Ma ine En i onmen al Resea ch 190 (2023) 106098
A ailable online 8 July 2023
0141-1136/© 2023 The Au ho s. Published by Else ie L d. This is an open access a icle unde he CC BY license (h p://c ea i ecommons.o g/licenses/by/4.0/).
Sho - e m esponse o mac oalgal communi ies o ocean wa ming in he
Sou he n Bay o Biscay
O. A iaga
a
,
*
, P. Waw zynkowski
b
,
1
, H. Ib´
a˜
nez
a
, N. Mugue za
a
, I. Díez
a
, I. P´
e ez-Ruza a
c
,
J.M. Go os iaga
a
, E. Quin ano
a
, M.A. Bece o
b
a
Labo a o y o Bo any, Depa men o Plan Biology and Ecology, Fac. o Science and Technology & Resea ch Cen e o Expe imen al Ma ine Biology and Bio echnology
PIE-UPV/EHU, Uni e si y o he Basque Coun y (UPV/EHU), PO Box 644, 48080, Bilbao, Spain
b
The BITES Lab, Cen e o Ad anced S udies o Blanes (CEAB-CSIC), Access Cala S F ancesc 14, 17300, Blanes, Gi ona, Spain
c
Depa men o Biodi e si y, Ecology and E olu ion, Complu ense Uni e si y o Mad id (UCM), C/Jos´
e An onio No ais, 12, 28040, Mad id, Spain
ARTICLE INFO
Keywo ds:
Clima e change
Tempe a u e
Mac oalgae
Communi y empe a u e index (CTI)
Canopy
Sub idal
Ibe ian Peninsula
Moni o ing
ABSTRACT
Clima e change is causing signi ican shi s in biological communi ies wo ldwide, including he deg ada ion o
ma ine communi ies. P e ious esea ch has p edic ed ha sou he n Bay o Biscay canopy- o ming sub idal
mac oalgal communi ies will shi in o u - o ming Medi e anean-like communi ies by he end o he cen u y.
These p edic ions we e based on a communi y-en i onmen ela ionship model ha used mac oalgal abundance
da a and IPCC en i onmen al p ojec ions. We ha e es ed he sho - e m accu acy o ha model by esampling
he same communi ies and loca ions ou yea s la e and ound he sho - e m p edic ions o be consis en wi h
he obse ed communi ies. Changes in sea su ace empe a u e we e posi i ely co ela ed wi h changes in he
Communi y Tempe a u e Index, sugges ing ha mac oalgal communi ies had esponded quickly o global
wa ming. The changes o e ou yea s we e signi ican , bu canopy- o ming mac oalgae we e mo e esilien in
local si es wi h a ou able empe a u e condi ions. Ou s udy demons a ed ha upda ing p edic i e models wi h
new da a has he po en ial o yield eliable p edic ions and in o m e ec i e conse a ion s a egies.
1. In oduc ion
An h opogenic ac i i ies, especially he combus ion o ossil uels,
ha e led o a conce ning inc ease in g eenhouse gas emissions and a
signi ican wa ming o he Ea h (Al-Ghussain, 2019). Since 1880,
Ea h’s empe a u e has isen by 0.08 ◦C pe decade, bu ha igu e has
mo e han doubled since 1981 o a cu en a e o 0.18 ◦C pe decade
(Lindsey and Dahlman, 2022). The a e age empe a u e o he plane ’s
land and ocean su ace in 2021 was 1.06 ◦C wa me han in
p e-indus ial imes (1880–1900; NOAA, 2023). The ocean has abso bed
mo e han 90% o he excess hea , which has led o an inc ease in he
Ocean Hea Con en (OHC) in he uppe 2000 m laye o he wo ld’s
oceans (Cheng e al., 2021). Due o he expec ed inc ease in OHC, Ea h
will likely each 1.5 ◦C abo e p e-indus ial le els in he nea e m
(2021–2040) unless we ake signi ican measu es o educe ca bon
emissions (IPCC, 2023).
Tempe a u e plays a c ucial ole in shaping species dis ibu ions
(Chen e al., 2011; Ti enso e al., 2010). Global wa ming is causing
many species wo ldwide o shi polewa d, bo h on land (Chen e al.,
2011; De ic o e al., 2012) and in he oceans (Ko sch e al., 2015;
Kumagai e al., 2018; Pinsky e al., 2020). Ma ine species a e shi ing
polewa d a an a e age a e o 72 km pe decade, a ull o de o
magni ude as e han he a e o e es ial species (Poloczanska e al.,
2013). This shi means ha he “wa ming” o “ he mophilisa ion” o
biological communi ies is one o he main consequences o global
change (Bowle and B¨
ohning-Gaese, 2017; Pa mesan and Yohe, 2003).
In many empe a e a eas, cold-adap ed species a e declining while
wa m-adap ed species a e inc easing in ela i e abundance (Go ied
e al., 2012).
Mac oalgae a e impo an p ima y p oduce s and ecosys em engi-
nee s ha modi y hei en i onmen and o e shel e and ood o
associa ed o ganisms (Ha ley e al., 2012). They also p o ide many
* Co esponding au ho .
E-mail add esses: [email p o ec ed] (O. A iaga), [email p o ec ed] (H. Ib´
a˜
nez), [email p o ec ed] (N. Mugue za), [email p o ec ed]
(I. Díez), [email p o ec ed] (I. P´
e ez-Ruza a), [email p o ec ed] (J.M. Go os iaga), [email p o ec ed] (E. Quin ano), [email p o ec ed]
(M.A. Bece o).
1
Uni e si y o Gi ona, Ins i u e o Aqua ic Ecology, C/Ma ia Au `
elia Capmany 69, Gi ona, E-17003, Ca alonia, Spain. [email p o ec ed]
Con en s lis s a ailable a ScienceDi ec
Ma ine En i onmen al Resea ch
jou nal homepage: www.else ie .com/loca e/ma en e
h ps://doi.o g/10.1016/j.ma en es.2023.106098
Recei ed 8 Ma ch 2023; Recei ed in e ised o m 4 July 2023; Accep ed 7 July 2023
Ma ine En i onmen al Resea ch 190 (2023) 106098
2
ecosys em goods and se ices since hey ope a e as ca bon sinks and
help p e en en i onmen al dis u bances such as s o ms o loodings
(R¨
onnb¨
ack e al., 2007). The e is ample e idence o mac oalgal com-
muni y deg ada ion including a dec ease in canopy- o ming species ha
esul s in u -domina ed communi ies (Filbee-Dex e and We nbe g,
2018; O lando-Bonaca e al., 2021), inc eased o e g azing leading o
ba en g ound o ma ion (Kumagai e al., 2018; Ve g´
es e al., 2014), and
he con ac ion and expansion o cold-a ini y and wa m-a ini y species
(Bu ows e al., 2019; Smale and We nbe g, 2013; We nbe g e al.,
2016). Mac oalgal communi y deg ada ion is a complex p ocess d i en
by nume ous in e wined ac o s. Tempe a u e is o en epo ed as he
main d i e o change and is he ocus o ou s udy. Ye , hea wa es,
s o ms, wa e exposu e, o e g ow h by epiphy es, pollu ion, eu ophi-
ca ion, species in asion, o ha es ing may also play a ole and co a y
wi h wa ming (Bo ja e al., 2013, 2018; Fe n´
andez, 2011; Filbee-Dex e
and We nbe g, 2018; Mugue za e al., 2017).
The Sou he n Bay o Biscay o e s an excellen oppo uni y o
in es iga e changes in mac oalgal communi y s uc u e esul ing om
ising empe a u es. Fi s , he egion has a s ong he mal g adien , wi h
a colde wes e n pa in luenced by upwelling condi ions du ing he
summe and a wa me eas e n pa (La ín e al., 2006). Second, he
Can ab ian Sea ha bo de s he no he n coas o he Ibe ian Peninsula
has wa med by 0.22 ◦C pe decade since he 1970s (Chus e al., 2022;
deCas o e al., 2009), exceeding he global end o 0.15 ◦C pe decade
(Rhein e al., 2013). This wa ming end is mos p ominen du ing
sp ing and summe (Díez e al., 2012; G´
omez-Ges ei a e al., 2008, 2011;
Izquie do e al., 2022). Thi d, se e al s udies epo a ma ked dec ease
in canopy- o ming sub idal mac oalgae such as kelp species, he
wa m- empe a e ed algae Gelidium co neum, and he ucoid Gongola ia
bacca a, which ha e s a ed o e ac om he eas e n end o he Can-
ab ian Sea owa ds he wes (Bo ja e al., 2013; Casado-Amezúa e al.,
2019; Díez e al., 2012; Fe n´
andez, 2011; Mugue za e al., 2017). A he
wes e nmos egion o he s udy a ea (Coas o Galicia), hese changes
a e bu e ed by he e ec o cold wa e upwellings in summe (Casa-
do-Amezúa e al., 2019). Howe e , less p onounced declines o se e al
cold- empe a e canopy- o ming species ha e been ecen ly epo ed o
he Galician and no he n Po uguese Coas s (Mon ei o e al., 2022).”
A p ac ical app oach o shed ligh on he e ec o empe a u e on
mac oalgal communi ies is o use he mal me ics ha can a ge em-
pe a u e e ec s alone. The Communi y Tempe a u e Index (CTI) is he
abundance-weigh ed mean o he species’ op imal empe a u e. CTI
helps unde s and he he mal p e e ences o bi ds (Bowle and
B¨
ohning-Gaese, 2017; De ic o e al., 2012), ish (Bowle and
B¨
ohning-Gaese, 2017; Bu ows e al., 2019; Day e al., 2018), and in-
e eb a es (Flanagan e al., 2019; S ua -Smi h e al., 2015). Wha li le
in o ma ion is a ailable on he he mal p e e ences o mac oalgal
communi ies s ems p ima ily om expe imen al app oaches o a ew
ecologically- ele an mac oalgal species, bu he e is less in o ma ion
a ailable a he communi y le el o o ganisa ion (Ande son, 2006;
G aba-Land y e al., 2020; O anidis, 1991).
Unde s anding how mac oalgal communi ies will espond o global
wa ming in he u u e is c ucial o he s udy o he impac o clima e
change on ben hic communi ies and o making p edic ions abou u u e
scena ios. Mugue za e al. (2022a) de eloped a
communi y-en i onmen ela ionship model o he no he n Ibe ian
Peninsula o o ecas changes in sub idal mac oalgal communi ies unde
mul iple clima e change scena ios. They ound ha wa e empe a u e is
he p ima y ac o in luencing he dis ibu ion o mac oalgal commu-
ni ies, while nu ien a ailabili y plays a seconda y ole. They sugges ed
ha no he n Ibe ian communi ies could unde go a me idionalisa ion
end by he end o he cen u y. This me idionalisa ion will occu om
eas o wes (Mugue za e al., 2022a). Howe e , o es he model’s
p edic i e capaci y i is essen ial o ga he upda ed biological and
en i onmen al da a o see whe he mac oalgal communi ies a e shi ing
and i so whe he hey ollow he end p edic ed by hei model.
He e, we combined global species occu ence da a wi h g idded
empe a u e da ase s o calcula e he Species Tempe a u e Index (STI) o
o e 200 mac oalgal species and quan i ied he impac o empe a u e
inc ease on mac oalgal communi ies. A e ou yea s, we esampled he
loca ions in es iga ed in 2015 by Mugue za e al. (2022a) in hei s udy.
Fi s , we quan i ied he ac ual sho - e m communi y shi s and de e -
mined hei e olu ion. Second, we es ed he model’s sho - e m p e-
dic i e capaci y. To do so, we compa ed he model’s p edic ed
communi ies wi h he obse ed na u al communi ies in 2019. Thi d, o
isola e he ole o empe a u e in he obse ed mac oalgal shi s, we
used species’ he mal ai s o calcula e a Communi y Tempe a u e
Index (CTI). E en in he sho e m, we an icipa ed ha some signs o he
eas -wes me idionalisa ion o ecas ed by hei model may become
isible (H
0
: no sho - e m communi y change). We expec ed a good
co ela ion be ween modelled and obse ed communi ies (H
0
: no p e-
dic i e capaci y o he model). Conside ing ha Mugue za e al. (2022a)
iden i ied wa e empe a u e as he p ima y ac o in luencing he dis-
ibu ion o he species, and in he ace o he ongoing global wa ming,
we also hypo hesized ha SST could pa ially explain he obse ed
communi y shi s (H
0
: no co ela ion be ween changes in SST and
changes in CTI).
2. Me hods
2.1. S udy a ea
In he summe s o 2019–2020 ( om July o Sep embe ), we quan-
i ied species composi ion and abundance in he exac same loca ions
sampled in 2015 by Mugue za e al. (2022a). We s udied eigh loca ions
in he sou he n Bay o Biscay in 2019 (L1: Malpica; L2: Cedei a; L3:
Lua ca; L4: Las es; L5: San Vicen e; L6: Somocue as; L7: Koba on; and
L8: Ea), and wo e e ence loca ions in he Medi e anean Sea in 2020:
one in he Albo an Sea (L9: La He adu a) and he o he in he Wes e n
Medi e anean Sea (L10: Cabo Palos) (Fig. 1, Appendix a).
Ou s udy a ea has no able di e ences in en i onmen al condi ions.
We ocus he e on sea su ace empe a u e (SST) and ni a e concen a-
ion (NIT) as he p ima y d i e s o communi y change (Mugue za e al.,
2022a). The sou he n Bay o Biscay has a dis inc wes - o-eas he mal
g adien , wi h a summe upwelling sys em ha cools SST o 16 ◦C du ing
upwelling condi ions in he wes e n a ea (G´
omez-Ges ei a e al., 2008).
He e, SST anges om 14 ◦C in win e o 19.5 ◦C du ing summe
downwelling condi ions (G´
omez-Ges ei a e al., 2008; Ospina-Al a ez
e al., 2010). The in luence o his upwelling weakens owa ds he eas ,
mainly because Cape Pe˜
nas ac s as a bounda y o he upwelling sys-
em’s a ea o in luence (La ín e al., 2006; Valencia e al., 2004).
Consequen ly, he ange o annual a ia ion in SST in he eas e nmos
a ea is highe han in he wes e n a ea, anging om 12 ◦C in win e up
o 22 ◦C in summe (Bo ja e al., 2000).
The loca ions on he Medi e anean Sea a e wa me on a e age, wi h
SST in he Albo an Sea anging om 15.5 ◦C in win e o 22.8 ◦C in
summe (Shal ou and Oms ed , 2014). P oximi y o he A lan ic Ocean
and he in luence o an upwelling sys em ha mainly occu s du ing
sp ing and summe cool he Albo an Sea SST o 17 ◦C du ing hese
mon hs. The Wes e n Medi e anean Sea is wa me han he Albo an
Sea, wi h SST anging be ween 15 ◦C in win e and 25 ◦C in summe
(Shal ou and Oms ed , 2014).
Ni a e concen a ion in su ace wa e s is lowe in summe due o he
s a i ica ion o he wa e column, and highe in win e due o he
mixing induced by wa es and wind (Se e e al., 1999). In he wes e n
a ea o he Sou he n Bay o Biscay, ni a e concen a ion anges om
0.3 mmol m
−3
in summe o a ound 5 mmol m
−3
in win e (Gonz´
alez-Gil
e al., 2018), whe eas in he eas e n a ea hese alues a e a ound 1
mmol m
−3
in summe o 4–5 mmol m
−3
in win e (Ba˜
na e al., 2020;
Mu˜
niz e al., 2018). In he Albo an Sea, ni a e concen a ion anges
om 5 * 10
−4
mmol m
−3
in summe o 1.2 * 10
−3
mmol m
−3
in win e
(Lazza i e al., 2016). Howe e , he summe upwelling sys ems in he
sou hwes Bay o Biscay and in no he n Albo an Sea b ing up deep,
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
3
nu ien - ich, cool wa e s. In sou h-eas e n Bay o Biscay, his sys em has
li le o no in luence, as e idenced by he inc ease in empe a u e and
he s a i ica ion o he wa e column, so he nu ien inpu comes
mainly om i e s (Fe n´
andez-Salas e al., 2015). The Wes e n Medi-
e anean Sea is oligo ophic, since he in luence o he A lan ic de-
c eases owa ds he eas , and he main inpu is i e ine bu i has a low
annual p ecipi a ion a e (Valdes-Abellan e al., 2017). He e he ni a e
concen a ion anges om 7.4 * 10
−4
mmol m
−3
in summe o 1.3 *
10
−3
mmol m
−3
in win e (Lazza i e al., 2016).
2.2. Da a collec ion
2.2.1. Field da a collec ion
Following he same me hodology as Mugue za e al. (2022a), we
conduc ed sampling a 5 m below cha da um. Two si es we e selec ed
pe loca ion, a leas 15 m apa . We andomly placed eigh 50 ×50 cm
su aces wi hin each si e a leas 1 m apa , on ocky pla o ms o s able
ocks, la ened o gen ly sloping, and wi h low sedimen a ion le els,
always a oiding special habi a s such as c e ices o boulde s. We
accessed he loca ions by boa and used SCUBA o quan i y each su -
ace’s mac oalgae composi ion and abundance in si u. To es ima e
abundance, we used a 5% in e al-scale co e ange ( om 5 o 100%).
Fo mac oalgal co e below 5% we used a 1% in e al-scale (1, 2, 3, 4,
5%). Fo mac oalgal co e below 1% we assigned a alue o 0.5% o he
axa. All e ical s a a o he communi y we e sampled (c us ose, basal,
canopy, and epiphy ic s a a) and hus, he o al co e o he ege a ion
could exceed 100%. We ollowed he axonomic nomencla u e used in
AlgaeBase (Gui y and Gui y, 2023). We iden i ied axa a he species
le el in si u whene e possible. Samples o axa ha could no be
de e mined in si u ( u species) we e collec ed and anspo ed o he
labo a o y o u he iden i ica ion. Samples we e anspo ed in
mois ened co on bags and ozen wi hin a ew hou s. We used binocula
and op ical mic oscopes o eliable axonomical iden i ica ion, ca ied
ou by he same esea che s in bo h pe iods (2015 and 2019–2020).
2.2.2. En i onmen al da a collec ion
The en i onmen al da a included in his s udy was downloaded om
E.U. Cope nicus Ma ine Se ice In o ma ion (Me chan e al., 2019). SST
was ob ained om he Mul i Obse a ion Global Ocean 3D Tempe a u e
Salini y Heigh Geos ophic Cu en and MLD da ase (h ps://doi.o g/
10.48670/moi-00052) and NIT was ob ained om he Global Ocean
Biogeochemis y hindcas da ase (h ps://doi.o g/10.48670/
moi-00019), bo h wi h a spa ial esolu ion o 0.25 ×0.25◦(abou
27.75 ×27.75 km) and a mon hly empo al esolu ion.
2.3. Da a ea men and analyses
2.3.1. Mac oalgal communi y s uc u e
In his s udy, we used squa e- oo ans o med species co e da a
based on B ay-Cu is dis ance o analyse he simila i y be ween pai s o
a e aged si e-samples. Squa e- oo ans o ma ion was applied o
educe he s ong in luence o dominan axa in communi y analyses and
allow o a b oade numbe o species o play a pa (Cla ke and Wa -
wick, 2001). We used he clus e classi ica ion echnique o explo e
po en ial mac oalgal communi y g oups and ep esen ed he esul s in a
dend og am. To de e mine wha species con ibu ed mos o he simi-
la i y wi hin g oups, a simila i y pe cen age analysis (SIMPER) was
conduc ed. We compa ed he classi ica ion ob ained in 2015 wi h ha
ob ained in 2019–2020. We also examined he species ichness o each
yea and loca ion and assessed o any signi ican di e ences be ween
yea s and loca ions. These analyses we e pe o med using PERMA-
NOVA + o PRIMER so wa e (Ande son e al., 2008).
2.3.2. P edic i e capaci y o he model
Using dis ance-based linea models, Mugue za e al. (2022a) showed
ha sp ing SST and, o a lesse deg ee, win e NIT we e he main
en i onmen al a iables esponsible o he a ia ion in he spa ial
pa e n o mac oalgae. Using hese p edic o a iables, hey un h ee
eg essions o calcula e “modelled ecological dis ances” o each pai o
loca ions. To assess he p edic i e capaci y o hei model, hey also
calcula ed he “obse ed ecological dis ances”, which a e he dis ance
be ween he cen oids o loca ions de ec ed in he nMDS (based on he
ma ix o simila i ies be ween mac oalgal communi ies). They hen
plo ed he “obse ed ecological dis ances” wi h he “modelled ecolog-
ical dis ances”. He e, o assess he p edic i e capaci y o hei model in
he sho e m, we compiled mon hly SST (◦C) and NIT (mmol*m
−3
)
Fig. 1. Map o he s udy a ea showing he en sampling loca ions (L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San Vicen e; L6: Somocue as; L7: Koba on;
L8: Ea; L9: La He adu a; and L10: Cabo Palos) and he mean sea su ace empe a u e dis ibu ion o 2019, om Cope nicus da abase. Sou ce: own elabo a ion
gene a ed by A cGIS P o 2.2.0 so wa e (h ps://www.es i.com/en-us/a cgis/p oduc s/a cgis-p o/o e iew)".
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
4
da a om he cell g id a each sampling loca ion o he yea 2019 o
he sou he n Bay o Biscay and 2020 o he Medi e anean loca ions.
We de e mined a mean sp ing SST by a e aging he SSTs o Ap il, May,
and June and a mean win e alue by a e aging he NITs o Janua y,
Feb ua y, and Ma ch. We hen used he upda ed en i onmen al da a o
un he same model as Mugue za e al. (2022a) and ob ained “modelled
ecological dis ances” be ween all pai s o loca ions o 2019–2020. We
also cons uc ed a nMDS (based on he ma ix o simila i ies be ween
mac oalgal communi ies) wi h he communi y da a ga he ed in
2019–2020 o quan i y he “obse ed ecological dis ances” ou (and
i e o Medi e anean loca ions) yea s a e he ini ial sampling by
Mugue za e al. (2022a), using PERMANOVA + o PRIMER so wa e
(Ande son e al., 2008). We hen co ela ed he modelled and obse ed
ecological dis ances o 2019–2020 o es he model’s abili y o p edic
sho - e m mac oalgal communi y changes. The Pea son co ela ion
coe icien p o ided a quan i a i e es ima e o he model’s accu acy. We
u ned he modelled ecological dis ances be ween loca ions in o simi-
la i y alues (by sub ac ing his dis ance om 100) o cons uc a nMDS
based on he model and compa e i wi h he nMDS pe o med wi h he
obse ed da a.
2.3.3. Tempe a u e and CTI co ela ion
The simila i y be ween si es wi hin each loca ion was high (o e 80%
on a e age), so we conduc ed he ollowing analyses a he loca ion
le el. The model de eloped by Mugue za e al. (2022a) iden i ied em-
pe a u e as he p ima y en i onmen al a iable in luencing communi y
s uc u e. Gi en ha wa ming in he a ea was mainly obse ed du ing
sp ing and summe (Díez e al., 2012; G´
omez-Ges ei a e al., 2008, 2011;
Izquie do e al., 2022), we used Dis ance-based linea model analysis
(DISTLM) o examine he impac o mean annual SST, sp ing SST (Ap il,
May, June), and summe SST (July, Augus , Sep embe ) on he mac o-
algal communi y s uc u e. We plo ed dis ance-based edundancy an-
alyses (dbRDA) o isualise he ela ionship and de e mined which
empe a u e- ela ed a iables bes explained he obse ed a ia ion in
mac oalgal communi y s uc u e, using PERMANOVA (Ande son e al.,
2008). We hen co ela ed his en i onmen al a iable wi h he Com-
muni y Tempe a u e Index (CTI).
Fo each eco ded species, he Species Tempe a u e Index (STI) was
calcula ed as he a e age empe a u e o he species occu ence ange,
conside ed a p oxy o he species’ dependence on empe a u e
(De ic o e al., 2012). We ob ained he global dis ibu ion da a o each
species om he open-access da abases “Ocean Biodi e si y In o ma ion
Sys em” (OBIS) (h ps://www.obis.o g/) and “Global Biodi e si y In-
o ma ion Facili y” (GBIF) (h ps://www.gbi .o g/), by using he special
packages obis (P o oos and Bosch, 2019) and gbi (Chambe lain
e al., 2021) om he open-sou ce so wa e R (R De elopmen Co e
Team, 2023; RS udio Team, 2016). The ime- ame conside ed o he
dis ibu ion da a was 1993–2020. We downloaded mon hly SST da a o
he si es o occu ence o e e y species om he Cope nicus da abase o
calcula e annual means. We calcula ed he CTI o each sampling uni o
measu e he a e age he mal a ini y o he mac oalgal communi ies.
The CTI is he abundance-weigh ed STI a e age o all species in a
sampling uni (De ic o e al., 2008, 2012). We hen calcula ed he
a e age CTI o each loca ion and yea . Di e ences in CTI we e es ed
wi h a uni a ia e PERMANOVA analysis based on Euclidean dis ance
wi h ime and loca ion as ixed and andom ac o s, espec i ely. Fo
pos -hoc pai wise compa isons Gosse -s a is ic was used (Ande son
e al., 2008).
Mac oalgal species ha e a ying li espans and many ha e a li e cycle
ha exceeds one yea (i.e. Gelidium co neum), so cu en and pas
en i onmen al condi ions may de e mine he cu en s a e o he com-
muni y (Chus e al., 2022; Ramos e al., 2020). To es he deg ee o
associa ion be ween empe a u e and CTI, we analysed he co ela ion
be ween he change in empe a u e and he change in CTI. SST changes
we e calcula ed using he mean o he sampling yea and he wo p e-
ious yea s and compa ed 2017–2019 (2018–2020 o he
Medi e anean) o 2013–2015 o accommoda e he mul iannual SST
a iance ha mul iple mac oalgal species may expe ience (Appendix b).
Fo he CTI change, we calcula ed he di e ence be ween CTI alues in
2019 (2020 o Medi e anean loca ions) and 2015.
3. Resul s
3.1. Changes in he communi y s uc u e
Based on he 43% simila i y le el used by Mugue za e al. (2022a),
we ound loca ions clus e ed in ou g oups wi h dis inc species com-
posi ions. We ound h ee geog aphic a eas in he Sou he n Bay o Biscay
mac oalgal communi ies (wes e n, cen al, and eas e n sec ions) and
ano he in he Medi e anean (Fig. 2b). The kelp Sacco hiza polyschides
and he genicula e calca eous mac oalga Co allina o icinalis domina ed
in he wes e nmos Bay o Biscay loca ions (G oup A: L1, L2, and L3).
Gelidium co neum and he enc us ing Co allinales Mesophyllum expansum
domina ed in he cen al Bay o Biscay loca ions (G oup B: L4 and L6).
Mesophyllum expansum and he epheme al ilamen ous Ce amiales
Aphanocladia s ichidiosa domina ed in he eas e nmos Bay o Biscay
loca ions (G oup C: L5, L7, and L8). The Co allinales Li hophyllum
inc us ans and Jania peduncula a a . adhae ens domina ed he Medi e -
anean loca ions (G oup D: L9 and L10). See Appendix c o a isual
ep esen a ion o hese species in each loca ion.
The h ee sec ions in he sou he n Bay o Biscay emained dis inc in
2019 and 2015, al hough G oup A was sligh ly mo e simila o G oups B
and C in 2019 (33.15%) han in 2015 (29.75%). Loca ion composi ion in
he cen al sec ion di e ed om 2015 o 2019 (Appendix d). L5 shi ed
om he cen al a ea in 2015 o he eas e n a ea in 2019. In ou yea s,
he pe cen co e o Gelidium co neum in his loca ion dec eased om
59.1% o 23.4%, while he pe cen co e o Aphanocladia s ichidiosa
inc eased om 0% o 7.2% (Appendix e).
We also ound he wo Medi e anean mac oalgal communi ies o be
mo e simila in 2020 (54.13%) han in 2015 (38.63%). Li hophyllum
inc us ans and Jania peduncula a a . adhae ens eplaced p e iously
dominan species Halop e is scopa ia and Padina pa onica in he Medi-
e anean loca ions (Appendix d). Unde ec ed in 2015, Jania peduncula a
a . adhae ens showed a pe cen co e o 15.63 in he Albo an Sea and
50.63 in he wes e n Medi e anean in 2020 (Appendix e).
The species ichness also di e ed om one loca ion and yea o
ano he , excep in Ea (L8) (Fig. 3, Appendix ). The lowes alue co -
esponded o Somocue as (L6) in bo h su eys (a mean o 12 axa in
2015 and a mean o 8 axa in 2019). The highes alues we e ound in
he wo Medi e anean loca ions and in Lua ca (L3) (a ound 27 axa in
2015 and 34 in 2019), ollowed by no h-eas e n loca ions. In ou yea s,
he numbe o axa dec eased in he wes e nmos loca ion (L1, om 19
o 14) and in he cen al g oup (L4, om 27 o 19 and L6 om 12 o 8),
bu in he o he loca ions an a e age inc ease o 7 axa was obse ed
(Fig. 3).
3.2. P edic i e capaci y o he model
We ound a posi i e co ela ion (R =0.740, p <0.0001) be ween he
obse ed and modelled spa ial dis ibu ion in 2019–2020 (Fig. 4).
O e all, loca ions om he sou he n Bay o Biscay (L1 o L8) we e
close o each o he han o ecas ed, pa icula ly Cedei a (L2), i.e, hey
we e mo e simila in species composi ion and abundance. Con a y o
model’s p edic ions, he loca ions he e did no ollow a succession along
he coas , bu ins ead, hey became mo e simila , hey homogenized.
Somocue as (L6) emained mo e dis inc om he o he no he n lo-
ca ions, and San Vicen e (L5) shi ed close o he eas e n communi ies
o Koba on (L7) and Ea (L8) in he obse ed pa e n. The Medi e anean
loca ions o La He adu a (L9) and Cabo de Palos (L10) emained dis an
om he Bay o Biscay loca ions bu we e mo e simila han he model
p edic ed (Fig. 5).
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
5
3.3. The e ec o empe a u e on spa ial dis ibu ion
Annual SST and summe SST (SSTsu) we e he bes i -explana o y
a iables, explaining 42.4% o he o al a ia ion (Dis ance-Based
Linea Model, dis LM). Annual SST disc imina ed be ween he Sou he n
Bay o Biscay and Medi e anean communi ies, and SSTsu disc imina ed
wi hin he Sou he n Bay o Biscay communi ies, ollowing an eas -wes
g adien (Fig. 6, Appendix g). Annual SST also dis inguished be ween
he wo pe iods o he Medi e anean loca ions and o loca ions L4 o
L8, whe eas o loca ions L1 o L3 he di e ence be ween he wo pe-
iods was es ablished by summe SST.
We also ound signi ican di e ences in he Communi y Tempe a u e
Index (CTI) ac oss loca ions and yea s (Fig. 7, Appendix h). Medi e a-
nean loca ions (L9 and L10) showed he highes CTI alues bo h in 2015
and 2020, wi h a e age alues anging om 14.7 ◦C o 16.34 ◦C in L9,
and 16.5 ◦C o 17.3 ◦C in L10. The wes e nmos loca ions o he Bay o
Biscay had he lowes CTI alues, wi h a e age alues o 13.5 ◦C in 2015,
and 13.3 ◦C in 2019 (Fig. 7). CTI also a ied om yea o yea in six ou
o he en loca ions (Fig. 7). On a e age, CTI dec eased by 2.38% a L1,
L2, L3 (G oup A), and L8, bu inc eased by 4.88% a he emaining lo-
ca ions. We ound a signi ican posi i e co ela ion be ween he changes
in SSTsu and in CTI (R =0.835, p =0.003, Fig. 8).
4. Discussion
Accu a ely p edic ing he impac o global change on ma ine ben hic
communi ies is c ucial o help p ese e ou ecosys ems and he se ices
hey p o ide. While models can help us simula e po en ial e ec s,
in o m p e en i e measu es, and aid in adap a ion s a egies, alida ing
hei accu acy using eal-wo ld da a is c ucial. Mugue za e al. (2022a)
used spa ial da a o o ecas ha mac oalgal communi ies in he Can-
ab ian Sea would esemble hose in he Medi e anean egion mo e
closely han hose along he Galician coas by he end o he cen u y,
which would ollow an eas - o-wes g adien . Ou s udy ocused on
es ing he sho - e m p edic ions o his model using new obse a ional
da a ga he ed ou yea s a e he ini ial assessmen s. Despi e elying on
spa ial da a o long- e m p ojec ions, we ound ha he sho - e m
p edic ions aligned wi h ac ual obse a ions o he same communi ies,
indica ing he model’s obus ness (Mugue za e al., 2022a). Sho - e m
empe a u e changes we e posi i ely co ela ed wi h changes in he
Communi y Tempe a u e Index (CTI), sugges ing ha mac oalgal com-
muni ies quickly adap o empe a u e changes, po en ially igge ing
he obse ed phase shi in he egion. We also de ec ed disc epancies
be ween he model’s p ojec ions and he obse ed communi ies,
p o iding addi ional insigh s in o clima e-induced changes in commu-
ni y composi ion.
In ou s udy, loca ions wes o Cape Pe˜
nas (L1, L2, and L3) o med a
Fig. 2. Hie a chical clus e ing dend og am o sampling si es, based on B ay-Cu is simila i ies calcula ed on squa e- oo ans o med abundance da a. Dashed lines
indica e he 43% simila i y le el. “L” e e s o loca ion (L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San Vicen e; L6: Somocue as; L7: Koba on; L8: Ea; L9: La
He adu a; and L10: Cabo Palos). Each loca ion had wo eplica ed si es, labelled as “0.1” and “0.2”. a) 2015, b) 2019–2020.
Fig. 3. A e age numbe o axa pe su ace o each loca ion in 2015 and 2019–2020. “L” e e s o loca ion (L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San
Vicen e; L6: Somocue as; L7: Koba on; L8: Ea; L9: La He adu a; and L10: Cabo Palos). As e isk indica e signi ican di e ences be ween yea s wi hin each loca ion:
*p <0.05, **p <0.01, ***p <0.001.
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
6
consis en geog aphic sec ion cha ac e ized by he wa m- empe a e kelp
Sacco hiza polyschides, wi h a he mal op imum o 10.3 ◦C (Casado-A-
mezúa e al., 2019; Fe n´
andez, 2016; Mugue za e al., 2017). Eas o
Cape Pe˜
nas, a cen al egion (L4, L6) was domina ed by he
canopy- o ming Gelidium co neum, which has a he mal op imum o
12.5 ◦C, and he eas e nmos a ea (L5, L7, and L8) was domina ed by he
mo phologically simple Aphanocladia s ichidiosa, wi h a he mal op i-
mum o 17.2 ◦C (Casado-Amezúa e al., 2019; Mugue za e al., 2022a).
These dis ibu ion pa e ns align wi h p e ious s udies desc ibing he
e ea o S. polyschides and G. co neum owa d he wes (Assis e al.,
2017; Bo ja e al., 2018; Go os iaga 1995). Mugue za e al. (2022a)
al eady epo ed his same dis ibu ion o he dominan species in 2015,
showing a hallus size dec ease wi h inc easing empe a u e, which
leads o a s uc u al simpli ica ion o he communi ies.
Ou analyses e ealed changes in he dis ibu ion o dominan
canopy- o ming species om 2015 o 2019, suppo ing he p edic ed
eas -wes me idionalisa ion o he sou he n Bay o Biscay (Mugue za
e al., 2022a). Speci ically, he mac oalgal communi ies o San Vicen e
(L5) shi ed om he cen al sec ion o join he eas e n a ea, accompa-
nied by a dec ease in he co e o G. co neum and an inc ease in he
numbe o axa (Díez e al., 2012; Mugue za e al., 2017). This ansi ion
esul ed in a communi y domina ed by mo phologically simple o ms
(Aphanocladia s ichidiosa and Ce amium spp.) and co alline species
(Jania squama a, Ellisolandia elonga a, and Co allina o icinalis), which is
consis en wi h he phase shi s om canopy-domina ed mac oalgal
communi ies o u - o ming communi ies obse ed wo ldwide (Bene-
de i-Cecchi e al., 2001; Díez e al., 2012; Pe kol-Finkel and Ai oldi,
2010; Smale and We nbe g, 2013; Voe man e al., 2013; We nbe g e al.,
2016). No ably, we also ound ha he Medi e anean communi ies
ha e unde gone mo e signi ican changes and ha e become mo e
Fig. 4. Associa ion (linea eg ession) be ween he obse ed and modelled ecological dis ances o 2019–2020. Ecological dis ance is he dis ance be ween cen oids
as de ec ed in he non-me ic mul idimensional scaling (nMDS).
Fig. 5. Non-me ic mul idimensional scaling (nMDS) diag ams (Ande son e al., 2008) o he 10 loca ions (L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San
Vicen e; L6: Somocue as; L7: Koba on; L8: Ea; L9: La He adu a; and L10: Cabo Palos) based on squa e- oo ans o med abundances and B ay-Cu is simila i ies. a)
obse ed pa e n. B) modelled pa e n. Colou s a e based on 43% simila i y clus e ing (Fig. 2b).
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
7
homogeneous, wi h a shi owa ds co alline-domina ed communi ies.
Inc eased empe a u e, wa e anspa ency, and sola adia ion may
ha e s imula ed co alline calci ica ion and g ow h a es (Díez e al.,
2012; Jian-Zhang e al., 2010; S elle e al., 2007). Howe e , i is un-
ce ain whe he hese indings apply o he b oade Medi e anean e-
gion, as ou s udy p ima ily ocused on he sou he n Bay o Biscay and
included only wo Medi e anean loca ions as e e ences (Mugue za
e al., 2022a; Ramos e al., 2020).
Disc epancies be ween he model p ojec ions and he obse ed
communi ies also p o ided insigh s in o he complex dynamics o
clima e-d i en communi y changes. Fo example, he model p edic ed
educed dis ances be ween Somocue as (L6) and he eas e n loca ions,
bu ac ual obse a ional da a did no suppo hese p edic ions. The
unique cha ac e is ics o Somocue as (L6), si ua ed nea he mou h o
he Ri e Pas and in luenced by i s eshwa e inpu , may explain he
dispa i y be ween he model and eali y. The i e ’s cu en eshwa e
in low likely cools he wa e and p o ides addi ional nu ien s, sup-
po ing he h i ing Gelidium co neum communi ies in his a ea (Go -
os iaga, 1995). Somocue as (L6) exhibi ed he bes -p ese ed G.
co neum-domina ed communi y in ou s udy, cha ac e ized by low
species ichness and lo is ic homogenei y, consis en wi h o he
G. co neum-domina ed communi ies such as Las es (L4, see Appendix
d).
Ou s udy e ealed an inc ease in G. co neum and associa ed
epiphy ic species (Dic yo a dicho oma and Plocamium ca ilagineum) in
Las es (L4). Con e sely, we obse ed a dec ease in co alline (Elliso-
landia elonga a, Co allina o icinalis, and Jania ubens) and Ce amiales
(Gayliella laccida, Mic ocladia glandulosa, Ve eb a a u iculosa) species
(see Appendix d). The G. co neum canopy expansion led o a signi ican
dec ease in species ichness. In he summe o 2014, be o e ou ini ial
sampling, Las es (L4) expe ienced he highes summe empe a u e o
he en i e decade (2010–2020), causing an imbalance in he G. co neum
communi y, mani es ed by s ess symp oms such as ond yellowing and
an inc ease in epiphy ic ce amiaceous species. Simila s ess symp oms
occu ed in San Vicen e (L5) du ing he same yea . Howe e , unlike San
Vicen e (L5), which con inued o de e io a e p og essi ely in 2019,
mac oalgal communi ies in Las es (L4) displayed g ea e esilience,
wi h an inc eased pe cen co e o G. co neum. The coole wa e em-
pe a u e and po en ially mo e nu ien - ich condi ions in Las es (L4)
compa ed o San Vicen e (L5) may accoun o he success o G. co neum
in Las es, as obse ed in Somocue as (L6), whe e G. co neum s ands
ha e h i ed o e ime. This phenomenon may be analogous o he e -
ec s o upwellings in o he coas al a eas (Lou enço e al., 2016). The
p esence o e uge loca ions wi h a ou able local en i onmen al con-
di ions, such as Somocue as (L6), is ecologically and biologically sig-
ni ican as hey can sa egua d he gene ic he i age o h ea ened
ounda ional species in he ace o clima e change e ec s (Assis e al.,
2017; Ga cía e al., 2021). These indings unde sco e he impo ance o
combining model p edic ions wi h empi ical da a o unde s and
ecosys em esponses o global change comp ehensi ely.
Models a e c ucial o unde s and communi y shi s unde global
change, o e ing aluable insigh s in o u u e scena ios and iden i ying
Fig. 6. Dis ance-based edundancy analysis (dbRDA) o dina ion plo s showing
he ela ionship be ween he empe a u e- ela ed en i onmen al a iables ha
bes explain he a ia ion o mac oalgal communi ies o 2015 and 2019–2020.
L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San Vicen e; L6: Somo-
cue as; L7: Koba on; L8: Ea; L9: La He adu a; and L10: Cabo Palos. SST
(annual sea su ace empe a u e). SSTsu (summe sea su ace empe a u e). The
colou g adien ep esen s he SSTsu g adien along he s udy a ea.
Fig. 7. Communi y Tempe a u e Index (CTI) o each loca ion in 2015 and 2019–2020. L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San Vicen e; L6:
Somocue as; L7: Koba on; L8: Ea; L9: La He adu a; and L10: Cabo Palos. As e isk indica es signi ican di e ences om one yea o ano he wi hin each loca ion: *p
<0.05, **p <0.01, ***p <0.001.
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
8
key d i e s o ecological ans o ma ions. He e, we alida ed Mugue za
e al.’s (2022a) model using eal-wo ld da a and showed e idence o he
model’s consis ency and accu acy in he sho e m, ein o cing he
model’s obus ness. Ye , he model unde discussion has some limi a-
ions. Fi s ly, he e is a c i ical o e sigh in he model as i ails o
conside bio ic in e ac ions, such as he bi o y o compe i ion o e-
sou ces, which can s ongly impac he o ganiza ion and unc ioning o
ma ine ecosys ems (Falkenbe g e al., 2013; S eneck e al., 2002). Sec-
ondly, collec ing on-si e en i onmen al da a, including empe a u e and
ni a e concen a ion, would help ob ain mo e p ecise es ima es o local
condi ions. The model’s cu en esolu ion (0.25◦×0.25◦) co e s o e
750 km
2
, which may no ully ep esen he local condi ions o ou
sampling si es. Reco ding on-si e en i onmen al da a could imp o e
es ima es o local condi ions and he model’s accu acy. The model
would also bene i om accoun ing o he impac o i e ine inpu s o
small upwelling sys ems, as hese ac o s can signi ican ly in luence
ecosys em dynamics. Finally, imp o ing he model’s accu acy could also
in ol e inc eased eplica ion and a b oade spa ial scale, including he
wes e n Ibe ian Peninsula and addi ional Medi e anean si es. Howe e ,
gi en ou goal o compa ing Mugue za e al. (2022a) p edic ions o
ac ual communi ies ou yea s la e , we could no modi y he model.
The e is inc easing e idence wo ldwide ha canopy-domina ed
mac oalgal communi ies a e shi ing o s uc u ally simple al e na e
s a es (Benede i-Cecchi e al., 2001; Fe n´
andez, 2016; O lando-Bonaca
e al., 2021; Pe kol-Finkel and Ai oldi, 2010; We nbe g e al., 2016). The
ac o s behind phase shi s a e nume ous and in e wined, bu empe -
a u e is an impo an pa ame e a ec ing species dis ibu ion (Husa
e al., 2008; Mülle e al., 2009; Sjø un e al., 2015; Ti enso e al., 2010;
We nbe g e al., 2016). Ou da a p o ided e idence o suppo he
con en ion ha he sou he n Bay o Biscay phase shi om
h ee-dimensional mac oalgal communi ies o u -domina ed commu-
ni ies may be empe a u e d i en. Ou s udy ound a s ong posi i e
co ela ion be ween changes in wa e empe a u e and changes in he
Communi y Tempe a u e Index (CTI), sugges ing ha mac oalgal com-
muni ies esponded quickly o ocean empe a u e change. The
inc easing empe a u e may a ou species wi h wa me a ini ies and
add s ess o hose wi h colde a ini ies, which may s ongly in luence
species abundance and dis ibu ion. We used he Species Tempe a u e
Index (STI) as a p oxy o he mal a ini y. Gi en ha he CTI is he
abundance-weigh ed a e age o he STI, shi s in CTI ep esen changes
in he he mal a ini y o he sys em. A highe CTI ep esen ed a g ea e
dominance o wa me species in he communi y, d i en ei he by an
inc ease in hei pe cen co e o a dec ease in he pe cen co e o
colde a ini y species (McLean e al., 2021). The sou he n Bay o Biscay
has been wa ming since he ea ly 80s (Anad´
on e al., 2009; Chus e al.,
2022; Cos oya e al., 2015; Fe n´
andez, 2011; Voe man e al., 2013).
Colde a ini y species, such as Gelidium co neum may be subjec ed o
mo e signi ican s ess, unlike wa me a ini y species, such as ce am-
iaceous o co alline species, which may igge he phase shi . We ound
one no ewo hy excep ion o his pa e n in Ea (L8), in he eas e nmos
a ea o he sou he n Bay o Biscay. Con a y o expec a ions, he wa m
a ini y species Aphanocladia s ichidiosa and Mesophyllum expansum
declined in his loca ion. The eason behind his decline is unclea , gi en
he ising empe a u es and abundance ends o hese species in he
a ea o e he las ew decades (Mugue za e al., 2017, 2022b). This
loca ion had a bloom o Os eopsis siamensis co e ing an es ima ed 25%
o he subs a um (au ho ’s obse a ion). This epiphy ic dino lagella e is
on he inc ease in he sou h-eas e n Bay o Biscay (D oue e al., 2021),
and i con ains se e al oxic chemicals ha cause mo ali y in ma ine
o ganisms, including mac oalgae (Acco oni e al., 2015). The canopy
ha domina ed he a ea was almos non-exis en , and he communi y
had shi ed o small, as -g owing, oppo unis ic u species.
U ilizing species’ he mal ai s o p edic species dis ibu ion and
abundance p o ides aluable insigh s in o he impac s o clima e change
on ma ine communi ies. Ou s udy showed ha he Species Tempe a u e
Index (STI) and Communi y Tempe a u e Index (CTI), in combina ion
wi h SST p edic ions, enhance ou unde s anding o how empe a u e
in luences communi y changes. The STI o e s a p oxy o e alua e spe-
cies’ esponses o empe a u e a ia ions by assessing he mal a ini y.
The CTI, as an abundance-weigh ed a e age o he STI, enables us o
quan i y changes in he he mal a ini y o he en i e communi y. In e-
g a ing hese indices wi h SST p ojec ions would allow o mo e accu-
a e p edic ions o u u e ma ine communi y shi s associa ed wi h
clima e change, empowe ing e ec i e conse a ion and managemen
s a egies.
Global open-access da abases a e no pe ec . The lack o abundance
Fig. 8. Associa ion (linea eg ession) be ween changes in summe SST (x axis) and changes in CTI (y axis). L1: Malpica; L2: Cedei a; L3: Lua ca; L4: Las es; L5: San
Vicen e; L6: Somocue as; L7: Koba on; L8: Ea; L9: La He adu a; and L10: Cabo Palos.
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
9
da a makes i di icul o accu a ely calcula e species’ he mal op imum.
Howe e , Webb e al. (2020) al eady showed a s ong co ela ion be-
ween expe imen ally de i ed he mal maxima and he he mal a ini y
de i ed om ma ching global sea empe a u e da abases wi h occu -
ence eco ds. Ou s udy p o ided u he suppo o he use ulness o
global da ase s in calcula ing species’ he mal ai s. Gi en he speed
and scale a which communi ies a e shi ing, he use o global
open-access da abases should no be o e looked in his con ex o apid
clima e change. The in o ma ion in hose global da abases may help us
assess he ulne abili y o housands o species o global wa ming, ind
possible e ugees o cold-a ini y species, o p o ec hose species a
g ea e isk. In ou s udy a ea, we ound a loca ion in he cen al a ea o
he sou he n Bay o Biscay ha ope a ed as a e uge o cold-a ini y
species ha we e disappea ing a adjacen si es. This is pa icula ly
signi ican since many s udies p o ide e idence o a weakening in-
ensi y o he sou h-wes e n Bay o Biscay upwelling sys em associa ed
wi h changes in wind egimes (G´
omez-Ges ei a e al., 2011; Lemos and
Pi es, 2004; P´
e ez e al., 2010). The loss o he in luence o upwelling in
he sou he n Bay o Biscay could limi he dis ibu ion o kelp species o
locally colde and nu ien - iche habi a s.
In summa y, accu a e p edic ion o global change impac s on ma ine
ben hic communi ies is c ucial o ecosys em p ese a ion. Ou s udy
demons a ed ha sho - e m p edic ions based on Mugue za e al.’s
(2022a) model aligned wi h eal-wo ld obse a ions, building con i-
dence in p edic i e models. We obse ed de ia ions om he model,
shedding ligh on clima e-d i en communi y changes. Tempe a u e
eme ged as he p ima y d i e , wi h mac oalgal communi ies showing
apid esponses. Gi en he widesp ead deg ada ion o mac oalgal
communi ies wo ldwide, clima e-d i en mac oalgal phase shi s may be
a cu en eali y a he han a long- e m p edic ion. Tes ing ecological
models may be c ucial o p edic ing he impac s o global change on ou
na u al communi ies.
C edi au ho s a emen
Ola z A iaga: Concep ualiza ion, In es iga ion, Me hodology,
W i ing-O iginal D a , Visualiza ion. Paul Waw zynkowski: So wa e,
Da a Cu a ion, Fo mal analysis. Hec o Iba˜
nez: In es iga ion, Re-
sou ces. Nahia a Mugue za: In es iga ion, W i ing - Re iew & Edi ing.
Isabel Díez: In es iga ion, W i ing - Re iew & Edi ing. Isabel Pe ez-
Ruza a: In es iga ion, Resou ces. Jose Ma ía Go os iaga: Concep u-
aliza ion, In es iga ion, W i ing - Re iew & Edi ing, Supe ision,
Funding Acquisi ion, P ojec adminis a ion. Endika Quin ano: In es-
iga ion, W i ing - Re iew & Edi ing, Supe ision. Mikel Bece o:
Concep ualiza ion, Me hodology, W i ing - Re iew & Edi ing, Supe i-
sion, Funding Acquisi ion.
Decla a ion o compe ing in e es
The au ho s decla e ha hey ha e no known compe ing inancial
in e es s o pe sonal ela ionships ha could ha e appea ed o in luence
he wo k epo ed in his pape .
Da a a ailabili y
Da a will be made a ailable on eques .
Acknowledgemen s
This wo k was suppo ed by he DIVERSAT p ojec (Spanish Minis y
o Science, Inno a ion and Uni e si ies RTI2018-098970-B-I00) and he
Ca alan Go e nmen BEG 2017SGR-378.
The main au ho is inancially suppo ed by a Basque Go e nmen
p edoc o al g an (Re e ence N◦: PRE_2022_2_0127)
APPENDICES.
Appendix a. GPS posi ioning o he sampling loca ions
Loca ion La i ude Longi ude
L1: Malpica 43◦21
′
07.4
″
N 08◦49
′
52.2
″
W
L2: Cedei a 43◦39
′
48.8
″
N 08◦05
′
34.8
″
W
L3: Lua ca 43◦33
′
24.4
″
N 06◦32
′
50.4
″
W
L4: Las es 43◦31
′
09.4
″
N 05◦15
′
59.3
″
W
L5: San Vicen e de la Ba que a 43◦24
′
06.0
″
N 04◦23
′
59.4
″
W
L6: Somocue as 43◦28
′
15.1
″
N 03◦56
′
28.1
″
W
L7: Koba on 43◦21
′
11.2
″
N 03◦08
′
56.3
″
W
L8: Ea 43◦23
′
18.3
″
N 02◦34
′
57.7
″
W
L9: La He adu a 36◦44
′
07.4
″
N 03◦45
′
36.1
″
W
L10: Cabo Palos 37◦38
′
08.3
″
N 00◦41
′
17.5
″
W
Appendix b. Summe Sea Su ace Tempe a u e (SST) alues o he sampling yea s and he wo p e ious yea s o each loca ion
Summe SST (◦C)
Loca ions 2013 2014 2015 2017 2018 2019 2020
L1: Malpica 16.492 17.410 16.650 17.272 16.308 16.525 –
L2: Cedei a 17.120 17.686 17.046 17.504 15.889 16.980 –
L3: Lua ca 18.528 19.130 18.872 19.110 18.190 18.370 –
L4: Las es 19.827 20.490 19.862 19.919 20.109 20.058 –
L5: San Vicen e 20.498 20.846 20.323 20.429 21.036 20.741 –
L6: Somocue as 20.698 20.978 20.526 20.430 21.142 20.603 –
L7: Koba on 21.160 21.287 20.777 20.946 21.764 20.997 –
L8: Ea 21.582 21.869 21.400 21.229 22.217 21.590 –
L9: La He adu a 22.999 21.716 22.400 – 23.279 22.738 23.303
L10: Cabo Palos 24.926 25.683 25.952 – 26.144 25.703 25.716
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
16
Cos oya, X., deCas o, M., G´
omez-Ges ei a, M., San os, F., 2015. Changes in sea su ace
empe a u e seasonali y in he Bay o Biscay o e he las decades (1982–2014).
J. Ma . Sys . 150, 91–101. h ps://doi.o g/10.1016/j.jma sys.2015.06.002.
Day, P.B., S ua -Smi h, R.D., Edga , G.J., Ba es, A.E., 2018. Species’ he mal anges
p edic changes in ee ish communi y s uc u e du ing 8 yea s o ex eme
empe a u e a ia ion. Di e s. Dis ib. 24, 1036–1046. h ps://doi.o g/10.1111/
ddi.12753.
deCas o, M., G´
omez-Ges ei a, M., Al a ez, I., Ges ei a, J.L.G., 2009. P esen wa ming
wi hin he con ex o cooling–wa ming cycles obse ed since 1854 in he Bay o
Biscay. Con inen . Shel Res. 29 (8), 1053–1059. h ps://doi.o g/10.1016/j.
cs .2008.11.016.
De ic o , V., Jullia d, R., Cou e , D., Jigue , F., 2008. Bi ds a e acking clima e
wa ming, bu no as enough. P oceedings o he Royal Socie y B 275, 2743–2748.
h ps://doi.o g/10.1098/ spb.2008.0878.
De ic o , V., an Swaay, C., B e e on, T., B o ons, L., Chambe lain, D., Heli¨
ol¨
a, J.,
He ando, S., Jullia d, R., Kuussaa i, M., Linds ¨
om, Å., Rei , J., Roy, D.B.,
Schweige , O., Se ele, J., S e anescu, C., Van S ien, A., Van Tu nhou , C.,
Ve mouzek, Z., WallisDeV ies, M., Wynho , I., Jigue , F., 2012. Di e ences in he
clima ic deb s o bi ds and bu e lies a a con inen al scale. Na . Clim. Change 2,
121–124. h ps://doi.o g/10.1038/nclima e1347.
Díez, I., Mugue za, N., San ola ia, A., Ganzedo, U., Go os iaga, J.M., 2012. Seaweed
assemblage changes in he eas e n Can ab ian Sea and hei po en ial ela ionship o
clima e change. Es ua . Coas Shel Sci. 99, 108–120. h ps://doi.o g/10.1016/j.
ecss.2011.12.027.
D oue , K., Jauzein, C., He io -Hea h, D., Ha i i, S., Laza-Ma inez, A., Lecade , C.,
Plus, M., Seoane, S., Sou isseau, M., Lem´
ee, R., Siano, R., 2021. Cu en dis ibu ion
and po en ial expansion o he ha m ul ben hic dino lagella e Os eopsis c . siamensis
owa ds he wa ming wa e s o he Bay o Biscay, No h-Eas A lan ic. En i on.
Mic obiol. 23 (9), 4956–4979. h ps://doi.o g/10.1111/1462-2920.15406.
Falkenbe g, L.J., Russell, B.D., Connell, S.D., 2013. Con as ing esou ce limi a ions o
ma ine p ima y p oduce s: implica ions o compe i i e in e ac ions unde en iched
CO2 and nu ien egimes. Oecologia 172, 575–583. h ps://doi.o g/10.1007/
s00442-012-2507-5.
Fe n´
andez, C., 2016. Cu en s a us and mul idecadal biogeog aphical changes in ocky
in e idal algal assemblages: he no he n Spanish coas . Es ua ine. Coas al Shel Sci.
171, 35–40. h ps://doi.o g/10.1016/j.ecss.2016.01.026.
Fe n´
andez, C., 2011. The e ea o la ge b own seaweeds on he no h coas o Spain: he
case o Sacco hiza polyschides. Eu . J. Phycol. 46, 352–360. h ps://doi.o g/10.1080/
09670262.2011.617840.
Fe n´
andez-Salas, L.M., Du ´
an, R., Mendes, I., Galpa so o, I., Lobo, F.J., B´
a cenas, P.,
Rosa, F., Rib´
o, M., Ga cía-Gil, S., Fe ín, A., Ca a a, G., Roque, C., Canals, M., 2015.
Shel es o he ibe ian Peninsula and he balea ic islands (I): mo phology and
sedimen ypes. Bol. Geol. Min. 126, 327–376.
Filbee-Dex e , K., We nbe g, T., 2018. Rise o u s: a new ba le on o globally
declining kelp o es s. Bioscience 68 (2), 64–76. h ps://doi.o g/10.1093/biosci/
bix147.
Flanagan, P.H., Jensen, O.P., Mo ley, J.W., Pinsky, M.L., 2019. Response o ma ine
communi ies o local empe a u e changes. Ecog aphy 42, 214–224. h ps://doi.o g/
10.1111/ecog.03961.
Ga cía, A.G., Olaba ia, C., Al a ez-Losadaa, O., Viejo, R.M., 2021. Di e en ial esponses
o ailing-edge popula ions o a ounda ion alga o he mal s es. Eu . J. Phycol. 56
(4), 373–388. h ps://doi.o g/10.1080/09670262.2020.1842909.
GBIF.o g, 2022. GBIF home page. h ps://www.gbi .o g.
G´
omez-Ges ei a, M., deCas o, M., Al a ez, I., G´
omez-Ges ei a, J.L., 2008. Coas al sea
su ace empe a u e wa ming end along he con inen al pa o he A lan ic A c
(1985–2005). J. Geophys. Res. 113, C04010 h ps://doi.o g/10.1029/
2007JC004315.
G´
omez-Ges ei a, M., Gimeno, L., deCas o, M., Lo enzo, M., Al a ez, I., Nie o, R.,
Taboada, J., C espo, A., Ramos, A., Iglesias, I., G´
omez-Ges ei a, J., San o, F.,
Ba ioped o, D., T igo, I., 2011. The s a e o clima e in NW Ibe ia. Clim. Res. 48,
109–144. h ps://doi.o g/10.3354/c 00967.
Gonz´
alez-Gil, R., Gonz´
alez Taboada, F., C´
ace es, C., La gie , J.L., Anad´
on, R., 2018.
Win e -mixing p econdi ioning o he sp ing phy oplank on bloom in he Bay o
Biscay. Limnol. Oceanog . 63, 1264–1282. h ps://doi.o g/10.1002/lno.10769.
Go os iaga, J.M., 1995. Subli o al seaweed ege a ion o a e y exposed sho e on he
Basque Coas (N. Spain). Bo . Ma . 38 h ps://doi.o g/10.1515/bo m.1995.38.1-6.9.
Go ied, M., Pauli, H., Fu schik, A., Akhalka si, M., Ba anˇ
cok, P., Beni o Alonso, J.L.,
Coldea, G., Dick, J., E schbame , B., Fe n´
andez Calzado, M.R., Kazakis, G., K ajˇ
ci, J.,
La sson, P., Mallaun, M., Michelsen, O., Moisee , D., Moisee , P., Molau, U.,
Me zouki, A., Nagy, L., Nakhu s ish ili, G., Pede sen, B., Pelino, G., Puscas, M.,
Rossi, G., S anisci, A., Theu illa , J.-P., Tomaselli, M., Villa , L., Vi oz, P.,
Vogia zakis, I., G abhe , G., 2012. Con inen -wide esponse o moun ain ege a ion
o clima e change. Na . Clim. Change 2, 111–115. h ps://doi.o g/10.1038/
nclima e1329.
G aba-Land y, A.C., Lo le , Z., McClu e, E.C., P a che , M.S., Hoey, A.S., 2020.
Impai ed g ow h and su i al o opical mac oalgae (Sa gassum spp.) a ele a ed
empe a u es. Co al Ree s 39, 475–486. h ps://doi.o g/10.1007/s00338-020-
01909-7.
Gui y, M.D., Gui y, G.M., 2023. AlgaeBase. Wo ldwide Elec onic Publica ion. Na ional
Uni e si y o I eland, Galway. h ps://www.algaebase.o g. sea ched on 12 Janua y
2023.
Ha ley, C.D.G., Ande son, K.M., Demes, K.W., Jo e, J.P., Ko das, R.L., Coyle, T.A.,
G aham, M.H., 2012. E ec s o clima e change on global seaweed communi ies.
J. Phycol. 48, 1064–1078. h ps://doi.o g/10.1111/j.1529-8817.2012.01224.x.
Husa, V., Sjø un, K., B a enbo g, N., Lein, T.E., 2008. Changes o mac oalgal di e si y in
subli o al si es in sou hwes No way: impac o an in oduced species o highe
empe a u e? Ma . Biol. Res. 4, 414–428. h ps://doi.o g/10.1080/
17451000802232874.
IPCC, 2023. AR6 Syn hesis Repo : Clima e Change 2023. Syn hesis Repo o he IPCC
Six h Assessmen Repo (AR6): Summa y o Policymake s.
Izquie do, P., Rico, J.M., Taboada, F.G., Gonz´
alez-Gil, R., A on es, J., 2022.
Cha ac e iza ion o ma ine hea wa es in he Can ab ian Sea, SW bay o Biscay.
Es ua ine. Coas al Shel Sci. 274, 107923 h ps://doi.o g/10.1016/j.
ecss.2022.107923.
Jian-Zhang, S., Xiu-Ren, N., Feng-Feng, L., Wan-Dong, C., Ding-Gen, Z., 2010. Long e m
changes o biodi e si y o ben hic mac oalgae in he in e idal zone o he Nanji
Islands. Ac a Ecol. Sin. 30, 106–112. h ps://doi.o g/10.1016/j.chnaes.2010.03.010.
Ko sch, S., P imice io, R., Fossheim, M., Dolgo , A.V., Aschan, M., 2015. Clima e change
al e s he s uc u e o a c ic ma ine ood webs due o polewa d shi s o bo eal
gene alis s. P oceedings o he Royal Socie y B 282, 20151546. h ps://doi.o g/
10.1098/ spb.2015.1546.
Kumagai, N.H., Ga cía Molinos, J., Yamano, H., Takao, S., Fujii, M., Yamanaka, Y., 2018.
Ocean cu en s and he bi o y d i e mac oalgae- o-co al communi y shi unde
clima e wa ming. P oc. Na . Acad. Sci. U.S.A. 115, 8990–8995. h ps://doi.o g/
10.1073/pnas.1716826115.
La ín, A., Vald´
es, L., S´
anchez, F., Abaunza, P., Fo es , A., Bouche , J., Lazu e, P., Anne
Jegou, A.M., 2006. The Bay o Biscay: he encoun e ing o he ocean and he shel .
In: Robinson, A.R., B ink, K.H. (Eds.), The Global Coas al Ocean: In e disciplina y
Regional S udies and Syn heses. Ha a d P ess, pp. 933–999.
Lazza i, P., Solido o, C., Salon, S., Bolzon, G., 2016. Spa ial a iabili y o phospha e and
ni a e in he Medi e anean Sea: a modeling app oach. Deep-Sea Res. Pa I
Oceanog . Res. Pap. 108, 39–52. h ps://doi.o g/10.1016/j.ds .2015.12.006.
Lemos, R.T., Pi es, H.O., 2004. The upwelling egime o he Wes Po uguese Coas ,
1941–2000. In . J. Clima ol. 24, 511–524. h ps://doi.o g/10.1002/joc.1009.
Lindsey, R., Dahlman, L., 2022. Na ional cen e o a mosphe ic esea ch. Clim. Change:
Global Tempe a u e.
Lou enço, C.R., Za di, G.I., McQuaid, C.D., Se ˜
ao, E.A., Pea son, G.A., Jacin o, R.,
Nicas o, K.R., 2016. Upwelling a eas as clima e change e ugia o he dis ibu ion
and gene ic di e si y o a ma ine mac oalga. J. Biogeog . 43, 1595–1607. h ps://
doi.o g/10.1111/jbi.12744.
McLean, M., Mouillo , D., Mau eaud, A.A., Ha ab, T., MacNeil, M.A., Gobe ille, E.,
Lindeg en, M., Engelha d, G., Pinsky, M., Aube , A., 2021. Disen angling
opicaliza ion and debo ealiza ion in ma ine ecosys ems unde clima e change.
Cu . Biol. 31, 4817–4823.e4815. h ps://doi.o g/10.1016/j.cub.2021.08.034.
Me chan , C.J., Embu y, O., Bulgin, C.E., Block, T., Co le , G.K., Fiedle , E., Good, S.A.,
Mi az, J., Rayne , N.A., Be y, D., Eas wood, S., Taylo , M., Tsushima, Y.,
Wa e all, A., Wilson, R., Donlon, C., 2019. Sa elli e-based ime-se ies o sea-su ace
empe a u e since 1981 o clima e applica ions. Sci. Da a 6, 223. h ps://doi.o g/
10.1038/s41597-019-0236-x.
Mon ei o, C., Pe ei a, J., Seab a, R., Lima, F.P., 2022. Fine-scale su ey o in e idal
mac oalgae e eals ecen changes in a cold-wa e biogeog aphic s onghold. F on .
Ma . Sci. 9, 880074 h ps://doi.o g/10.3389/ ma s.2022.880074.
Mugue za, N., A iaga, O., Díez, I., Bece o, M.A., Quin ano, E., Go os iaga, J.M., 2022a.
A spa ially-modelled snapsho o u u e ma ine mac oalgal assemblages in sou he n
Eu ope: owa ds a b oade Medi e anean egion? Ma . En i on. Res. 176, 105592
h ps://doi.o g/10.1016/j.ma en es.2022.105592.
Mugue za, N., Díez, I., Quin ano, E., Bus aman e, M., Go os iaga, J.M., 2017. S uc u al
impo e ishmen o he sub idal ege a ion o sou heas e n Bay o Biscay om 1991
o 2013 in he con ex o clima e change. J. Sea Res. 130, 166–179. h ps://doi.o g/
10.1016/j.sea es.2017.06.006.
Mugue za, N., Díez, I., Quin ano, E., Go os iaga, J.M., 2022b. Decades o biomass loss in
he shallow ocky sub idal ege a ion o he sou heas e n Bay o Biscay. Ma .
Biodi e s. 52, 28. h ps://doi.o g/10.1007/s12526-022-01268-2.
Mülle , R., Laepple, T., Ba sch, I., Wiencke, C., 2009. Impac o oceanic wa ming on he
dis ibu ion o seaweeds in pola and cold- empe a e wa e s. Bo . Ma . 52, 617–638.
h ps://doi.o g/10.1515/BOT.2009.080.
Mu˜
niz, O., Rod íguez, J.G., Re illa, M., Laza-Ma ínez, A., Seoane, S., F anco, J., 2018.
Seasonal a ia ions o phy oplank on communi y in ela ion o en i onmen al
ac o s in an oligo ophic a ea o he Eu opean A lan ic coas (sou heas e n Bay o
Biscay). Regional S udies in Ma ine Science 17, 59–72. h ps://doi.o g/10.1016/j.
sma.2017.11.011.
NOAA Na ional Cen e s o En i onmen al In o ma ion, 2022. Mon hly Global Clima e
Repo o Annual published online Janua y 2023. h ps://www.ncei.noaa.go /
access/moni o ing/mon hly- epo /global/202213. (Accessed 11 Ap il 2023).
OBIS, 2022. Ocean Biodi e si y In o ma ion Sys em. In e go e nmen al Oceanog aphic
Commission o UNESCO. www.obis.o g.
O anidis, S., 1991. Tempe a u e esponses and dis ibu ion o mac oalgae belonging o
he wa m- empe a e Medi e anean-A lan ic dis ibu ion g oup. Bo . Ma . 34, 12.
h ps://doi.o g/10.1515/bo m.1991.34.6.541.
O lando-Bonaca, M., Pi acco, V., Lipej, L., 2021. Loss o canopy- o ming algal ichness
and co e age in he no he n Ad ia ic Sea. Ecol. Indica . 125, 107501 h ps://doi.
o g/10.1016/j.ecolind.2021.107501.
Ospina-Al a ez, N., P ego, R., ´
Al a ez, I., deCas o, M., ´
Al a ez-Osso io, M.T., Pazos, Y.,
Campos, M.J., Be n´
a dez, P., Ga cia-So o, C., G´
omez-Ges ei a, M., Va ela, M., 2010.
Oceanog aphical pa e ns du ing a summe upwelling-downwelling e en in he
no he n Galician ias: compa ison wi h he whole ia sys em (NW o Ibe ian
Peninsula). Con inen . Shel Res. 30, 1362–1372. h ps://doi.o g/10.1016/j.
cs .2010.04.018.
Pa mesan, C., Yohe, G., 2003. A globally cohe en inge p in o clima e change impac s
ac oss na u al sys ems. Na u e 421, 37–42. h ps://doi.o g/10.1038/na u e01286.
P´
e ez, F.F., Padín, X.A., Pazos, Y., Gilco o, M., Cabanas, M., Pa do, P.C., Do al, M.D.,
Fa ina-Bus o, L., 2010. Plank on esponse o weakening o he Ibe ian coas al
O. A iaga e al.
Ma ine En i onmen al Resea ch 190 (2023) 106098
17
upwelling. Global Change Biol. 16, 1258–1267. h ps://doi.o g/10.1111/j.1365-
2486.2009.02125.x.
Pe kol-Finkel, S., Ai oldi, L., 2010. Loss and eco e y po en ial o ma ine habi a s: an
expe imen al s udy o ac o s main aining esilience in sub idal algal o es s a he
Ad ia ic Sea. PLoS One 5, e10791. h ps://doi.o g/10.1371/jou nal.pone.0010791.
Pinsky, M.L., Selden, R.L., Ki chel, Z.J., 2020. Clima e-d i en shi s in ma ine species
anges: scaling om o ganisms o communi ies. Ann. Re . Ma . Sci 12, 153–179.
h ps://doi.o g/10.1146/annu e -ma ine-010419-010916.
Poloczanska, E.S., B own, C.J., Sydeman, W.J., Kiessling, W., Schoeman, D.S., Moo e, P.
J., B ande , K., B uno, J.F., Buckley, L.B., Bu ows, M.T., Dua e, C.M., Halpe n, B.S.,
Holding, J., Kappel, C.V., O’Conno , M.I., Pandol i, J.M., Pa mesan, C., Schwing, F.,
Thompson, S.A., Richa dson, A.J., 2013. Global imp in o clima e change on ma ine
li e. Na . Clim. Change 3, 919–925. h ps://doi.o g/10.1038/nclima e1958.
P o oos , P., Bosch, S., 2019. " obis: R Clien o Access Da a om he OBIS API." Ocean
Biogeog aphic In o ma ion Sys em. In e go e nmen al Oceanog aphic Commission
o UNESCO. R package e sion 2.1.8. h ps://c an. -p ojec .o g/package= obis.
R De elopmen Co e Team, 2023. R: A Language and En i onmen o S a is ical
Compu ing. R Founda ion o S a is ical Compu ing, Vienna, Aus ia. URL, A ailable
a : h ps://www.R-p ojec .o g/.).
Ramos, E., Guinda, X., Puen e, A., de la Hoz, C.F., Juanes, J.A., 2020. Changes in he
dis ibu ion o in e idal mac oalgae along a longi udinal g adien in he no he n
coas o Spain. Ma . En i on. Res. 157, 104930 h ps://doi.o g/10.1016/j.
ma en es.2020.104930.
Rhein, M., Rin oul, S.R., Aoki, S., Campos, E., Chambe s, D., Feely, R.A., Gule , S.,
Johnson, G.C., Josey, S.A., Kos ianoy, A., Mau i zen, C., Roemmich, D., Talley, L.D.,
Wang, F., 2013. Obse a ions: ocean. In: S ocke , T.F., Qin, D., Pla ne , G.-K.,
Tigno , M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P.M.
(Eds.), Clima e Change 2013: he Physical Science Basis. Con ibu ion o Wo king
G oup I o he Fi h Assessmen Repo o he In e go e nmen al Panel on Clima e
Change. Camb idge Uni e si y P ess, Camb idge, Uni ed Kingdom and New Yo k,
NY, USA.
R¨
onnb¨
ack, P., Kau sky, N., Pihl, L., T oell, M., S¨
ode q is , T., Wennhage, H., 2007.
Ecosys em goods and se ices om Swedish coas al habi a s: iden i ica ion,
alua ion, and implica ions o ecosys em shi s. AMBIO A J. Hum. En i on. 36,
534–544. h ps://doi.o g/10.1579/0044-7447(2007)36[534:EGASFS]2.0.CO;2.
RS udio Team, 2016. RS udio. In eg a ed de elopmen o R. RS udio, Inc., Bos on, MA.
h p://www. s udio.com/.
Se e , P., Fe n´
andez, E., Sos es, J.A., Anad´
on, R., 1999. Seasonal compensa ion o
mic obial p oduc ion and espi a ion in a empe a e sea. Ma . Ecol. P og. Se . 187,
43–57. h ps://doi.o g/10.3354/MEPS187043.
Shal ou , M., Oms ed , A., 2014. Recen sea su ace empe a u e ends and u u e
scena ios o he Medi e anean Sea. Oceanologia 56, 411–443. h ps://doi.o g/
10.5697/oc.56-3.411.
Sjø un, K., Husa, V., Asplin, L., Sand ik, A., 2015. Clima ic and en i onmen al ac o s
in luencing occu ence and dis ibu ion o mac oalgae - a jo d g adien e isi ed.
Ma . Ecol. P og. Se . 532, 73–88. h ps://doi.o g/10.3354/meps11341.
Smale, D.A., We nbe g, T., 2013. Ex eme clima ic e en d i es ange con ac ion o a
habi a - o ming species. P oceedings o he Royal Socie y B 280, 20122829. h ps://
doi.o g/10.1098/ spb.2012.2829.
S elle , D., He nandez-Ay´
on, J., Riosmena-Rod íguez, R., Cabello-Pasini, A., 2007. E ec
o empe a u e on pho osyn hesis, g ow h and calci ica ion a es o he ee-li ing
co alline alga Li hophyllum ma ga i ae. Cienc. Ma . 33, 441–456. h ps://doi.o g/
10.7773/cm. 33i4.1255.
S eneck, R.S., G aham, M.H., Bou que, B.J., Co be , D., E landson, J.M., Es es, J.A.,
Tegne , M.J., 2002. Kelp o es ecosys ems: biodi e si y, s abili y, esilience and
u u e. En i on. Conse . 29, 436–459. h ps://doi.o g/10.1017/
S0376892902000322.
S ua -Smi h, R.D., Edga , G.J., Ba e , N.S., Kininmon h, S.J., Ba es, A.E., 2015.
The mal biases and ulne abili y o wa ming in he wo ld’s ma ine auna. Na u e
528, 88–92. h ps://doi.o g/10.1038/na u e16144.
Ti enso , D.P., Mo a, C., Je z, W., Lo ze, H.K., Rica d, D., Be ghe, E.V., Wo m, B., 2010.
Global pa e ns and p edic o s o ma ine biodi e si y ac oss axa. Na u e 466,
1098–1101. h ps://doi.o g/10.1038/na u e09329.
Valdes-Abellan, J., Pa do, M.A., Tenza-Ab il, A.J., 2017. Obse ed p ecipi a ion end
changes in he wes e n Medi e anean egion: obse ed p ecipi a ion ends in
wes e n Medi e anean. In . J. Clima ol. 37, 1285–1296. h ps://doi.o g/10.1002/
joc.4984.
Valencia, V., F anco, J., Bo ja, A., Fon ´
an, A., 2004. Hyd og aphy o he sou h-eas e n
bay o Biscay. In: Bo ja, A., Collins, M. (Eds.), Oceanog aphy and Ma ine
En i onmen o he Basque Coun y, ol. 70. Else ie Oceanog aphy Se ies,
pp. 159–187. h ps://doi.o g/10.1016/S0422-9894(04)80045-X.
Ve g´
es, A., S einbe g, P.D., Hay, M.E., Poo e, A.G.B., Campbell, A.H., Balles e os, E.,
Heck, K.L., Boo h, D.J., Coleman, M.A., Fea y, D.A., Figuei a, W., Langlois, T.,
Ma zinelli, E.M., Mize ek, T., Mumby, P.J., Nakamu a, Y., Roughan, M., an
Sebille, E., Gup a, A.S., Smale, D.A., Tomas, F., We nbe g, T., Wilson, S.K., 2014. The
opicaliza ion o empe a e ma ine ecosys ems: clima e-media ed changes in
he bi o y and communi y phase shi s. P oceedings o he Royal Socie y B 281,
20140846. h ps://doi.o g/10.1098/ spb.2014.0846.
Voe man, S.E., Lle a, E., Rico, J.M., 2013. Clima e d i en changes in sub idal kelp o es
communi ies in NW Spain. Ma . En i on. Res. 90, 119–127. h ps://doi.o g/
10.1016/j.ma en es.2013.06.006.
Webb, T.J., Lines, A., Howa h, L.M., 2020. Occupancy-de i ed he mal a ini ies e lec
known physiological he mal limi s o ma ine species. Ecol. E ol. 10, 7050–7061.
h ps://doi.o g/10.1002/ece3.6407.
We nbe g, T., Benne , S., Babcock, R.C., de Be ignies, T., Cu e, K., Depczynski, M.,
Du ois, F., F omon , J., Ful on, C.J., Ho ey, R.K., Ha ey, E.S., Holmes, T.H.,
Kend ick, G.A., Rad o d, B., San ana-Ga con, J., Saunde s, B.J., Smale, D.A.,
Thomsen, M.S., Tucke , C.A., Tuya, F., Vande kli , M.A., Wilson, S., 2016. Clima e-
d i en egime shi o a empe a e ma ine ecosys em. Science 353, 169–172. h ps://
doi.o g/10.1126/science.aad8745.
O. A iaga e al.
