Wa e Resea ch 234 (2023) 119793
A ailable online 23 Feb ua y 2023
0043-1354/© 2023 The Au ho (s). Published by Else ie L d. 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/).
High Hg biomagni ica ion in No h A lan ic coas ecosys ems and limi s o
he use o δ
15
N o es ima e ophic magni ica ion ac o s
M. Te esa Boque e
a
,
*
, Jesús R. Aboal
a
, Rub´
en Villa es
b
, Uxía Do ado-Ga cía
a
, J.
´
Angel Fe n´
andez
a
a
CRETUS Ins i u e, Depa men o Func ional Biology, Ecology Uni , Uni e sidade de San iago de Compos ela, 15782 San iago de Compos ela, Spain
b
Depa men o Func ional Biology, Ecology Uni , Escola Poli ´
ecnica Supe io de Enxe˜
na ía, Uni e sidade de San iago de Compos ela, 27002 Lugo, Spain
ARTICLE INFO
Keywo ds:
Dogwhelk
Food chains
Mussel
Ni ogen iso ope a io
Ma ine pollu ion
ABSTRACT
Me cu y con amina ion is a global en i onmen al p oblem. This pollu an is highly oxic and pe sis en which
makes i ex emely suscep ible o biomagni y, i.e. inc ease i s concen a ions as i mo es up he ood chain,
eaching le els ha h ea en wildli e and, ul ima ely, ecosys ems’ unc ion and s uc u e. Me cu y moni o ing is
hus c ucial o de e mine i s po en ial o damage he en i onmen . In his s udy, we assessed he empo al ends
o he concen a ions o Hg in wo coas al animal species closely connec ed by a p eda o -p ey in e ac ion, and
e alua ed i s po en ial ans e be ween ophic le els using he δ
15
N signa u es o he wo species. Fo his, we
pe o med a mul i-yea su ey o he concen a ions o o al Hg and he alues o δ
15
N in he mussel My ilus
gallop o incialis (p ey) and he dogwhelk Nucella lapillus (p eda o ) sampled along ~1500 km o he No h
A lan ic coas o Spain o e a 30-yea pe iod ( i e su eys be ween 1990 and 2021). Concen a ions o Hg
dec eased signi ican ly be ween he i s and he las su ey in he wo species s udied. Excep o he 1990
su ey, he concen a ions o Hg in mussels we e amongs he lowes egis e ed in he li e a u e o he No h
Eas A lan ic Ocean (NEAO) and he Medi e anean Sea (MS) be ween 1985 and 2020. None heless, we de ec ed
Hg biomagni ica ion in almos all su eys. Wo yingly, ophic magni ica ion ac o s ob ained he e o o al Hg
we e high and compa able o he ound in he li e a u e o me hylme cu y, he mos oxic and eadily bio-
magni ied o m o his elemen . The δ
15
N alues we e use ul o de ec Hg biomagni ica ion unde no mal ci -
cums ances. Howe e , we ound ha ni ogen pollu ion o coas al wa e s di e en ially a ec ed he δ
15
N
signa u es o mussels and dogwhelks limi ing he use o his pa ame e o his pu pose. We conclude ha Hg
biomagni ica ion could cons i u e an impo an en i onmen al haza d e en when ound a e y low concen-
a ions in he lowe ophic le els. Also, we wa n ha use o δ
15
N in biomagni ica ion s udies when he e is some
unde lying ni ogen pollu ion p oblem migh lead o misleading conclusions.
1. In oduc ion
Me cu y is one o he mos oxic elemen s on Ea h ha ing impo an
e ec s a neu al, ho monal, and ep oduc i e le els wi hin indi iduals
(Boening, 2000; Fe nandes Aze edo e al., 2012; Tan e al., 2009) wi h
po en ial demog aphic consequences a he popula ion le el (Gou e
e al., 2014). This elemen occu s na u ally and can be eleased o he
en i onmen h ough olcanic e up ions, ock wea he ing, and e apo-
a ion om he ocean (Boening, 2000). Human ac i i ies like coal
combus ion and mining, howe e , ha e mobilized me cu y om he
li hosphe e deposi s and inc eased i s concen a ions in he a mosphe e
by 450% abo e na u al le els (UN En i onmen P og amme, 2019).
Me cu y is o emos emi ed o he a mosphe e in elemen al o m ha is
highly ola ile and has an a mosphe ic li e ime o abou one yea ,
making i ema kably suscep ible o long- ange a mosphe ic anspo
(Fi zge ald and Lambo g, 2003). E en ually, Hg eleased in o he a -
mosphe e will be deposi ed di ec ly in o he oceans o on o land om
whe e i can be washed in o wa e bodies. This Hg can be e-emi ed o
he a mosphe e and deposi ed again (Selin e al., 2008). Deposi ed Hg on
oceans and land will ake abou 2000 yea s o e u n o mo e s able
e es ial and ocean ese oi s (Selin e al., 2008; Sunde land and
Mason, 2007).Thus, an h opogenic Hg emissions can nega i ely impac
he en i onmen o hund eds o housands o yea s om hei i s
elease (UN En i onmen P og amme, 2019).
* Co esponding au ho : M. Te esa Boque e, Rúa Lope G´
omez de Ma zoa, s/n, 15705, San iago de Compos ela, Spain.
E-mail add ess: [email p o ec ed] (M.T. Boque e).
Con en s lis s a ailable a ScienceDi ec
Wa e Resea ch
jou nal homepage: www.else ie .com/loca e/wa es
h ps://doi.o g/10.1016/j.wa es.2023.119793
Recei ed 5 No embe 2022; Recei ed in e ised o m 31 Janua y 2023; Accep ed 21 Feb ua y 2023
Wa e Resea ch 234 (2023) 119793
2
I is undeniable ha me cu y con amina ion is a se ious and global
en i onmen al p oblem. Inge Ande sen, he Uni ed Na ions Depu y
Sec e a y Gene al and Execu i e Di ec o o he Uni ed Na ions En i-
onmen P og am, has ecen ly de ined i as “one o he g ea es challenges
o he en i onmen and human heal h” (UNEP, 2019). The magni ude o
his p oblem is such ha , pa ly d i en by he Minama a Con en ion on
Hg ( he i s globally legally binding ins umen es ablishing he mea-
su es o be unde aken o p o ec human heal h and he en i onmen
om Hg and i s compounds; (UNEP, 2013)), o ganiza ions like he
Uni ed Na ions (UN), he U.S. En i onmen al P o ec ion Agency (EPA),
and he Eu opean Union (EU) ha e de eloped coo dina ed p og ams o
speci ically p o ec he en i onmen om he nega i e impac s o Hg
eleased in o he ai , wa e , and soil (UN En i onmen P og am Global
Me cu y Pa ne ship -h ps://www.unep.o g/globalme cu ypa ne sh
ip/-, EPA Me cu y -h ps://www.epa.go /me cu y-, and EU Global
Me cu y Obse a ion Sys em -h ps://www.gmos.eu/). These p og ams
highligh he necessi y o de elop long- e m spa io empo al obse a-
ions o Hg in he en i onmen o be e p edic i s impac as well as o
e alua e he e ec i eness o he p o ec i e measu es unde aken.
Ino ganic Hg ha eaches aqua ic sys ems can be biome hyla ed by
mic oo ganisms o o m me hylme cu y, he main o m in which his
elemen is accumula ed in bo h humans and wildli e (D’I i, 1991). Once
inco po a ed in o o ganisms’ issues di ec ly om he wa e o h ough
ood consump ion, his o ganic o m binds s ongly o sul hyd yl g oups
in p o eins, esul ing in low a es o exc e ion (Be nha d and And eae,
1984). Thus, Hg biomagni ica ion is one o he mos conce ning issues
ela ed o Hg con amina ion. Biomagni ica ion is de ined as he p o-
g essi e buildup o pollu an s in o ganisms h ough he ood web
(Zweig, 1973). Acco dingly, he concen a ions o pollu an s in o gan-
isms o highe ophic le els will be highe han hose in hei die .
Biomagni ica ion is hus a special case o pollu an bioaccumula ion
p ocess in which he main exposu e ou e is he o ganism’s die (Con-
nell, 1989; G ay, 2002). Me cu y biomagni ica ion in ma ine ood webs
has been epo ed be o e (Kidd e al., 2011), wi h he mos classical and
agic example being he dea hs o he Minama a popula ion as a esul
o Hg poisoning om he consump ion o con amina ed ish and shell ish
(D’I i, 1991). De ec ing and quan i ying biomagni ica ion p ocesses in
na u al ecosys ems is hus c ucial o assess how he p esence o Hg in
aqua ic en i onmen s migh ansla e in o local o global exposu e isk.
Pollu an biomagni ica ion p ocesses can be iden i ied h ough he
es ima ion o he ophic magni ica ion ac o (TMF) as he slope o he
eg ession be ween he concen a ions o he pollu an on each membe
o he ophic chain/web agains i s ophic le el. A signi ican and
posi i e TMF would be indica i e o biomagni ica ion whe eas a sig-
ni ican bu nega i e TMF would poin o biodilu ion. The use o s able
ni ogen iso ope a io (δ
15
N =
15
N:
14
N) o in es iga e pollu an bio-
magni ica ion p ocesses has been p oposed as a mo e quan i a i e
app oach han adi ional me hods like ood composi ion analyses.
(B oman e al., 1992; Chou elon e al., 2018; Fos e e al., 2012; Hong
e al., 2013; Keh ig e al., 2013; La oie e al., 2013). The eliabili y o
his me hod, howe e , depends upon he quali y o he δ
15
N signa u e as
a good ood web desc ip o (Cabana and Rasmussen, 1994). I is well
known ha ni ogen con amina ion p ocesses can al e he δ
15
N signa-
u es o o ganisms (Hea on, 1986; McClelland and Valiela, 1998). Unde
such ci cums ances, he δ
15
N signa u e could no be a eliable ool o
TMF es ima ion. Ye , o he bes o ou knowledge, no single s udy has
add essed his issue so a .
Conside ing all o he abo e, we p esen he e a da ase o he con-
cen a ions o o al Hg ( ha includes bo h o ganic – me hylme cu y –
and ino ganic o ms o his elemen ) and he δ
15
N alues in wo common
dwelle s o he in e idal ocky sho e o he No heas A lan ic Ocean
closely connec ed by a p eda o -p ey in e ac ion: he Medi e anean
mussel My ilus gallop o incialis (p ey) and he A lan ic dogwhelk Nucella
lapillus (p eda o ). These species we e collec ed along ~1500 km o he
No h A lan ic coas o Spain du ing i e su eys spanning 30 yea s
be ween 1990 and 2021. This s udy his aimed a (i) in es iga ing he
empo al ends o he concen a ions o Hg in hese wo animal species;
(ii) e alua ing i s po en ial ans e be ween ophic le els as well as
po en ial changes in ophic ans e o e ime; and (iii) assessing he
u ili y o δ
15
N o iden i y and moni o Hg biomagni ica ion pa e ns.
2. Ma e ial and me hods
2.1. Sample collec ion and p ocessing
We collec ed samples o wo coas al animal species belonging o wo
di e en ophic le els and using di e en eeding s a egies: he bi al e
mollusc My ilus gallop o incialis (Lama ck, 1819), a il e - eede (Deu-
de o e al., 2009); and he gas opod mollusc Nucella lapillus (Linnaeus,
1758), a p eda o (C o he s, 1985) ha p e e en ially eeds on mussels
(Hughes and D ewe , 1985). Samples we e collec ed in summe du ing
ou ex ensi e (1990, 2001, 2003 and 2021) and one in ensi e (2017)
sampling su eys a 89 di e en sampling si es (SS) sp ead ac oss he
Galician coas (NW Spain; Fig. 1). In 1990, he su ey included a o al o
58 SS wi h M. gallop o incialis collec ed a 49 SS and N. lapillus a 16 SS
(7 SS in common). In 2001, we sampled 24 SS wi h M. gallop o incialis
collec ed a 22 SS and N. lapillus a 12 SS (10 SS in common). In 2003, we
sampled 37 SS wi h M. gallop o incialis collec ed a 37 SS and N. lapillus
a 25 SS (25 SS in common). In 2017, we in ensi ied he sampling in wo
ias ( idal inle s) ha we e mos se iously a ec ed by Hg con amina ion
(P ego and Cobelo-Ga cía, 2003): i) he Ría de Fe ol (Zone E in Fig. 1);
and ii) he Ría de Pon e ed a (second sou he nmos ia in Zone D,
Fig. 1). Bo h ias a e a ec ed by di e en pollu ion sou ces, such as
highly popula ed u banized zones, indus ial acili ies (i.e. shipya ds
and s eel wo ks in Fe ol and a chlo -alkali in Pon e ed a) and busy
comme cial po s. The e o e, in his su ey we sampled a o al o 8 SS,
wi h M. gallop o incialis collec ed in all 8 SS and N. lapillus in 6 SS (6 SS
in common). Finally, in 2021 we conduc ed he las ex ensi e su ey
which included 32 SS, wi h M. gallop o incialis collec ed in all 32 SS and
N. lapillus in 23 SS (23 SS in common). All si es sampled pe su ey and
species a e shown in Table S1.
All SS we e loca ed mo e han 300 m om was e pipes, po s and
indus ial ins alla ions, and mo e han 150 m om he mou hs o p i-
ma y o seconda y e luen s. The sampling was always conduc ed a low
ide in he in e idal zone ollowing a zigzag pa h be ween poin s on he
coas line sepa a ed by a linea dis ance o 50 m. A each SS, we collec ed
a leas 25 specimens o M. gallop o incialis (shell leng h ≥6 cm) and 30
specimens o N. lapillus (shell leng h ≥2 cm). All he specimens we e
washed in si u wi h seawa e and combined o o m a composi e sample
o each species pe si e be o e being anspo ed in cool boxes (ca. 4 ◦C)
o he labo a o y.
In he labo a o y, all he specimens we e pu ged o 48 o 72 h in
con inuously lowing, ae a ed and il e ed (ac i e ca bon) seawa e . The
samples we e hen s o ed ozen a −30 ◦C. P io o sample p epa a ion/
p ocessing, he ma e ial was hawed a oom empe a u e. Then, we
sepa a ed each specimen’s mea om i s shell wi h he aid o high-
densi y poly hene dissec ion ools. These samples we e homogenized
(Wa ing Blende 34BL99), d ied in a o ced ai o en a 40 ◦C, and again
homogenized in a mill (Re sch MM400 Ul a Cen i ugal Mill). A e
p ocessing, all samples we e s o ed a oom empe a u e in da kness
un il hey we e analyzed.
2.2. Chemical analysis
We de e mined he concen a ions o Hg in an elemen al analyze
(DMA 80 Miles one). Du ing he analysis, we included samples o wo
ce i ied e e ence ma e ial (TORT-1, lobs e hepa opanc eas; and ERM-
CE278k, Mussel) and analy ical blanks o quali y con ol. Also, all
samples we e analyzed in duplica e. The eco e y a e o he e e ence
ma e ial was highly sa is ac o y (106 and 90% espec i ely), while he
o e all e o o he analysis o duplica e samples was e y low (3%).
The limi o quan i ica ion, calcula ed om he alues ob ained om he
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
3
analy ical blanks (as Mean
blanks
+10*S dDe
blanks
), was 0.4 ng g
−1
.
To de e mine δ
15
N alues, we weighed aliquo s o 3.00 ±0.1 mg o
each sample in in capsules (Elemen al Mic oanalysis). The analy ical
de e mina ions we e conduc ed by he Resea ch Suppo Se ices a he
Uni e si y o A Co u˜
na (Spain), using an elemen analyze (Fla-
shEA1112, The moFinnigan) coupled o an iso ope a io mass spec-
ome e (Del aV Ad an age, The mo Scien i ic) ia an in e ace uni
(Con loIV). The accu acy o he p ocedu e was de e mined by analysis o
ace anilide as a calib a ion s anda d. Calib a ion o he e e ence gas
(N
2
) o a mosphe ic
15
N was ca ied ou wi h IAEA-N-1 ((NH
4
)
2
SO
4
),
IAEA-N-2 ((NH
4
)
2
SO
4
) and IAEA-NO-3 (KNO
3
) as s anda ds. The iso-
opic a io (
15
N /
14
N) in he samples was de e mined by compa ison
wi h a s anda d (a mosphe ic N
2
). The ela i e abundance o
15
N in he
sample (δ
15
N) was calcula ed using he o mula δ
15
N (‰) =[(R
sample
/
R
s anda d
) −1] ×1000, whe e R is he
15
N/
14
N a io. The o e all e o
calcula ed o he eplica e samples was e y low (3%).
The concen a ions o Hg and alues o δ
15
N o all he collec ed
samples (pe su ey and species) a e shown in Table S1.
2.3. S a is ical analysis
In he i s place, we assessed he amoun o in aspeci ic a ia ion a
he si e le el in he concen a ions o Hg and he δ
15
N alues in mussels
and dogwhelk. Fo his, we es ima ed he coe icien o a ia ion ( a io
o he s anda d de ia ion o he mean) in h ee biological eplica es o
each o he species consis ing o 10 indi iduals pe eplica e, in each o
18 SS ( o dogwhelks) and 8 SS (mussels) om he 1990 and 2017
su eys.
All s a is ical analyses we e conduc ed using R 4.2.1 (R Co e Team,
2022) implemen ed unde RS udio 1.2.5042 (RS udio Team, 2020). All
p- alues <0.05 we e conside ed signi ican . Fo all he models, we
e alua ed he no mali y and homoscedas ici y (homogenei y o a i-
ances) o he esiduals using he Shapi o and Le ene es s espec i ely,
as well as by isually inspec ing he plo s o he esiduals. When hese
assump ions we e no me , we applied ans o ma ions o he dependen
a iables o used al e na i e, non-pa ame ic es s.
Fi s , using he “ ull da ase ” (n =89 SS in o al; 85 SS wi h 148 da a
poin s ac oss su eys o mussels, and 45 SS wi h 82 da a poin s o
Fig. 1. Map showing he loca ion o he s udy egion in he NW o Spain (A), he ias whe e he sampling was ca ied ou wi hin he s udy egion (B), and a de ailed
iew o he sampling si es loca ed in he no he n (C, E, F, G) and wes e n (D) ias.
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
4
dogwhelks), we es ed o signi ican di e ences among su eys in he
mean concen a ions o Hg and δ
15
N alues sepa a ely o each species.
Fo Hg in bo h species and δ
15
N in dogwhelks, we un a one-way ANOVA
(analysis o a iance) using he unc ion ao om he base R package
“s a s”. Fo δ
15
N in mussels, we un he non-pa ame ic equi alen o
one-way ANOVA, i.e. K uskal-Wallis es , wi h he unc ion k uskal. es
om he package “s a s”. When he main ANOVA and K uskal-Wallis
es s esul ed signi ican , we pe o med all possible pai wise compa i-
sons be ween su eys using he unc ions pai wise. . es and dunn. es
(package “dunn. es ”) espec i ely, wi h he Hochbe g’s GT2 me hod,
designed o add ess unequal sample sizes. Using he “common da ase ”,
ha only included si es whe e bo h species we e collec ed oge he each
su ey (n =41 SS in o al wi h 77 da a poin s), we implemen ed simila
analyses o es i he a io be ween he concen a ions o Hg in dog-
whelks and in mussels (one-way ANOVA), and he di e ence be ween
δ
15
N alues in dogwhelks and in mussels (K uskal-Wallis es ) di e ed
signi ican ly among su eys. Las ly, in o de o con i m ha he di e -
ences obse ed be ween su eys e lec ed eliable empo al ends
a he han spa ial ends, we pe o med pai ed - es s using only he
subse o da a poin s ha we e common o each pai o su eys.
Second, we looked o unusually high concen a ions o Hg and
alues o δ
15
N in he ull da ase by es ima ing he alues o he ou lie s
as he sum be ween he hi d qua ile (Q3) and 1.5- imes he in e -
qua ile ange (IQR) o each elemen and species. Simila ly, we also
looked o unusually low alues as he i s qua ile (Q1) minus 1.5-
imes he in e qua ile ange (Q1 - 1.5*IQR).
Thi d, we used he “common da ase ” o s udy he ela ionship be-
ween he concen a ions o Hg and he alues o δ
15
N in N. lapillus and
in M. gallop o incialis. Fo his, we un wo sepa a e ANCOVAs wi h he
concen a ions o Hg and he δ
15
N in N. lapillus as esponse a iables, he
concen a ions o Hg and he δ
15
N in M. gallop o incialis as p edic o s,
and Yea ( ea ed as ac o wi h 5 le els) as a co a ia e in bo h models.
We es ed o he signi icance o he in e ac ion be ween he p edic o
and he co a ia e o e alua e whe he he ela ionship be ween he
concen a ion o Hg and δ
15
N in mussels and in dogwhelks changed o e
ime. In o de o check whe he he addi ion o he in e ac ion e m
imp o ed he i o he model, we used he unc ion ano a (package
“s a s”) o compa e he model wi h and wi hou he in e ac ion. Also,
using bo h he ull and he common da ase s, we es ima ed he co-
e icien s o dispe sion ( he a io be ween he median absolu e de ia-
ion, i.e. he median o he absolu e di e ence be ween each alue and
he median, o he median) o he concen a ions o Hg and δ
15
N alues
in mussels and dogwhelk o each su ey. We used his app oach
because i is less sensi i e o ex emely high/low alues han he a io o
he mean o he s anda d de ia ion.
Fou h, we es ima ed he ophic magni ica ion ac o (TMF) as he
slope (b) o he linea eg ession be ween he s able ni ogen iso ope
a io (δ
15
N) and he log
10
alue o he concen a ion o Hg in bo h
species, (log
10
Hg =a +b δ
15
N), o assess Hg biomagni ica ion be ween
ophic le els (Chou elon e al., 2018; Hong e al., 2013; Keh ig e al.,
2013; La oie e al., 2010). Addi ionally, we used ANOVA o e alua e
whe he he TMF a ied among yea s by es ing o he signi icance o
he in e ac ion be ween δ
15
N and Yea . Since he in e ac ion was sig-
ni ican , we un indi idual simple linea eg ession models o sepa a ely
es ima e he TMF o each su ey. Finally, ollowing he a gumen s by
(Isaacs, 1973), who s a ed ha mo e enclosed si es would be mo e likely
o show pollu an biomagni ica ion han open sea si es due o hei
di e ences in he a ie y o p ey a ailable o he p eda o s, we did he
same analyses bu sepa a ely on he sampling si es ha we e loca ed in
he inne pa s o he ias (inne si es) and on he si es loca ed in he
ou e mos pa o he ias (ou e si es).
3. Resul s
The coe icien s o a ia ion calcula ed om h ee biological epli-
ca es collec ed pe species in a numbe o SS o es ima e he in aspeci ic
and wi hin-si e a iabili y o ou da a we e low bo h o Hg (mean
alues o 8 and 17% o mussels and dogwhelks espec i ely) and
especially o δ
15
N (mean alues o 2 and 3% o mussels and dogwhelks
espec i ely). This low wi hin-si e a iabili y suppo s ha , o e all, ou
da a p o ide a good ep esen a ion o he ac ual concen a ions o Hg
and he δ
15
N alues in each species wi hin each si e.
Mean concen a ions o Hg di e ed signi ican ly among su eys in
bo h species (F =33.4 and p <0.001 in mussels; F =18.3 and p <0.001
in dogwhelks; Table 1). Al hough hese concen a ions showed a 3.4-
and a 7.8- old decline in mussels and dogwhelks espec i ely be ween
he i s (1990) and he las (2021) su ey, his dec ease was no g adual
(Fig. 2A, Table S2, Table S3). Bo h species showed a s ong dec ease
be ween 1990 and 2001. Then, mean Hg concen a ions in mussels
emain a he cons an be ween 2001 and 2017 and declined again
signi ican ly in 2021 compa ed o 2001 and 2017. Mean concen a ions
in dogwhelks ollowed a simila pa e n excep o he ac ha he
lowes mean concen a ions ound in 2021 only di e ed signi ican ly
om hose in 2017. Mean δ
15
N alues, on he o he hand, emained
cons an h oughou he s udy pe iod in dogwhelks (F =1.99 and p =
0.105; Table 1) and dec eased signi ican ly in mussels (Chi sq. =58.7
and p <0.001; Table 1). This dec ease was essen ially due o a decline in
δ
15
N be ween he i s and he second su ey (1990 o 2001); a e 2001,
mean δ
15
N alues in mussels emained unchanged (Fig. 2C, Table S3).
To al Hg concen a ions anged, ac oss all su eys, be ween 28.2 and
854 ng g
−1
in mussels and be ween 69.7 and 6254 ng g
−1
in dogwhelks.
We did no ind any unusually low (≤Q1 - 1.5*IQR) concen a ions o
Hg in any o he species. The alues o he uppe ou lie s we e 385 and
1124 ng g
−1
o Hg o mussels and dogwhelks espec i ely. We iden-
i ied a simila numbe o ou lie s o Hg in bo h species: eigh o
mussels (se en in 1990 and one in 2003) and se en o dogwhelks (six in
1990 and one in 2003), al hough none o hem coincided in he same
collec ion si es (bu hey only we e collec ed oge he in wo ou o hese
i een si es). The δ
15
N alues anged be ween 4.99 and 23.7 ‰ ac oss all
su eys in mussels and be ween 7.64 and 11.5 ‰ in dogwhelks. As wi h
Hg, we did no ind any unusually low δ
15
N alues in any o he species.
The alues o he uppe ou lie s we e 12.2 and 11.3 ‰ o mussels and
dogwhelks espec i ely and, con a y o wha we ound o Hg, we
iden i ied 24 ou lie s o δ
15
N in mussels (all o hem in 1990) and only
one in dogwhelks (in 2003). The concen a ions o Hg ended o be less
a iable in mussels han in dogwhelks (coe icien s o dispe sion anging
be ween 14 and 38% and 12–42% espec i ely including bo h he ull
and common da ase s) whe eas he δ
15
N alues we e mo e a iable in
mussels compa ed o dogwhelks (coe icien s o dispe sion anging be-
ween 3 and 28% and 2–7% o mussels and dogwhelks espec i ely
including bo h he ull and common da ase s) (Table S2).
The a io be ween he concen a ions o Hg in dogwhelks and in
mussels, co esponding o he SS in which bo h species we e collec ed a
he same ime, had a minimum alue o 1.5 and a maximum o 16.4
ac oss all su eys whe eas he median a io pe su ey anged be ween
2.3 - in 2001- and 4.5 - in 2017 (Fig. 2B). The o e all model es ing o
di e ences ac oss su eys in he mean alues o his a io was ma gin-
ally signi ican (F =2.55; p =0.047; Table 1); ye , he mul iple pai wise
compa isons showed no signi ican di e ences be ween su eys
(Table S3). Finally, he di e ence be ween he δ
15
N alues in N. lapillus
and in M. gallop o incialis anged be ween −10.7 and 4.8 ac oss all
su eys whe eas he median di e ence pe su ey anged be ween 0.74
(in 1990) and 1.89 (n 2003; Fig. 2D). The esul s o he model showed
signi ican di e ences among su eys in he mean alue o his di e -
ence (Chi sq. =16.6; p =0.002). This e ec was due o he low alues
epo ed in 1990, d i en by he unusually high δ
15
N alues in mussels in
his su ey as compa ed o all o he su eys (Fig. 2C and 2D; Table S3).
All hese esul s we e suppo ed by he pai ed- - es s despi e hei lowe
numbe o da a poin s pe su ey.
We ound a signi ican ela ionship be ween he concen a ions o Hg
in mussels and dogwhelks as well as be ween he δ
15
N alues in hese
wo o ganisms (Table 2). The in e ac ion be ween Yea and he
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
5
p edic o was no signi ican in any o he models indica ing ha he
e ec o hese wo a iables in mussels on he alues o hese a iables in
dogwhelk did no a y among yea s. Indeed, adding he in e ac ion e m
did no signi ican ly imp o e he i o he models (F =0.494, p =0.741
o Hg; F =2.424, p =0.058 o δ
15
N). In he model wi hou he in e -
ac ion, he a ia ion in he concen a ions o Hg in mussels signi ican ly
explained ~60% o he a ia ion in he concen a ions o Hg in dog-
whelks whe eas ha o δ
15
N only explained 15% (Table 2).
Finally, we ound a signi ican in e ac ion be ween Yea and δ
15
N
alues in he model used o es ima e he TMFs o he da ase including
all sampling si es, he da ase including only he si es om he inne pa
o he ias, and he da ase including si es om he ou e pa o he ias
(Table S4). The e o e, we sepa a ely es ima ed he TMF o each su ey
in each da ase (Table S5) ob aining he ollowing alues: (i) da ase
including all sampling si es: 1.4, 1.7, 2.7 and 1.4 espec i ely o he
2001, 2003, 2017 and 2021 su eys (Fig. 2); (ii) da ase including only
he si es in he inne pa o he ias: 3.1, 1.6, 2.5, 1.3 espec i ely o he
1990, 2003, 2017 and 2021 su eys; and (iii) da ase including only he
si es in he ou e pa o he ias: 1.5, 1.8, 1.5 espec i ely o he 2001,
2003, and 2021 su eys (Fig. S2). TMFs o he 1990 su ey in he ull
and ou e si es da ase s a e no p esen ed because he models we e no
signi ican (Table S5).
4. Discussion
In his s udy, we pe o med a mul i-yea su ey o he concen a ions
o Hg in wo animal species om di e en ophic le els sampled along
~1500 km o he No heas A lan ic coas line o e a 30-yea ime span.
We in es iga ed he empo al ends o he concen a ions o Hg on he
coas and e alua ed i s po en ial ans e be ween ophic le els. Addi-
ionally, we assessed he u ili y o δ
15
N o iden i y and moni o Hg
biomagni ica ion pa e ns. Fi s , we showed ha Hg pollu ion dec eased
signi ican ly wi hin he s udy egion be ween 1990 and 2021 (wi h he
mos d as ic decline happening be ween 1990 and 2001). This empo al
pa e n was obse ed ega dless o he ophic le el o he o ganism
in es iga ed and despi e ha one o he la es su eys (2017) only
included samples om he wo-mos con amina ed ias in he egion.
Second, we ound e idence o Hg biomagni ica ion in his ophic sys em
ha was sus ained o e ime despi e he empo al dec ease in Hg
con amina ion. This was demons a ed by: (i) he consis en ly highe
concen a ions o Hg in he p eda o (N. lapillus) compa ed o he p ey
(M. gallop o incialis) along wi h he empo al and spa ial s abili y o he
a io be ween he concen a ions o Hg in he p eda o and in he p ey;
(ii) he high amoun o a iance in he concen a ions o Hg in he
p eda o explained by i s concen a ions in he p ey; and, (iii) he ac
ha he signi ican TMFs we e all g ea e han one.
O e all, he concen a ions o Hg in M. gallop o incialis ound in his
s udy we e low. Following he Mussel Wa ch p og am c i e ia o bi-
al es including mussels o he genus My ilus (Kimb ough e al., 2008),
66% o ou da a poin s would be classi ied as ha ing low le els o Hg
(0–170 ng g
−1
), 25% as ha ing medium le els (170–350 ng g
−1
), and
only 9% as ha ing high le els (350–1280 ng g
−1
). Mos o he da a
poin s wi hin he medium o high le els belonged o he 1990 su ey (37
ou o 50, i.e. 74%) which showed he highes concen a ions o Hg in
bo h s udy species. Also, ou da a lay in he lowe end o he ange o
concen a ions epo ed o M. gallop o incialis in a li e a u e e iew ha
included s udies om nine egions sp ead ac oss he No h Eas A lan ic
Ocean (NEAO) and he Medi e anean Sea (MS) be ween 1985 and 2020
(Fig. S1A,B). Toge he , all hese da a poin s showed no o e all inc ea-
sing/dec easing end in he concen a ions o Hg o e ime ( = − 1.941,
p >0.05 in a gene alized linea model es ing o he change in con-
cen a ions o e ime; Fig. S1A). Howe e , when spli in o smalle and
mo e de ailed egional da ase s, he e we e signi ican empo al ends
as he o e all decline obse ed in ou da a. This ag ees wi h he indings
o he Mussel Wa ch p og am, which showed no signi ican coun y-wise
le el ends, bu signi ican inc eases and dec eases in he concen a-
ions o Hg in speci ic egions o he USA coas (Kimb ough e al., 2008;
Melwani e al., 2013). Al oge he , hese esul s sugges ha , o ob ain a
mo e eliable iew o he p oblem o Hg con amina ion in coas al sys-
ems, he le els o his elemen need o be moni o ed om di e en
spa io empo al pe spec i es.
He e we iden i ied a signi ican ans e o o al Hg be ween ophic
le els in all su eys (excep 1990 in he comple e and ou e si es da a-
se s). The TMFs es ima ed o 2001, 2003 and 2021 we e p e y simila
o each o he whe eas hose es ima ed o 1990 and 2017 we e
compa a i ely highe . In e es ingly, he i s co esponded o su eys in
which mos da a poin s we e classi ied as ha ing low Hg in mussels
whe eas he la e co esponded o he su ey wi h he highes his o ical
Hg le els (1990) and he one ha only included si es om he wo-mos
pollu ed ias o he egion (2017). Repo ed TMFs o o al Hg in he
li e a u e a e compa able o he ob ained in his s udy o 2001, 2003,
and 2021. Fo example, (Meng e al., 2015) ound alues o 1.2 in
mollusks, including di e en species o bi al es and gas opods, (Qu
e al., 2022) epo ed alues o 1.4 and 1.7 o in e eb a es and ish
espec i ely, and (La oie e al., 2010) epo ed a alue o 1.4 o a ood
web including pa icula e o ganic ma e , zooplank on, gas opods and
bi al es. Some o he abo e s udies also epo ed TMFs o me hyl-
me cu y, he mos oxic and e icien ly biomagni ied ac ion o Hg.
These, we e highe compa ed o hose o o al Hg, and compa able o he
ob ained he e o 1990 and 2017. Thus, (Meng e al., 2015) epo ed
alues o 1.9, whe eas (Qu e al., 2022) epo ed alues o 2.6 and 2.2 o
in e eb a es and ish espec i ely and (La oie e al., 2010) epo ed
alues o 1.6. Wo ks epo ing he ac ion o me hylme cu y o o al Hg
in mussels o he genus My ilus showed ha , o o al Hg concen a ions
wi hin he ange o he ound in ou s udy (35–830 ng g
−1
), me hyl-
me cu y could accoun o , a leas , almos hal o he o al concen a-
ions o Hg in mussels (33–98%; (Ipolyi e al., 2004; Jęd uch e al.,
2019)); o lowe o al concen a ions (2–30 ng g
−1
), he pe cen age o
Table 1
Resul s o he one-way ANOVA (uppe able) and K uskal-Wallis es (bo om able) ca ied ou o es o signi ican di e ences among su eys in he mean con-
cen a ions o Hg (ng g
−1
) and he δ
15
N (‰) alues in each o he species s udied. M.g.: My ilus gallop o incialis; N.l.: Nucella lapillus; N.l. / M.g.: a io be ween he
concen a ion o Hg in N. lapillus and in M. gallop o incialis; N.l. - M.g.: di e ence be ween he δ
15
N alues in N. lapillus and in M. gallop o incialis; D : deg ees o
eedom; Sum Sq: sum o squa es; Mean Sq: mean squa es; F alue: F s a is ic; P (>F): p- alue;
ns
: no signi ican ; *: p<0.05; **: p<0.01; ***: p<0.001.
Species Response P edic o D Sum Sq Mean Sq F alue P (>F)
M.g. Hg Yea 4 0.061 0.015 33.36 <2E-16***
Residuals 143 0.066 0.000
N.l. Hg Yea 4 0.017 0.004 18.34 1.3E-10***
Residuals 77 0.018 0.000
δ
15
N Yea 4 0.011 0.003 1.988 0.105ns
Residuals 77 0.108 0.001
N.l. / M.g. Ra io Hg Yea 4 0.141 0.035 2.552 0.0471*
Residuals 66 0.914 0.014
Species Response P edic o D K-W Chi-sq p- alue
M.g. δ
15
N Yea 4 58.73 5.4E-12***
N.l. - M.g. Di . δ
15
N Yea 4 16.62 0.0023**
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
6
me hylme cu y o o al Hg was much lowe (12–55%; (Knop e al.,
2020)). Taken oge he , hese esul s sugges ha o al Hg can bio-
magni y e en when ound a ela i ely low concen a ions (2001, 2003
and 2021 su eys) and ha he ac ion o me hylme cu y o o al Hg
migh inc ease unde highe Hg con amina ion le els leading o highe
TMFs.
The ex en o which a pollu an is biomagni ied does no only depend
on i s physicochemical cha ac e is ics bu also on biological, ecological
and en i onmen al ac o s. Acco ding o (Rein elde e al., 1998),
biological ac o s include inges ion a e (de e mined by he weigh o
he consume , ood a ailabili y, g ow h a e, e c.), pollu an assimila-
ion e iciency (de e mined by he composi ion o he ood, he con-
cen a ion o he elemen in he ood sou ce, he gu esidence ime,
e c.), pollu an e lux/elimina ion h ough eges ion ( emo al o undi-
ges ed ma e ) o exc e ion ( emo al o me abolic was e p oduc s), and
g ow h a e (po en ial dilu ion e ec ). Ecological ac o s include he
s uc u e and complexi y o he ood web (Cabana e al., 1994) and he
eeding habi (La oie e al., 2013), among o he s. Finally,
Fig. 2. Boxplo s o he concen a ions o Hg (ng g
−1
; A)
and he alues o δ
15
N (‰; C) in samples o My ilus gal-
lop o incialis and Nucella lapillus collec ed du ing i e
di e en sampling su eys (1990, 2001, 2003, 2017,
2021), as well as he a io be ween he concen a ion o
Hg in N. lapillus and in M. gallop o incialis (B) and he
di e ence be ween he δ
15
N alues in N. lapillus and in
M. gallop o incialis (D), a e also p esen ed. The le e s on
op o he boxplo s ep esen he esul s o he pos hoc
es s ca ied ou o look o signi ican di e ences be ween
su eys in he mean alues o each a iable. In g aph A,
lowe -case le e s co espond o he esul s o he mul iple
pai wise compa isons in M. gallop o incialis and uppe -
case le e s co espond o he esul s o hese compa i-
sons in N. lapillus. Shaded ho izon al band in g aph D:
expec ed di e ence in δ
15
N alues be ween consecu i e
ophic le els, i.e. heo e ical alue o he ophic-le el
ac iona ion ac o .
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
7
en i onmen al ac o s (e.g. pH, salini y o empe a u e) can in luence
bo h pollu an a ailabili y and he biological and ecological p ocesses
men ioned abo e. In his wo k, a iabili y in he concen a ions o o al
Hg in each o he species s udied and, consequen ly, in Hg bio-
magni ica ion pa e ns is likely d i en by all hese ac o s o some ex en
bu especially by en i onmen al ac o s. The Galician coas is a highly
complex sys em consis ing o a se ies o open sea a eas in e spe sed wi h
mo e closed es ua ies (i.e. ias). The la e a e e en mo e complex as
hey a e subjec o bo h oceanic and con inen al in luences de e mining
wa e ci cula ion pa e ns, sedimen a ion p ocesses, o ganic ma e and
nu ien con en s, as well as physicochemical pa ame e s like empe a-
u e, pH, and salini y (Figuei as e al., 2002; Lo enzo and Taboada,
2005). This en i onmen al complexi y p edomina es in ou s udy wi h
sampling si es loca ed inside and ou side o he ias leading o, po en-
ially, si e-speci ic g ow h a es and me abolic ac i i y o ou s udy
species, Hg dispe sion pa e ns, ac i i y o mic oo ganisms ans o ming
ino ganic Hg in o me hylme cu y, and cha ac e is ics o he sedimen s
and hei capaci y o emo e Hg om he wa e column and eci cula e
i again. The di e en pollu ion le els and sou ces o which mussels and
dogwhelks we e exposed ac oss hese si es add ye ano he laye o
complexi y o his sys em, as he no mal unc ioning o hese o ganisms
could be signi ican ly al e ed by pollu an exposu e.
We a gue, on he o he hand, ha he e ec o he ecological ac o s
on he a iabili y o he concen a ions o Hg ound in his s udy is mino
because bo h he die a y in e ences ex ac ed om he esul s o he
δ
15
N alues in hese species and he da a ex ac ed om he li e a u e,
poin owa ds a igh p eda o -p ey ela ionship be ween dogwhelks and
mussels ac oss space and ime. Based on he assump ion ha high
in aspeci ic a ia ion in δ
15
N alues among habi a s is indica i e o
di e ences in he ela i e ophic posi ion occupied by a species in hose
habi a s (Cabana and Rasmussen, 1994), he low le els o in aspeci ic
a ia ion o δ
15
N in dogwhelk in his s udy sugges ha dogwhelks’
die a y habi s a e consis en ac oss space and ime in he s udy egion
(despi e he wide ange o habi a s s udied and he long ime span
analyzed). Also, e en hough he low alues o he di e ences in δ
15
N
be ween dogwhelks and mussels ound he e (compa ed o he heo e -
ical 3.4–4 ‰ di e ence expec ed o consecu i e ophic le els (Mina-
gawa and Wada, 1984)) would poin owa ds a p e alen omni o ous
die in dogwhelks, esul s om a p e ious s udy in wo coas al si es
loca ed wi hin he same egion ound ha suspension eede s, including
M. gallop o incialis, could make up o 70% o he p ey biomass o
N. lapillus (Bode e al., 2006). O he s udies ound ha dogwhelks end
o p e e en ially eed on mussels o e ba nacles, especially he la ge
(shell leng h ≥1.4 cm) indi iduals (Hughes and D ewe , 1985; Mo on,
2010). Thus, e en hough bo h ba nacles and mussels we e p esen in
many o ou s udy si es, we sampled la ge dogwhelks (shell leng h ≥2
cm) which, acco ding o his, would mos ly eed on mussels. Finally, he
di e ence in li espan be ween mussels (~15–25 yea s; (Cecche elli and
Rossi, 1984; Sukho in e al., 2007) and dogwhelks (be ween 4 and 6
yea s; (C o he s, 1985) could also explain some o he a ia ion in hei
Hg concen a ions and lead o he unde es ima ion o he TMFs.
I is well known ha , in addi ion o being an indica o o he ela i e
ophic posi ion o species, δ
15
N signa u es o o ganisms can be u ilized
o ace an h opogenic ni ogen inpu s in o coas al a eas (McClelland
e al., 1997; Viana e al., 2011; Viana and Bode, 2013). Ni ogen inpu s
de i ed om ag icul u e a e o en deple ed in
15
N compa ed o seawa e
(leading o lowe δ
15
N alues), while inpu s om u ban sewage,
e es ial uno , o ish a m was e a e en iched in
15
N (leading o
inc eased δ
15
N alues) (Hea on, 1986; McClelland and Valiela, 1998).
The δ
15
N alues epo ed he e o M. gallop o incialis in he 1990 su ey
included 24 ou lie s wi h alues anging be ween 12.5 – 23.7 ‰ (me-
dian =14.7 ‰). These alues we e he highes among he epo ed o
his species in a li e a u e e iew ha included s udies om i e egions
sp ead ac oss he No h Eas A lan ic Ocean (NEAO) and he Medi e -
anean Sea (MS) be ween 1998 and 2018 (Fig. S1C,D), which sugges s
ha he signi ican en ichmen in δ
15
N obse ed in mul iple si es du ing
he 1990 su ey was he esul o an h opogenic sou ces in he s udy
egion. This en ichmen in 1990 was also obse ed in mac oalgae o he
same egion (Viana e al., 2011) bu no in dogwhelk. The abno mal
peaks o δ
15
N in mussels hus led o he al e a ion o he ela ionship
be ween δ
15
N and he log ans o med Hg concen a ions in mussels and
dogwhelks esul ing in he lack o a signi ican ela ionship be ween
hese wo a iables. Consequen ly, we did no ind e idence o Hg bio-
magni ica ion in ou sys em in 1990, excep in he inne si es da ase
which did no include ou lie s. Hence, o he i s ime o he bes o ou
knowledge, we showed ha an h opogenically-de i ed ni ogen sou ces
may di e en ly al e he δ
15
N signa u es o di e en ma ine species.
This has impo an implica ions o he use o δ
15
N o iden i y Hg bio-
magni ica ion p ocesses: unde na u al ci cums ances, δ
15
N could be
used as a eliable ace o Hg biomagni ica ion; when ni ogen
con amina ion p ocesses like he obse ed in he 1990 su ey, di e -
en ially al e he δ
15
N signa u e o di e en o ganisms, howe e , his
pa ame e should no be used o in e no quan i y pollu an bio-
magni ica ion unless addi ional da a a e ga he ed o accoun o he
con ounding e ec o pollu ion on δ
15
N signa u es.
Finally, he di e ence be ween mussels and dogwhelks in he
sensi i i y o hei δ
15
N signa u e o ni ogen con amina ion could be
due o di e ences in hei eeding mode. As il e eeding species,
mussels’ die consis s mainly o plank on as well as pa icula e and
dissol ed o ganic ma e p esen in he wa e . Indeed, (Bode e al.,
2006) es ima ed ha phy oplank on accoun ed o 40 o 100% o he
die o suspension eede species, including M. gallop o incialis, in h ee
coas al a eas o Galicia. Theo e ically, he capaci y o species o e lec
on hei iso opic signa u e changes in he inpu s o ni ogen o hei
en i onmen inc eases in species wi h as e g ow h and nu ien up ake
a es (Ga ne e al., 2002). Small algae (i.e. mic oalgae), o example,
showed signi ican ly as e ni ogen up ake a es han mac oalgae (Hein
e al., 1995). E en so, some mac oalgae can display al e ed δ
15
N alues
a e only se en days o exposu e o sewage-de i ed dissol ed ino ganic
ni ogen (Ga ne e al., 2002). Acco ding o his, we would expec
g ea e and as e changes in δ
15
N esul ing om ni ogen con amina-
ion in p ima y p oduce s (phy oplank on and mac oalgae), ollowed by
p ima y consume s (e.g. mussels) and inally, by seconda y consume s
(e.g. p eda o s like he dogwhelks).
Table 2
Resul s o he ANOVA es ca ied ou o assess he ela ionship be ween he
concen a ions o Hg (ng g
−1
) and he δ
15
N alues in Nucella lapillus ( esponse
a iable) and in My ilus gallop o incialis (p edic o ), including “Yea ” o he
sampling su ey as a co a ia e ( i s wo models) o no (las wo models). D :
deg ees o eedom; Sum Sq: sum o squa es; Mean Sq: mean squa es; F alue: F
s a is ic; P (>F): p- alue;
ns
: no signi ican ; **: p<0.01; ***: p<0.001; Adj. R
2
:
adjus ed R
2
(%).
P edic o D Sum Sq Mean
Sq
F alue P (>F) Adj.
R
2
[Hg] in M.g. 1 0.014 0.014 91.8 8.9E-14
***
57.5
Yea 4 0.001 0.000 2.44 0.056
ns
[Hg] in M.g.:
Yea
4 0.000 0.000 0.493 0.741ns
Residuals 61 0.009 0.000
δ
15
N in M.g. 1 0.010 0.010 8.87 0.004 ** 22.1
Yea 4 0.011 0.003 2.52 0.051
ns
δ
15
N in M.g.:
Yea
4 0.011 0.003 2.42 0.058
ns
Residuals 60 0.068 0.001
[Hg] in M.g. 1 0.014 0.014 94.7 2.6E-14
***
58.8
Yea 4 0.001 0.000 2.52 0.050
ns
Residuals 65 0.009 0.000
δ
15
N in M.g. 1 0.010 0.010 8.14 0.006 ** 15.2
Yea 4 0.011 0.003 2.31 0.067
ns
Residuals 64 0.079 0.001
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
8
5. Conclusions
In his s udy, we ound a signi ican decline in he concen a ions o
Hg in wo common dwelle s o he in e idal ocky sho e o he No h-
eas A lan ic Ocean be ween 1990 and 2021. In addi ion, using he δ
15
N
signa u es o he wo species, we p o ided obus e idence o Hg bio-
magni ica ion e en when his elemen was ound a ela i ely low
concen a ions in he p ey. Biomagni ica ion ac o s we e highes ,
compa able o he es ima ed in he li e a u e o me hylme cu y, o he
su ey wi h he highes his o ical Hg le els and he one only including
si es om he wo-mos pollu ed ias o he egion sugges ing ha he
ac ion o me hylme cu y o o al Hg inc eases unde highe Hg
con amina ion le els leading o inc eased biomagni ica ion. Finally, we
ound ha ni ogen con amina ion may ha e di e en e ec s on he
δ
15
N signa u es o he di e en species. In his case, an h opogenically-
de i ed ni ogen inpu s o he coas al sys em caused signi ican shi s in
he δ
15
N alues o he p ey (mussels) bu no in i s p eda o (dogwhelks)
making his pa ame e useless o de ec pollu an biomagni ica ion in
na u al ood chains unde hese ci cums ances. In ligh o hese esul s,
we conclude ha despi e he o e all dec ease in Hg emissions o he
en i onmen , Hg con amina ion and biomagni ica ion migh s ill be an
impo an en i onmen al p oblem in some coas al egions and ha he
δ
15
N signa u e is a eliable ace o Hg biomagni ica ion as long as he e
is no in e e ing ni ogen con amina ion p ocess.(Fig. 3)
CRediT au ho ship con ibu ion s a emen
M. Te esa Boque e: Concep ualiza ion, Da a cu a ion, Fo mal
analysis, W i ing – o iginal d a , W i ing – e iew & edi ing. Jesús R.
Aboal: Concep ualiza ion, Me hodology, Valida ion, Da a cu a ion,
W i ing – e iew & edi ing, Visualiza ion, Supe ision, Funding acqui-
si ion. Rub´
en Villa es: Concep ualiza ion, W i ing – e iew & edi ing,
Funding acquisi ion. Uxía Do ado-Ga cía: W i ing – e iew & edi ing,
Visualiza ion. J. ´
Angel Fe n´
andez: Concep ualiza ion, Me hodology,
Valida ion, Da a cu a ion, W i ing – e iew & edi ing, Visualiza ion,
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 .
Fig. 3. Sca e plo s depic ing he ela ionship be ween he s able ni ogen iso ope a io (δ
15
N; ‰) and he log
10
alue o he concen a ion o Hg (ng g
−1
) in Nucella
lapillus and My ilus gallop o incialis o he da ase including all common sampling si es wi hin each su ey (excep he 1990 su ey in which he ela ionship was no
signi ican ). The equa ion o he simple linea eg ession model and he coe icien o de e mina ion wi h i s signi icance a e also shown. ***: p<0.001.
M.T. Boque e e al.
Wa e Resea ch 234 (2023) 119793
9
Da a a ailabili y
The da a a e a ailable wi hin he elec onic supplemen a y
ma e ials.
Acknowledgemen s
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 Xun a de
Galicia and ERDF (EU). D . M. Te esa Boque e is suppo ed by he Ma ia
Zamb ano p og am om he Spanish Minis y o Science, Inno a ion
and Uni e si ies.
Supplemen a y ma e ials
Supplemen a y ma e ial associa ed wi h his a icle can be ound, in
he online e sion, a doi:10.1016/j.wa es.2023.119793.
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