Pelagic habi a and o sp ing su i al in he eas e n s ock o
A lan ic bluefin una
Pa icia Regle o
1,
*, Rosa Balbı´n
1
, F anciso Ja ie Abascal
2
, An onio Medina
3
,
Diego Al a ez-Be as egui
4
, Lei Rasmuson
5,6
, Bap is e Mou e
4
,Sa´ma Sabe
7
, Au elio O ega
8
,
Edu ne Blanco
1
, Fe nando de la Ga´nda a
8
, F anciso Ja ie Alemany
1
, G. Wal e Ing am J
9
, and
Manuel Hidalgo
1
1
Ins i u o Espa~
nol de Oceanog a ı´a, Cen e Oceanog a`fic de les Balea s, Ecosys em Oceanog aphy G oup (GRECO), Moll de Ponen s/n, 07015
Palma de Mallo ca, Spain
2
Cen o Oceanog a´fico de Cana ias, Ins i u o Espa~
nol de Oceanog a ı´a, 38180 San a C uz de Tene i e, Spain
3
Depa amen o de Biologı´a, Facul ad de Ciencias del Ma y Ambien ales, A da. Repu´blica Saha aui, s/n, 11510 Pue o Real, Ca´diz, Spain
4
Balea ic Islands Coas al Obse ing and Fo ecas ing Sys em, Pa c Bi , Nao e, Bloc A 28p. p a 3, Palma de Mallo ca, Balea ic Islands, Spain
5
Ma ine Resou ces P og am, O egon Depa men o Fish and Wildli e, 2040 SE Ma ine Science D i e, Newpo , OR, USA
6
NOAA, Na ional Ma ine Fishe ies Se ice, Sou heas Fishe ies Science Cen e , Miami Labo a o ies, 75 Vi ginia Beach D i e, Miami, FL, USA
7
Ins i u o Espa~
nol de Oceanog a ı´a, Cen o Oceanog a´fico de Ma´laga, Pue o Pesque o, s/n, 29640 Fuengi ola, Spain
8
Ins i u o Espa~
nol de Oceanog a ı´a, Cen o Oceanog a´fico de Mu cia, 30860 Pue o de Maza o´n, Mu cia, Spain
9
NOAA, Na ional Ma ine Fishe ies Se ice, Sou heas Fishe ies Science Cen e , Mississippi Labo a o ies, 3209 F ede ic S ee , Pascagoula, MS 39567, USA
*Co esponding au ho : el: þ34 971 133 720; e-mail: [email p o ec ed].
Regle o, P., Balbı´n, R., Abascal, F. J., Medina, A., Al a ez-Be as egui, D., Rasmuson, L., Mou e, B., Sabe , S., O ega, A., Blanco, E., de la Ga´nda a,
F., Alemany, F. J., Ing am, G. W., Hidalgo, M. Pelagic habi a and o sp ing su i al in he eas e n s ock o A lan ic bluefin una. – ICES Jou nal
o Ma ine Science, doi:10.1093/icesjms/ sy135.
Recei ed 14 Ma ch 2018; e ised 16 Augus 2018; accep ed 20 Augus 2018.
In his manusc ip , we es how an unde s anding o geog aphical a ia ion in la al fi ness in ela ion o empe a u e and habi a use could be a use ul
me hod o imp o e ou unde s anding o ec ui men and de elop be e indices o annual ec ui men . On he basis o he assump ion ha g ow h
and su i al o una la ae a e influenced by empe a u e, we ha e de eloped a po en ial la al su i al index o A lan ic bluefin una (Thunnus hyn-
nus) by combining empi ical da a om egg and la al ea ing expe imen s wi h empe a u e da a om hyd odynamic models. The expe imen s we e
designed o es he ull ange o empe a u e a iabili y ha bluefin la ae would expe ience in he field and p o ide a mechanis ic unde s anding o
he p ocesses d i ing egg and la al su i al. We hen de eloped a biological model using he empe a u e- ela ed g ow h exp essions and a size-
dependen su i al unc ion o he la ae. The biological model was applied o a ime-se ies o spa ially explici empe a u e da a o he wes e n
Medi e anean om he S ai o Gib al a o 6E, which includes he majo ecognized bluefin una eas e n s ock spawning a ea, he Balea ic Sea. Ou
esul s show ha a eas wi h high p obabili ies o la al su i al coincide wi h hose ha would be conside ed as op imal based on o he da a sou ces
(ich hyoplank on su eys, spawning emale loca ions om comme cial fishe ies da a, and adul acking da a). Howe e , e idence o spawning has
been ound in a eas wi h subop imal he mal habi a s, as p edic ed by he model, which we discuss ega ding sampling e o and salini y on s. The e
was a good ma ch be ween he su i al index and ec ui men indices om s anda dized CPUE fishe ies da a. These esul s ha e implica ions o ou
unde s anding o he ec ui men p ocess o he eas e n s ock o A lan ic bluefin una, since hey sugges ha he combined e ec s o empo al and
spa ial a iabili y o he en i onmen d i e ec ui men success, which has impo an implica ions o he managemen o he species.
Keywo ds: A lan ic bluefin una, fish la ae ec ui men , Medi e anean Sea, spawning s ock, empe a u e
V
CIn e na ional Council o he Explo a ion o he Sea 2018. All igh s ese ed.
Fo pe missions, please email: [email p o ec ed]
ICES Jou nal o Ma ine Science (2018), doi:10.1093/icesjms/ sy135
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In oduc ion
The en i onmen s in which ish ep oduce usually p o ide
a ou able ood condi ions o he la ae, sui able empe a u es
o egg and la al de elopmen , and/o sui able e en ion a eas
(Mullon e al., 2002). Gi en he di icul ies in di ec ly s udying
bo h spawning and ec ui men p ocesses o many species, pa -
icula ly la ge pelagic ish, a knowledge o he e ec s o en i on-
men al a iabili y on egg and la al g ow h and su i al a es can
be used al e na i ely o o ecas spawning loca ions, ep oduc i e
ou pu , and/o ec ui men s eng h. Mos ishe ies assessmen
models and much o ishe ies heo y is p edica ed on a ela ion-
ship be ween he numbe o spawne s and he e en ual ec ui s
ha hey p oduce. Al hough he e is s ong e idence o en i on-
men ally d i en ec ui men (Ve -P e e al., 2013;Szuwalski
e al., 2015), en i onmen al in o ma ion is a ely included in
s ock assessmen s o la ge pelagic ish. Unde s anding and moni-
o ing he physical and biological p ocesses ha con ol ec ui -
men , he ecological co ne s one o de e mining ish popula ion
dynamics, is essen ial o imp o ing cu en ishe ies s ock assess-
men s. Pa icula ly, he e is a need o ake in o accoun geog aph-
ical a iabili y in o sp ing i ness i spa ial managemen decisions
a e o be aken in he u u e (Be ge e al., 2017).
A lan ic blue in una (Thunnus hynnus) a e managed by he
In e na ional Commission o he Conse a ion o A lan ic Tunas
(ICCAT) as wo sepa a e s ocks: an eas e n and a wes e n s ock.
As wi h mos assessed ish, es ima es o ec ui men and he unc-
ional shape o he s ock– ec ui ela ionship a e majo sou ces o
unce ain y. The e is no consensus among expe s on which ype
o s ock– ec ui ela ionship o use, and ends in ec ui men o
he wo s ocks ha e been sugges ed o be co ela ed ei he wi h
spawning biomass o en i onmen al a iabili y (e.g. see e e ences
in Po ch and Lau e a, 2016). Fo he eas e n s ock, he unc ional
o m o he s ock– ec ui ela ionship emains elusi e, as e i-
denced by he clea asynch onous luc ua ion be ween spawning
biomass and ec ui men a a mul idecadal scale (Anonymous,
2017;Figu e 1), wi h high spawning biomass being associa ed
wi h low ec ui men e en s un il he 1990s, low spawning bio-
mass associa ed wi h high ec ui men e en s du ing he 1990–
2000s, and again high spawning biomass associa ed wi h low e-
c ui men e en s since 2008. On he o he hand, he inc easing
end in annual ec ui men om he 1970s o he ea ly 2000s has
been ela ed o inc easing summe empe a u es in he
Balea ic Sea (Ha o d e al., 2017), which sugges s a signi ican
en i onmen – ec ui men ela ionship. Howe e , he scena io
seems o be mo e complex since es ima es om he la es assess-
men show ha ec ui men is dec easing despi e he con inual
wa ming end (Anonymous, 2017;Figu e 1). This scena io sug-
ges s a po en ial densi y-dependen con ol a la ge empo al
scales ha , in combina ion wi h la ge-scale inc easing ends in
wa e empe a u e due o clima e wa ming in he Medi e anean,
may explain long- e m luc ua ions in ec ui men . Howe e ,
sho - e m a ia ions, pa icula ly he in e annual a ia ion ha
has occu ed in he las decade, challenge he hypo hesis o a di-
ec he mal in luence on in e annual a iabili y in ec ui men
(Figu e 1).
The cu en challenge o de eloping a model o he ec ui -
men dynamics o A lan ic blue in una is o unde s and he
mechanis ic in luence o egional en i onmen al d i e s ha link
spa ial pa e ns o la al pe o mance o in e annual a iabili y in
ec ui men . We applied labo a o y-de i ed, empe a u e-
dependen g ow h and su i al ela ionships o A lan ic blue in
una eggs and la ae o empe a u e eco ds om he wes e n
Medi e anean du ing he spawning season. We hen used hese
da a o de elop an annual index o po en ial la al su i al in one
o he p ima y spawning a eas o he eas e n s ock o A lan ic
blue in una. We es ed he hypo hesis ha he mal condi ions
which p omo e g ow h and su i al o A lan ic blue in eggs and
la ae coincide wi h he loca ion o a majo spawning g ound
a ound he Balea ic Islands in he wes e n Medi e anean basin.
Fu he , we hypo hesize ha hese he mal condi ions a e associ-
a ed wi h empo al a ia ion in annual ec ui men . We
compa ed ou index o a ailable indices o ec ui men om
ishe ies-dependen da a. Ou inal goal was o p oduce
mechanis ic-based knowledge ha will allow scien is s o include
en i onmen al a iabili y and i s spa ial ends in o u u e s ock
assessmen s o A lan ic blue in una.
Ma e ial and me hods
S udy si e and ime-se ies
A lan ic blue in una a e managed sepa a ely as wo s ocks.
The eas e n s ock is de ined as being eas o he 45W me idian
(Figu e 2a). This s udy ocuses on he wes e n Medi e anean
po ion o he eas e n s ock (Figu e 2b). The majo spawning and
b eeding a ea o he eas e n s ock o A lan ic blue in una
(Alemany e al., 2010;Ha o d e al., 2017) is he Balea ic Sea, lo-
ca ed in he cen e o he wes e n hal o he wes e n
Medi e anean Sea (Figu e 2c). The da a analysed in his s udy
we e om 2000 o 2014, he same yea s o which de ailed moni-
o ing o he spa ial dis ibu ion o la ae, spawne s, and acking
da a o A lan ic blue in una in he wes e n Medi e anean we e
a ailable o compa ison o he model esul s. This ime-se ies
includes yea s wi h a iabili y in he mal condi ions, ec ui men ,
and spawning-s ock biomass (Figu e 1).
Time-se ies o spa ially explici en i onmen al da a
The selec ion o en i onmen al da a o use in his s udy was based
on he abili y o he a ailable oceanog aphic models o ep oduce
he CTD obse a ions collec ed du ing 2000–2014. Using da a
om summe 2004, 72 CTD obse a ions (Alemany e al., 2010)
we e compa ed wi h empe a u e and salini y ields a 5-m dep h
om ou di e en oceanog aphic models o es how well he
models ep esen ed he spa ial a iabili y o hese a iables. The
ou di e en models include wo e sions o he Medi e anean
model a ailable om he Cope nicus Ma ine Se ice (CMEMS-
MED e sion 02 and s 03, h p://ma ine.cope nicus.eu), he
GLORYS2V1 e sion o MERCATOR (h ps://www.me ca o -
ocean. ), and he MEDAR-MEDATLAS summe clima ological
alues. Model da a we e ex ac ed om he g id-poin ha con-
ained he CTD s a ion. In his way, i was possible o cons uc a
ime-se ies o each model. The ou model ime-se ies we e com-
pa ed wi h he CTD obse a ions using a Taylo diag am (Taylo ,
2001). Dynamic heigh (DH) was calcula ed by e ically in eg a -
ing he speci ic olume ob ained om he CTD da a, using 600 m
as he le el o no mo ion, as desc ibed by Balbı´n e al. (2014). The
same me hodology was applied o he model and clima ological
da a.
2P. Regle o e al.
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Compa ison o empe a u es om he model da a o CTD
obse a ions indica es ha bo h o he CMEMS-MED model e -
sions we e he bes a eplica ing he spa ial pa e n o he CTD
obse a ions (wi h a co ela ion coe icien close o 0.9 and
a cen ed Roo -Mean-Squa e di e ence a ound 0.4)
(Supplemen a y Figu e S1). This indica es ha he ho izon al
s uc u e o empe a u e a iabili y was well eplica ed. In he
case o salini y, he MEDAR-MEDATLAS clima ological alues
we e he mos s ongly co ela ed wi h he obse a ions (wi h a
co ela ion coe icien o 0.6), while he CMEMS-MED models
p esen alues o only a ound 0.4 and a cen ed Roo -Mean-
Squa e di e ence a ound 0.3(Supplemen a y Figu e S2).
The e o e, salini y was no well ep esen ed in he models and
could no be used o calcula ions o he loca ion o on al a eas.
Taylo analysis o DH showed ha obse a ions om he
MEDAR-MEDATLAS we e co ela ed wi h obse a ions, wi h
co ela ion coe icien s o 0.65, and o all he o he models wi h
co ela ions coe icien s below 0.35 ( esul s no shown).
The e o e, he DH o mesoscale s uc u es was no well ep e-
sen ed in he models, demons a ing ha geos ophic cu en s
de i ed om he models we e no usable o de ailed calcula ions
o possible d i e ec s. As such, only empe a u e da a we e well
ep esen ed by he a ailable models o he pe iod o s udy
(2000–2014) and, he e o e, only he empe a u e model om
CMEMS-MED was used.
We compa ed he a e age empe a u e be ween 1 and 15 June
each yea om 2002 o 2014 in an a ea cen ed in he Balea ic
Islands (0.5–4.5E 38.2–40.5N) using he CMEMS-MED model
and sa elli e da a (L4 JPL MUR p oduc , only a ailable since
2002). This compa ison shows ha he CMEMS-MED model
eplica es e y well he in e annual a iabili y o empe a u e in
he a ea (Supplemen a y Figu e S3). The e o e, he model can be
used o model he empo al and spa ial a ia ions in empe a u e.
Gi en he low capabili y o he model o ep esen salini y, we
used maps o salini y de i ed om ield c uises o in es iga e he
dis ibu ion o la ae and adul s ela i e o his a iable wi hin
he spa ial co e age o he c uises cen ed in he a ea a ound he
Balea ic Islands ins ead. Summe su eys ca ied ou du ing
2001–2005 and 2012–2014 had enough spa ial esolu ion o
esol e he ypical egional mesoscale s uc u es, he e o e allow-
ing he iden i ica ion o he loca ion o salini y on s, while he
a ea co e ed in 2006 and 2011 was oo small (Supplemen a y
Figu e S4). No CTD salini y da a we e a ailable in 2007–2010.
Tempe a u e da a om SeaBi d 911þand SeaBi d 25 CTDs we e
p ocessed using he Sea-Bi d Elec onics Da a P ocessing ou-
ines, and salini y was calib a ed using IAPSO s anda d seawa e
and a Guildline 8400A salinome e (see de ails in Balbı´n e al.,
2014).
Geog aphical fi ness o la al su i al and annual
su i al index
Simula ions we e conduc ed o analyse whe he he spa io-
empo al a iabili y o en i onmen al a iables in luenced he
geog aphical i ness o la al su i al. Speci ically, we es ed he
in luence o he spa ial and empo al empe a u e a iabili y on
he su i al o eggs spawned each day o lexion s age h oughou
he spawning season. These simula ions we e conduc ed wi hou
explici ly inco po a ing any spa ial spawning s a egy.
Eggs we e eleased daily h oughou he wes e n
Medi e anean ( om 6W o6
E). Releases we e scaled using a
gi en p obabili y o being eleased (P) es ima ed om i ing a
polynomial unc ion o he gonadosoma ic index o 528 emales
sampled om he comme cial ishe y om he S ai o Gib al a
o he Balea ic Sea in he wes e n Medi e anean du ing sp ing-
summe 2003–2014 (Regle o e al., 2018a):
P¼28:3156 þ0:0024609 d27:4867e06 d34:5819 d0:5
(1)
whe e Pis he p obabili y o egg elease and dis he day o he
yea .
Daily p obabili y o egg elease was no malized so ha elease
p obabili ies summed o 1 a he end o each spawning season.
We made wo assump ions: (i) he same spawning window
applies o all yea s and (ii) he du a ion o an indi idual ish’s
spawning pe iod is independen o he spawne ’s body size. Fo
each day and posi ion, he eggs ha ched in o la ae ollowing a
Figu e 1. Es ima es o spawning-s ock biomass in housands o onnes (whi e do s) and ec ui men a age 1 in millions o fish (black do s)
om he 2017 assessmen o he eas e n s ock o A lan ic bluefin una (Anonymous, 2017) and inc easing a e age empe a u es in July o
he Balea ic Sea o e he yea s [c osses and fi ( empe a u e ¼0.0288 yea – 36.842;
2
¼0.16; p<0.01) as dash line].
Habi a and su i al o blue in una 3
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su i al unc ion ela ing ha ching success, H, o empe a u e T
(in C) in a empe a u e ange be ween 17 and 34C(Regle o
e al., 2018a) o mula ed as:
H¼–1:27T2þ63:78T–727:98; 2¼0:92;p<0:001
(2)
The eggs ha ched in o la ae wi h an ini ial a e age d y weigh
(W
0
) based on measu emen s o ecen ly ha ched la ae in he
labo a o y (W
0
¼0.018 mg DW, 60.007 s.d., n¼27; Regle o
e al., 2018a). G ow h om ha ching o he pos - lexion la al
s age was modelled o each daily coho in each spa ial uni as a
unc ion o empe a u e. These models we e de eloped using he
maximum po en ial speci ic g ow h a es a each empe a u e
ob ained using age–weigh ela ionships om labo a o y expe i-
men s o A lan ic blue in una la ae (Regle o e al., 2018a). The
maximum po en ial speci ic g ow h a es SGR (mg mg
1
d
1
) in-
c eased wi h empe a u e (T) and be e i a linea ela ionship
exp essed as:
SGR ¼0:0418T–0:8355 ð 2¼0:84;p<0:001Þ(3)
The applicable ange o empe a u e on which he ela ionship
is based is 22–29C(Regle o e al., 2018a).
Mo ali y (M) was modelled as a unc ion o la al size (W)
ollowing he exp ession (McGu k, 1986 ci ed in Regle o e al.,
2018a):
M¼0:00022W0:85 (4)
Equa ions (1)–(4) a e used o compu e daily la al g ow h and
mo ali y o he ime pe iod om ha ching un il he la ae each
he lexion s age. This assigns a su i al p obabili y o each posi-
ion and ini ial day. To isualize he p ocess, he accumula ed
su i al p obabili y o each posi ion was calcula ed as he ime
in eg al o he su i al p obabili ies o each ini ial day. Using di -
e en a eas, mean alues om hese maps we e calcula ed o
in e annual compa ison.
La al and adul spa ial da a
Annual geog aphical la al i ness om ou model was compa ed
wi h he obse ed spa ial dis ibu ion o la ae and adul ish in
he wes e n Medi e anean. A lan ic blue in una la ae we e
sampled on c uises conduc ed du ing sp ing and summe du ing
2001–2014 in an a ea ha co e ed 180 220 miles a ound he
Balea ic Islands wi h a 10-nau ical mile sepa a ion be ween s a-
ions (Alemany e al., 2010). Du ing 2001–2005, la ae we e col-
lec ed using Bongo ne s wi h a mou h diame e o 60 cm
equipped wi h 333-mm meshes down o 70 m dep h, whe eas
om 2006 onwa d, la ae we e collec ed using Bongo ne s wi h a
mou h diame e o 90 cm equipped wi h 500-mm meshes down o
30 m dep h (see Alemany e al., 2010;Ing am e al., 2017;Regle o
e al., 2018a o mo e de ails). Fish la ae om one eplica e, p e-
se ed in 4% bu e ed o malin in seawa e , we e so ed using a
s e eoscopic mic oscope, and he o al numbe o A lan ic blue in
una la ae was enume a ed. We selec ed only da a om s a ions
whe e p esence was posi i e and da a on da e, la i ude, and longi-
ude we e a ailable.
Fo he loca ion o A lan ic blue in una spawne s, posi ion
da a we e ob ained om comme cial ishing ac i i ies (pu se-
seine and longline) and elec onic agging in o ma ion.
In o ma ion on da e, la i ude, and longi ude o he se s o blue in
una schools by he pu se-seine essel “La F au II” was p o ided
by G up Bal ego´ o he yea s 2000–2014. On he basis o p e ious
his ological s udies (A anda e al., 2013a), all pu se-seine ope a-
ions in he a ea we e assumed o a ge schools o ac i ely
spawning ish. In con as , longlines a e se o e a b oade ex en-
sion in he wes e n Medi e anean and a ge a mo e di e se pop-
ula ion o A lan ic blue in una in e ms o ep oduc i e s a e
(Medina e al., 2007). Hence, GPS posi ions o longline ca ches
we e used only when hey cap u ed spawning emales. Spawning
condi ion was con i med by his ological analysis when he o a y
con ained pos o ula o y ollicles and/o mig a o y-nucleus
oocy es and/o hyd a ed oocy es.
A o al o 47 blue in una adul s we e agged unde wa e
wi hin he pu se-seine ne s du ing egula comme cial ishing
a ound he Balea ic Islands ea ly in he spawning seasons o 2009
(14 June), 2010 (8 June), and 2011 (9 June) (A anda e al.,
2013b). Ano he 24 blue in una we e agged, hal o hem unde -
wa e and hal onboa d he suppo essels, in he aps loca ed in
he S ai o Gib al a a ea ea ly in he 2011 spawning season
(Abascal e al., 2016). Fish we e agged wi h pop-up sa elli e ags
(MK10 and miniPAT; Wildli e Compu e s, Redmond, WA, USA)
a ached by a mono ilamen e he o a da , which was inse ed
Figu e 2. S udy a ea. (a) The dis ibu ion o he eas e n s ock o A lan ic bluefin una encompasses he egion o he A lan ic eas wa d om
he 45me idian and he Medi e anean Sea. (b) The wes e n Medi e anean is he a ea loca ed mos wes wi hin he Medi e anean Sea.
(c) The Balea ic Sea is loca ed in he wes e n Medi e anean Sea.
4P. Regle o e al.
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in o he do sal muscula u e a he base o he second do sal in.
T ansmi ed in o ma ion was i s p ocessed using he manu ac-
u e so wa e (DAP p ocesso ; Wildli e Compu e s). T acks we e
es ima ed by Collec e Localisa ion Sa elli e (CLS) using a Kalman
il e /smoo he app oach cons ained by ligh le el, sea su ace
empe a u e, and bo om opog aphy as desc ibed by Roye and
Lu ca age (2008). We only included pa hs o June and July,
which included pa o he ish mig a ion o he b eeding g ounds
(only in he case o ish agged in he una aps), he spawning
pe iod, and he e u n o he o aging a eas in he A lan ic Ocean.
Time-se ies o ec ui men
Time-se ies o ec ui men we e es ima ed using a ishe y-
dependen ec ui men index employed in he la es assessmen
o he eas e n s ock by ICCAT conduc ed in 2017 (Anonymous,
2017). We spli his ime-se ies in o wo ime-se ies due o
changes in ishing gea . The i s , 2000–2006, used an age-
agg ega ed index o 2- and 3-yea -old ish ha es ed by he
Spanish bai boa ishe y, whe eas he index a e 2006 used an
age-agg ega ed index o 5–6 yea olds. We did no conside es i-
ma es o ec ui men da a om VPA ou pu s, gi en he unce -
ain y in he VPA es ima es ha esul in un eliable alues o
ecen da es (Anonymous, 2017).
Resul s
Geog aphic pa e ns o spawning and la al su i al may be
explained by he ole ha empe a u e plays on he ea ly
li e s ages o A lan ic blue in una (Figu e 3;Supplemen a y
Figu e S5). Po en ial ha ching p obabili ies we e 40–60% e e y-
whe e in he wes e n Medi e anean excep in he no he n and
sou he n limi s (Gul o Lions and Albo an Sea, espec i ely)
whe e empe a u es we e usually lowe han 20C and, he e o e,
ha ching p obabili ies we e e y low (Figu e 3a–c; Supplemen a y
Figu e S5). Howe e , po en ial la al su i al a eas we e much
mo e es ic ed han po en ial ha ching a eas (Figu e 3d– ;
Supplemen a y Figu e S5). The a ea a ound he Balea ic Sea
emained op imal o la al su i al despi e annual di e ences in
empe a u e, sugges ing i o be he bes a ea in he wes e n
Medi e anean o blue in una la al su i al (Figu e 3d– ,
Supplemen a y Figu e S5). La i udes abo e 41N and below
36.5N always had he lowes la al su i al; in some cases, no
la ae su i ed (Figu e 3d– ,Supplemen a y Figu e S5). Wa me
summe s enla ged he longi udinal ex ension o po en ial a eas
wi h enhanced la al su i al, whe eas colde yea s sh unk po en-
ial la al habi a s (Figu e 3d and ). As a consequence o op imal
he mal condi ions o he eggs and la ae, 2003 and 2006
esul ed in good yea classes om he model, 2005 and 2009–
2010 in mode a e yea classes, and he es o he yea s in poo
yea classes (Figu es 3d– and 4, and Supplemen a y Figu e S5).
The geog aphic dis ibu ion o a eas ha p omo e inc eased
la al i ness a e consis en wi h he spa ial ep oduc i e s a egy
o blue in una, as shown by he spa ial o e lap o la ae and
spawning emales as well as o modelled da a (Figu e 3d– ,
Supplemen a y Figu e S5). The loca ions o spawne s, as obse ed
om ishe ies da a, we e spa ially es ic ed o he a ea o he ba-
sin a ound he Balea ic Sea as we e po en ial la al habi a s p e-
dic ed by he model and he p esence o la ae om
ich hyoplank on su eys (Figu e 3d– ,Supplemen a y Figu e S5).
T acks o adul s indica ed mo emen s om he S ai o Gib al a
owa ds he a eas wi h he highes la al su i al (Figu e 3 ,
Supplemen a y Figu e S5). Spawning was also obse ed in subop-
imal he mal habi a s, as p edic ed by he model, sou h o he
islands despi e sui able he mal habi a s nea by (Supplemen a y
Figu e S5). We could no es hese habi a s wi h he da a a ail-
able om obse a ions since ich hyoplank on su eys we e only
a ailable a local scales (10 s o km), and sampling was conduc ed
mos ly sou h o he islands and a ely no h (see sampled s a ions
as do s in Supplemen a y Figu e S4). No did indus ial and long-
line ishe ies o elec onic ags co e he o e all he mal sui able
habi a s (Figu e 3,Supplemen a y Figu e S5). Spa ial limi a ions
in sampling e o could be impo an in explaining dis ibu ions
a he local scale, such as in 2004 and 2007, when maps sugges
ha la ae and spawne s we e dis ibu ed in low-quali y he mal
habi a s, al hough highe -quali y habi a s we e loca ed nea by, o
in 2013, wi h ela i ely high-quali y habi a no h o he islands,
bu wi h la ae being dis ibu ed mos ly sou h (Supplemen a y
Figu e S5).
The p esence o spawning in subop imal he mal habi a s, ye
in ela i ely s able loca ions, (in e e y yea , i is obse ed mainly
sou h o he islands, and seldom o a ely o he no h), could
also be an indica ion ha he adul s use o he cues o de e mine
spawning loca ions a a smalle spa ial scale. Besides empe a u e,
cha ac e iza ion o habi a equi emen s and p e e ences a he
local scale could be in luenced by he o ma ion o salini y g a-
dien s due o he con e gence o less-saline ecen A lan ic
wa e s and mo e-saline- esiden A lan ic wa e s (Supplemen a y
Figu e S4). The no he nmos a ea o he Balea ic a chipelago is
usually occupied by esiden A lan ic wa e , whe eas he con lu-
ence o new and esiden A lan ic wa e usually occu s a he
sou he n bo de o he su eyed a ea, sou h o he islands, as o
example in 2002, 2003, 2004, and 2012 o c ossing he Mallo ca
Channel owa ds Cab e a Island, as in 2001 and 2005
(Supplemen a y Figu e S4). The po en ial la al su i al index
om he model and he ec ui men index om he bai boa
ishe y ollowed a simila end (Figu e 5), sugges ing a di ec
he mal in luence on in e annual a iabili y in ec ui men a he
sho - e m scale in ecen yea s. The s ong signal o he 2003
yea class bo h in he model and in he bai boa ishe y da a is
pa icula ly ema kable.
Discussion
Ou wo k co obo a es p e ious hypo heses ha he Balea ic Sea
is an op imal a ea o A lan ic blue in una egg and la al su i al,
ega dless o in e annual a iabili y in summe empe a u e.
O sp ing always ha e a highe chance o su i ing o he lexion
s age he e han in any o he egion/a ea o he analyzed wes e n
Medi e anean. We ha e moni o ed he occu ence o A lan ic
blue in una la ae and spawning emales in he a ea since 2000
and ha e con i med ha blue in una epea edly spawn in he
Balea ic Sea, a spa ial ep oduc i e s a egy ha op imizes he
chances o su i al o he o sp ing in e ms o empe a u e. The
geog aphic ange o bes la al su i al expands sou hwes wa d
in wa me yea s, whe eas i is es ic ed o he Balea ic Sea in
colde yea s. This con ac ion–expansion o po en ial la al habi-
a is e lec ed in he annual su i al index, highes in he wa m-
es yea s and lowes in he coldes yea s. The index complemen s
p e ious empe a u e indices (e.g. Ha o d e al., 2017), down-
scaling he p ocess o a egional index ha mechanis ically e lec s
he in luence o empe a u e on eggs and la ae, bu also changes
in he spa ial dis ibu ion o sui able spawning a eas.
Habi a and su i al o blue in una 5
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Figu e 3. Spa ial dis ibu ion o he cumula i e p opo ion o eggs success ully ha ching o (a) 2003, (b) 2005, and (c) 2011. Spa ial
dis ibu ion o he cumula i e p opo ion o la al su i al o he pos -flexion s age o (d) 2003 (good la al su i al index), (e) 2005
(mode a e la al su i al index), and ( ) 2011 (poo la al su i al index). No e he di e en scales in he figu e o each yea . Posi i e loca ions
o he p esence o A lan ic bluefin una la ae ( ed do s), spawning emales cap u ed by pu se-seine (g een do s), and by longline (pink do s)
a e shown on op o he la al su i al. Mo emen s o bluefin una adul s du ing June–July a e shown in g ey om agged fish in 2011.
6P. Regle o e al.
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The basis o de i ing he habi a sui abili y index in ou s udy
was labo a o y-de i ed la al g ow h and weigh -a -age models a
di e en empe a u es unde he assump ion ha his ela ion-
ship e lec s g ow h a es in na u e. Resul s om o he labo a o y
expe imen s on cul u ed la al Paci ic blue in (Thunnus o ien a-
lis) and yellow in (T. albaca es) una ha e also shown a clea in-
c ease in g ow h a es wi h empe a u e when he e ec
o empe a u e was isola ed om o he a iables (Tanaka e al.,
2008;Kimu a e al., 2010;Wexle e al., 2011), sugges ing a po-
en ial ela ionship be ween g ow h and empe a u e. The e a e
e y ew ield-based g ow h es ima es o A lan ic blue in una,
and hose a ailable ha e been es ima ed o a na ow he mal
ange o age in e al ei he in he Medi e anean (Ga cı´a e al.,
2006) o in he Gul o Mexico (Malca e al., 2017), o indica e
how simila labo a o y g ow h a es a e o hose om ield-
cap u ed la ae a compa able empe a u es. The e a e indica-
ions ha g ow h a es may inc ease wi h empe a u e, al hough
mo e s udies on g ow h a es a e needed be o e we can use a
ield-de i ed ela ionship o es ima e speci ic g ow h a es in ela-
ion o empe a u e (see e iew in Muhling e al., 2017). Po en ial
di e ences be ween labo a o y es ima es and ield a es could a -
ec in e p e a ions o ime–space a iabili y in he mal habi a
su i al indices. On he o he hand, he e could be a si ua ion
whe e he mal condi ions o habi a a e good o maximal, bu
o he condi ions, e.g. poo ood a ailabili y, in which he habi a
index would o e es ima e su i al p obabili y. Timing o spawn-
ing in A lan ic blue in una has been shown o be ela ed o bo h
empe a u e and ood abundance o la ae, while compe i ion
and p eda ion among una la ae, ia cannibalism o pisci o y,
can a ec la al su i al in a e y oligo ophic a ea (Regle o
e al., 2011,2018a). Nowadays, dis ibu ion o ood a he basin
spa ial scale can only be app oached om chlo ophyll measu e-
men s, bu since he e is no co ela ion be ween spa ial pa e ns
in chlo ophyll and ood a ailabili y o una la ae (Regle o e al.,
2017), we canno ye cha ac e ize po en ial su i al habi a s e-
ga ding ood a ailabili y.
Long- e m a e age inc easing empe a u es in he
Medi e anean may explain he posi i e end in ec ui men o e
long ime-se ies (decadal scale), bu may no wo k in he sho -
e m (in e annual scale), pa icula ly in he las decade
(Figu e 1). Ou index shows ha he mal condi ions in 2003 and
2006 we e op imal o A lan ic blue in una egg and la ae
su i al compa ed wi h o he yea s. The 2003 yea class is ecog-
nized as one o he s onges , domina ing ca ches om he
Japanese longline and he Spanish bai boa ishe ies (Rod ı´guez-
Ma ı´n e al., 2013;Suzuki e al., 2013;Kimo o and I oh, 2017),
which i s well wi h op imal en i onmen al condi ions in he
spawning g ounds. Yea 2003 was cha ac e ized by anomalous
wa m wa e ha has been conside ed as a majo hea wa e in
Medi e anean wa e s. E idence in he ishe ies da a o a s ong
2006 yea class is no as clea . Mos o he 2004–2007 yea classes
we e no conside ed by he ICCAT Blue in Tuna Wo king G oup
o be ealis ic (Anonymous, 2017). In o ma ion on ecen ec ui -
men is cu en ly highly unce ain, because no ishe y cap u es
eas e n blue in una un il abou age 7 o 8 (Anonymous, 2017),
and ends in cap u e pe uni e o (CPUE) o hese age classes
can be subjec o o he cumula i e sou ces o a ia ion, o he han
ec ui men . Compa ing he model o he Spanish bai boa ishe -
ies index, based on an index o 2- and 3-yea -olds in 2000–2004,
o he wise 5- and 6-yea -olds, sugges an e ec o empe a u e on
ec ui men . In he case o ages 2–3, he i be ween he su i al
index and he ishe ies index is e y good, al hough sho , and in
he case o ages 5 and 6, he e is a ma ch in spi e o all he sou ces
o unce ain y in he CPUE s anda diza ion and all he ac o s ha
a e ac ing be ween ec ui men and he ime ish each ha age.
The e a e some di icul da a issues wi h he ec ui men da a
om i ual popula ion analysis (VPA) models used in assess-
men s ha educes he likelihood o a meaning ul link be ween e-
c ui men es ima ed om he assessmen and he new indices we
ha e de eloped. The e o e, we ha e no made quan i a i e use o
VPA da a (B ooks and De oba, 2015). Cu en da a a ailabili y o
his s ock limi s ou unde s anding o ec ui men p ocesses and
he abili y o esol e which ac o s d i e a ia ions in his species.
The e a e s ill some issues ha may limi he applica ion o
he su i al index de eloped in his s udy o he en i e
Medi e anean (A lan ic blue in una eas e n s ock). The habi a
index shown in ou s udy is only o he wes e n Medi e anean,
whe eas some a eas wi hin he eas e n and cen al Medi e anean
a e also spawning a eas o his species (Regle o e al., 2018a).
Con ibu ions o o he spawning a eas o he su i al index, as i
Figu e 4. Time-se ies o he po en ial la al su i al index ob ained
om he model o 2000–2014.
Figu e 5. Va ia ion in ec ui men and he po en ial la al su i al
index o he eas e n s ock o A lan ic bluefin una. Annual a ia ion
in he ec ui men co esponds o ages 2–3 (black do s) and ages
5–6 (whi e do s) es ima ed om he bai boa index (Anonymous,
2017) (co ec ed o ime lag o 2 and 5 yea s, espec i ely) and
su i al index (c osses). No e da a a e only a ailable o 2000–2010
wi hin he ime-se ies conside ed in his s udy.
Habi a and su i al o blue in una 7
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is es ima ed now, a e assumed o ha e cons an p opo ions in all
yea s, which is an un es ed hypo hesis, since egg p oduc ion ha
occu s in he di e en a eas has no ye been documen ed. I he
con ibu ion o each egion only depends on empe a u e, hen
simila empe a u e egimes ac oss a eas would esul in simila
egg p oduc ion o a gi en a ea. Howe e , spa ial con ibu ions
o o al s ock egg p oduc ion in he di e en a eas ha e no been
es ed, and p opo ions migh change om yea o yea .
I has been shown ha salini y and salini y on s a e impo -
an in de ining blue in una spawning places in he wes e n
Medi e anean (Regle o e al., 2012;Al a ez-Be as egui e al.,
2014,2016), and bo h empe a u e and salini y should ideally be
used o de eloping ec ui men models, so ha bo h e ec s a e
inco po a ed. One p ocedu e could be o use salini y o de ine
he loca ion and size o he mo e p obable spawning a ea in each
yea and hen, gi en ha egion, de ine i s he mal sui abili y o
g ow h and su i al (i.e. a measu e o habi a quali y) using he
ela ionships de i ed om he labo a o y. In his way, habi a
size, loca ion, and quali y migh be con igu ed mo e ep esen a-
i ely han hey a e in exis ing indices and could pe haps explain
mo e a iabili y in ec ui men . Un o una ely, hyd og aphic
models we e unable o desc ibe salini y a ia ions, and he many
CTD da a om ou ex ensi e ieldwo k we e only a ailable o a
small a ea wi hin he en i e wes e n Medi e anean. The e o e, we
cu en ly do no ha e ools o de elop a salini y-de i ed habi a
index.
We ha e combined di e en samplings o p o ide he mos ac-
cu a e spa ial spawning dis ibu ion in ela ion o empe a u e,
al hough some bias occu s due o di e en sampling e o s. In
some yea s, he only da a a ailable we e om he ishe ies since
no la al su ey could be conduc ed (e.g. 2007). Sampling e o
du ing la al su eys is mo e concen a ed sou hwa d han no h
o he islands. Pu se-seine s ha e ecen ly been aking hei quo a
in jus a ew days o less, so he spa ially de i ed da a om he
pu se-seine lee p o ides ela i ely ew da a poin s. Also, in he
ishe ies da a, we ha e included only hose cap u es whe e we
we e assu ed ha he ish we e ac ually spawning, as in e ed
om o a ian his ological analyses. The e is qui e a demand o
link egg–la al ecology o ec ui men o his s ock ha equi es
con inui y in sampling, as he ones used in ou s udy, bu also
new sampling (e.g. seasonal- epea ed su eys, o oli h analyses o
he su i o s) co e ing a wide spa ial and empo al scale.
P io i ies o his species should be iden i ied in he ICCAT wo k-
ing g oups oge he wi h s akeholde s and scien is s.
A c i ical ool o imp o e ou unde s anding o geog aphical
i ness in e ms o la al g ow h and su i al is he use o ealis ic
hyd odynamic models ha simula e ealis ic d i ajec o ies
coupled o indi idual-based models ha can include beha iou
(Fiksen e al., 2007). Limi a ions o his app oach a ise om he
lack o well-calib a ed and alida ed ci cula ion models a e-
gional scales, he lack o species-speci ic o mula ions o g ow h
and su i al h ough on ogeny, he lack o in e annual spa ial
dis ibu ion da a o bo h adul s and o sp ing, and he lack o
ime-se ies alida ion o ci cula ion models ha gene ally a e
upda ed wi hou main aining con inui y o ime-se ies, which is
c i ical o ishe ies s udies. To minimize he me hodological bias
and suppo he po en ial ope a ionaliza ion and u u e imple-
men a ion o an indi idual-based model, in he p esen s udy, we
ha e ensu ed: (i) a ca e ul alida ion o empe a u e da a om
he hyd odynamic model in he s udy a ea, (ii) he use o g ow h
exp essions ob ained om labo a o y expe imen s speci ically o
A lan ic blue in una and applied o obse ed empe a u e
eco ds du ing he spawning season, and (iii) a compa ison o
model esul s wi h ield obse a ion da a o geog aphic dis ibu-
ions o la ae and adul s.
While ci cula ion models mimic cu en s well a la ge spa ial
and empo al scales, hey may pe o m poo ly a he egional spa-
ial and sho empo al scales. Ou alida ion shows ha a ailable
models, wi h a su icien ly long ime-span o be o use o ou e-
sea ch, a e no capable o accu a ely ep oducing he spa ial dis-
ibu ion o di e en wa e masses, cha ac e ized by hei salini y,
and mesoscale ac i i y in he a ea. This limi ed ou abili y o
(i) ep oduce on al s uc u es and (ii) include d i ajec o ies
o es ima e he la al su i al index. Blue in una spawning is
ela ed o pa e ns in wa e masses ha explain in e annual di e -
ences in he spa ial dis ibu ion o la ae in he a ea (Al a ez-
Be as egui e al., 2016). The ci cula ion models es ed did no
p o ide accu a e salini y da a and, he e o e, spa ial pa e ns in
salini y and on s could no be ep oduced p ope ly. As such,
d i ajec o ies could no be es ima ed accu a ely and, he e o e,
we e no included in he es ima ion o he po en ial la al su i al
index. Howe e , loca ion o he densi y on in he Balea ic Sea,
iden i ied om salini y g adien s, would signal he bes a eas o
o sp ing su i al. While ci cula ion model ou pu s may ep o-
duce well gene al pa e ns o e en ion-dispe sal in la ge a eas o
he Medi e anean, hey ail o ep oduce de ailed in e annual
pa e ns in he s udy a ea when hey s ongly depend on meso-
scale ci cula ion. No el mul ipla o m obse ing sys ems, linking
modelling capabili ies and in si u da a, can p o ide alida ed
high- esolu ion models o ecen yea s o assess he oceano-
g aphic mesoscale scena io in he wes e n Medi e anean
(Tin o e´ e al., 2013;Juza´ e al., 2016). Ou s udy ep esen s a
ade-o be ween empo al a ailabili y o modelling p oduc s
and he capabili y o models o ep oduce di e en en i onmen-
al a iables and key ecological p ocesses.
One common p ocedu e in he li e a u e is o use o mulae e-
la ing empe a u e and g ow h o di e en species han he p i-
ma y s udy species unde he assump ion ha he unc ions a e
simila . Howe e , o mulae and adap a ions o local en i on-
men s ha e been shown o be species-speci ic, and we should be
cau ious when using exp essions ha a e no speci ic o he popu-
la ion unde s udy. In ou case, we we e able o design a se o
expe imen s using A lan ic blue in una and co e he ull ange
o empe a u e a iabili y obse ed in he ield (Regle o e al.,
2018a). On he o he hand, we know ha su ace empe a u es
a e good desc ip o s o egg and la al habi a o his species,
which always occupies he i s me e s o he wa e column and
show no clea e ical mig a ion pa e ns (Regle o e al., 2018b).
We ha e assumed he same spawning window o all he yea s
ha may esul in sligh ly highe mo ali ies in yea s when he
wa e wa ms la e since eggs will be p oduced, bu no su i e.
Despi e he ac ha we de eloped speci ic g ow h unc ions o
A lan ic blue in una, we used a size-dependen mo ali y cu e
de i ed om McGu k (1986). One ecommenda ion is o es i-
ma e species-speci ic mo ali y cu es, which will need o be con-
side ed in he u u e.
Di ec ly including en i onmen al a iabili y in s ock assess-
men models o including ishe ies-independen ec ui men in-
dices a e wo ways o imp o e cu en s ock assessmen models
o he eas e n spawning s ock o A lan ic blue in una. The index
we p oposed may be mo e use ul, no as a measu e o absolu e e-
c ui men , bu as a ela i e index in he s ock assessmen .
8P. Regle o e al.
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New assessmen wo king g oups o his species may need o dis-
cuss he bes me hodology o inco po a ing obse ed en i on-
men al e ec s on blue in una g ow h and su i al in cu en
assessmen s. Su i al maps combined wi h ha ching a eas would
allow he implemen a ion o spa ial egula ions ha would mini-
mize byca ch o blue in una spawne s and maximize o sp ing
su i al in he wes e n Medi e anean. These could be use ul
ools i spa ial decisions a e o be aken o he managemen o
he eas e n s ock o A lan ic blue in una o i clima e change
e ec s in spa ial dis ibu ions a e o be aken in o accoun a di -
e en empo al scales (Tommasi e al., 2017).
Supplemen a y da a
Supplemen a y ma e ial is a ailable a he ICESJMS online e -
sion o he manusc ip .
Acknowledgemen s
We hank he people in ol ed in he ex ensi e ield sampling, in-
ol ed in he expe imen al wo k and da a p ocessing, and in pa -
icula Melissa Ma in o he help wi h he la al sampling. We
a e g a e ul o Bal ego´ S.L. o p o iding loca ions o ishing ac-
i i ies o he yea s o s udy, Calade os del Medi e a´neo SL o
p o iding blue in una eggs o he expe imen s. We hank
ICCAT o p o iding he assessmen da a. We hank J. Co o
use ul discussions on he assessmen da a and blue in una ecol-
ogy. This esea ch has ecei ed pa ial unding om he
Eu opean Union’s Ho izon 2020 esea ch and inno a ion p o-
g amme unde g an ag eemen No. 678193 (CERES) and he
Blue in una P ojec (IEO-SOCIB ag eemen ). E.B. and M.H. ac-
knowledge he p edoc o al FPI Fellowship and pos doc o al g an
suppo , espec i ely, om he egional go e nmen o he
Balea ic Islands, Conselle ia d’Educaccio´, Cul u a i Uni e si a s,
selec ed as pa o an ope a ional p og am co inanced by he
Eu opean Social Fund. All expe imen s we e ca ied ou in acco -
dance wi h ele an guidelines on animal expe imen a ion on
ish. The me hods used in he cu en s udy we e accep ed by he
Minis y o Economy, Indus y and Compe i i eness o Spain
and he S ee ing Commi ee o he p ojec CTM2011-29525-C04-
02. We a e e y g a e ul o wo anonymous e e ees and he edi o
who p o ided e y use ul commen s o imp o e he pape .
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