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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
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PCB pollu ion con inues o impac
popula ions o o cas and o he
dolphins in Eu opean wa e s
Paul D. Jepson1, Rob Dea ille1, Jona han L. Ba be 2, Àlex Aguila 3, Asunción Bo ell3,
Sinéad Mu phy1, Jon Ba y2, And ew B ownlow4, James Ba ne 5, Simon Be ow6,
And ew A. Cunningham1, Nicholas J. Da ison4, Ma iel en Doescha e4, Ru h Es eban7,
Ma isa Fe ei a8, And ew D. Foo e9, Tilen Geno 10,11,12, Joan Giménez13, Jan Lo e idge14,
Ángela Lla ona15, Vidal Ma in16, Da id L. Maxwell2, Alexand a Papachlimi zou2,
Rod Pen ose17, Ma hew W. Pe kins1, B ian Smi h18, Renaud de S ephanis13, Nick T egenza14,
Philippe Ve bo gh7, An onio Fe nandez19 & Robin J. Law1,2
O ganochlo ine (OC) pes icides and he mo e pe sis en polychlo ina ed biphenyls (PCBs) ha e well-
es ablished dose-dependen oxici ies o bi ds, ish and mammals in expe imen al s udies, bu he
ac ual impac o OC pollu an s on Eu opean ma ine op p eda o s emains unknown. He e we show ha
se e al ce acean species ha e e y high mean blubbe PCB concen a ions likely o cause popula ion
declines and supp ess popula ion eco e y. In a la ge pan-Eu opean me a-analysis o s anded (n = 929)
o biopsied (n = 152) ce aceans, h ee ou o ou species:- s iped dolphins (SDs), bo lenose dolphins
(BNDs) and kille whales (KWs) had mean PCB le els ha ma kedly exceeded all known ma ine
mammal PCB oxici y h esholds. Some loca ions (e.g. wes e n Medi e anean Sea, sou h-wes Ibe ian
Peninsula) a e global PCB “ho spo s” o ma ine mammals. Blubbe PCB concen a ions ini ially
declined ollowing a mid-1980s EU ban, bu ha e since s abilised in UK ha bou po poises and SDs in he
wes e n Medi e anean Sea. Some small o declining popula ions o BNDs and KWs in he NE A lan ic
we e associa ed wi h low ec ui men , consis en wi h PCB-induced ep oduc i e oxici y. Despi e
egula ions and mi iga ion measu es o educe PCB pollu ion, hei biomagni ica ion in ma ine ood
webs con inues o cause se e e impac s among ce acean op p eda o s in Eu opean seas.
The se e e impac on op p eda o s o he bioaccumula ion o DDT and o he o ganochlo ine (OC) pes icides
in ood webs was i s iden i ied in he ea ly 1960s
1
. Mos OC pollu an s we e banned in de eloped coun ies in
1Ins i u e o Zoology, Zoological Socie y o London, Regen ’s Pa k, London NW1 4RY, UK. 2Cen e o En i onmen ,
Fishe ies and Aquacul u e Science, Pake ield Road, Lowes o , NR33 0HT, UK. 3Depa men o Animal Biology and
Biodi e si y Resea ch Ins i u e (IRBio), Uni e si y o Ba celona, Ba celona, Spain. 4Sco ish Ma ine Animal S anding
Scheme, SRUC Ve e ina y Se ices D ummondhill, S a he ick Road, In e ness, IV2 4JZ, UK. 5En i onmen
and Sus ainabili y Ins i u e, Uni e si y o Exe e , Co nwall Campus, Pen yn, Co nwall TR10 9EZ, UK. 6Ma ine
and F eshwa e Resea ch Cen e, Galway-Mayo Ins i u e o Technology, Galway, I eland. 7CIRCE, Conse a ion,
In o ma ion and Resea ch on Ce aceans, Cabeza de Manzaneda 3, Algeci as, 11390, Spain. 8Ma ine Animal
Tissue Bank – Po ugal, Soc. Po uguesa de Vida Sel agem, Dep. Biologia - Uni . do Minho & CESAM, Po ugal.
9E olu iona y Biology Cen e, Uppsala Uni e si y, No by ägen 18D, SE-752 36 Sweden. 10Mo igenos-Slo enian
Ma ine Mammal Socie y, Kid iče o nab ežje 4, 6330 Pi an, Slo enia. 11Ins i u e o Biodi e si y S udies, Science and
Resea ch Cen e, Uni e si y o P imo ska, Kope , Slo enia. 12Depa men o Biodi e si y, Facul y o Ma hema ics,
Na u al Sciences and In o ma ion Technologies, Uni e si y o P imo ska, Kope , Slo enia. 13Depa men o
Conse a ion Biology, Es ación Biológica de Doñana (EBD-CSIC), Ame ico Vespuccio S/N, Isla Ca uja, 42092, Se illa,
Spain. 14Co nwall Wildli e T us Ma ine S andings Ne wo k, Fi e Ac es, Alle , T u o, TR4 9DJ, UK. 15Coo dinado a
pa a o Es udio dos Mamí e os Ma iños (CEMMA), Apa ado 15, 36380 Gondoma , Pon e ed a, Spain. 16Sociedad
de Es udios de Ce áceos en Cana ias (SECAC), Lanza o e, Spain. 17Ma ine En i onmen al Moni o ing, Penwalk,
Llech yd, Ca digan, Ce edigion, SA43 2PS, UK. 18The Na u al His o y Museum, C omwell Road, London SW7 5BD,
UK. 19Facul ad de Ve e ina ia, Uni e sidad de Las Palmas de G an Cana ia, G an Cana ia, Spain. Co espondence and
eques s o ma e ials should be add essed o P.D.J. (email: [email p o ec ed])
Recei ed: 28 July 2015
Accep ed: 23 No embe 2015
Published: 14 Janua y 2016
OPEN
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
1970s–1980s and some e es ial wildli e popula ions eco e ed1–3. Expe imen al s udies ha e es ablished ha
OC pes icides and he mo e pe sis en polychlo ina ed biphenyls (PCBs) ha e a ange o species-speci ic and
dose-dependen oxic e ec s such as immunosupp ession and ep oduc i e impai men in all mammalian species
es ed, including ma ine mammals
4–7
. Howe e , he impac o his o ic and cu en exposu e o ma ine pollu an s
on Eu opean ce acean op p eda o s is s ill la gely unknown.
To in es iga e his issue we conduc ed a me a-analysis o Eu opean da a on summed 18–25 chlo obiphenyl
congene s (∑PCB) concen a ions (mg/kg lipid weigh (lw)) in ce aceans ha we e s anded and nec opsied o
ee-li ing and biopsied. Da a came om 1,081 animals o ou species:- ha bou po poise (Phocoena phocoena,
HP)(n = 706), s iped dolphin (S enella coe uleoalba, SD)(n = 220), bo lenose dolphin (Tu siops unca us, BND)
(n = 131) and kille whale (O cinus o ca, KW)(n = 24). The ∑PCB was mainly de i ed om wo di e en labo-
a o ies, bu wi h bo h using in e na ionally s anda dised me hodology enabling ull in eg a ion o da a. The
Figu e 1. Tempo al ends in ∑PCBs in UK-s anded ha bou po poise (Phocoena phocoena) and s iped
dolphins (S enella coe uleoalba) in he wes e n Medi e anean Sea. To assess he ∑PCBs end we ha e i ed
a Gene alised Addi i e Model (GAM) o he da a using he R (R De elopmen Co e Team, 2013) package mgc .
We used hin pla e eg ession splines o do he smoo hing and he deg ee o smoo hing was de e mined by
gene alised c oss alida ion. (A) Ln ∑PCBs (sum 18–25CB) mg/kg lipid concen a ions in UK ha bou po poise
blubbe agains da e o all da a o 1990–2012 (n = 706). The con inuous line ep esen s he smoo hed end
om a Gene alized Addi i e Model i ed o he da a. The end is s a is ically signi ican (p < 0.001, F = 11.76,
esidual d = 701.97, end d = 3.03) agains he null hypo hesis o no end. The dashed lines ep esen he 95%
boo s apped Con idence In e als. The yellow line ep esen s ln ∑PCBs equi alen o 20.0 mg/kg lipid and he
ed line 40 mg/kg lipid. (B) Ln ∑PCBs (sum 18–25CB) lipid concen a ions in biopsied s iped dolphin blubbe
om he Medi e anean Sea agains da e o all da a o 1990–2009 (n = 220). Figu e shows he na u al logs
(ln) o he whole da a se plo ed agains he da e ound. The con inuous line ep esen s he smoo hed end
om a Gene alized Addi i e Model i ed o he da a. The end is s a is ically signi ican (p < 0.001, F = 55.45,
esidual d = 212.03, end d = 6.97) agains he null hypo hesis o no end. The dashed lines ep esen he 95%
boo s apped Con idence In e als. The yellow line ep esen s ln ∑PCBs equi alen o 20.0 mg/kg lipid and he
ed line 40 mg/kg lipid.
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
analysis included s a is ical e alua ion o long- e m empo al ends in ∑PCB concen a ions in UK-s anded HPs
(1990–2012) and Medi e anean SDs (1990–2009). We compa ed mean ∑PCB concen a ions in all ou species
wi h a ange o es ablished PCB oxici y h esholds o ma ine mammals5–7. The lowes PCB oxici y h eshold
was a widely used and ela i ely low PCB oxici y h eshold o onse o physiological impac s and equi alen o
9 mg/kg lipid as ∑PCB
6
in his s udy. We also used he e y highes PCB oxici y h eshold epo ed o ma ine
mammals, o p o ound ep oduc i e impai men in inged seals (Phoca hispida) in he Bal ic Sea, and equi alen
o 41mg/kg lipid as ∑PCB in his s udy6.
We compa ed mean PCBs concen a ions in UK-s anded HPs ha we e “heal hy” and died o acu e phys-
ical auma (n = 345) (con ol g oup) wi h mean PCBs concen a ions in HPs ha died o in ec ious diseases
(n = 252) (case g oup) o s a a ion (n = 42). Whe e da a pe mi ed, sex di e ences in mean PCB concen a ions
we e in es iga ed o assess ma e nal o loading o PCBs ia lac a ion. Finally, we e iewed he cu en popula ion
and ep oduc i e s a us o he ex an odon oce e popula ions in Eu opean wa e s using sys ema ic local and
in e na ional obse a ional su ey and o he da a collec ed o e he pas 15–20 yea s (e.g. In e na ional Union o
Conse a ion o Na u e assessmen s)8.
Resul s
Spa ial and empo al ends and sex di e ences in ∑PCB exposu e. The empo al end in ln
∑PCB lipid concen a ions in UK HPs (1990–2012) and SDs om he wes e n Medi e anean Sea (1990–2009)
is shown in Fig.1A,B. The empo al end in bo h popula ions was highly s a is ically signi ican (p < 0.001).
In UK-s anded HPs, ln ∑PCB concen a ions declined slowly om 1990 o 1998 and hen emained ela i ely
s able om 1998 o 2012 agains he null hypo hesis o no end (p < 0.001, F = 11.76, esidual d = 701.97, end
d = 3.03) (Fig.1A). In Medi e anean SDs, ln ∑PCB concen a ions showed a ma ked decline om an ini ial peak
in 1990, bu hen s abilized om 2003 o 2008, bu wi h blubbe ∑PCB concen a ions s ill consis en ly exceeding
all mammalian oxici y h esholds. The end is s a is ically signi ican (p < 0.001, F = 55.45, esidual d = 212.03,
end d = 6.97) agains he null hypo hesis o no end (Fig.1B).
Some geog aphical egions in his s udy we e global PCB “ho spo s” o ce aceans. Mean ∑PCB lipid concen-
a ions in BNDs and KWs om he NE A lan ic and in BNDs and SDs om he Medi e anean we e among
he highes eco ded in ce aceans globally9, wi h males and emales ma kedly exceeding all known PCB oxici y
h esholds o ma ine mammals (Figs2–5). Resul s o ke nel smoo hing es ima es show e y high isk o PCB
oxici y o KWs in NE A lan ic, BNDs o SW Ibe ia and in he no he n Ad ia ic Sea and BNDs/SDs in he wes e n
Figu e 2. Mean ∑PCBs concen a ions in male and emale ce aceans ( ou species; all ages) The blue ba s
a e males and he g ey ba s a e emales. The lowe line is he equi alen ∑PCBs concen a ions h eshold
(9.0 mg/kg lipid) o onse o physiological e ec s in expe imen al ma ine mammal s udies6. The uppe line
is he equi alen ∑PCBs concen a ions h eshold (41.0 mg/kg lipid) o he highes PCB oxici y h eshold
published o ma ine mammals based on ma ked ep oduc i e impai men in inged seals in he Bal ic Sea6.
Mean ∑PCBs concen a ions in male (n = 388) and emale (n = 318) UK-s anded ha bou po poises (HPs)
in 1990–2012. Mean blubbe ∑PCBs (mg/kg lipid) concen a ions in subse s o male (n = 201) and emale
(n = 144) UK-s anded HPs ha died o acu e physical auma and male (n = 120) and emale (n = 132)
HPs ha died o in ec ious disease om he same 1990–2012 pe iod. Mean blubbe ∑PCBs (mg/kg lipid)
concen a ions (1990–2012) shown o s anded/biopsied male (n = 29) and emale (n = 17) bo lenose
dolphins (BNDs) om UK and I eland; male (n = 28) and emale (n = 24) BNDs om A lan ic coas o Spain
and Po ugal and male (n = 9) and emale (n = 11) BNDs om wes e n Medi e anean Sea. Male (n = 50) and
emale (n = 39) s iped dolphins om wes e n Medi e anean Sea (1991–2009) and male (n = 5) and emale
(n = 19) KWs om NE A lan ic (1994–2012). E o ba s = 1S anda d E o o he Mean (SEM).
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
Medi e anean (Fig.6). ∑PCB da a om biopsies o 152 ee-li ing indi iduals cons i u ed 38/131 (29.0%) o all
BNDs; 99/220 (45.0%) o he SDs; and 15/24 (62.5%) o he KWs in his s udy. All HPs in he UK we e s anded.
Al hough biases can po en ially occu wi h oppo unis ically sampled s anded ce aceans, he s udy popula ion
used he e consis ed o bo h comp omised diseased indi iduals as well as heal hy auma cases, and no clea di -
e ences be ween mean ∑PCB concen a ions in s anded and biopsied BNDs (1990–2012), SDs (1991–2009) and
KWs (1994–2012) we e obse ed (Fig.7). Mo e speci ically, mean ∑PCB concen a ions in s anded male and
emale SDs we e sligh ly highe han biopsied male and emale SDs bu biopsied male BNDs had sligh ly highe
∑PCB concen a ions han s anded male BNDs. Fo KWs, biopsied males and s anded emales had highe ∑PCB
concen a ions han s anded male and biopsied emale KWs, espec i ely (Fig.7). Box and whiske plo s (male
emale) we e gene a ed o ∑PCB and ln ∑PCB concen a ions in all s anded and biopsied HPs (1990–2012),
BNDs (1990–2012), SDs (1990–2008) and KWs (1994–2012) (Fig.8A–D).
We compa ed ∑PCB concen a ions among egions wi hin he NE A lan ic and Medi e anean Sea. Since ou
∑PCB da a is logno mal, we a e able o use he sample geome ic mean o es ima e he popula ion median (Tables1
and 2), and ha his es ima o is unbiased o doing his
10
. Mean ∑PCB concen a ions and geome ic means (wi h
uppe and lowe 95% con idence in e als) we e gene a ed o males and emales o each ce acean species and
egion o all a ailable da a (n = 1,009) (Table1) and o adul s only (n = 401) (Table2). These abula ed da a we e
p esen ed along wi h minimum and maximum alues (i.e. ange) o males and emales o each species and egion
(Tables1 and 2). In gene al, he ∑PCB sample geome ic means (as es ima o o popula ion median alues) we e
25–65% lowe han he (a i hme ic) means o he same species, bu s ill exceeded e en he e y highes ma ine
mammal PCB oxici y h eshold (∑PCB = 41 mg/kg lipid) o some BND, SD and KW g oups in bo h NE A lan ic
and Medi e anean Sea egions (Tables1 and 2).
Fo males and emales (all ages), high mean ∑PCB concen a ions (> 100.0g/kg lw) we e ound o BNDs
o Ibe ian Peninsula (NE A lan ic), wes e n Medi e anean and no he n Ad ia ic Sea; o SDs in wes e n
Medi e anean and o KWs (NE A lan ic) (Fig.2). Among adul s, high indi idual emale ∑PCB concen a ions
(> 100mg/kg lw) we e ound in KWs om all NE A lan ic egions, in BNDs om England and Wales, and in SDs
om he wes e n Medi e anean Sea (Table2). Mean ∑PCB concen a ions in adul emale KWs (176.8 mg/kg lipid)
in he NE A lan ic g ea ly exceeded mean concen a ions in adul emale sou he n esiden (55.4 mg/kg lipid) and
ansien (58.8 mg/kg lipid) KWs11 o B i ish Columbia (NE Paci ic). Adul emale KWs in he UK and I eland had
he highes mean ∑PCB concen a ions (224.8 mg/kg lipid) ollowed by KWs in he S ai o Gib al a (215.4 mg/
kg lipid). Mean ∑PCB concen a ions in adul emale BNDs (61.8–158.3 mg/kg lipid) and SDs (84.5–523.7 mg/kg
lipid) in some wes e n Eu opean popula ions also ma kedly exceeded hose in sou he n esiden and ansien
KWs o B i ish Columbia11 (Fig.3)(Table2). Mean ∑PCB concen a ions g ea ly exceeded all ma ine mammal
Figu e 3. Mean ∑PCBs concen a ions in male and emale ce aceans ( ou species; adul s only). The blue
ba s a e adul males and he g ey ba s a e adul emales. The lowe line is he equi alen ∑PCBs concen a ions
h eshold (9.0 mg/kg lipid) o onse o physiological e ec s in expe imen al ma ine mammal s udies6. The
uppe line is he equi alen ∑PCBs concen a ions h eshold (41.0 mg/kg lipid) o he highes PCB oxici y
h eshold published o ma ine mammals based on ma ked ep oduc i e impai men in inged seals in he
Bal ic Sea6. Mean ∑PCBs concen a ions (mg/kg lipid) in adul male (n = 146) and emale (n = 134) UK-
s anded ha bou po poises in 1990–2012. Mean blubbe ∑PCBs (mg/kg lipid) concen a ions (1990–2012)
shown o s anded/biopsied adul male (n = 20) and emale (n = 14) bo lenose dolphins om UK and I eland
and he A lan ic coas o Spain and Po ugal (NE A lan ic). Mean blubbe ∑PCBs (mg/kg lipid) concen a ions
shown o adul male (n = 8) and emale (n = 14) s iped dolphins om he wes e n Medi e anean Sea (1991–
2009). Finally, mean blubbe ∑PCBs (mg/kg lipid) concen a ions shown o adul male (n = 3) and emale
(n = 18) kille whales om he NE A lan ic (1994–2012). E o ba s = 1SEM.
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
PCB oxici y h esholds in ma u e (Fig.3) and imma u e (Fig.4) BNDs, SDs and KWs. Indi iduals o which he
ma u i y s a us could no be es ablished, mean ∑PCB concen a ions s ill exceeded all ma ine mammal oxici y
h esholds in BNDs and SDs (Fig.5).
The oxicological da a show ha hese popula ions g ea ly exceed concen a ions a which se e e oxic e ec s
a e known o occu . Pa hological indings on nec opsy consis en wi h immunosupp ession and inc eased sus-
cep ibili y o disease included mac o-pa asi ic and bac e ial pneumonias, high lung and gas ic mac o-pa asi e
bu dens, and gene alised bac e ial in ec ions (sep icaemias). These we e egula ly ound on nec opsy in s anded
HPs5, BNDs and KWs. In Medi e anean SDs dis empe due o ce acean mo billi i us (CeMV) in ec ion9 was
equen ly seen. Se e al s anded KWs also had mul iple den al in ec ions leading o la ge mandibula abscesses
iden i ied on nec opsy
12
. High ∑PCB con amina ion can cause immunosupp ession
7
and may be a signi ican
con ibu ing ac o in he dea h o many o he s anded indi iduals ha had a al in ec ious diseases on nec opsy.
Fo nec opsied ce aceans s anded in he UK (1990–2012), ∑PCB da a was ob ained o 706 HPs, 38 BNDs and
7 KWs (Tables1 and 2). Fo BNDs (UK), causes o dea h included auma (n = 5 male; n = 2 emale); in ec ious
disease (n = 2 male; n = 4 emale). Fo he UK-s anded KWs, causes o dea h included s a a ion (n = 2), in ec-
ious disease (n = 2) and li e s anding (n = 2). A cause o dea h could no be de e mined o 25 HPs, 11 BNDs and
1 KWs. ∑PCB lipid concen a ion in UK-s anded male HPs o all ages om 1990–2012 was signi ican ly highe
(sample mean = 19.4 mg/kg lw; sample median = 11.5 mg/kg lw; n = 388) han o emales o all ages (sample
mean = 13.8 mg/kg lw; sample median 8.35 mg/kg lw; n = 318) (ANOVA, P < 0.001) (Fig.2).
∑PCB lipid concen a ions in subg oups o “heal hy” male UK-s anded HPs ha we e gene ally in good
nu i i e condi ion and died o acu e physical auma (sample mean = 13.8 mg/kg lw; sample median = 9.57 lw ;
n = 201) had signi ican ly lowe ∑PCB han male HPs ha we e in poo e condi ion and died o a ange o in ec ious
diseases (sample mean = 26.5 mg/kg lw; sample median = 18.9 mg/kg lw; n = 120) (ANOVA, P < 0.001). In emale
UK-s anded HPs ha died o acu e physical auma, ∑PCB lipid concen a ions (sample mean = 8.50 mg/kg lw;
sample median = 6.41 mg/kg lw; n = 144) we e signi ican ly lowe han emale HPs ha died due o a ange o
in ec ious diseases (sample mean = 16.8 mg/kg lw; sample median = 12.2 mg/kg lw; n = 132) om he same pe iod
(ANOVA, P < 0.001) (Fig.2). Male and emale HPs ha died o s a a ion we e all in a poo o emacia ed condi ion.
Bo h male HP s a a ion cases (sample mean = 20.7 mg/kg lw; sample median = 12.5 mg/kg lw; n = 26) and emale
HP s a a ion cases (sample mean = 27.9 mg/kg lipid; sample median = 9.74 mg/kg lw; n = 16) had highe ∑PCB
concen a ions han he physical auma g oup. Fo UK-s anded HPs (bo h sexes), mean ∑PCB mg/kg lipid was
150–328% g ea e in in ec ious disease o s a a ion cases as compa ed o auma cases. The inc ease in ∑PCB on
a sample median basis was 130–198% g ea e o HP disease o s a a ion cases as compa ed o HP auma cases.
Figu e 4. Mean ∑PCBs concen a ions in male and emale ce aceans ( ou species; ju eniles only). The
blue ba s a e ju enile males and he g ey ba s a e ju enile emales. The lowe line is he equi alen ∑PCBs
concen a ions h eshold (9.0 mg/kg lipid) o onse o physiological e ec s in expe imen al ma ine mammal
s udies6. The uppe line is he equi alen ∑PCBs concen a ions h eshold (41.0 mg/kg lipid) o he highes PCB
oxici y h eshold published o ma ine mammals based on ma ked ep oduc i e impai men in inged seals
in he Bal ic Sea6. Mean ∑PCBs concen a ions (mg/kg lipid) in ju enile male (n = 233) and emale (n = 180)
UK-s anded ha bou po poises (HPs) in 1990–2012. Mean blubbe ∑PCBs (mg/kg lipid) concen a ions
(1990–2012) shown o s anded/biopsied ju enile male (n = 20) and emale (n = 14) bo lenose dolphins
om UK and I eland and he A lan ic coas o Spain and Po ugal (NE A lan ic). Mean blubbe ∑PCBs (mg/
kg lipid) concen a ions shown o ju enile male (n = 17) and emale (n = 15) s iped dolphins om wes e n
Medi e anean Sea (1991–2009). Finally, mean blubbe ∑PCBs (mg/kg lipid) concen a ions shown o ju enile
male (n = 2) and emale (n = 0) kille whales om NE A lan ic (1994–2012). E o ba s = 1SEM.

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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
Popula ion Dynamics. Such sus ained and ele a ed PCB bu dens a e likely o ha e signi ican e ec s a
he popula ion le el in Eu opean BNDs, SDs and KWs. Al hough we canno di ec ly and causally link high
∑PCB exposu es o ce acean popula ion declines, many o hese popula ions a e ei he e y small, o show
e idence o majo and long- e m declines o a signi ican con ac ion o ange. Only e y small KW popula-
ions a e now ound in indus ialised egions o Eu ope13–15. The e is only one esiden popula ion in sou he n
Eu ope14: a una- eeding KW subpopula ion in he s ai o Gib al a comp ising wo pods o alling 36 indi id-
uals13. These animals ha e been moni o ed e e y yea since 1999. Only six ma u e emales we e epo ed o ha e
cal ed be ween 1999 and 2011 and hese p oduced only i e cal es li ing mo e han 1 yea . This 6.4% annual
emale ecundi y a e o e a 13-yea pe iod is one o he lowes eco ded ep oduc i e a es o KWs globally
and he subpopula ion was ecommended o lis ing as “C i ically Endange ed” due o small popula ion size14.
A ound NW Sco land and Wes e n I eland, a small g oup o only nine KWs is egula ly seen15. This g oup o
ma ine-mammal-ea ing KWs comp ises ou adul males, wo adul emales and h ee adul emale o sub-adul
males. Al hough s udied o e a 19-yea pe iod, no cal es ha e e e been epo ed wi hin his g oup15. No o he
esiden o coas al KW g oups a e ound o he Ibe ian Peninsula o in he Bay o Biscay, al hough occasional o -
sho e KW sigh ings occu (e.g.
16). Long- e m ce acean s anding eco ds in he Ne he lands show ha KWs we e
i s eco ded on he Du ch No h Sea coas line in 1783, obse ed egula ly om 1918 o 1963 and comple ely
ceased he ea e un il wo single KW s andings in 2009 and 201017.
His o ic s andings da a sugges ha mul iple BND esiden o coas al g oups in Eu ope became deple ed
o locally ex inc in he la e-1960s o mid-1970s, including hose in he UK (e.g. Mo ecambe Bay; Eas coas o
England)
18
and he No h Sea Du ch coas
19
. The las membe o a esiden BND popula ion a A cachon, F ance,
died in 2003
20
and he small esiden BND g oup (cu en census n = 27) in he Sado Es ua y, Po ugal, showed
decline due o low cal su i al o e se e al decades21. Blubbe PCB le els o wo emales and one male BND
(sampled be ween 1995 and 1997) om his popula ion anged om 37.1 o 114.0 mg/kg lw. The Medi e anean
Sea emains a global PCB ho spo
1
whe e mos o he ex an ma ine mammal species, including SDs, BNDs and
sho -beaked common dolphins (CDs)(Delphinus delphis) ha e declined o e decades
14,22
. The cu en IUCN
Red Lis conse a ion s a us o BNDs and SDs in he Medi e anean Sea is “Vulne able”. The Medi e anean CD
subpopula ion is now classi ied as “Endange ed” a e expe iencing majo and gene alized decline o e he las
40–50 yea s, pa icula ly in he no he n Ad ia ic Sea and in he eas e n Ionian Sea
8
. Blubbe PCB concen a ions
a e signi ican ly highe in CDs and SDs in he Medi e anean Sea compa ed o he much mo e abundan NE
A lan ic popula ions23.
Fo HPs in he NE A lan ic, a single con inuous popula ion anges om F ance o no he n No way. A sepa a e
much smalle Ibe ian popula ion is es ima ed o comp ise only 4,398 (CV = 0.92) po poises
24
. In he Bal ic Sea, wo
Figu e 5. Mean ∑PCBs concen a ions in male and emale ce aceans ( h ee species; sexual ma u i y
unknown). The blue ba s a e males and he g ey ba s a e emales. The lowe line is he equi alen ∑PCBs
concen a ions h eshold (9.0 mg/kg lipid) o onse o physiological e ec s in expe imen al ma ine mammal
s udies6. The uppe line is he equi alen ∑PCBs concen a ions h eshold (41.0 mg/kg lipid) o he highes
PCB oxici y h eshold published o ma ine mammals based on ma ked ep oduc i e impai men in inged
seals in he Bal ic Sea6. Mean ∑PCBs concen a ions (mg/kg lipid) in male (n = 9) and emale (n = 4) UK-
s anded ha bou po poises o unknown sexual ma u i y (1990–2012). Mean blubbe ∑PCBs (mg/kg lipid)
concen a ions (1990–2012) shown o s anded/biopsied male (n = 16) and emale (n = 13) bo lenose
dolphins (BNDs) om he A lan ic coas o Spain and Po ugal and male (n = 8) and emale (n = 11) BNDs
om he wes e n Medi e anean Sea (all sexual ma u i y unknown). Mean blubbe ∑PCBs (mg/kg lipid)
concen a ions shown o male (n = 25) and emale (n = 10) s iped dolphins om wes e n Medi e anean Sea
(1991–2009) (sexual ma u i y unknown). E o ba s = 1SEM.
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
sepa a e HP subpopula ions exis : one in he wes e n wa e s (Ka ega , he Bel Seas) es ima ed a 40,475 indi id-
uals (CV = 0.235) and lis ed as “Vulne able” (by HELCOM)25, and ano he in he Bal ic Sea p ope , which is now
e y small and has su e ed decades o decline and is lis ed as “C i ically Endange ed”
8
. A his o y o hun ing, high
ALL AGES MALE FEMALE
Species Mean Median Geomean Lowe CI Uppe CI Min Max Mean Median Geomean Lowe CI Uppe CI Min Max
ALL UK Ha bou po poise
(HP) 19.41 11.51 12.35 11.21 13.62 0.44 150.47 13.49 8.36 8.01 7.15 8.96 0.40 159.68
HP-Wales 22.50 16.28 14.98 12.35 18.17 0.44 150.47 12.89 8.89 8.79 7.31 10.56 1.44 86.99
HP-England 23.52 14.97 15.97 13.97 18.24 2.09 108.36 17.98 11.00 10.07 8.26 12.28 0.40 159.68
HP-Sco land 11.46 7.53 7.52 6.38 8.86 0.99 69.99 9.43 4.74 5.81 4.84 6.98 0.66 61.44
HP- Isle o Man 20.14 20.14 20.14 NA NA 20.14 20.14 33.46 33.46 33.46 NA NA 33.46 33.46
UK - Kille whale (KW) 107.77 107.77 67.33 8.64 524.58 23.62 191.91 241.98 110.46 126.68 42.98 373.34 33.41 819.81
KW-I eland NA NA NA NA NA NA NA 138.90 138.90 138.90 NA NA 138.90 138.90
KW-Cana y Islands 180.18 180.18 180.18 NA NA 180.18 180.18 108.13 91.95 88.87 52.80 149.58 27.53 247.16
KW-S ai o Gib al a 243.43 243.43 232.55 128.01 422.47 171.49 315.36 186.74 50.13 82.11 32.27 208.94 43.27 857.92
ALL UK Bo lenose dolphin
(BND) 96.74 51.86 47.62 29.90 75.85 1.76 697.99 69.54 19.12 26.09 12.84 53.05 1.52 358.48
BND-England 176.94 119.54 96.60 25.43 366.95 22.13 446.55 91.17 40.61 31.26 7.93 123.24 4.11 358.48
BND-Sco land 96.61 51.86 41.59 20.23 85.49 1.76 697.99 46.13 25.40 30.14 13.31 68.21 8.53 125.08
BND-Wales 91.81 91.82 58.70 15.55 221.66 8.15 175.44 111.91 19.12 37.68 4.62 307.64 9.10 307.50
BND-I eland 46.87 41.49 36.26 18.66 70.46 12.99 95.10 11.37 11.37 5.68 0.43 75.21 1.52 21.22
BND-Po ugal 85.73 110.96 66.76 36.17 123.24 19.38 164.70 88.45 56.94 67.96 34.73 133.01 35.01 226.78
BND-Slo enia 126.83 79.58 103.79 57.53 187.26 58.00 293.23 28.64 28.64 28.64 NA NA 28.64 28.64
BND-NW Spain 118.92 91.46 40.24 7.33 220.87 5.08 382.20 34.70 26.23 22.96 9.77 53.93 5.41 81.99
BND-Gul o Cadiz 247.34 234.56 219.34 161.02 298.79 98.45 445.26 149.98 141.49 62.49 21.55 181.20 3.69 426.38
BND-S ai o Gib al a 324.01 233.56 153.31 39.39 596.75 28.30 879.33 123.11 168.85 85.71 21.34 344.30 20.75 179.72
BND-Wes e n Medi e anean 182.70 141.08 142.58 83.08 244.68 27.40 398.96 193.23 167.45 144.94 89.58 234.52 45.29 601.39
S iped dolphin (SD) -Wes e n
Medi e anean 482.15 150.43 216.91 163.78 287.28 16.80 2668.64 312.29 167.15 147.27 106.47 203.72 5.09 1518.64
Table 1. ∑PCBs exposu e (mean; sample median; geome ic mean wi h uppe and lowe 95% CI; ange)
(mg/kg lipid) by species, egion and sex (all ages).
ADULTS ONLY MALE FEMALE
Species Mean Median Geomean Lowe CI Uppe CI Min Max Mean Median Geomean Lowe CI Uppe CI Min Max
ALL UK Ha bou po poise
(HP) 27.83 18.57 18.96 16.25 22.12 0.44 150.47 12.58 5.22 6.32 5.19 7.69 0.40 138.83
HP-Wales 39.85 36.46 29.19 20.49 41.57 0.44 150.47 8.97 5.12 6.07 4.51 8.17 1.44 42.16
HP-England 34.28 31.13 25.84 20.92 31.92 2.09 95.59 18.73 8.66 8.03 5.47 11.80 0.40 138.83
HP-Sco land 14.73 10.62 10.94 8.94 13.38 2.40 69.99 10.34 4.70 5.43 4.01 7.36 0.66 61.44
KW-UK 107.77 107.77 67.33 8.64 524.58 23.62 191.91 241.98 110.46 126.68 42.98 373.34 33.41 819.81
KW-I eland NA NA NA NA NA NA NA 138.90 138.90 138.90 NA NA 138.90 138.90
KW-Cana y Islands 180.18 180.18 180.18 NA NA 180.18 180.18 108.13 91.95 88.87 52.80 149.58 27.53 247.16
KW-S ai o Gib al a NA NA NA NA NA NA NA 215.43 51.39 93.34 31.01 280.88 43.65 857.92
ALL UK Bo lenose dolphin
(BND) 140.42 75.64 79.03 45.77 136.46 12.99 697.99 86.88 21.22 27.07 9.65 75.97 1.52 358.48
BND-England 446.55 446.55 446.55 NA NA 446.55 446.55 110.12 38.95 30.35 4.11 223.88 4.11 358.48
BND-Sco land 171.88 80.31 107.36 54.85 210.16 42.44 697.99 58.63 32.34 42.11 13.84 128.17 18.46 125.08
BND-Wales 175.44 175.44 175.44 NA NA 175.44 175.44 158.30 158.30 52.90 1.68 1665.98 9.10 307.50
BND-I eland 46.87 41.49 36.26 18.66 70.46 12.99 95.10 11.37 11.37 5.68 0.43 75.21 1.52 21.22
BND-Po ugal 103.54 110.96 86.13 34.62 214.27 34.96 164.70 61.77 61.77 56.63 24.73 129.67 37.11 86.42
BND-Slo enia 126.83 79.58 103.79 57.53 187.26 58.00 293.23 28.64 28.64 28.64 NA NA 28.64 28.64
BND-NW Spain 236.83 236.83 186.97 46.04 759.28 91.46 382.20 5.41 5.41 5.41 NA NA 5.41 5.41
BND-Wes e n Medi e anean 141.08 141.08 141.08 NA NA 141.08 141.08 NA NA NA NA NA NA NA
S iped dolphin (SD) -Wes e n
Medi e anean 968.55 824.91 616.89 400.47 950.26 67.59 2668.64 336.69 227.56 144.69 84.38 248.08 5.09 1518.64
Table 2. ∑PCB exposu e (mean; sample median; geome ic mean wi h uppe and lowe 95% CI ange)
(mg/kg lipid) by species and egion (sexually ma u es only).
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
chemical pollu an exposu e and acciden al en apmen in comme cial ishing gea (byca ch) a e hough o ha e
been esponsible o his decline24. A o al o 375,358 (95% CI = 256,304–549,713) po poises was es ima ed o EU
A lan ic con inen al shel wa e s including he Ibe ian and wes e n Bal ic (sub-)popula ions (July 2005)16. Fo he
NE A lan ic (UK) HP popula ion, a longe cal ing in e al, lowe p egnancy a e and la e ma u a ion and highe
a es o ep oduc i e abno mali ies we e also ecen ly iden i ied in a nec opsy s udy o 329 emale UK-s anded
HPs (1990–2012), as compa ed o HP popula ions in much less PCB-pollu ed egions like Iceland and he Gul o
Maine/Bay o Fundy (NW A lan ic)
26
. Di ec obse a ions o ep oduc i e ailu e ( oe al dea h, abo ion, dys ocia
o s illbi h) we e obse ed in 25/127 (19.7%) o nec opsied ma u e emale HPs in he same s udy26.
Conside a ion o al e na i e causes o mo ali y. Acciden al en apmen in comme cial ishing gea
(byca ch) is o en conside ed o be he g ea es conse a ion h ea globally o small ce aceans8,27. In UK s and-
ings and nec opsy da a (1990–2013 inclusi e) byca ch was diagnosed as he cause o dea h o 296/615 (48.1%)
o UK-s anded common dolphins (Delphinus delphis) (CDs) and 338/1983 (17.0%) o HPs. In con as , only
9/130 (6.9%) UK-s anded SDs; 4/71 (5.6%) BNDs and 0/7 (0.0%) KWs we e diagnosed as byca ch du ing he
same pe iod. Byca ches eco ded unde he 2013 UK dedica ed byca ch sampling p og amme included 101
days on pelagic awls and 346 days on s a ic gea essels and included obse ed byca ches o 18 HPs, 11 CDs,
wo SDs and a single BND. Six common dolphins we e eco ded in pelagic awls. All o he ce acean byca ches
we e eco ded om s a ic ne ishe ies. P elimina y byca ch es ima es o he en i e UK lee du ing 2013 om
Figu e 6. (A–D) Dis ibu ion map (smoo h mean densi y ke nel plo s) o ∑PCBs da a poin s in Eu ope – all
ce acean species (all ages) om 1996–2012. (A) – HPs (n = 548); (B) – BNDs (n = 110); (C) – SDs (n = 71) and
(D) – KWs (n = 21). Spa ial dis ibu ion o ∑PCB lipid concen a ions p oduced in Es i A cMap 10.1 (www.es i.
com). Maps a e displayed in he WGS84 co-o dina e sys em. Da a poin s a e shown along wi h local a e ages.
These a e ages we e calcula ed by ke nel smoo hing using a polynomial o de 5 ke nel wi h powe = 0, idge
pa ame e = 50 and bandwid h based on he spa ial dis ibu ion o he obse a ions o each species: bo lenose
dolphin 0.75 deg ees; ha bou po poise 0.5 deg ees; kille whale 1.2 deg ees; s iped dolphin 0.5 deg ees. Bo h
he da a poin s and he local a e ages a e displayed in h ee colou s: yellow (∑PCB concen a ion = < 20 mg/
kg); o ange (∑PCB concen a ion = 20–40 mg/kg lw); and ed (∑PCB concen a ion = > 40 mg/kg lw).
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
sys ema ic obse e -based s udies p o ided es ima es o HP byca ch o a ound 1917 animals assuming no pinge s
(acous ic byca ch de e en de ices) we e used (CV = 0.126) and 1652 animals i all UK boa s o e 12 m used
pinge s co ec ly (unde EU egula ion 812)(CV = 0.147)28. O he es ima es o he en i e UK lee in 2013 indi-
ca e a ound 320 CDs and a ound 470 seals we e bycaugh 28. Byca ch o BNDs, howe e , was conside ed oo a e
o es ima e o he en i e UK lee and KW byca ch was no eco ded28. A byca ch obse e s udy o he I ish
albaco e una (Thunnus alalunga) d i -ne ishe y unde aken in o sho e wa e s o he NE A lan ic in he 1990s
ound he highes byca ch a es in CDs ollowed by SDs, wi h much lowe numbe s o bycaugh BNDs and no
KW byca ch29. The highes byca ch a es gene ally occu in he mos nume ically abundan species in he NE
A lan ic egion, HPs and CDs, bu wi h much lowe a es o byca ch in BNDs and byca ch un eco ded in KWs
in ecen yea s30. Ve y low numbe s o byca ches we e ound in he long- e m obse e -based s udies o he es-
iden Eu opean BND popula ions:- BNDs in Shannon es ua y, I eland (popula ion size = 107–140; ze o byca ch
eco ded since 1993)[S. Be ow, unpublished da a]; Sado es ua y, Po ugal (popula ion size = 27; ze o byca ch
eco ded om 1983–2013) (Manuel E. Dos San os, pe s. com.) and Slo enia, no he n Ad ia ic Sea (popula-
ion size es ima e = 74; 95% CI = 57–90; 2 cases o byca ch since 2002) [T. Geno , unpublished da a, see also31].
Collec i ely, hese nec opsy and ishe ies byca ch obse e s udies om app oxima ely 1990 onwa ds indica e ha
byca ch is unlikely o be d i ing popula ion declines o BNDs o KWs a ound he UK o in he wide NE A lan ic
du ing his pe iod.
O he po en ial causes o ce acean mo ali y include ship-s ike; acous ic dis u bance om high-in ensi y/
an h opogenic acous ic sou ces; nu i ional limi a ion caused by educed p ey a ailabili y (e.g. o e ishing o
clima e change); bio oxins (ha m ul algal blooms) and in ec ious disease (e.g. ce acean mo billi i us, CeMV)
32
.
Using CSIP UK s andings and nec opsy da a (1990–2013 inclusi e) ship-s ike was a ela i ely in equen cause
o dea h accoun ing o only 17/1983 (0.8%) s anded HPs; 0/130 (0.0%) SDs; 0/71 (0.0%) BNDs and 0/7 (0.0%)
KWs nec opsied in he UK. All es s o bio oxins in UK-s anded ce acean issues we e nega i e (o a ace le els)
since 199032,33.
The po en ial impac s o an h opogenic high-in ensi y acous ic sou ces on ce aceans include mass s and-
ing e en s (MSEs) ha ha e occu ed on a global basis, p edominan ly in ol ing beaked whales exposed o
mid- equency ac i e sona s in na al exe cises34–36. Non-beaked whale MSEs wi h a p obable acous ic cause ha e
occu ed, such as a 2008 CD MSE in he UK, bu a e e y a e in Eu opean wa e s
32
. No acous ically-induced MSEs
we e eco ded in HPs, SDs, BNDs o KWs in Eu opean wa e s. Acous ically-induced ce acean MSEs ha e been
eco ded in he Medi e anean Sea bu also p ima ily in ol ed beaked whales36,37.
In he Medi e anean and Black Seas, all ce acean species whe e popula ion assessmen s ha e occu ed a e
conside ed o be declining
8,14,22
. A ange o h ea s has been p oposed including hun ing (his o ically); byca ch;
o e ishing/p ey deple ion; habi a deg ada ion; mo billi i us in ec ion and chemical and acous ic pollu ion8,14,22.
Empi ical e idence o he e ec s o p ey deple ion (e.g. due o o e ishing o clima e change e ec s) leading o
nu i ional limi a ion is limi ed o ce aceans, bu die /nu i ion e ec s ha e been linked o ec ui men in KWs
and in whales (Balaenop e a physalus) [ e iewed in26]. Such p ocesses would po en ially inc ease PCB oxici y in
malnou ished animals by mobilising lipophilic PCBs om blubbe o o he body compa men s7,23. A ecen global
e iew o Ce acean Mo billi i us (CeMV) ound ha SDs ha e been nega i ely impac ed by CeMV epizoo ics
Figu e 7. Mean ∑PCB concen a ions in s anded and biopsied BNDs (1990–2012), SDs (1991–2009) and
KWs (1994–2012) – all ce acean species (all ages). The blue ba s a e males and he g ey ba s a e emales. The
lowe line is he equi alen ∑PCBs concen a ions h eshold (9.0 mg/kg lipid) o onse o physiological e ec s
in expe imen al ma ine mammal s udies6. The uppe line is he equi alen ∑PCBs concen a ions h eshold
(41.0 mg/kg lipid) o he highes PCB oxici y h eshold published o ma ine mammals based on ma ked
ep oduc i e impai men in inged seals in he Bal ic Sea6. E o ba s = 1SEM.
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16
Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
43.
K ahn, M. M. e al. Use o chemical ace s in assessing he die and o aging egions o eas e n No h Paci ic kille whales. Ma
En i on Res 63, 91–114 (2007).
44.
K ahn, M. M. e al. S a i ica ion o lipids, a y acids and o ganochlo ine con aminan s in blubbe o whi e whales and kille whales.
J Ce acean Res Manag 6:175–189 (2004).
45.
Balme , B. C. e al. Rela ionship be ween pe sis en o ganic pollu an s (POPs) and anging pa e ns in common bo lenose dolphins
(Tu siops unca us) om coas al Geo gia, USA. Sci. To . En i on. 409, 2094–2101. doi: 10.1016/j.sci o en .2011.01.052 (2011).
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on he use o ibu yl in in an i ouling pain s (1992–2005 & 2009). Ma . Poll. Bull. 64, 2576-2580. doi: 10.1016/j.ma polbul.2012.07.014
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Acknowledgemen s
The esea ch was conduc ed by he UK Ce acean S andings In es iga ion P og am (CSIP) and he Cen e o
En i onmen , Fishe ies and Aquacul u e Science (Ce as) unde con ac o he UK Depa men o En i onmen ,
Food and Ru al A ai s (De a) and he De ol ed Go e nmen s o Sco land and Wales. Addi ional unding o
oxicological analyses was p o ided by ASCOBANS unde con ac “SSFA2010-3” and by he Fundació Ba celona
Zoo. The Gul o Cádiz and S ai o Gib al a samples collec ion we e sponso ed by Lo o Pa que Founda ion,
Fundación Biodi e sidad, CEPSA and ECOCET P ojec (CGL2011-25543) and logis ical suppo o sample sexing
was p o ided by Labo a o io de Ecología Molecula , Es ación Biológica de Doñana, CSIC (LEM-EBD). Samples
om Galicia we e ob ained wi h he suppo o Di eccion Xe al de Conse acion da Na u eza-Xun a de Galicia,
co- inanced wi h Eu opean Regional De elopmen Funds (ERDF/FEDER). S. Mu phy was suppo ed by a Ma ie
Cu ie In e na ional Ou going Fellowship wi hin he Se en h Eu opean Communi y F amewo k P og amme. R. de
S ephanis and J. Giménez we e suppo ed by he Se e o Ochoa P og amme o Cen es o Excellence in R + D + I
(SEV-2012-0262). A. D. Foo e was suppo ed by a Lawski Founda ion s ipend.
Au ho Con ibu ions
P.D.J., R.D., À.A., A.B., S.M., J.B., A.B., J.B., S.B., N.D., R.E., M.F., T.G., J.G., J.L., Á.L., V.M., R.P., M.W.P., B.S., R.de.S.,
N.T., P.V. and A.F. assis ed wi h collec ion o blubbe samples and associa ed biological and o he da a. P.D.J., R.D.,
.J.L.B., À.A., A.B., S.M., J.B., A.B., M. D., D.L.M. and R.L.L. helped o analyse he da a. J.L.B., À.A., A.B., D.L.M.,
A.P. and R.J.L. conduc ed chemical analysis o blubbe samples. P.D.J., R.D., J.L.B., À.A., A.B., S.M., J.B., A.B., J.B.,
S.B., A.A.C., M. D., N.D., R.E., M.F., A.D.F., T.G., J.G., J.L., Á.L., V.M., D.L.M., A.P., R.P., M.W.P., B.S., R.deS., N.T.,
P.V., A.F. and R.J.L. helped wi h w i ing and edi ing inal manusc ip .
Addi ional In o ma ion
Supplemen a y in o ma ion accompanies his pape a h p://www.na u e.com/s ep
Compe ing inancial in e es s: The au ho s decla e no compe ing inancial in e es s.
How o ci e his a icle: Jepson, P. D. e al. PCB pollu ion con inues o impac popula ions o o cas and o he
dolphins in Eu opean wa e s. Sci. Rep. 6, 18573; doi: 10.1038/s ep18573 (2016).

www.na u e.com/scien i ic epo s/
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Scien i ic RepoR s | 6:18573 | DOI: 10.1038/s ep18573
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