RESEARCH ARTICLE
Cumula i e human impac s on global ma ine
auna highligh isk o biological and
unc ional di e si y
Casey C. O’Ha aID
1
*, Melanie F azie
1
, Mi eia ValleID
1,2,3
, Na halie Bu
4,5
,
K is in Kaschne
6
, Ca issa Klein
5
, Benjamin S. Halpe n
1,7
1Na ional Cen e o Ecological Analysis and Syn hesis, Uni e si y o Cali o nia, San a Ba ba a, San a
Ba ba a, Cali o nia, Uni ed S a es o Ame ica, 2AZTI, Ma ine Resea ch, Basque Resea ch and Technology
Alliance (BRTA), Suka ie a, Spain, 3Basque Cen e o Clima e Change (BC3), Scien i ic Campus o he
Uni e si y o he Basque Coun y (UPV-EHU), Leioa, Spain, 4The Na u e Conse ancy, Sou h B isbane,
Queensland, Aus alia, 5Cen e o Biodi e si y and Conse a ion Science, School o he En i onmen , The
Uni e si y o Queensland, B isbane, Queensland, Aus alia, 6Depa men o Biome y and En i onmen al
Sys em Analysis, Albe -Ludwigs-Uni e si y o F eibu g, F eibu g, Ge many, 7B en School o En i onmen al
Science & Managemen , Uni e si y o Cali o nia, San a Ba ba a, San a Ba ba a, Cali o nia, Uni ed S a es o
Ame ica
*[email p o ec ed]b.edu
Abs ac
An h opogenic s esso s o ma ine ecosys ems om clima e change and human ac i i ies
inc ease ex inc ion isk o species, dis up ecosys em in eg i y, and h ea en impo an eco-
sys em se ices. Add essing hese s esso s equi es unde s anding whe e and o wha
ex en hey a e impac ing ma ine biological and unc ional di e si y. We model cumula i e
isk o human impac upon 21,159 ma ine animal species by combining in o ma ion on spe-
cies-le el ulne abili y and spa ial exposu e o a ange o an h opogenic s esso s. We
apply his species-le el assessmen o human impac s o examine pa e ns o species-
s esso in e ac ions wi hin axonomic g oups. We hen spa ially map impac s ac oss he
global ocean, iden i ying loca ions whe e clima e-d i en impac s o e lap wi h ishing, ship-
ping, and land-based s esso s o help in o m conse a ion needs and oppo uni ies. Com-
pa ing species-le el modeled impac s o hose based on ma ine habi a s ha ep esen
impo an ma ine ecosys ems, we ind ha e en ela i ely un ouched habi a s may s ill be
home o species a ele a ed isk, and ha many species- ich coas al egions may be a
g ea e isk han indica ed om habi a -based me hods alone. Finally, we inco po a e a ai -
based me ic o unc ional di e si y o iden i y whe e impac s o unc ionally unique species
migh pose g ea e isk o communi y s uc u e and ecosys em in eg i y. These complemen-
a y lenses o species, unc ion, and habi a p o ide a iche unde s anding o h ea s o
ma ine biodi e si y o help in o m e o s o mee conse a ion a ge s and ensu e sus ain-
abili y o na u e’s con ibu ions o people.
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OPEN ACCESS
Ci a ion: O’Ha a CC, F azie M, Valle M, Bu N,
Kaschne K, Klein C, e al. (2024) Cumula i e
human impac s on global ma ine auna highligh
isk o biological and unc ional di e si y. PLoS
ONE 19(9): e0309788. h ps://doi.o g/10.1371/
jou nal.pone.0309788
Edi o : Abdul Azeez Pokka happada, Cen al Ma ine
Fishe ies Resea ch Ins i u e, INDIA
Recei ed: June 17, 2024
Accep ed: Augus 19, 2024
Published: Sep embe 18, 2024
Pee Re iew His o y: PLOS ecognizes he
bene i s o anspa ency in he pee e iew
p ocess; he e o e, we enable he publica ion o
all o he con en o pee e iew and au ho
esponses alongside inal, published a icles. The
edi o ial his o y o his a icle is a ailable he e:
h ps://doi.o g/10.1371/jou nal.pone.0309788
Copy igh : ©2024 O’Ha a e al. This is an open
access a icle dis ibu ed unde he e ms o he
C ea i e Commons A ibu ion License, which
pe mi s un es ic ed use, dis ibu ion, and
ep oduc ion in any medium, p o ided he o iginal
au ho and sou ce a e c edi ed.
Da a A ailabili y S a emen : All da a used as
inpu s o his assessmen a e eely a ailable om
o iginal sou ces. All o iginal code and da a
esul ing om his analysis has been deposi ed a
In oduc ion
An h opogenic s esso s om human ac i i ies on land and sea coupled wi h hose om
an h opogenic clima e change a e d i ing deg ada ion o coas al ecosys ems, ma ine egime
shi s, and inc eased ex inc ion isk o h ea ened species [1–6], h ea ening he biological and
unc ional di e si y ha unde pin ecosys em se ices upon which we depend [7–11]. The
Kunming-Mon eal Global Biodi e si y F amewo k [12] calls o u gen ac ion o educe
ex inc ion isk, imp o e ecosys em in eg i y, and ensu e sus ainabili y o na u e’s con ibu-
ions o people. To hese ends, unde s anding whe e and o wha deg ee an h opogenic s ess-
o s impose impac s on ma ine biological and unc ional di e si y will be c i ical o designing,
alloca ing, and moni o ing e ec i e conse a ion ac ions a scale [13].
To assess he isk o ad e se impac s on ma ine ecosys ems, cumula i e human impac
models ha e been de eloped o in eg a e in o ma ion on ulne abili y o elemen s o ecological
conce n (e.g., habi a s, species, unc ional g oups) and exposu e o hose elemen s o an h o-
pogenic s esso s [14]. Habi a -based es ima es o ecosys em ulne abili y o (e.g., [15]) and
impac om (e.g., [7,14,16]) a ious s esso s ely upon an unde s anding o undamen al
s uc u al and unc ional simila i y be ween, say, a Ca ibbean co al ee and an Indonesian
co al ee , o a Cali o nian kelp o es and a Namibian kelp o es ecosys em, hough he e
may be li le o e lap in he species ha inhabi each sys em. Such a habi a -based app oach
p o ides aluable insigh s on po en ial impac s o he gene al ophic s uc u e and unc ion-
ing o an ecosys em as well as he ypes o ecosys em se ices ha may be a ec ed, bu i may
miss impo an di e ences in ulne abili y s emming om he e ogenei y o species composi-
ion be ween o he wise simila ma ine communi ies.
A species-based app oach o es ima ing impac s may be be e able o cap u e he e ogenei y
o species’ ulne abili y o s esso s [3,17–19], p o iding insigh s on impac s o indi idual spe-
cies and communi y s uc u e. S udies assessing an h opogenic impac s on ma ine species
(e.g., [18,20–23]) gene ally ha e been limi ed in scope o a ew selec axa and/o s esso s,
la gely due o lack o a sys ema ic means o es ima ing species ulne abili y ac oss mul iple
axa and s esso s [19,24]. O’Ha a e al [3] pa sed h ea in o ma ion om IUCN Red Lis
assessmen s o es ima e sensi i i y and impac s om mul iple an h opogenic s esso s ac oss
mul iple ma ine axa globally o e an ele en-yea pe iod, bu ha s udy was necessa ily
es ic ed o hose species ca ego ized as h ea ened and nea - h ea ened, excluding he as
majo i y o ma ine species. Howe e , a ecen ly de eloped ai -based amewo k o es ima e
species ulne abili y b oadly ac oss axa and s esso s [19] g ea ly expands he se o ma ine
species a ailable o such cumula i e impac assessmen . Addi ionally, a species-based
app oach o es ima ing isk o impac , coupled wi h in o ma ion on ai s associa ed wi h eco-
logical unc ion, enables iden i ica ion o unc ionally unique species and g oups whose loss
may pose g ea e isk o ecosys em unc ioning and esilience han simila impac s on unc-
ionally edundan species [25–28].
He e we p o ide a axonomically-di e se spa ial analysis o cumula i e human impac s o
13 an h opogenic s esso s on 21,159 ma ine animal species and subpopula ions. Fo each spe-
cies/s esso combina ion, we in e sec he species’ ange wi h he spa ial dis ibu ion o he
s esso ; impac in each pixel is modeled as he p oduc o s esso in ensi y and he species’
es ima ed ulne abili y o ha s esso (See S1 Fig in S1 File. o concep ual o e iew o me h-
ods). We spa ially agg ega e species impac dis ibu ions o es ima e mean impac ac oss spe-
cies and axa, p o iding a axonomically de ailed unde s anding o how an h opogenic
p essu es impose isk o impac o ma ine biodi e si y. We hen compa e hese esul s o
cumula i e impac es ima es based on ep esen a i e habi a s o de e mine whe e and how
species- s. ecosys em-le el ulne abili y d i es po en ial impac . Finally, we use a se o ai s
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Figsha e. DOI: 10.6084/m9. igsha e.26454106. A
li ing e sion o he code and da a can be ound a
h ps://gi hub.com/mapping-ma ine-spp- uln/spp_
uln_mapping.
Funding: CK, BSH: Na ional Philan h opic T us
(h ps://www.np us .o g/), SB200099 CCO:
Na ional Science Founda ion ia Belmon Fo um
(h ps://belmon o um.o g/abou ), 2019902 No
unde s played any ole in s udy design, da a
collec ion, analysis, decision o publish, o
p epa a ion o he manusc ip .
Compe ing in e es s: The au ho s ha e decla ed
ha no compe ing in e es s exis .
o classi y species in o unc ional en i ies (sensu Mouillo e al. [26]) and use hese g oupings o
calcula e a weigh ed mean impac , emphasizing impac s o species who uniquely ep esen a
posi ion in unc ional ai space. The species, unc ional en i y, and habi a app oaches o es i-
ma ing cumula i e impac p o ide di e en bu syne gis ic lenses h ough which o es ima e
ou impac on ma ine ecosys ems: a eas o ag eemen be ween hese me hods ein o ce
u gency o conse a ion, while a eas o signi ican di e ence may p o ide conse a ion
insigh s by highligh ing impac s on ulne able and unc ionally impo an species in o he wise
esilien ma ine ecosys ems.
Me hods
Analysis g id
All spa ial analyses we e calcula ed on a g idded global map using a Mollweide equal-a ea p o-
jec ion coo dina e e e ence sys em (CRS), g idded o 10 km x 10 km esolu ion. See SI Me h-
ods in S1 File o addi ional de ails on p epa ing he analysis g id.
Species dis ibu ions
The 21,159 species (including subpopula ions) conside ed in his assessmen a e limi ed o
hose animal species wi h da a on spa ial dis ibu ion as well as su icien ai da a o es ima e
ulne abili y and assign species o unc ional en i ies. These species ep esen only a small sub-
se o he >240,000 ma ine species iden i ied in he Wo ld Regis e o Ma ine Species
(WoRMS, [29]); howe e , his subse includes mos known ma ine mammals, ma ine ep iles,
seabi ds, and ca ilaginous ishes, as well as abou hal o ma ine bony ishes and wa m-wa e
co als (S1 Table in S1 File by class, S2 Table in S1 File e eb a es by o de ). Toge he hese
species ep esen mos op p eda o s, many mid- ophic species, and ecologically c i ical habi-
a - o ming species. Rela i ely ewe o he in e eb a es we e included, as mos lacked spa ial
da a, ai da a, o bo h.
Species dis ibu ion da a we e aken om AquaMaps [30] (n = 18,480) and IUCN species
dis ibu ion maps [31,32] (n = 2,679). Fo species appea ing in bo h dis ibu ion map da ase s,
he AquaMaps dis ibu ion maps, based on anspa en and epea able algo i hms using pub-
licly a ailable da a, we e p e e ed o e IUCN ange maps, which in eg a e da a and expe
knowledge bu may include mapping decisions ha a e di icul o eplica e. Fo species ep e-
sen ed by he AquaMaps da ase , p esence was calcula ed as any 0.5˚ cell wi h a p obabili y o
occu ence o 0.5 o g ea e ; he esul ing cells we e hen ep ojec ed o he 10 km Mollweide
analysis g id. Fo species ep esen ed by IUCN Red Lis angemaps, he polygons we e ep o-
jec ed and as e ized o he esolu ion and CRS o he analysis g id. See SI Me hods in S1 File
o addi ional de ails on p epa ing species dis ibu ions. See S2 Fig in S1 File. o a map o spe-
cies ichness gene a ed om hese species dis ibu ions.
Vulne abili y es ima es
Vulne abili y weigh s, i.e., he ela i e e ec o a gi en s esso on he i ness/heal h o a gi en
species, we e de e mined based on me hods o Bu e al. [19]. B ie ly, ha s udy es ima ed ul-
ne abili y o species o each o a sui e o s esso s based on p esence o ce ain ai s ha a e
likely o inc ease he species’ physiological sensi i i y (e.g., calcium ex e nal s uc u es indica e
highe sensi i i y o ocean acidi ica ion), abili y o adap o o a oid ha speci ic s esso (e.g.,
high mobili y makes i easie o a oid localized s esso s), and li e his o y and popula ion-le el
ai s ha a ec he popula ion’s abili y o adap o o eco e om dis u bances in gene al
(e.g., high ecundi y sugges s easie eco e y om a dis u bance). A bina y exposu e mul iplie
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(ze o o one) p e en s nonsensical esul s o ce ain s esso s whe e exposu e is limi ed o ce -
ain dep hs o ocean zones, e.g., ship s ikes will no a ec mesopelagic species. T ai alues o
species we e ga he ed h ough expe elici a ion and p o ided as o dinal o nominal ca ego i-
cal alues. Vulne abili y weigh s ange om 0 (a s esso does no a ec a species) o 1 (a
s esso imposes ex eme ad e se e ec s on a species).
See SI Me hods in S1 File and S3 Table in S1 File o de ails on ai s and calcula ions.
S esso laye s o species- ocused analysis
Fo he species- ocused analysis, he in ensi y o exposu e o a s esso depends on he spa ial
dis ibu ion o he s esso ela i e o he spa ial dis ibu ion o he species. Spa ial da a o
s esso s is ypically a ailable as g idded da a o some physical quan i y ela ed o an h opo-
genic ac i i y, e.g., b igh ness o nigh ime ligh s, onnes o nu ien e ilize uno , popula-
ion densi y wi hin 25 km o coas , o alue o a agoni e sa u a ion s a e. Fo each s esso , a
e e ence alue was de e mined om he da a ( ypically 99.9 h pe cen ile o obse ed alues),
a his o ic baseline (e.g., mean/s anda d de ia ion o sea su ace empe a u e om 1985–2015),
o ecologically ele an alue (e.g., a agoni e sa u a ion s a e o 1) (S4 Table in S1 File). We cal-
cula ed s esso dis ibu ions as a alue om 0 (s esso no p esen ) o 1 (s esso a e e ence
poin , indica ing maximum in ensi y).
Fo mos o he included s esso s, a single map o ela i e s esso in ensi y was c ea ed
om g idded da a and applied o all species, al hough ulne abili y o he s esso a ied by
species. These s esso s include sea su ace empe a u e (SST) ex emes, ocean acidi ica ion,
ul a iole adia ion, sea le el ise, nu ien pollu ion ( uno ), di ec human dis u bance, ligh
pollu ion, shipping (ship s ikes), and habi a des uc ion d i en by deme sal des uc i e ish-
ing and he oo p in o ben hic s uc u es.
Howe e , he e we e also se e al s esso s o which in ensi y (again anging om 0 o 1)
depends on species-speci ic in o ma ion. These s esso s include byca ch (dependen on wa e
column posi ion, i.e., ben hic, pelagic, o bo h), biomass emo al (dependen on ca ch ha is
di ec ly a ge ing ha species), and inc ease in mean SST (dependen on species he mal ole -
ance). Fo hese s esso s, indi idual maps we e gene a ed o each species (biomass emo al,
SST ise) o o each wa e -column posi ion ca ego y (byca ch).
See SI Me hods in S1 File and S4 Table in S1 File o de ails on he da a sou ce, ans o ma-
ion, and e e ence poin used o hese s esso laye s.
S esso laye s o habi a - ocused analysis
The habi a - ocused analysis was simila o ha o species, wi h he in ensi y o exposu e o a
s esso depending on he spa ial dis ibu ion o he s esso ela i e o he dis ibu ion o he
habi a . Fo his app oach, ishe ies s esso s we e calcula ed using he same sou ce as he spe-
cies-le el s esso s, i.e., Wa son [33], bu agg ega ed by ishing gea , dep h, and scale acco ding
o hei e ec s on a ious habi a ypes as desc ibed in Halpe n e al. [7]: comme cial pelagic
and deme sal low byca ch, comme cial pelagic high byca ch, comme cial deme sal des uc i e,
and a isanal/small scale ishing. Fo SST ex emes, ocean acidi ica ion, ul a iole adia ion,
sea le el ise, nu ien pollu ion ( uno ), di ec human dis u bance, ligh pollu ion, shipping,
ben hic s uc u es, and deme sal des uc i e ishing, we used he iden ical s esso laye s p e-
pa ed o he species-le el analysis. The species-speci ic s ess o inc easing mean SST ela i e
o hei he mal ole ance was omi ed, as i would no be easible o de e mine an analogous
habi a -le el he mal ole ance. See SI Me hods in S1 File and S4 Table in S1 File o de ails on
he da a sou ce, ans o ma ion, and e e ence poin used o hese s esso laye s.
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Cumula i e human impac s: Species me hod
Es ima ing impac a species le el pe g id cell. We modeled he impac on species io
s esso j21:Jin a gi en loca ion (i.e., g id cell) as he p oduc o s esso in ensi y s
j
and ul-
ne abili y o ha species o ha s esso
ij
:
Ij
i¼ ijsj
Cumula i e impac on species iin a gi en loca ion was de e mined by summing impac s
ac oss all s esso s (o subse , e.g., clima e s. non-clima e s esso s) in ha loca ion:
Icml
i¼X
J
j¼1
ijsj
No e ha his addi i e model does no accoun o compound e ec s o mul iple s ess-
o s ac ing in combina ion, i.e., syne gis ic o an agonis ic e ec s. Me a-analyses examining
wo-s esso in e ac ions [34,35] ha e obse ed some non-addi i e s esso in e ac ions,
bu addi i e e ec s we e mo e commonly epo ed. Addi ionally, an addi i e model
equi es ewe assump ions, is concep ually ac able, and likely esul s in mo e conse a-
i e esul s.
Es ima ing species-le el mean cumula i e impac ac oss species ange. Fo each
species i, we calcula ed a cumula i e impac sco e Xaccoun ing o impac s ac oss i s en i e
ange as an a e age o pe -g id-cell impac s o all cells cin he species’ ange R
i
. Fo a single
s esso j:
Xj
i¼1
RiX
c2Ri
Ij
ic
Cumula i e impac sco es ac oss mul iple s esso s (clima e, non-clima e, and o al) we e
de e mined as he sum o single-s esso impac sco es.
Es ima ing impac ac oss species pe g id cell. The species-mean me hod o calcula ing
he impac sco e o s esso jin a gi en cell was de e mined by aking an unweigh ed mean
ac oss all Nspecies p esen (o a axonomic subse , e.g., all elasmob anchs):
Ij
spp ¼1
NX
N
i¼1
ijsj
and he cumula i e impac is he sum o impac s ac oss all (o a subse o ) s esso s wi hin ha
cell.
Cumula i e human impac s: Habi a me hod
To compa e he esul s o ou species-based cumula i e impac app oach o hose o a habi a -
based app oach (e.g., [14]; [7]), we ec ea ed habi a maps a he same esolu ion and p ojec-
ion as he species-based analysis, agg ega ing habi a p esence maps a ~1 km esolu ion o
de e mine p opo ional habi a ep esen a ion wi hin each 10 km g id cell. Using hese habi a
maps, we applied habi a ulne abili y weigh s om Halpe n e al. [7] o de e mine impac s
based on la gely he same s esso maps da a sou ces used o he species-based assessmen .
To iden i y ulne abili y o each habi a o a ious s esso s we used he ma ix o habi a
ulne abili y om Halpe n e al. [7].
Pe -g id-cell habi a impac sco es o each s esso jwe e c ea ed as he p oduc o habi a
ulne abili y o each habi a h21: Hand in ensi y o s esso j, a e aged o e he p opo ional
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inclusion o ha habi a p
h
in a gi en cell:
Ij
hab ¼X
H
h¼1
ph hj
Cumula i e impac pe pixel is he sum o habi a -based impac s ac oss all (o subse ) o
s esso s.
Cumula i e human impac s: Func ional en i y me hod
Func ional en i ies. To es ima e cumula i e impac on unc ional di e si y, we i s
assigned species o unc ional en i ies based on ca ego ical alues o ou ai s (maximum
body leng h, adul mobili y, posi ion in wa e column, and adul ophic le el) ha oughly
de e mine a species’ ecological niche wi h ega d o egula ion o ood webs and nu ien
cycling, ollowing Mouillo e al. [26]. Due o limi ed ai da a a ailable ac oss a b oad ange
o axa, we elied on a smalle se o ai s ( hose ou no ed p e iously) o assignmen o unc-
ional en i y han he six ai s used in Mouillo e al. [26], esul ing in ewe bu mo e popu-
lous unc ional en i ies and he e o e a mo e conse a i e es ima e o unc ional ulne abili y.
T ai alues we e gleaned om [19,36,37]; missing alues we e impu ed using Mul iple
Impu a ion by Chained Equa ion (MICE) in he R package mice [38] using all o he ai s plus
ecundi y (whe e a ailable), gene a ion ime (whe e a ailable), o de , and amily. See SI Me h-
ods in S1 File o de ails on he ai alues used o assign unc ional en i ies, along wi h analy-
ses o es sensi i i y o unc ional ulne abili y and cumula i e impac o po en ial e o in
impu a ion o ai s.
Es ima ing impac a unc ional en i y le el pe g id cell. Fo each unc ional en i y k21:
Kconsis ing o some subse o species in a pa icula loca ion, he impac o s esso jon he
unc ional en i y is he mean impac ac oss all species in ha unc ional en i y in ha loca ion:
Ij
k¼1
NFE X
NFE
i¼1
Ij
i
Cumula i e impac o all s esso s on his unc ional en i y in his loca ion is he sum o
impac s ac oss all s esso s (o a subse ).
Es ima ing impac ac oss unc ional en i ies pe g id cell. The unc ional en i y me hod
o calcula ing he impac sco e o s esso jin a gi en loca ion was de e mined by aking a
weigh ed mean ac oss all K unc ional en i ies p esen . Weigh ing o each unc ional en i y
was based on he unc ional ulne abili y, sensu Mouillo e al. [26] wi h a sligh modi ica ion
(see below).
Ij
FE ¼1
PK
k¼1FVkX
K
k¼1
FVkIj
k
Mouillo e al. [26] sco ed ulne abili y o a unc ional en i y as 1 i ha en i y was ep e-
sen ed by a single species and 0 o he wise. He e we calcula ed unc ional ulne abili y based
on an in e se exponen ial o he numbe o species ha ep esen ha unc ional en i y in ha
loca ion, whe e unc ional ulne abili y o en i y kwas calcula ed as FVk¼1
2
�Nk1, accoun ing
o low-membe ship en i ies bu apidly asymp o ically app oaching ze o as membe ship
inc eases.
As o he species-based app oach, he cumula i e impac is he sum o impac s ac oss all
(o a subse o ) s esso s wi hin ha cell.
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Code and packages
All analysis was pe o med in R s a is ical so wa e, e sion 4.0.4 [39], elying p ima ily on
packages idy e se [40], e a [41], s [42], axize [43,44], ishbase [45].
Resul s
Mean impac s on he assessed species a ied d ama ically ac oss and wi hin axa (Fig 1A–1C).
Compa ing ac oss axa, mean isk o impac was highes o co als, ollowed by o he in e e-
b a e g oups, d i en in la ge pa by highe ulne abili y o inc easing sea su ace empe a u e
and ocean acidi ica ion. O e eb a e axa, elasmob anchs we e on a e age a g ea es isk,
d i en by ising empe a u es and high ishing p essu e. Fo species and axa whose ange
ex ended beyond he con inen al shel , coas al impac s om non-clima e s esso s we e gene -
ally highe han when assessed ac oss hei ull ange (i.e., sugges ing ela i ely lowe impac s
away om he con inen al shel ), hough coas al and ull- ange clima e s esso s we e o simi-
la magni ude. A e age impac sco es o e eb a e axa ell below hose o in e eb a es,
hough he e is conside able a ia ion wi hin each axon, esul ing in ou lie s: he op 1% o
Fig 1. Cumula i e p oduc i i y-weigh ed mean impac s on species anges by axon. (A) Dis ibu ion o mean p edic ed
impac ac oss species anges ( ull ange and coas al po ions o ange) om an h opogenic s esso s by axonomic g oup. (B)
Dis ibu ion o mean cumula i e impac om i e clima e s esso s. (C) Dis ibu ion o mean cumula i e impac om eigh
non-clima e s esso s. Ve ical black line indica es mean ac oss all species in axon; whi e poin indica es median. Boxes
ep esen in e qua ile ange (IQR, qua ile Q1 o Q3); whiske s indica e obse a ions 1.5x IQR below (abo e) Q1 (Q3) o box;
ou lie s omi ed om plo o cla i y. (D) Con ibu ion o indi idual s esso s o mean cumula i e impac ac oss species anges
by axon. Clima e s esso s ou lined in ed.
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species by impac sco e (n = 211 o 21,159) con ain a disp opo iona ely high numbe o elas-
mob anchs (n = 66, 31.3% o he highes impac subse ), molluscs (n = 70, 33.2%), and co als
(n = 13, 6.1%) ela i e o hei ep esen a ion in he o e all da ase (5.3%, 13.8%, and 4.7%
espec i ely). The bo om 1% o species by impac sco e also con ain a disp opo iona e num-
be o elasmob anchs (n = 46, 21.8% o he lowes impac subse ), as well as polychae es
(n = 22, 10.4%) and ay- inned ishes (n = 140, 66.4%).
Sea su ace empe a u e ise (long- e m ends) and ex emes (sho - e m e en s, e.g.,
ma ine hea wa es) we e subs an ial con ibu o s o impac s ac oss all axa (Fig 1D). Ocean
acidi ica ion was a dominan s esso on all in e eb a e species, bu imposes li le o no di ec
e ec on e eb a es. Ul a iole adia ion impac ed mos in e eb a es p ima ily due o ul-
ne abili y o plank onic la al li e s ages. Ta ge ed ishing imposed he g ea es isk o impac
o all non-clima e s esso s on a e age, e en conside ing ha many axa a e no a ge ed and
he e o e no di ec ly impac ed (and hus a e sco ed as ze o in he calcula ion o mean impac ).
Fishe ies byca ch impac ed species b oadly ac oss all axa.
Spa ial dis ibu ion o impac s is calcula ed as he mean impac om all s esso s, o some
subse o s esso s, ac oss all species p esen in each analysis cell. Cumula i e impac s end o
be highes along coas lines, pa icula ly hea ily popula ed coas al zones whe e human popula-
ions gene a e mo e localized s esso s while o e lapping wi h highe magni ude o di use cli-
ma e s esso s (e.g., No he n Eu opean wa e s, he Medi e anean Sea, and he Indo-Paci ic
egion, Fig 2A). Lowe cumula i e impac s we e obse ed in emo e a eas whe e low ishing
and shipping ac i i y coincided wi h ela i ely low clima e s esso s (e.g., Sou heas e n Aus a-
lia, equa o ial Eas e n Paci ic, Sou he n A lan ic, No he n A lan ic nea G eenland). The e y
lowes cumula i e impac s we e obse ed in a eas domina ed by pe manen o seasonal sea ice
(A c ic Ocean, coas al An a c ica). Clima e s esso s b oadly impac species ac oss coas al and
open ocean egions, wi h highes alues in opical Indo-Paci ic wa e s, he Ca ibbean Sea, and
no he n Paci ic and A lan ic (Fig 2B). Non-clima e s esso s a e p edominan ly d i en by
ishe ies s esso s ( a ge ed ishing and byca ch), pa icula ly along coas lines and in e na-
ional wa e s jus beyond he bo de o na ional Exclusi e Economic Zones (Fig 2C).
Examining modeled impac s by qua ile, a he han magni ude, allows o compa ison o
whe e pa icula ly high impac s om clima e s esso s (which canno be mi iga ed in he sho
un, bu may bene i om adap a ion) o e lap wi h high impac s om non-clima e s esso s
(which can be e ec i ely mi iga ed h ough ac ions such as ma ine p o ec ed a eas o ishe ies
managemen ). Reclassi ying impac s ac oss hese wo agg ega ed ca ego ies in o qua iles,
based on global alues, e eals 10.3% o ocean a ea whe e clima e impac ho spo s (i.e., spa ial
cells in he op qua ile o global agg ega ed impac wi hin he ca ego y) o e lap wi h ho spo s
o non-clima e impac s (e.g., Sou heas Asia, Eas China Sea, Gul o Mexico, Ca ibbean Sea,
in e na ional opical Paci ic wa e s, Ba en s Sea, Be ing Sea, Fig 2D), and 8.8% o a ea whe e
cool spo s (i.e., bo om qua ile) o clima e and non-clima e impac s o e lap (e.g., Sou he n
po ions o Paci ic, A lan ic, and Indian oceans; Weddell Sea; na ional wa e s o se e al sou h-
e n Paci ic and A lan ic small island s a es, Fig 2D). These ho spo s and cool spo s ep esen
he wo mos common ins ances o impac qua ile o e lap; con e sely, high clima e/low non-
clima e (2.9%) and low clima e/high non-clima e (3.1%) ep esen he a es ins ances o o e -
lap (S3A Fig in S1 File).
Pa e ns o p edic ed impac s based on he species me hod s. ep esen a i e habi a s
me hod (Fig 3; see S3B and S4 Figs in S1 File. o habi a analog o Fig 2 and S3A Fig in S1 File.
espec i ely) show some clea di e ences, d i en by a ia ions in ulne abili y ac oss species
and ecosys em ype, despi e he unde lying s esso dis ibu ions being la gely he same. Com-
pa ing o e lap be ween habi a and species me hods o clima e impac s (Fig 3A) e eals a eas
whe e he wo me hods disag ee (Sø ensen simila i y index 61%), indica ing he species
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me hod p edic s g ea e isk om clima e change in equa o ial Indian and Indo-Paci ic wa e s
(pu ple ones) ela i e o he habi a me hod, la gely due o he inclusion o species-speci ic
impac s as sea su ace empe a u e ises ela i e o species he mal ole ance. Resul s based on
Fig 2. Dis ibu ion o modeled isk o impac based on species-speci ic ulne abili y and exposu e o
an h opogenic s esso s. (A) Mean cumula i e impac ac oss all species, summing ac oss all s esso s. (B) Mean
cumula i e impac ac oss all species, summing ac oss all clima e- ela ed s esso s. (C) Mean cumula i e impac ac oss
all species, summing ac oss all non-clima e s esso s. (D) Bi a ia e compa ison o dis ibu ions o clima e impac s
(o ange) s. non-clima e impac s (pu ple) by qua ile wi hin each s esso g oup.
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necessi a ing conse a ion ac ion o mi iga e non-clima e s esso s (e.g., educ ion o land-
based uno ) o allow o imp o ed ecosys em esilience o clima e change [55,56]. While
well-en o ced no- ake ma ine p o ec ed a eas a e an e ec i e conse a ion ool ha can p o-
ide mul iple co-bene i s [55,71–73], in ce ain cases, sus ainable-use ma ine p o ec ed a eas
wi h a ge ed exclusions may p o ide subs an ial ecological bene i a lowe social cos [74].
Conside a ion o human impac s ac oss lenses o species, unc ion, and habi a p o ides a
iche unde s anding o ma ine ecosys ems, and highligh s ha impac s in species- ich coas al
egions may pose g ea e isk o biodi e si y han indica ed om habi a -based me hods
alone. Ou da a can be used wi h socioeconomic in o ma ion o help p io i ize e ec i e, eco-
nomically e icien , and socially equi able conse a ion ac ions o bes bene i na u e and
people.
Suppo ing in o ma ion
S1 File.
(PDF)
Acknowledgmen s
We hank he Na ional Cen e o Ecological Analysis and Syn hesis (NCEAS) o compu a-
ional suppo .
Au ho Con ibu ions
Concep ualiza ion: Casey C. O’Ha a, Melanie F azie , Na halie Bu , Ca issa Klein, Benjamin
S. Halpe n.
Da a cu a ion: Casey C. O’Ha a.
Fo mal analysis: Casey C. O’Ha a.
Funding acquisi ion: Ca issa Klein, Benjamin S. Halpe n.
Me hodology: Casey C. O’Ha a, Melanie F azie , Mi eia Valle, Na halie Bu , Ca issa Klein,
Benjamin S. Halpe n.
So wa e: Casey C. O’Ha a.
Supe ision: Ca issa Klein, Benjamin S. Halpe n.
Visualiza ion: Casey C. O’Ha a.
W i ing – o iginal d a : Casey C. O’Ha a.
W i ing – e iew & edi ing: Casey C. O’Ha a, Melanie F azie , Mi eia Valle, Na halie Bu ,
K is in Kaschne , Ca issa Klein, Benjamin S. Halpe n.
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