he maximum and
minimum alues.
A. V´
azquez-A ias e al.
Jou nal o Haza dous Ma e ials 459 (2023) 132216
5
ma e ial can po en ially be p ese ed o a long ime unde d y condi-
ions. Howe e , he de i alized seaweeds we e much less du able han
esh ansplan s (ei he in bags o a ached o ocks), he weigh o
which emained app oxima ely cons an . The di e ences in weigh o
he esh seaweeds in bags and on ocks we e negligible, and bo h p e-
se ed su icien ma e ial, al hough he a ia ion in he weigh o he
Fig. 2. Ne en ichmen o he ansplan s wi h di e en ea men s h oughou he exposu e pe iod. The poin s ep esen he a e age o he i e expe imen al
eplica es, and he e ical ba s ep esen he minimum and maximum concen a ions. Al, V, Fe, and Ni ollowed he same pa e n as Cu; he concen a ions a e
shown in Fig. S2.
Fig. 3. No malized abso p ion spec a o 14 samples in he egion om 600 o 1800 cm
−1
.
A. V´
azquez-A ias e al.
Jou nal o Haza dous Ma e ials 459 (2023) 132216
6
ansplan s a ached o ocks was much g ea e because hey we e no
weighed be o e exposu e, ( he quan i y was de e mined on he basis o
he numbe o halli). Thus, ega ding weigh loss, bags wi h esh ma-
e ial a e as good as he mo e na u al app oach o a aching he whole
halli o he ocks.
The o he main conside a ion in selec ing he bes ea men is he
di e ences in hei me al-up ake capaci y. The concen a ions o mos
elemen s we e much highe in he de i alized ansplan s (bo h
me hods) han in he li e seaweed. P e ious s udies ha e shown
di e en e ec s in me al up ake depending on he o ganism and
elemen : in e es ial mosses, Sphagnum palus e did no cap u e mo e
Pb a e de i aliza ion [12]; in Pseudoscle opodium pu um he concen-
a ions o PTEs in li e moss anged om sligh ly lowe o much highe
han in o en-d ied samples [3]; in Hypnum cup essi o me bo h simila
[21] and highe up ake le els [20] ha e been epo ed; and he up ake
o ace elemen s in de i alized Pla yhypnidium ipa ioides was simila o
sligh ly highe han in li e ansplan s [7]. The only s udies ha ha e
compa ed he di e ences in he accumula ion o me als be ween de i-
alized and li e seaweed a e bio emedia ion s udies, in which he bio-
so p ion o seaweed biomass (some imes g ound ma e ial) has been
es ed. In hese s udies, highe le els o up ake by de i alized seaweed
ha e been sugges ed [32]; howe e , he only ecen s udy compa ing
up ake le els showed ha li e Ul a lac uca can emo e mo e Hg om
spiked wa e han de i alized ma e ial [27].
The highe elemen up ake in de i alized ansplan s han in li e
ansplan s suppo s he hypo hesis ha he main up ake mechanism o
me al accumula ion in seaweed is chemical adso p ion a he han
ac i e in e naliza ion [41], as de i alized seaweeds a e no capable o
he la e . Howe e , he eason why he concen a ions o elemen s in
de i alized ansplan s ange om simila o mo e han one o de o
magni ude highe han in li e ansplan s equi es u he explana ion.
Nume ous ac o s may con ibu e o hese di e ences: 1) up u e o cell
memb anes du ing he de i aliza ion p ocess, which may expose bind-
ing si es in he in e io o he memb anes; 2) hea -induced chemical
al e a ion o he cell walls and memb anes, which can inc ease he a -
ini y o ce ain elemen s, as occu s wi h o he p e-exposu e ea men s
[18]; 3) inac i a ion o he adap a ions p esen in li e seaweed o p e-
en he up ake o oxic elemen s; he mechanisms in ol ed include he
sec e ion o exuda es o cap u e hese elemen s [38], and possibly he
exc e ion o chela ed elemen s h ough ac i e anspo , bo h o which
would con ibu e o lowe ing he concen a ions o esh seaweed; 4)
di e en ial loss o ma e ial in he de i alized ansplan s: i all o he
componen s in seaweed do no ha e he same a ini y o each elemen ,
he p e e en ial loss o some componen s o e o he s could cause di -
e ences in he accumula ion capaci y o he di e en ansplan s; 5)
g ow h o esh ansplan s; in he case o esh moss ansplan s, g ow h
has been ound o lead o some a ia ion in elemen al concen a ions
due o he di e en ial accumula ion o di e en ly aged plan pa s [14],
in which me al concen a ions a e di e en in F. esiculosus [16]; and 6)
physical modi ica ion o he seaweed su ace, allowing
pollu an -con aining pa icles o adhe e mo e easily o he su ace o he
de i alized ansplan s.
Two esul s ha helped us es hese hypo heses we e he compa ison
o Al-no malized concen a ions in samples and sedimen , and he FTIR
spec a o esh and d ied samples. Fo mos elemen s, Al a ios we e
highe in de i alized samples, which indica es ha a g ea e pe cen age
o hose elemen s can be accoun ed o by he con ibu ion om sedi-
men s, sugges ing ha de i alized samples may ha e mo e adhe ed
pa icles han esh samples. This pa e n was obse ed o almos all o
he elemen s, excep V, Fe, and Pb. One possible explana ion may be ha
he sedimen is he main con ibu o o he concen a ion o hese ele-
men s in all samples. This is u he suppo ed by he ac ha SS4 is he
only si e whe e he e we e di e ences be ween esh and de i alized
ansplan s in he Al a ios o Fe and Pb. The o igin o hese elemen s is
usually geologic, and his SS is a ec ed by a me allu gic indus y ha
may be eleasing hem in soluble o m, so he al e a ion o hei Al a ios
may indica e ha his is he only case in which he soluble concen a-
ions a e high enough o make a signi ican di e ence. This esul sup-
po s he hypo hesis ha he de i aliza ion p ocess al e s he physical
p ope ies o he ansplan s, allowing mo e sedimen pa icles o adhe e
o hem.
The FTIR spec a o esh and d ied samples showed di e ences in
he IR abso p ion p o iles, and he PCA (Figu e 6SM) clus e ed hem in
clea ly de ined g oups. The g oup o samples wi h he mos dis inc
p o iles was he d ied ansplan s a e exposu e, bu di e ences we e
also obse ed in he spec a o exposed esh samples and he con ols,
whe eas he spec a o he wo con ol g oups we e much mo e simila o
each o he . The e a e a ew signi ican egions whe e he di e en
ea men s yielded di e en peaks: he peaks a a ound 750–950 cm
−1
ha e been ela ed o C-O and C-H bonds in u onic and mannu onic
esidues o algina e polysaccha ides [22]; bo h he con ols and exposed
esh samples gene a ed peaks o di e en in ensi y a a ound 820, 880
and 930 cm
−1
, while he exposed d ied samples did no p oduce peaks a
880 and 930 cm
−1
, ha ing a peak a 910 cm
−1
ins ead. The b oad peak
om 1220 o 1260 cm
−1
was common o bo h con ols and esh sam-
ples, bu i appea ed shi ed o 1210 cm
−1
in exposed d ied samples.
This peak is ela ed o sulpha e es e g oups ound in ucoidan [8]. In he
1300–1800 cm
−1
egion all excep he exposed d ied samples also
sha ed he same pa e ns, wi h wo peaks a ound 1410 and 1600 cm
−1
,
which ha e been ela ed o he ca boxyla e g oups p esen in algina e
[22,30]. Exposed d ied samples, on he o he hand, gene a ed h ee
peaks, wi h shi s owa ds highe wa enumbe s. The di e en spec a in
hese egions imply ha he quan i ies and/o composi ion o he bio-
molecules bea ing he unc ional g oups o which ace elemen s a ach
a e also di e en , and he e o e he al e a ions caused by he de i ali-
za ion p ocess (a leas in he case o o en d ying) a e pa ly esponsible
o he di e ences in accumula ion. Howe e , esh and d ied con ols
ha e simila IR p o iles, indica ing ha he hea exposu e i sel is no
su icien o al e he composi ion o he seaweed, and mos o he
changes occu du ing he exposu e pe iod. This sugges s ha he mod-
i ica ions occu ei he due o he di e en ial loss o componen s, o ha
he de i aliza ion allows chemical al e a ion o occu du ing he expo-
su e pe iod, possibly h ough decomposi ion.
The ac ha hese wo accumula ion mechanisms (adhesion o
sedimen pa icles and chemical binding o ex acellula componen s)
seem o be able o make a sizable con ibu ion o he accumula ion o
PTEs sugges s ha , e en in li e seaweed, in e naliza ion is no a
necessa y up ake pa hway o PTE accumula ion. This is key o unde -
s and how seaweed in e ac wi h pollu an s in hei en i onmen , o a
ew easons: i sugges s ha mos o he PTEs ha seaweeds a e exposed
o a e unable o a ec he in acellula componen s, which helps o
unde s and he high ole ance hese o ganisms ha e o pollu ion [19]; i
also implies ha knowing he chemical species o PTEs and whe he hey
a e a ached o pa icles is necessa y o p edic hei impac on sea-
weeds, as he ex acellula componen s a e able o cap u e mos species
o many PTEs; inally, i also poin s o he e ec i eness o he p o ec ion
mechanisms seaweeds ha e agains pollu an s, since hey can con ol
hei ex acellula composi ion o a oid in e naliza ion [1]. Fu he -
mo e, hese indings also ha e p o ound implica ions o he in e p e-
a ion o biomoni o ing s udies, due o he implica ion ha o ex ac
p ecise in o ma ion o he concen a ions o seaweeds, i is necessa y o
know in which cellula compa men s he PTEs a e.
Ano he unexpec ed inding was he a ia ion be ween elemen s.
Whe eas de i alized ansplan s we e able o ake up much highe
amoun s o mos elemen s han li e ones, he concen a ions o Mn and
Cd in hem dec eased du ing he exposu e pe iod. One possible expla-
na ion o he loss o Mn is ha , as his elemen is essen ial o pho o-
syn hesis [24], seaweeds main ain high in acellula concen a ions ha
could be los due o memb ane dis up ion caused by he de i aliza ion
p ocesses. Howe e , his does no explain he dec ease in Cd, which is a
oxic elemen wi h e y li le biological unc ion, i any. Ano he
possible explana ion is he chemical modi ica ion o he unc ional
A. V´
azquez-A ias e al.
Jou nal o Haza dous Ma e ials 459 (2023) 132216
7
g oups p esen on he su ace o he cells o which PTEs can be bound,
such as ca boxyl, amino, sulpha e and hyd oxyl g oups [9,26]. The
al e a ion o c ea ion o new unc ional g oups du ing he de i aliza ion
p ocess could a ec he a ini y o he ma e ial o speci ic elemen s.
Howe e , he up ake pa e ns o some elemen s a e di icul o explain;
o example, i has been sugges ed ha he a ini y o chemical elemen s
o di e en ligands depends on hei ionic and co alen index [33,35],
bu he accumula ion o Cu and Cd, which a e e y simila in his ega d,
was comple ely di e en in he p esen s udy.
All o hese pa e ns help us o unde s and he ad an ages and lim-
i a ions o using li e and de i alized seaweed ansplan s. In li e
ansplan s, he mechanisms o egula ing PTE up ake a e he same as
in o ganisms occu ing na u ally in he ecosys em, and he e o e hey
be e e lec he elemen s a ec ing hem. Li e ansplan s a e also mo e
esilien and du able because hey can main ain hei s uc u e which
makes longe exposu e pe iods possible; howe e , hey a e s ill capable
o g ow h, which a ec s he eliabili y o he da a. De i alized ans-
plan s, on he o he hand, ha e some ad an ages: 1) elemen al con-
cen a ions a e no a ec ed by g ow h o he seaweed; 2) he
concen a ions o mos elemen s a e highe , which can be impo an o
he de ec ion o elemen s ha display low concen a ions such as Pb;
some o he ini ial concen a ions o his elemen in ou expe imen we e
below he LOD, bu he pos -exposu e concen a ions o de i alized
ansplan s we e much highe ; and 3) hey a e also easie o use om a
logis ical poin o iew, as d ied seaweed can be kep in he labo a o y
o longe . I would he e o e be possible o collec la ge amoun s o
ma e ial, d y i , and used i o a long pe iod, hus p e en ing di e ences
in he ini ial concen a ions such as hose we ound o Ba.
Based on hese p ope ies, bo h ypes o ansplan s may be use ul in
di e en scena ios. F esh ansplan s would be be e o p oducing e-
sul s ep esen a i e o longe pe iods, and when he objec i e is o
ob ain in o ma ion on he impac o PTEs on he ecosys em. By con as ,
de i alized ansplan s would p obably be be e o ob aining eliable
da a on he me al concen a ions in seawa e in a sho ime, al hough
u he in o ma ion abou he ela ionship be ween he concen a ions
in ansplan s and wa e mus be ob ained o con i m his possibili y.
5. Conclusions
•Fo F. esiculosus, ansplan s consis ing o esh apices in bags a e
easie o use and as e ec i e o ace elemen biomoni o ing as
ansplan s o whole halli (imi a ing na u al condi ions).
•De i alizing he seaweeds a ec s he consis ency and du abili y o
he ansplan s, leading o comple e disin eg a ion o he ma e ial in
as li le as 8 days, making hei use o pe iods longe han a week
in iable.
•Up ake o ace elemen s was much highe in de i alized ansplan s
han in esh ansplan s, indica ing he possibili y o using he
o me o sho exposu e pe iods.
•The physicochemical modi ica ions caused by he de i aliza ion
p ocess a ec he elemen al up ake. A e exposu e, de i alized
ansplan s con ain di e en polysaccha ides and unc ional g oups,
which a ec s hei a ini y o di e en elemen s.
•De i alized ansplan s con ain highe concen a ion o elemen s
associa ed wi h he sedimen , p obably due o physical modi ica ion
o he su ace ha enables binding o g ea e numbe s o pa icles.
•PTEs physically o chemically bound o he su ace o he seaweeds
a e e y signi ican o me al accumula ion, highligh ing he
impo ance o unde s anding he accumula ion mechanisms o un-
de s and how hey a e a ec ed by PTE pollu ion.
Funding
This s udy is pa o he p ojec PID2022–142802NB-I00 awa ded by
he Spanish Minis e io de Ciencia e Inno aci´
on. The au ho s belong o
he G upo de Re e encia Compe i i a GRC GI-1252/GPC2020–23
(ED431C 2020/19) which is co- unded by ERDF (EU). A. V´
azquez-A ias
is g a e ul o he Spanish Minis e io de Ciencia, Inno aci´
on y Uni-
e sidades o a g an awa ded wi hin he P og ama de Fo macion de
P o eso ado Uni e si a io (g an numbe FPU19/01989).
En i onmen al Implica ion
Hea y me als such as he ones s udied in his a icle a e some o he
pollu an s wi h he g ea es impac on coas al en i onmen s. This wo k
imp o es he use o biomoni o iza ion wi h seaweeds in se e al aspec s:
s udying he use o de i aliza ion and he applica ion o de i alized
ansplan s; helping o unde s and he esul s o biomoni o iza ion
s udies; and ad ancing ou unde s anding o he unde lying up ake
mechanisms. This way, i enables he use o a aluable ool o con ol
pollu ion in seawa e .
CRediT au ho ship con ibu ion s a emen
An ´
on V´
azquez-A ias: In es iga ion, Fo mal analysis, W i ing –
o iginal d a . Jesús R. Aboal: Concep ualiza ion, W i ing – e iew &
edi ing, Supe ision, Funding acquisi ion. J. ´
Angel Fe n´
andez:
Concep ualiza ion, W i ing – e iew & edi ing, Supe ision, Funding
acquisi ion.
Decla a ion o Compe ing In e es
The au ho s decla e ha hey ha e no known compe ing inancial
in e es s o pe sonal ela ionships ha could ha e appea ed o in luence
he wo k epo ed in his pape .
Da a a ailabili y
Da a will be made a ailable on eques .
Acknowledgemen s
The au ho s a e g a e ul o Ve ´
onica Fe n´
andez and Pablo Gi ´
aldez
o hei con ibu ion o he expe imen al phase, and o RIAIDT-USC o
he use o hei analy ical acili ies. We also owe hanks o he anony-
mous e iewe whose commen s helped us imp o e he manusc ip .
Appendix A. Suppo ing in o ma ion
Supplemen a y da a associa ed wi h his a icle can be ound in he
online e sion a doi:10.1016/j.jhazma .2023.132216.
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