Endogenous and environmental factors shaping growth rate variability in bivalves

Endogenous and en i onmen al ac o s shaping
g ow h a e a iabili y in bi al es
Physiological, his ological and cellula assessmen
Mai ane Pé ez Ceb ecos
In e na ional Ph.D. Thesis - 2024
Facul y o Science and Technology
Resea ch Cen e o Expe imen al Ma ine Biology and Bio echnology
Plen zia, Sep embe 2024
Endogenous and en i onmen al ac o s shaping
g ow h a e a iabili y in bi al es
Physiological, his ological and cellula assessmen
Mai ane Pé ez Ceb ecos
Supe iso s: I in zi Iba ola Bellido, U zi Izagi e A amaiona
This disse a ion is submi ed o he deg ee o
Philosophiae Doc o
(cc) 2024 Mai ane Pé ez Ceb ecos (by-nc-sa 4.0)
The ollowing esea ch wo k was unded by he Uni e si y o he Basque Coun y (UPV/EHU) h ough he
UPV/EHU Resea ch G oup g an (GIU21/028). I was also unded by he Basque Go e nmen h ough he
Consolida ed Resea ch G oup g an “Cell Biology in En i onmen al Toxicology” (CBET g oup, IT8010-B),
and he p e-doc o al and mobili y ellowships awa ded o Mai ane Pé ez Ceb ecos.
ii

iii
Al que a eglaba pa aguas. Al que se escondía en ellos.
i
A eces el des ino se pa ece a una pequeña empes ad de a ena que
cambia de di ección sin cesa . Tú cambias de umbo in en ando e i a la. Y en onces
la o men a ambién cambia de di ección, siguiéndo e a i. Tú uel es a cambia de
umbo. Y la o men a uel e a cambia de di ección, como an es. Y es o se epi e una y
o a ez. [...] Y la azón es que la o men a no es algo que enga de lejos y que no gua de
elación con igo. Es a o men a, en de ini i a e es ú. Es algo que se encuen a en u
in e io . Lo único que puedes hace es esigna e, me e e en ella de cabeza, apa e
con ue za los ojos y las o ejas pa a que no se e llenen de a ena e i a a esándola paso
a paso. Y en su in e io no hay sol, ni luna, ni di ección, a eces ni siquie a exis e el
iempo. Allí solo hay una a ena blanca y ina, como pol o de huesos, danzando en lo
al o del cielo. Imagína e una o men a como és a. Y cuando la o men a de a ena haya
pasado, ú no comp ende ás cómo has log ado c uza la con ida. ¡No! Ni siquie a
es a ás segu o de que la o men a haya cesado de e dad. Pe o una cosa sí queda á cla a.
Y es que la pe sona que su ja de la o men a no se á la misma pe sona que pene ó en
ella. Y ahí es iba el signi icado de la o men a de a ena.
Ha uki Mu akami, Ka ka en la o illa
I ’s easy o o ge ha ques ions don’ demand answe s. They demand unde s anding.
Pa ick Ro h uss, The wise man’s ea
i
xiii
in isibles bajo el sol en busca de la luna. Nues os mundos di e en es se en emezcla on y solapa on
en e sí su ilmen e, como cuando las aguas dulces y saladas se mezclan en la desembocadu a de un
ío con el subi y baja de la ma ea. Es os úl imos meses hab ían sido in ini amen e más di íciles
sin u apoyo; me sien o ag adecida de que hayas sido pa e de es e úl imo suspi o. G acias po
las con e saciones inspi ado as, las oces sua es, el oma e allado, el yogu con u a y miel, la
búsqueda del eso o en las o illas y el sua e baile acompañado po la oz de Allen a la luz de la
luna. G acias po hace me sen i comp endida, po el s acca o, po la chispa. G acias po can a
canciones que solo yo puedo escucha , po se el ien o que espuma las olas de mi ma .
El ma es el des ino inal del ío, donde culmina su iaje y encuen a su descanso. Es la as a
inmensidad que lo acoge, donde sus aguas, después de eco e mon añas, alles y llanu as, se
en egan po comple o. Pa a el ío, el ma es más que un simple inal; es su p opósi o, el ab azo
in ini o que lo ans o ma y lo enue a, dando sen ido a su exis encia. Eso sois pa a mi os os, mi
amilia. Ai i e, Amama, Izeko, eske ik asko po ene la pue a siemp e abie a, po las his o ias del
case ío, po las de Valencia. G azas amén aos desa e a na que os ca ballos e os abedu es compi en
polo espazo; onde o ma , xene oso e indómi o, desp ega a súa o za e o seu mis e io. Amama Emilia,
g azas po es i as miñas b omas coa úa isa. G azas Ca los, Elsa, Leo e An ía, sodes o e án
in encible no medio do in e no, semp e es ades a en os a min, aínda sen acelo os ácil. Leo, An ía,
os meus xiki ines, g azas po se esa e a mollada que chei a a espe anza, a paz inocen e que aínda
igno a aquelas cousas que an es emece a ida. Qué o os moi o.
Sin emba go, los que más me ecen se ag adecidos son los de casa, Ama, Ai a y Julen, po aguan a me,
po apoya me. Ama, g acias po enseña me que uno siemp e cuen a con el p i ilegio de la pausa,
po da me el pe miso he moso de ena . G acias po enseña me a que si enía que hace algo, debía
oma me mi iempo y hace lo bien. G acias po las ho as que pasamos en la ía. Lle o u luz y u
olo po donde quie a que aya. Ai a, g acias po empeña e en en ende lo que hago, po u humo ,
po el b illi o de o gullo en us ojos. G acias po la in ensidad, pese a que nos en en e. Julen, a
i que iluminas mi camino, us ab azos son el e ugio que necesi o cuando el mundo se ambalea.
G acias po u p o undidad, po u isa con agiosa, u empa ía, u admi ación. Ojalá un día llegues a
e e a a és de mi mi ada. G acias po se la es elli a que ilumina mi oscu o cielo. Todo lo que
hago, odo, se ía imposible sin oso os. Los ecue dos que compa imos nunca se des anece án;
como la sal en el ma , son ya pa e de noso os.

xi
Acknowledgemen s
Wi hou i s ibu a ies, he i e would lack li e and pu pose. They en ich and s abilise i , p e en ing
i om d ying up, o e lowing, o losing i s way. Simila ly, he w i en piece in you hands would
no ha e he appea ance and essence i has wi hou he people I men ion below, and I would like o
hank hem all. I hope I don’ o ge anyone. Thanks o hose who we e and a e noise in my silence,
o hose who a e and we e silence in my noise.
The main con ibu o s o he exis ence o his p ojec a e you, my supe iso s, I in zi Iba ola and
U zi Izagi e. You plan ed he seed, nu u ed he plan , and ended he lowe . Thank you bo h o
allowing you sel es o be decei ed ou yea s ago when I knocked on you doo and you us ed in
me. Thank you also o pu ing up wi h my ex a agan ideas and o showing me he way h ough
his maze. I in zi, hank you o he coun less hou s o da a analysis and ou many discussions
on science and beyond. Thank you o in using his ex wi h elegance and igou , always ea ing
i wi h ca e and pa ience. You u n my whims in o ideas. U zi, hank you o eaching me he
impo ance o a well-c a ed expe imen al design, o double e lec ions and key ques ions. Thank
you o smoo hing my edges and eaching me o pick my ba les, o calming my ne es when doub s
assailed me. You keep me om alling in o he abyss; you a e a sa e nes on he cli .
A c ea u e does no h i e ou side i s ecosys em, as i elies on he complex web o in e ac ions and
esou ces i p o ides. A hesis is no di e en . Wi hou a suppo i e esea ch g oup behind you, i
would be eally ough, i no impossible, o ge h ough a esea ch p ojec .
I would like o s a by hanking he g oup o Ene ge ic Physiology o Bi al e Mollusks a he Facul y
o Science, UPV/EHU. Thank you, Iñaki, o you wo ds o encou agemen , o showing me ha
no hing is as impo an as i seems. Mi en, you a e a model o s eng h and esilience. Thank you
o he behind-closed-doo s con e sa ions, o you unde s anding, and o you suppo ; I know I
can always coun on you. K is, hank you o he co ee-scen ed b ea hs, o you cons an eadiness,
and o you pe sis ence. Thank you, also, o b inging Alex in o my wo ld. Alex, hank you o he
discussions on philosophy, his o y, and poli ics. I lea n so much jus by alking wi h you. Thank
you o aking me se iously, e en i some imes you don’ unde s and me. I hope Ganeko someday
ealises how lucky he is o ha e you bo h. Xabi, hank you o ag eeing o pa icipa e in he c aziness
o my hesis (e en hough you did no know whe e you we e ge ing in o), wi hou you, he second
chap e would no exis . Thank you o sha ing endless hou s in he lab wi h me, o he music, he
x
walks, and he con idences. You we e a small es in he cou se o he i e , a lake o se ene wa e s
whe e I could ind calm.
The i e is bo n in he quie o a sp ing, whe e he ea h whispe s and he wa e eme ges in a
delica e sigh. F om he dep hs, hidden benea h he hills, i lows as a cu en ha wi h each d op
ca esses he land, ma king he beginning o a jou ney. You ha e been ha sp ing o me, Dani.
Wi hou you, his would no ha e e en s a ed. You ha e been he a chi ec o much o his hesis,
especially he wo k ha is no isible. Thank you o you dedica ion, you skill, o being ha
eache who allows mis akes wi hou judgemen , wi h laugh e and in ini e pa ience. You augh me
o handle all he machines and gadge s in he lab; and mos impo an ly, o manage wi hou hem. I
oday I am capable o concei ing and execu ing expe imen s success ully, i is hanks o you (e en
i I end up soaked). I will always admi e you p oblem-sol ing abili y, you composu e in acing
challenges, and you inexhaus ible gene osi y. Thank you o pu ing up wi h me, o indulging me,
and o you iendship.
I would like o hank he Animal Eco oxici y and Wa e Quali y g oup o hei suppo , hose on
he o he side o he doo . Thank you, Mai e and Pila , o you a ec ion, o pe cei ing me wi h a
wa m h I may no dese e. Mai e, hank you o awakening in me a cu iosi y o bi ds. Pila , hank
you o you winged alphabe . I especially hank you, Iñigo, o appea ing behind ha doo e e y
mo ning. Thank you o he na iga ing con e sa ions, o he endless s eam o ideas ha in e wine
and ans o m, o eaching me e e y hing I know abou cinema. Thank you o in oducing me o
So en ino and o s opping me om opening a bake y in Bu gos. Thank you o no needing me o
explain my silence, o unde s anding wha is no said.
I canno mo e o wa d wi hou i s hanking he i e side o es ha appea ed o emb ace he
i e . Thank you o he wonde ul people a he Plen zia Ma ine S a ion (Plen ziako I sas Es azioa -
PiE, UPV/EHU) and, in pa icula , o he Cellula Biology in En i onmen al Toxicology g oup. I
do no know wha would ha e become o me i you had no appea ed in he middle o my jou ney.
Thank you, Ibon and Oihane, o being he i s d ops o he haw, o gi ing me he oppo uni y o
ake my i s s eps in esea ch. Thank you especially o you, Oihane, o you cons an suppo and
us . Thanks also o you, Jon, Feli, Ca los, and Lo ea, o keeping wa ch o e he cas le. Thank you
o accep ing jokes, o going along wi h hem, and o making li e easie o all o us. Lo ea, hank
you o you kindness in his inal s age. Asie , hank you o he excu sions o he b eakwa e and
o all he help wi h he boxes. Only you (and you whis le) wi nessed he look on my ace when I
x i
saw all hose emp y shells. Jon, I ne e hough i would be possible o ge along wi h a physicis
and, e en less, o laugh so much. Thank you o being pa o he F iday Tuppe wa e eam and o
helping us (I hink) unde s and wha a momen is. Thanks o you, I ha e been able o del e in o he
amazing wo ld o LaTeX; you a e he b idge be ween he obse able and he comp ehensible. Ne ea,
Go i, hank you o being he gen le mis ha se les o e he i e ; you ha e always had kind wo ds
o me and you a e an example o e o and skill. Manu and Mu i, I hank you bo h o being he
ees ha , wi h hei b anches ex ended, bend owa ds he wa e like gua dians, o e ing a canopy
o shade ha e eshes and mi iga es he hea o he sun. Manu, i you did no exis , we would ha e
o in en you. Thank you o you closeness, o he ban e , o alking o us abou e e y hing, and
o you gene osi y. You ha e made me eel welcome om day one. Mu i, hank you o sha ing
you expe ience, o you p ecision wi h wo ds, bu also o he ons o mussels, o ligh ening he
mood, and o belie ing in me. I une, hank you o ensu ing he cons an low, o being he i al
pulse ha sus ains he i e on i s jou ney. Wi hou you, he i e would lose i s essence, and li e
along i s banks would ade in o silence. O , o pu i ano he way, wha would we do wi hou you?
Wi hou ou double agen , as Denis would say. Thank you o he laugh e , he knowing glances,
you b illiance, and you dedica ion, o aking ca e o us e en when we do no dese e i . Though
no always isible, he oo s a e c ucial o s abilising he i e banks and p o ec ing agains e osion.
Yes, ha ’s you, Pamela. Thank you o eaching me o see he wo ld h ough you eyes, o showing
me ha he e’s ano he way o do hings, o sha ing ha sense o iendship and eamwo k. Fo
speaking openly, o being he mi o in which I like o ecognise mysel . You’ e wo h much mo e
han you hink, do no o ge i .
Ti and Tame , I deeply app ecia e you ole as elde siblings, always eady o sha e a co ee and a
con e sa ion. Ti , you unde s and me be e han anyone in ce ain aspec s. Thank you o o e ing
solace, o you conce n, and o pa ien ly endu ing my clumsy a emp s a speaking F ench. You
a e like a wa e lily ha un u ls pa ien ly om he dep hs o he i e . Tame , you a e he hidden
da e among he ui box, an unexpec ed easu e ha b ings joy and swee ness o he simples o
momen s. Thank you o lis ening, o unde s anding, and o he sha ed unce ain ies. We a e uly
o una e o ha e you.
Simila o a sp ing, ye en i ely di e en , ain nou ishes he i e om a dis inc o igin, uni ed in
i s pu pose o gi ing li e. Bo h a e mu mu s ha keep he i e ib an , me ging opposing wo lds
in o a sha ed cu en . Each aind op il e s in o he ea h, eplenishing hidden aqui e s, which, like
x ii
disc ee sp ings, con inue o eed he i e when he sky emains clea . You a e ha ain, Denis. You
ell om he sky, ensu ing ha he wa e s lowed ceaselessly, e en in he imes o g ea es d ough .
Thank you o making me laugh, especially when I ake li e oo se iously. Thank you o including
me, o conside ing me, o he samplings, he s andings (e en wi h a ski ), he music, o he
laugh e , he ea s, he hugs. I admi e you sense o jus ice, you insigh and in ui ion, and, o cou se,
you igo ous wo k, wi hou which much o his hesis would no be wha i is. I eel e y o una e
o ha e you close.
A b aided i e is one ha e uses o be con ained, spli ing in o a my iad o b igh cu en s ha
wis and u n, o e e in e wining like he s ands o a loose b aid. In hese i e s, he banks and
channels a e nei he igid no ixed, bu a e in a cons an s a e o change, shaped by he elen less
low o wa e . Flowing wi h a sense o u gency, b aided i e s pain he landscape wi h hei e e -
changing pa e ns. Collabo a ions in science a e somewha like his. I ha e had he g ea pleasu e
and wonde ul o une o spending ime a he Caw h on Ins i u e in Nelson, New Zealand. Many
hanks o Zoë and No man, my supe iso s he e, o welcoming me om he e y momen I in zi
picked up he phone. Thanks o all he s a wi h whom, o g ea e o lesse ex en , I had he pleasu e
o wo king du ing my s ay. Alyssa, Jolene, Ca ol, Jess, Jo dan, Anne, Julien, Pe a, Ca he ine, Ca a,
Ch is, hank you o you p o essionalism and willingness; wi hou you, I would no ha e been
able o ca y ou hose wo seemingly impossible expe imen s. Tuiana, hank you o showing me
ha he e a e hings ha canno be augh , o you wa m h, o you se eni y. I hope no one e e
s ops us om imme sing ou sel es in he i e . Thanks also o you, Ellie, he seag ass gi l, o he
knowing laugh e and you ene gy. Thanks, o cou se, o you, Na alí and Leo, my Chilean iends;
no only o he comings and goings bu also o you ad ice and encou agemen , wi h o wi hou
bee s. Cecilia, hank you o you kindness, o sha ing my sense o humou , and o he ca ha ic
momen s. Ma in and Mena, hank you bo h o c ossing my pa h. Ma in, you we e he pe ec
hos when I a i ed; by he way, I owe you a b eak as . Mena, he connec ion was almos ins an ;
hank you o you c aziness, o he days we spen in Auckland, o he nonsensical laugh e . Ha,
do you emembe ha he ini ial goal was o alk abou ou p ojec s? We s ill need o do ha .
E iden ly, my ad en u e in he an ipodes would no ha e been he same, no by a long sho , wi hou
you, Zoë and Reuben. I belie e he h ee o us oge he o med a small, well-bonded amily. Zoë,
hank you o showing me how o be whole in e e y hing I do, o eaching me ha I mus pu all
o mysel in o e en he smalles hings. Thank you also o you wonde ul ecipes, he nigh ime
x iii
con e sa ions, he li e lessons. When a i e changes i s cou se, i no only adap s o he new
con ou s o he land bu also opens new pa hs o beau y and disco e y. Zoë, you ha e changed
he way I see he wo ld; hank you o ha gi . Reuben, he joy o he house, he swee oo h, he
li le el ; hank you o you hugs, o sha ing you inne uni e se wi h me, o in oducing me o
he unexpec ed wo ld o Lego, o making me o ge abou wo k. Thank you bo h o being an
indispensable suppo and o he ips wi hou ki chen u ensils. Thanks also o you, Jude and Ash,
o you spa kle, wa m h, and cu iosi y; how can humou be so simila e en when we come om
such dis an places? Thanks o all ou o you and he es o he amily, o being mine as well.
In he i e , s ones play a ole as sub le as i is i al. They a e he silen gua dians o he cu en ,
shaping he i e bedwi h hei p esenceandc ea ingenchan edha ens o aqua icli e. Bydis up ing
he low o wa e , he s ones c ea e a mosaic o swi and se ene cu en s, whe e small c ea u es
ind hei home. Aina a, you ha e always been ha s ead as and s able ock. Thank you o being
he e, uncondi ionally, and I apologise o le ing his hesis s eal so much o ou ime. No e e yone
eaches ou when hey’ e hidden away, and you always manage o ind me, e en when I’m a away.
The way o uly ge o know each o he is by sha ing hings ha seem i ele an , le ing wo ds low
eely and i esponsibly un il we en u e in o isky e i o ies. Tha ’s how we go o know each
o he , Eneko. We ha e always danced wi h g ea ca e, no knowing exac ly wha music he o he
was lis ening o, no e en su e i he o he was dancing a all. Ye , we ha e sha ed so much. Thank
you o endu ing my hough s on mussel shells, o he walks o he dam, and o always being he e
whene e I asked. I’m glad you ook my ad ice o s a a hesis.
I saso, Maide , I ia, and I xaso, he li le blossoms o colou and joy ha ado n he i e . I saso,
you a e like he wa e c ow oo , he wise and silen one, whose whi e lowe s loa wi h a se eni y
ha calms he wa e s, like a men o guiding wi h pa ience and unde s anding. Thank you o you
o e whelming insigh and in elligence; you a e he ay o sunshine peeking h ough he clouds.
Maide , you a e he lobelia, he inspi ing isiona y, wi h you ib an and colou ul lowe s adia ing
ene gy and c ea i i y. You ha e always been my hope and daily companion o yea s— hank you o
Biolum, o he laugh e , and o he us ; Ams e dam will always be ou special memo y. I ia, you
a e he wa e plan ain, o e ing a delica e e uge and sus enance o hose dwelling by he i e wi h
you hea -shaped lea es and lo al spikes. You a e he mo he who wa ches o e us bu also knows
when o be i m; you innocence is wonde ul, and I would choose you again and again. I xaso, you
a e he i eweed, in pu ple o cou se, b inging wa m h and luminosi y, shining e en in he mos

xix
ad e se condi ions. Thank you o sha ing my silliness, o you s eng h, and o you s ead as ness.
Toge he , we make he mos i edeemably hila ious cynical duo ha can exis . Thank you o le ing
me be me. The ou o us oge he sha e memo ies ha will ne e lea e ou bones; like sal in he
sea; hey became pa o us.
Li e is complica ed, bu when you ha e b eak as wi h you iends, alk abou books and mo ies,
sha e you anxie ies, and al hough hey don’ disappea , he wo ld seems much kinde a e wa ds.
Nago e, Ma , hank you o ge ing up ea ly o ha e b eak as oge he . I I had o choose one hing
o ake away om his p ocess, i would undoub edly be you. You can w ap me in you gaze du ing
my silences and de end me wi h a smile agains my wo ds. Thank you o showing me new ways o
hinking and new pe spec i es on li e. You a e he bes eam I could ha e chosen. Ma , hank you o
you wi , you swee ness, and you laugh e ha ills he oom. I was a ue pleasu e disco e ing
he sec e o mussel la ae wi h you. You a en ion and encou agemen ha e been essen ial on
mo e han one occasion. Thank you o being he in incible smile behind my ea s, he unceasing
calm amids he chaos. The hesis will only be you beginning; I’m con inced a b igh u u e awai s
you. Nago e, I don’ know whe e o s a , so I’ll simply say ha we we e o una e when a e decided
o b ing us oge he , jus when we we e eady o i . Mee ing you was like eeling a wa m b eeze
unde he shade o a ee in he middle o he summe . Thank you o e e y hing — hank you o
he connec ion, o being so unin en ionally unny, o he ha mony, and you hones y. You a e my
ouchs one. You judgemen and excellen wo k will su ely be e lec ed in you hesis. You know
he s eps, now dance i ou . Ha ing you bo h makes me happy because no ma e how ha d he
wo ld pushes agains me, I know you’ll always be pushing back. I would no be ai o elegan o
o ge you, Nico, a his poin . Thank you o you calmness, you pe spec i e, and o being such a
an as I am o books and mo ies whe e “no hing happens”. A e we all ge oge he wi h a glass o
wine o some IPAs, si ing by he i e bank, I walk away and e u n home wi h a small glowing ball
o golden, adian ligh in my ches . Hea ing you laugh e and suppo eels like w apping you sel
in a so , d y, and wa m owel a e a cold ba h in he i e . Thank you, and hank you a housand
imes o e .
Milan Kunde a once sugges ed ha pe haps a man and a woman ind hei closes connec ion simply
in knowing he o he exis s. They a e g a e ul o ha exis ence and he knowledge o one ano he .
In his simple awa eness, hey ind happiness. I am g a e ul, laz ana, I am g a e ul ha you exis .
Jus ha . Thank you o being he d agon who led me o i s ha en, guiding me wi h in isible wings
xx
benea h he sun in sea ch o he moon. Ou di e en wo lds in e wined and o e lapped sub ly, like
when esh and sal wa e blend a he mou h o a i e wi h he ise and all o he ide. These pas
mon hs would ha e been immeasu ably ha de wi hou you suppo ; I am g a e ul ha you we e
pa o his inal sigh. Thank you o he inspi ing con e sa ions, he so oices, he g a ed oma o,
he yogu wi h ui and honey, he easu e hun along he sho e, and he gen le dance o Allen’s
oice in he moonligh . Thank you o making me eel unde s ood, o he s acca o, o he spa k.
Thank you o singing songs ha only I can hea , o being he wind ha o hs he wa es o my sea.
The sea is he i e ’s inal des ina ion, he place whe e i s jou ney culmina es and i inds peace. I
is he as expanse ha welcomes i , whe e i s wa e s, a e winding h ough moun ains, alleys,
and plains, su ende wholly. Fo he i e , he sea is mo e han jus an end; i is i s pu pose, he
immense emb ace ha ans o ms and enews i , u ning i s long jou ney in o some hing a g ea e
and e e nal. I gi es meaning o i s exis ence. Jus as you, my amily, do o me. Ai i e, Amama, Izeko,
hank you o keeping you doo always open, o he s o ies o he a mhouse, o hose o Valencia.
My g a i ude also ex ends o hose on he land whe e oaks and alde s ie o space, whe e he sea,
gene ous and un amed, e eals i s s eng h and mys e y. Amama Emilia, hank you o ado ning
my jokes wi h you laugh e . Thank you, Ca los, Elsa, Leo, and An ía, o being he unshakeable
summe in he middle o win e . You’ e always he e o me, e en when i ’s no easy. Leo and An ía,
my li le ones, hank you o being ha mois ea h ha smells o hope, ha innocen peace s ill
un ouched by li e’s ha she eali ies. I lo e you e y much.
Bu he ones who dese e he mos hanks a e hose a home: Ama, Ai a, and Julen, o pu ing up
wi h me and suppo ing me. Ama, hank you o showing me he alue o aking a pause, o gi ing
me he beau i ul gi o slowing down. Thank you o eaching me ha i some hing needs o be
done, i ’s wo h aking my ime o do i igh . I che ish he hou s we spen by he es ua y. You ligh
and scen go wi h me whe e e I go. Ai a, hank you o making he e o o unde s and wha I
do, o you humou , and o he p ide ha shines in you eyes. Thank you o you in ensi y, e en
when i challenges us. Julen, you ligh up my pa h, and you hugs a e he e uge I need when he
wo ld eels shaky. Thank you o you dep h, you in ec ious laugh e , you empa hy, and you
admi a ion. I hope one day you see you sel h ough my eyes. Thank you o being he li le s a
ha b igh ens my da kes nigh s. E e y hing I do would be impossible wi hou you. The memo ies
we ha e made will ne e ade; like sal in he sea, hey ha e become a pa o us.
xxi
Con en s
Gene al in oduc ion 1
1 Bi al e li es yle .................................... 2
2 Habi a di e ences in bi al e popula ions .................... 4
2.1 En i onmen al condi ioning . . . . . . . . . . . . . . . . . . . . . . . . . 5
3 O gans in ol ed in ood acquisi ion and p ocessing .............. 8
3.1 Thegill .................................... 8
3.1.1 Gill ana omy, his ology and pa icle e en ion e iciency . . . . 8
3.1.2 Physiological pa ame e s conce ning he gill and hei plas ici y 10
3.2 Ana omy and his ology o he diges i e gland . . . . . . . . . . . . . . . . 12
4 O gans in ol ed in ene gy usage and s o age: man le and gonad ....... 14
5 Ene ge ic physiology and g ow h ......................... 17
5.1 Explana o y models o in e -indi idual g ow h- a e a iabili y . . . . . 17
6 Fac o s a ec ing he capaci y o ene gy acquisi ion .............. 19
6.1 In e -indi idual di e ences in he il e ing capaci y . . . . . . . . . . . . 19
6.2 In e -indi idual di e ences in diges i e capaci y . . . . . . . . . . . . . . 20
7 Fac o s a ec ing he ene gy expendi u e ..................... 22
7.1 S anda d me abolic a e . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
7.2 Rou ineme abolic a e............................ 23
7.3 Fac o s a ec ing he me abolic a e . . . . . . . . . . . . . . . . . . . . . 23
7.3.1 Body size. Allome y . . . . . . . . . . . . . . . . . . . . . . . 23
7.3.2 Physiological s a us . . . . . . . . . . . . . . . . . . . . . . . . 25
7.3.3 Geno ype ............................. 26
7.3.4 Fa y acid composi ion and ROS p oduc ion . . . . . . . . . . 27
Hypo hesis and objec i es 61
Hypo hesis ...................................... 62
Objec i es ....................................... 62
Chap e 1 63
1 In oduc ion ..................................... 65
2 Ma e ials and me hods ............................... 67
2.1 Collec ion o mussel seeds and expe imen al se up . . . . . . . . . . . . . 67
2.2 Biome y ................................... 68
Gene al in oduc ion 3
ins ance, bi al es a e highly e icien a e aining phy oplank on and small o ganic de i us bu less so wi h
e y ine pa icula e ma e .
Once cap u ed, he pa icles a e so ed and di ec ed owa ds he mou h by he labial palps, an o gan ha
akes pa in ejec ing unsui able pa icles ha will be expelled as pseudo aeces. The abili y o so and
di e en ia e be ween pa icles is e e ed o as selec ion e iciency. These s uc u es a e co e ed wi h cilia ed
g oo es and idges ha anspo and so pa icles based on size, shape, su ace p ope ies and possibly
chemical composi ion (Beninge and S -Jean, 1997; Wa d and Shumway, 2004). Desi able pa icles a e mo ed
owa ds he mou h, while undesi able ones a e bound in mucus and expelled as pseudo eces. Labial palps can
dis inguish be ween nu i ious pa icles (e.g., phy oplank on, o ganic de i us) and non-nu i ious o ha m ul
ones (e.g., sil , sand, deb is).
Edible pa icles a e di ec ed in o he diges i e sys em, whe e hey a e b oken down and abso bed. The
oesophagus is in cha ge o anspo ing ood om he mou h o he s omach, necessa y o mechanical and
enzyma ic diges ion o begin. The s omach is also whe e he diges i e enzymes sec e ed by he diges i e
gland a e i s ac i a ed and begin he b eakdown o ood pa icles in o simple molecules. The diges i e
gland consis s o lobes loca ed a ound he s omach connec ed by duc s ha se es no only in he sec e ion o
enzymes ha acili a e ex acellula diges ion, bu also is he p ima y si e o nu ien abso p ion. In acellula
diges ion also happens wi hin he cells o diges i e gland, u he b eaking down ood pa icles ha ha e been
abso bed in o hese cells. The in es ine ex ends om he s omach, o en looping h ough he body be o e
ending a he anus nea he exhalan siphon. The lining o he in es ine abso bs emaining nu ien s, which
a e hen anspo ed in o he ci cula o y sys em o bi al es. Mo eo e , he undiges ed ma e ial and was e
is compac ed in he in es ine, which will be e en ually expelled om he body. Consequen ly, he s omach,
diges i e gland and in es ine a e in ica ely connec ed, o ming a highly e icien sys em o diges ion and
abso p ion.
E icien eeding and nu ien abso p ion a e c ucial o suppo ing bo h soma ic (so - issue and shell)
and ep oduc i e (gonad) g ow h. The ene gy and nu ien s ob ained om eeding a e sha ed be ween
main enance, g ow h and ep oduc ion. Fo ins ance, nu ien s can be used o p oduce and main ain so
issues, including he man le, gills, and muscles. The man le issue, in pa icula , plays an essen ial ole in
g ow h as i sec e es he o ganic ma ix componen s and ca ies ou he deposi ion o calcium ca bona e
laye s, aiding in o e all body enla gemen . Shell g ow h occu s a he ma gins o he man le and is egula ed
by he a ailabili y o calcium and ca bona e ions, as well as en i onmen al ac o s. The man le issue is
also undamen al in suppo ing game ogenesis as hey a e bo h closely in e connec ed and c i ical o he
g ow h, ep oduc ion and o e all su i al o he bi al es. Gonads a e embedded wi hin he man le issue

4 Gene al in oduc ion
o closely associa ed wi h i , consis ing o ollicles whe e game e de elopmen occu s. Du ing pe iods o
high ood a ailabili y, bi al es can alloca e su icien nu ien s and ene gy o bo h soma ic and ep oduc i e
g ow h. In con as , du ing pe iods o low ood a ailabili y o en i onmen al s ess, bi al es may p io i ise
one ype o g ow h o e he o he , o en a ou ing su i al (soma ic main enance) o e ep oduc ion. Hence,
bi al es usually exhibi seasonal g ow h pa e ns, wi h soma ic g ow h occu ing du ing pe iods o high ood
a ailabili y and gonad de elopmen peaking be o e spawning seasons. A e spawning, a pe iod o soma ic
eco e y usually ollows, whe e ene gy is di ec ed back o issue and shell g ow h. A s ong, well-main ained
shell educes he isk o p eda ion and en i onmen al damage, indi ec ly suppo ing ep oduc i e success
ensu ing a sa e en i onmen o game ogenesis.
The co ela ion be ween eeding e iciency, ene gy in ake, and g ow h capaci y unde sco es he de elopmen
o g ow h pheno ypes in bi al es. E icien eeding mechanisms allow o g ea e ene gy in ake, which
di ec ly suppo s g ow h and ep oduc i e capaci y. This in ica e ela ionship be ween eeding p ocesses and
ene gy dynamics p o ides a ounda ional unde s anding o he ecological and physiological ac o s d i ing
g ow h pheno ypes in bi al es.
2 Habi a di e ences in bi al e popula ions
Descendan indi iduals o he same spawning e en , such as mussels o oys e s, can end up inhabi ing ei he
he sub idal zone o di e en zones along he in e idal. This e ical zona ion o he bi al e communi ies
is especially ele an no only due o he di e en se o luc ua ions and subsequen challenges ha each
zone subdues he animals o; bu also, because, as long as hey a e sessile, hey canno mo e o e ade he
en i onmen al s esses. Bi al es ha e been p o en o display a wide ange o compensa o y physiological
mechanisms ha allow hem o p ese e he biological ac i i y and g ow h in such a a iable en i onmen
(Thompson and Bayne, 1974; Okumus and S i ling, 1994; Na a o e al., 1994; Pe ne e al., 2007). In o he
wo ds, bi al es possess a high le el o physiological plas ici y ha esul s in a complex beha iou when
dealing wi h he en i onmen al luc ua ions, which makes i in e es ing o es he de elopmen o as and
slow g owing indi iduals unde hese condi ions.
The sub idal zone encompasses a wide ange o dep hs, om he shallow sub idal a eas nea he low ide
ma k o deep-sea enches and abyssal plains. The sub idal habi a is cha ac e ized by s able en i onmen al
condi ions, including ela i ely cons an empe a u e, salini y and wa e a ailabili y (Be ness e al., 1999).
Wa e mo emen , d i en by ides, cu en s and wa es is a p ominen ea u e o sub idal habi a s (Bi d e al.,
2017), which in luence nu ien a ailabili y, sedimen anspo and la al dispe sal, shaping communi y
s uc u e and ecosys em dynamics (Denny e al., 2003; Th ush e al., 2008).
Gene al in oduc ion 5
Bi al es li ing in in e idal egions a e equen ly exposed o la ge changes in hei physical en i onmen .
Those en i onmen al challenges, in addi ion, a e o en mo e p onounced and se e e he uppe in he in e idal.
In ac , a inc easingly highe le els on he sho e, ma ine o ganisms will be expe iencing inc easingly longe
pe iods o ime spen in ai , i.e., eme sion. The shi be ween imme sion and eme sion is ough o bi al es, as
seawa e and ai ha e e y unalike, o en con a y cha ac e is ics (Dejou s, 1989). The e o e, animals exposed
o long eme sion imes a e exposed o desicca ion s ess, ex eme empe a u es, UV adia ion and ace
di icul ies wi h ni ogenous was e exc e ion (Nybakken, 1993; Moyle and Cech, 1996; Ra aelli and Hawkins,
1999; W igh and Tu ko, 2016). Fu he mo e, in e idal animals also equen ly expe ience diel hypoxia
(Richa ds, 2011; Schul e, 2022) and, in ocky in e idal zones, animals a e also exposed o physical s ess om
wa e ac ion and/o ice dis u bance (Ra aelli and Hawkins 1999). Mo eo e , due o he il e - eeding na u e
o bi al es, equen eme sion limi s he ime hey ha e o eeding, which can educe he amoun o ene gy
a ailable o g ow h and ep oduc ion (Bayne e al., 1988) ha condi ion in u n he diges i e cycles (Izagi e
e al., 2008).
2.1 En i onmen al condi ioning
Sub idal en i onmen s a e consis en ly subme ged benea h he low ide ma k, wi h minimal exposu e o ai .
As a esul , desicca ion is no a di ec conce n o sub idal o ganisms, bu i su e is o in e idal bi al es,
due o he exposu e o ai du ing low ide. The mos common adap a ion o high in e idal animals agains
desicca ion is a oiding wa e loss o educing wa e loss a e when eme ged (Leeuwis and Gampe l, 2022)
by minimising he exposed su aces, which is ma e ialised as igh ly closing hei shells (Denny and Gaines,
2007; Gleason e al., 2017).
Bi al es in he high in e idal zone expe ience, in gene al, much highe empe a u es han hose in he
low in e idal o sub idal zones, bo h on a diu nal and seasonal basis (Pe es e al., 2008; Fangue e al., 2011;
Richa ds, 2011; Gleason e al., 2017; Monaco e al., 2017; S ickle e al., 2017). In ac , se e al physiological
and biochemical mechanisms p o ide hem wi h highe hea ole ance. Fo ins ance, some high in e idal
molluscs ha e de eloped a highe empe a u e o ca diac ailu e (Dong and Williams, 2011) wi h a highe
hea s abili y o he me abolic enzymes han hei low in e idal ela i es, d i en by bo h pheno ypic plas ici y
and e olu ion (Dong and Some o, 2009; Liao e al. 2021). Coope a i ely, hea shock p o ein (Hsp) exp ession
le els ise a he onse o cellula hea s ess (Fangue e al., 2011). Hsp-s pe o m chape on unc ions by
s abilising o he p o eins, being no only he mop o ec i e du ing hea exposu e in high in e idal o ganisms,
bu also being used as a p epa a i e de ence agains s ess (Robe s e al., 1997; Halpin e al., 2004; G acey e
al., 2008). This la e s a egy in ol es he main enance o high cons i u i e Hsp le els (Nakano and Iwama,
2002; Dong e al., 2008), which likely equi es he alloca ion o ene gy (Hawkins, 1985; Houlihan, 1991),
al hough he associa ed me abolic cos is likely ou weighed by he bene i s (Tomanek, 2010).
6 Gene al in oduc ion
Compa ed o wha is known abou hea esilience- ela ed adap a ions in in e idal animals, in o ma ion
ega ding he d i e s o pa e ns o eezing ole ance is s ill limi ed. The eezing o body luids is isky
because ice c ys als cause physical damage o delica e cell s uc u es, and ice c ys al g ow h leads o desicca ion
by emo ing in acellula wa e (Denny and Gaines, 2007). The compensa ing mechanisms in di e en mussel
species comp ise he deposi ion o ice-nuclea ing p o eins in he ex acellula space (Lundheim, 1997; Denny
and Gaines, 2007), he accumula ion o compa ible o ganic osmoly es inside he cell (S o ey, 1997) and e en a
gill-associa ed bac e ium ha se es as an ice-nuclea ing agen (Loomis and Zinse , 2001).
Hypoxia can a ec bo h in e idal and sub idal en i onmen s, albei in di e en ways due o hei dis inc
cha ac e is ics. In deepe sub idal habi a s, bi al es may expe ience p olonged exposu e o low oxygen
concen a ions (Espinosa e al., 2010). Howe e , in he high idal zone oxygen le els d op o alues nea
ze o du ing low ide, making animals o expe ience hypoxemia (i.e., in e nal hypoxia) when eme ged, as a
esul o he collapse o he espi a o y s uc u es (Ra aelli and Hawkins, 1999; Wolco and Wolco , 2001;
Tu ko e al., 2014). The e o e, in e idal bi al es a e much mo e used o ace hypoxia han sub idal ones.
Relying on anae obiosis o su i e eme sion is a majo s a egy in bi al es (Segu a e al., 2015), e en o hose
species ha ely on gaping o enhance hei ae ial oxygen up ake (Bayne e al., 1976; Widdows and Shick,
1985; Zippay and Helmu h, 2012), as he e ained oxygen is deple ed wi hin minu es once in eme sion (Bayne
e al., 1976; Zippay and Helmu h, 2012). Fu he mo e, he e is also a ade-o be ween opening he shells o
a oid hypoxia and closing hem o a oid desicca ion (Nicas o e al., 2010). The inc eased anae obic abili y
is usual and pe sis en (Conno and G acey, 2012; G acey and Conno , 2016), and i migh be achie ed by
being able o accumula e compa a i ely mo e anae obic p oduc s (Gleason e al., 2017) o by inc easing he
amoun o anae obic uel sou ces (Sokolo a and Pö ne , 2001a). The disad an age o his anae obic s a egy
is ha an oxygen deb mus be epaid du ing e-imme sion o allow o he ae obic p ocessing o anae obic
end p oduc s, as seen in se e al bi al e species (Bayne e al., 1976; Widdows and Shick, 1985; Zippay and
Helmu h, 2012).
P ecisely o a oid he oxygen deb , in e idal animals appea o use he s a egy o me abolic dep ession o he
g ea es ex en (e.g., Ma shall and McQuaid, 1992; Sokolo a and Pö ne , 2001a). In My ilids his me abolic
dep ession has been linked o b adyca dia (Conno and G acey, 2012; Cu is e al., 2000), which would educe
he oxygen equi emen s o he hea and he whole o ganism. Down egula ion o o e all p o ein syn hesis,
ion anspo and lowe enzyme ac i i ies (pe manen o empo a y) ha e also been obse ed in high in e idal
animals (S o ey and S o ey, 1990; Pano a and Johannesson, 2004; Sokolo a and Pö ne , 2001b; G eenway
and S o ey, 2001; I anina e al., 2016), which migh acili a e me abolic dep ession by educing he ene gy
demands.
Ano he challenge o he in e idalindi iduals a e he b oad luc ua ions insalini y, which sub idalindi iduals
Gene al in oduc ion 7
do no ace. The i s coping mechanism ela ing o salini y challenges is beha iou al, ocusing on seeking
shel e in a mo e a ou able mic ohabi a , o educing he amoun o exposed su ace-a ea (Segu a e al., 2015),
simila o beha iou al de ences agains desicca ion. Physiological mechanisms used o con on salini y s ess
in ol e egula ing cellula olume by accumula ing o ca abolising in acellula o ganic osmoly es (Yancey,
2005). By con as , changes in UV adia ion le els a ec bo h sub idal and in e idal habi a s, al hough he
in e idal zone s ill expe iences mo e UV adia ion (Pe e son, 1991; Shick and Dunlap, 2002). Adap a ions
ha a e pa icula o unique o his ype o s esso include he use o UV-abso p i e pigmen s in he skin and
mucus, and an ioxidan s ha quench and deac i a e eac i e oxygen species (ROS) (Cockell and Knowland,
1999; Shick and Dunlap, 2002).
Because o he b eaking wa es ha a e o med a he sea- o-land ansi ion, animals in he in e idal zone
expe ience conside ably mo e wa e ac ion han hose in he sub idal. Howe e , wa e ac ion is no necessa ily
s ess ul and can e en be bene icial, as i helps wi h he supply o oxygen and nu ien s, in wa me clima es
o e s some cooling, and ce ain p eda o s (e.g., Ca cinus maenas) may also be less abundan (e.g., Ki ching e
al., 1966; Hughes and Elne , 1979; Gibbs, 1993). S ill, being swep away om he subs a e by wa es can ha e
se e e consequences: inc easing ulne abili y o sub idal p eda ion o causing physical damage (Denny and
Gaines, 2007). To a oid i , in e idal animals use se e al s a egies o s ongly adhe e o he subs a e: o
example, by sec e ing byssus h eads (Denny and Gaines, 2007). Con e sely, sub idal indi iduals a e subjec
o hyd odynamic o ces such as cu en s, which can in luence eeding e iciency, a achmen s eng h and
habi a sui abili y (Th ush e al., 2008).
P eda ion can in luence bi al e popula ion dynamics, communi y s uc u e, and ecosys em s abili y (Beck e
al., 2011). The p eda ion p essu e in sub idal compa ed o in e idal habi a s can a y based on a numbe o
ac o s including p eda o species, habi a complexi y and en i onmen al condi ions. Howe e , he sub idal
zone is an a ea wi h ypically highe di e si y and abundance o p eda o s: sea s a s, c abs, ish and d illing
gas opods a e mo e common and ac i e in he sub idal, and can exe signi ican p eda ion p essu e on he
bi al es inhabi ing i (F eeman, 2007). In ac , p eda ion p essu e has been epo ed o be signi ican ly mo e
consis en and highe in sub idal zones due o he p esence o a di e se p eda o assemblage and he s able
en i onmen ha allows p eda o s o be cons an ly ac i e, leading o sus ained p eda ion p essu e (Seed and
Suchanek, 1992; Gosling, 2003).
Disease ou b eaks and pa asi e in es a ions can cause mo ali y, educe ep oduc i e ou pu , and weaken
bi al e popula ions (La e y e al., 2015). The p e alence o pa asi es in sub idal compa ed o in e idal
indi iduals can a y depending on he en i onmen al condi ions, p eda o -p ey in e ac ions, and hos
physiology. Sub idal zones o e mo e s able en i onmen al condi ions, which may a ou he su i al and
p oli e a ion o ce ain pa asi e species. Ac ually, sub idal bi al es a e suscep ible o a ious diseases and
8 Gene al in oduc ion
pa asi ic in ec ions, including bac e ial pa hogens, p o ozoans, and pa asi ic la wo ms (Cheng e al., 2016).
In addi ion, he sub idal gene ally suppo s highe biomass and di e si y o po en ial hos s, p o iding mo e
oppo uni ies o pa asi es o comple e hei li e cycles (Poulin and Mou i sen, 2006). Concu en ly, in e idal
zones expe ience g ea e en i onmen al luc ua ions as men ioned abo e, which impose physiological s ess
no only on hos s bu also on pa asi es. In he mussel Pe na canaliculus a highe p e alence and in ensi y o
in ec ion by ema ode pa asi es was ound in he sub idal mussel popula ion when compa ed o he in e idal
popula ion (Kop i nika e al., 2010). In My ilus edulis, howe e , i has been ound ha while some pa asi es
we e mo e p e alen in sub idal popula ions, o he s showed no signi ican di e ence be ween idal zones
(Bollache and Kopp, 2007).
3 O gans in ol ed in ood acquisi ion and p ocessing
3.1 The gill
3.1.1 Gill ana omy, his ology and pa icle e en ion e iciency
Bi al es a e il e ing o ganisms and so he ood acquisi ion p ocess is bo ne by he gill and labial palps. The
gill o c enidia a e ound in he pallial ca i y and consis o ou pai s o demib anches o med by descending
and ascending lamellae, suspended on each side o he body om a c enidial axis. The ascending lamellae
use o he man le and isce al mass by cilia y o issue unions. The plica ion o he lamellae o o m la ge,
e ically aligned agg ega ions o ilamen s is usually how he c enidia achie e an o e all inc ease in he
su ace a ea.
In bo h mussels and oys e s, he gill does no o e ly unc ion as an o gan o selec ion ( his unc ion being
much mo e he esponsibili y o he palps), and all cu en s a e di ec ed o ally (Mo on, 1983). Howe e , he
oys e gill is olded (“plica e”) and he olds con ain h ee di e en ypes o ilamen s (o dina y, ansi ional
and p incipal) (Yonge, 1926), so he gill is said o be he e ohabdic (di e en shaped and sized gill ilamen s).
These di e en ilamen ypes ha e a disc e e di ision o asks. The sides and c es s o he plicae possess
do sally bea ing sho cilia and en ally bea ing long cilia, hus an inhe en so ing mechanism is s ill p esen
in he gills. La ge pa icles a e en ally passed on he c es s o he plicae o he ma ginal ood g oo es,
which can close by apposi ion o all bu he smalles ma e ials, so ha la ge pa icles may d op o on o he
man le o discha ge as pseudo aeces (see Bayne, 2017 o e iew). In ac , pa icle selec ion by he c enidia o
wo oys e species including Magallana gigas has been demons a ed (Wa d e al., 1994b; Wa d e al., 1998
a
).
Ne e heless, his ological s udies and obse a ions o su gically al e ed specimens sugges ha he labial
palps a e impo an o gans o pa icle selec ion in mos bi al e species (Kellogg, 1915; Menzel, 1955; Nelson,

Gene al in oduc ion 9
1960; Gal so , 1964; Jø gensen, 1966; Mo on, 1969), including hose species ha u ilize he c enidium o
pa icle selec ion (Wa d e al., 1994b, 1998a).
In My ilacea, he c enidia a e homo habdic (iden ical gill ilamen s) and non-plica e. All in e cep ed ma e ial
is anspo ed o he en al g oo e in a homogeneous, in e media e iscosi y mix u e o mucopolisaca ids,
such ha he e is no dis inc ion be ween he asks o inges ion ( eeding) and ejec ion (cleaning). In his case,
c enidia show a p og essi e loss o hei selec i e unc ion, excep o he p ima y so ing ha happens in he
en al ma ginal ood g oo es. The ma e ial is ans e ed, unusually, om he en al ma ginal g oo e o
he ou e demib anch o ha o he inne (Fankbone , 1971; Mo on, 1983), being he gill cilia ion almos
wholly en ally di ec ed. Rega dless o hese speci ic de ails, i is clea ha he so ing unc ion p imi i ely
possessed by he gill is now he unc ion o he labial palps, wi h a clea end away om la ge, plica e c enidia
o mo e p imi i e bi al e lineages owa ds smalle , simple c enidia.
The ole o he gill cilia has been ex ensi ely s udied (e.g., Wa d e al., 1998; Riisgå d and La sen, 2010).
Acco ding o he cu en iew, he bea ing la e al cilia se e as he pump on he gill ilamen s (Bayne, 2017),
a phenomenon ha has been di ec ly e idenced by Seo e al., (2014) in My ilus gallop o incialis. These cilia
a e p esen along he sides o he ilamen s, c ea ing cu en s ha pull wa e in o he pallial ca i y, d i e
i h ough he in e ilamen a spaces o he c enidia, and ou o he exhalan siphon o ape u e (Rosa e
al., 2018). They occu a in e als o be ween 2 o 3 µm and p ojec ou wa ds o do m a s i g id be ween
ilamen s. They bea a igh angles o he long axis o he ilamen , so ha he pa icles hey sie e a e licked
on o he on al cilia (Owen, 1974; Huges, 1975). F on al cilia a e p esen on he incu en - acing su ace o
he ilamen s, which a e esponsible o c ea ing su ace cu en s and ca ying he pa icles embedded in
mucus o he en al ma gins o he c enidia (Rosa e al., 2018). Howe e , he pa icles en e ing he pallial
ca i y a e ei he di ec ly in e cep ed by he on al su ace o he ilamen s o apped by cu en s c ea ed by
he la e o on al cilia/ci i and hen di ec ed on o he on al su ace. As a gene al ule, each la e o on al
ci i a ises om a single cell and consis s o cilia a anged in wo pa allel ows, he numbe o cilia comp ising
each ci us being a species-speci ic ai . In ac , mussels ha e a ilib anchia e homo habdic c enidium wi h
la ge compound la e o on al ci i ha could accoun o he epo ed high cap u e e iciency o pa icles
in he 4 o 10 µm size ange (Rosa e al., 2015). On he o he hand, oys e s ha e a pseudolamellib anchia e
he e o habdic c enidium wi h de eloped la e o on al ci i ha a e less complex han hose o my ilids (Owen
and McC ae, 1976; Ribelin and Collie , 1977), bu gene ally ha e highe cap u e e iciency o pa icles
g ea e han 3 µm han mussels. In My ilidae, he so-called p o ola e o on al cilia occu be ween he on al
and la e o on al cilia, smalle cilia closely packed in wo al e na ing ows (Owen, 1978). In Os eidae, A kins
(1938) desc ibed subsidia y pa ala e o on al cilia be ween he on al and la e o on al cilia, which ha e
been p o ed o be essen ially equal o he p o ola e o on al cilia o My ilidae (Owen, 1978). The gene al
appea ance o a gill ilamen has been pic u ed in Fig. 1.
10 Gene al in oduc ion
La e al cilia
Eu-la e o- on al
cilia
La e o- on al cilia F on al cilia
Mucocy e cell
Figu e 1. Gene al appea ance o a gill ilamen in bi al es. Adap ed om Owen and McC ae (1976).
In spi e o he hesi ancy o MacGini ie (1941, 1945), Fos e -Smi h (1975), Vahl (1973) and Jø gensen (1975,
1976, 1981), ha pos ula ed mucus shee o be he p ima y sc een o pa icles, i seems e iden now ha he
cilia y a angemen o he c enidial ilamen s is he e ec i e il e o he pa icles suspended in he wa e
column. Al hough his may be aided by mucus sec e ion o make pa icles s icky (Tammes and D al, 1955;
D al, 1967).
I should be no ed ha he e aining e iciency o he pa icles in he gill depends la gely on he size o he
pa icles hemsel es. In gene al, cap u e e iciency inc eases non-linea ly wi h inc easing pa icle size o a
maximum. A oiding in e -speci ic di e ences, i is accep ed ha o e all he e aining e iciency o he gill
is close o 100 % when pa icles a e la ge han 3 µm in diame e , bu i can cu down o alues a ound 50
% in smalle sized pa icles (Mølenbe g and Riisgå d, 1978; S ua and Klumpp, 1984; Riisgå d, 1988; De
Villie s and Allanson, 1988). Besides pa icle size, quali a i e ac o s can also in luence pa icle cap u e in
he gills. Fo ins ance, equally sized pa icles o ye di e en chemical composi ion ha e been shown o be
di e en ly e ained in expe imen s pe o med wi h oys e s (Os ea edulis) (Shumway e al., 1985), mussels (M.
edulis) (Newell e al., 1989) and scallops (Placopec en magellanicus) (Lesse e al., 1991).
3.1.2 Physiological pa ame e s conce ning he gill and hei plas ici y
The analysis o he ac i i y ca ied ou by he gill in he ood pa icle acquisi ion is done by he de e mina ion
o a se ies o pa ame e s ha a e shown nex . The clea ance a e (CR: L·h
-1
) is he adi ionally used pa ame e
ha desc ibes he speed a which bi al es il e he wa e o acqui e ood pa icles om i . The clea ance
Gene al in oduc ion 11
a e is de ined as he wa e olume ha is o ally pa icle-clea ed pe uni o ime. The il a ion a e (FR:
mg·h
-1
) ep esen s he o al mass o e ained o il e ed pa icles in he gill pe uni o ime, and i is ob ained
as he esul o he clea ance a e and he concen a ion o he ma e in suspension, p o ided ha he
e aining e iciency pe cen age o he pa icles in suspension eaches he 100 %. The ejec ion a e (RR:
mg·h
-1
) ep esen s he o al mass o pa icles ejec ed in he o m o pseudo aeces pe uni o ime. The
quan i y o inges ed pa icles pe uni o ime o inges ion a e (IR: mg·h
-1
) is ob ained ou o he di e ence
be ween il a ion a e and ejec ion a e. In he absence o ood ejec ion in he o m o pseudo aeces, he
il a ion and inges ion a es a e equal.
As a ule, i has been obse ed ha p e-inges ion p ocesses o bi al es display an ou s anding physiological
plas ici y ha allows hese o ganisms o adjus he clea ance and ejec ion a es o he cons an luc ua ions
o he die cha ac e is ics o wa e empe a u e. The cha ac e is ics o he pa icula e ma e in suspension,
essen ially he concen a ion and quali y o o ganic pe cen age o i , exe a decisi e e ec upon he clea ance
a e o bi al es. On many occasions, unde labo a o y o na u al condi ions, i has been obse ed he exis ence
o an in e se ela ionship be ween pa icle concen a ion and clea ance a e (Win e , 1973, 1978; Fos e -
Smi h, 1975; Bayne and Newell, 1983; Galimany e al., 2011; Tamayo e al., 2016; Kang e al., 2016; P ie o e al.,
2018). This educ ion in clea ance a e has been in e p e ed as a egula ion mechanism o inges ion a e, he
main i ue o which is p obably o keep he gu passage ime o ood in adequa e alues o main ain high le els
o abso p ion e iciency. The e ec o he a ion o he pa icle concen a ion depends la gely on he quali y
o p opo ion o o ganic ma e in he die . Na a o e al., (1994) analysed he a ia ion o he clea ance
and inges ion a es in he cockle Ce as ode ma edule subdued o changes in he quali y and concen a ion o
ood. They obse ed ha he highe he quali y o he die , he highe he educ ion in clea ance a e ha
happened when inc easing he ood a ion. In a la e s udy, Na a o e al., (1996) de e mined he clea ance
a e o he mussel M. gallop o incialis ed wi h simila ood a ions o 5 die s wi h di e en o ganic con en s
( om 16 o 91 %) and obse ed a ise in clea ance a e as he o ganic pe cen age o he die declined o alues
o a ound 30 %, al hough he educ ion in o ganic con en o e en lowe alues ( om 30 o 16 %) ga e ise o
he opposi e phenomenon, educing he clea ance a es. Acco ding o he au ho s, he in e ac ion be ween
quan i y and quali y o ood upon he clea ance a e is explained by he selec ion p ocess and p e-inges ion
ejec ion pe o med by he labial palps. The selec ion e iciency o he labial palps is highly dependen on
he quali y o he ood in suspension (Iglesias e al., 1992; U u ia e al., 1996; Hawkins e al., 1996). Unde
high quali y die s, when he o ganic con en o he die is high, he p e-inges ion selec ion e iciency o he
pa icles is limi ed, in such a way ha he adjus men o he inges ion a e is done by modula ing he clea ance
a e (Widdows e al., 1979; Bayne e al., 1989).
12 Gene al in oduc ion
3.2 Ana omy and his ology o he diges i e gland
The bi al e alimen a y sys em consis s o a ela i ely sho , la ened oesophagus opening in o a complex
s omach (Mo on, 1983). The oesophagus is composed o a cilia ed co e age epi helium in e spe sed wi h
mucocy es ha sec e e acid and neu al mucopolysaccha ides, e en when he animal is no ea ing (Beninge
and Le Pennec, 1991). The unc ion o he oesophagus is no o diges bu o anspo he pa icles o he
s omach. The c ys alline s yle is p ojec ed om he back end o he s omach along i agains he gas ic shield.
The inges ed pa icles a e mixed wi h he diges ion enzymes eleased om he c ys alline s yle (Gosling,
2008). F om he s omach a ise a numbe o openings in o he diges i e gland, he o gan o abso p ion and
in acellula diges ion. The diges i e di e icula comp ise a se ies o blind-ending ubules (diges i e al eoli)
ha communica e wi h he s omach ia a sys em o duc s (Fig. 2). Inside he seconda y duc s he low is
cons an and bidi ec ional (Fig. 2): he pa icles go h ough he duc s and he al eoli o be diges ed and
abso bed, while he was es a e expelled o he s omach and in es ines.
Diges i e al eoli
Non-cilia ed
seconda y duc s
Cilia ed p ima y duc s
S omach
Diges i e al eoli
Seconda y
duc s
Exc e o y sphe eExhalan duc
Inhalan duc F ee pa icles
Main
duc
Figu e 2. On he le , duc sys em o he diges i e gland o bi al es. On he igh , c oss-sec ion o he diges i e
gland o bi al es showing he abso p ion and in acellula diges ion. Adap ed om Owen (1955).
The ex acellula diges ion o he ood begins wi hin he s omach bu is no limi ed o i : he epi helial cells
o he diges i e duc s, he basophilic cells o he diges i e ubules and he lining o he mid-gu also sec e e
enzymes in o he lumen (Ma he s, 1973; Palme , 1979; Hen y e al., 1991; Iba ola e al., 2000). Abso p ion
happens mainly in he diges i e ubules (Fig. 3), al hough i also occu s in he s omach and mid-gu .
The epi helium o he diges i e al eoli a e comp ised o wo cell ypes: diges i e cells and basophiles (Mo on,
1983)(Fig. 4). Du ingno mal eedinganddiges ion, hediges i ecellsa e he mos abundan ones(Ma igómez
e al., 1990; Zaldiba e al., 2008), columna cells wi h a well-de eloped endolysosomal sys em ha ca y ou
Gene al in oduc ion 19
Me abolic e iciency model. The me abolic e iciency model holds ha he di e ences in g ow h a e be ween
indi iduals a e based on he di e ence in he ene gy cos s pe uni o g ow h. In o he wo ds, in he e iciency
o he ene gy in es men in he syn hesis p ocess o new issues. Less cos s o g ow h in he indi iduals wi h
highe g ow h a es ha e been desc ibed in an ample amoun o s udies (To o and Ve ga a, 1998; Ga on e
al., 1984; Bayne and Hawkins, 1997; Bayne e al., 1999; Bayne 1999; 2000; Pace e al., 2006; Tamayo e al.,
2011, 2013, 2014; P ie o e al., 2018, 2020). In addi ion, in mos o hese s udies, he di e ences in g ow h
cos s a e accompanied by di e ences ela ed o ene gy acquisi ion capaci y (acquisi ion model).
No wi hs anding he abo e, and despi e he s udies ocused on he cha ac e iza ion o he physiological basis
esponsible o he in e -indi idual di e ences in he g ow h a e o bi al es, he e is s ill no ag eemen
a ound he physiological causes o such a iabili y. As i can be app ecia ed by he li e a u e a o emen ioned,
he use o di e en popula ions along wi h he he e ogenei y o expe imen al designs migh be he eason o
he di e ences in he ela i e con ibu ion ha di e se au ho s ha e assigned o he physiological p ocesses
in he de e mina ion o he in aspeci ic di e ences in g ow h a e. Recen ly, in he se ies o expe imen s un
by P ie o e al., (2018, 2019, 2020a,b) wi h M. gallop o incialis i has been shown ha he di e en ial ene gy
balance be ween indi iduals selec ed unde di e en nu i ional condi ions a e highe and less dependan on
he cha ac e is ics o he expe imen al die in as g owing indi iduals han in slow g owing mussels. The
hypo hesis ha di e en expe imen al condi ions may al e he physiological basis upon which he di e en ial
g ow h is sus ained was also p o ed o be ue, a leas o di e en ood a ailabili y and wa e empe a u e.
Such a e i ica ion allows o indica e ha he di e ences in g ow h a e do no obey o di e ences in jus
one physiological p ocess, bu o mul iple physiological ai s, he con ibu ion o which o he p omo ion
o in e -indi idual di e ences in g ow h a e depends upon he en i onmen al cha ac e is ics in which
indi iduals g ow. F om he expe imen s es ing he di e en ood a ailabili ies, he au ho s de ined wha
migh be in e p e ed as wo basic pheno ypes o as g owing indi iduals in he mussel: i) hose ha display a
highe inna e capaci y o acqui e and p ocess ood – as eede s, and ii) hose ha show a highe capaci y
o educe he basal me abolic cos s, which allows hem o spend less ene gy in s a a ion pe iods – ene gy
sa e s. Mo eo e , hese wo pheno ypes a e easily in e changed depending on he expe imen al condi ions.
6 Fac o s a ec ing he capaci y o ene gy acquisi ion
6.1 In e -indi idual di e ences in he il e ing capaci y
In mussels, di e encesin in e -indi idualg ow h a es canbeachie edbya highe capaci y o someindi iduals
o acqui e and p ocess ood, wi hou esul ing on ei he lowe abso p ion e iciencies o highe me abolic
a es (P ie o e al., 2018). Howe e , he causes p omo ing such endogenous di e ences a e no clea . Tamayo
e al., (2011) and P ie o e al., (2018, 2020) ound a close ela ionship be ween clea ance a e and gill-su ace

20 Gene al in oduc ion
a ea in clams and mussels, espec i ely: indi iduals ha we e able o de elop highe il e ing a es we e
also he ones displaying la ge gill-su ace a eas. Gill su ace-a ea has been ound o modula e acco ding o
exogenous ac o s, such as pa icle a ailabili y, composi ion and eeding ime (Theisen, 1977; Essink e al.,
1989; F anz, 1993; Payne e al., 1995; Honkoop, 2003; Du e e e al., 2007; P ie o e al., 2018). This indica es
ha gill su ace-a ea is submi ed o a conside able pheno ypic plas ici y. Mo eo e , bo h in e -speci ic
(Iba ola e al., 2012) and size ela ed in a-speci ic allome ic-scaling di e ences (Meyhö e , 1985; Riisgå d,
1988; Jones e al., 1992; Pou eau e al., 1999) in clea ance a es a e explained by co esponding di e ences in
gill su ace-a eas (Honkoop e al., 2003). Hence, hese s udies se ou he possibili y ha he di e ences in he
il e ing capaci y migh be ela ed o ana omic di e ences: he size o he gills.
In consequence, he gill seems o be an o gan playing a majo ole in de e mining he in e -indi idual
g ow h a e di e ences. P ie o e al., (2019) sea ched o candida e genes unde lying he biological p ocesses
accoun ing o g ow h di e ences a he molecula le el in he gills o M. gallop o incialis. They ound 117
di e en ially exp essed genes in as and slow g owing mussels, mainly ela ed o di e ences in he esponse
o s imulus, g ow h and cellula ac i i y p ocesses. Fas g owing mussels showed up- egula ion o myos a in,
insulin like g ow h ac o , epide mal g ow h ac o -like domain (EGF), and genes in ol ed in he s uc u e and
unc ionali y o connec i e issue: laminin, ibulins and deco ins. On he con a y, slow g owing indi iduals
showed up- egula ion o a cell-coun ing ac o ha limi s he maximum size o he mul icellula s uc u e,
i.e., inhibi ion o de elopmen al p ocesses in he gill. Anae obic me abolic pa hways we e also enhanced, a
symp om o impai men in he ae obic ATP p oduc ion o he gill.
A ew o he s udies (Wang e al., 2010; Saa ed a e al., 2017; Zhang e al., 2019; Xie e al., 2020; Nie e al., 2021)
on gill ansc ip omic analysis o as e sus slow g owing specimens ha e also shown ha in e -indi idual
g ow h a e di e ences imply la ge amoun s o di e en ially exp essed genes (DEG). The analysis o hose
DEG in hese s udies indica e ha he di e ences in he gene ic exp essions codi y o ibosomal p o eins
and enzymes in ol ed, basically, in ene gy me abolism, p o ein syn hesis and mic o ubula mo o , a he
g ow h-con olling genes. Indeed, Saa ed a e al. (2017) speci ically sea ched o di e en ial exp ession o
genes om he g ow h Con ol Gene Co e in as e sus slow g owing Rudi apes decussa us, bu ailed o ind
i .
6.2 In e -indi idual di e ences in diges i e capaci y
Abso p ion e iciency is in luenced by he quali y and composi ion o inges ed o ganic ma e . When ood is
abundan , bi al es may dec ease hei CR o p e en excessi e sho age o gu passage ime ha could educe
he ime a ailable o ood pa icle b eakdown, diges ion and abso p ion and hence ood abso p ion e iciency.
This allows hem o p ocess he a ailable ood mo e e icien ly wi hou was ing ene gy on il e ing excessi e
Gene al in oduc ion 21
amoun s o wa e (Bayne e al., 1993). In en i onmen s wi h low ood a ailabili y, bi al es can inc ease hei
CR o maximize he in ake o a ailable nu ien s, ensu ing hey mee hei me abolic needs (Hawkins e al.,
1996). Bi al es end o ha e highe AE when consuming high-quali y ood sou ces ich in o ganic ma e ial,
such as phy oplank on, compa ed o de i us o ino ganic pa icles (Na a o e al., 1991; Bayne e al., 1993).
This egula ion ensu es ha he diges i e o gans a e no o e whelmed, allowing o mo e e icien p ocessing
and abso p ion o nu ien s (Iglesias e al., 1992). When he inges ed ma e ial is high in o ganic con en ,
bi al es can a o d o lowe hei CR sligh ly o allow mo e ime o diges ion and abso p ion, hus inc easing
AE (Na a o e al., 1991). Con e sely, i he ood is low in o ganic con en , main aining o inc easing CR can
help ensu e ha enough o ganic ma e is inges ed o mee nu i ional needs, e en i AE is lowe (Hawkins
and Bayne, 1985).
Gi en ha a unc ional engagemen exis s be ween abso p ion e iciency and inges ion a e, he capaci y o
acqui e mo e ood would no necessa ily esul in highe abso p ion a es, unless he e is also an inc ease in
diges i e capaci y. Se e al s udies (e.g., Iba ola e al., 1998, 1999, 2000; Laba a e al., 2002; Fe nández-Rei iz,
2004) p o ed acclima ion p ocesses in which he ise in enzyme ac i i ies allow o highe CR and inges ion
a es, keeping he AE cons an and no ably inc easing AR. Due o his adjus men s, i.e., plas ici y, o he
diges i e gland, i is easonable o conside ha such an adjus men can also di e be ween di e en g owing
pheno ypes, he analysis o which would bene i om he his ological app oach.
The diges i e gland has ecei e li le a en ion in he con ex o in e -indi idual g ow h di e ences. I is he
main o gan o in acellula diges ion and abso p ion, bu i is also he s o age si e o me abolic ese es and
a pa icipan in he ans e ence o me abolic ese es o o he o gans (Ca ie e al., 2004). Mo eo e , i s
mo phological appea ance has been p o ed o be o g ea plas ici y unde di e en ood a ailabili y scena ios
(e.g., Mo on, 1983; Robinson e al., 1981; Robinson, 1983). In ac , he size o he diges i e di e icula and
hei cellula olume is known o modula e (Iba ola e al., 2000). Howe e , he e is no a ailable da a on
whe he his ype o adjus men s happen along wi h ood acquisi ion capaci y o di e en g ow h a es.
Fu he mo e, expe imen s pe o med on di e en ly g owing Rudi apes decussa us clam indi iduals ailed o
ind signi ican di e ences be ween as and slow g owing indi iduals in he s anda dized size o he diges i e
glands, p o ein con en o speci ic cellulose ac i i y (Tamayo e al., 2011). These s udies p o ided he basic
knowledge o unde s and he diges i e egula ion o bi al es bu mus be comple ed wi h mo phological
assessmen s ha uphold he physiological pe o mances o di e en ially g owing indi iduals.
22 Gene al in oduc ion
7 Fac o s a ec ing he ene gy expendi u e
The p ocesses ha con ibu e o ene gy loss in bi al es a e he exc e ion o ni ogenous was e (ammonium)
and he ene gy in es ed in me abolism. Ene gy loss esul ing om he exc e ion o ammonium in he u ine
is gene ally a mino p opo ion o he o al ene gy loss in bi al es. I has been es ima ed o accoun o
a ound 1-10 % o o al me abolic expendi u e. Since i s in luence on he ene gy balance is mino , i is a
physiological pa ame e ha is usually no conside ed in ene gy balance de e mina ions (Bayne and Newell
1983; Bayne e al. 1987; Bei as e al. 1995). The e o e, in he p esen disse a ion, we will be ocusing solely
on he me abolism. Wi hin me abolic a e, wo di e en le els ha e been s ablished: he s anda d me abolic
a e (SMR) and he ou ine me abolic a e (RMR).
7.1 S anda d me abolic a e
The s anda d me abolic a e co esponds o he sel -main enance cos s o he o ganism o he cellula
homeos asis and unc ional in eg i y. The p ocesses ha con ibu e o a g ea ex en o he s anda d me abolic
expendi u e a e basically h ee: i) he p o ein u no e (cons an syn hesis and deg ada ion o cellula
p o eins), ii) he ac i i y o he ansmemb ane sodium-po assium pump o he ac i e anspo o sodium
and po assium, and iii) he p o on leak h ough he mi ochond ial memb ane (Hawkins and Bayne, 1992).
The p o ein u no e can con ibu e up o a 70 % o he s anda d me abolic a e in M. edulis (Hawkins and
Bayne, 1985; Hawkins e al., 1986, 1989). In ac , he con inuous adjus men s in he gene ic exp ession
accoun o 9-13 J o ene gy pe p o ein mg in My ilus sp. and mos animals (Hawkins e al., 1986; Mo gan
e al., 2000), which makes i he mos impo an componen o main enance me abolism. The ac i i y o
he ansmemb ane sodium-po assium pump has been measu ed in many mammalian issues and p o ed
me abolically cos ly, accoun ing o a ound 20 % o he ene gy expendi u e o issues (Milligan and McB ide,
1985; Clausen e al. 1991). In sea u chins (S ongylocen o us pu pu a us) he ac i i y was indeed simila
(18 %) o ed la ae, al hough i can be up o 60 % when s a ed (Leong, 1998). “Fu ile” p o on cycling, i.e.,
p o on leakage h ough he mi ochond ial memb ane, comes a a emendous ene ge ic cos . In mammals, i
can ep esen 20 o 50 % o o al basal me abolic a e (e.g., B and e al., 1994; Rol e e al., 1999). Simila o he
con ibu ion o Na+/K+ pump o he s anda d me abolic cos s in non-mammals, he e is e y li le e idence
abou he impo ance o p o on cycling oo. B and e al. (1991) in es iga ed hepa ocy es om he bea ded
d agon, a liza d simila in mass and body empe a u e o a a . The esul s sugges ed ha mi ochond ial
p o on cycling accoun ed o up o 30 % o espi a ion a e in he ep ile cells, simila o he alue in a
hepa ocy es.
Gene al in oduc ion 23
7.2 Rou ine me abolic a e
The ou ine me abolic a e is used o de ine he me abolic ac i i y o an o ganism unde no mal ac i i y
and eeding condi ions. The e o e, he ou ine me abolism is he esul o adding o he s anda d me abolic
expendi u es a o emen ioned he ood acquisi ion, diges ion, assimila ion and s o age expendi u es, and
hose associa ed wi h g ow h, de elopmen and ep oduc ion (Pa y, 1983; Glazie , 2005). In bi al es, he
cos s o hese p ocesses a e commonly e e ed o as cos s o g ow h and due o he eeding s a egy o hese
o ganisms, hey con o m a cons an inc ease in ela ion o he s anda d me abolism, p o ided ha he animal
can eed i sel . The cos s o ood acquisi ion, diges ion, assimila ion and s o age expendi u es, and hose
associa ed wi h g ow h, de elopmen and ep oduc ion cons i u e he cos s o g ow h in bi al es.
Hawkins and Bayne di ided he componen s o he ou ine me abolic a e in i) he cos s o cilia y ac i i y,
ii) he cos s o diges ion and abso p ion p ocesses and iii) he cos s o g ow h. The cos s o cilia y ac i i y
comp ise he il a ion p ocess accomplished by he ac i i y o he gills and labial palps, ep esen ing a ound
3 % o o al me abolic expendi u e (Sil es e and Sleigh , 1984; Jo gensen, 1986; Clemmesen and Jo gensen,
1987). The cos s o diges ion and abso p ion p ocesses we e measu ed by Widdows and Hawkins (1989) and
cons i u e a ound 17 % o o al me abolic cos s. Addi ional me abolic cos s ela ed o diges ion and abso p ion
a e me abolic aecal losses and ni ogenous compounds, al hough hese a e no me abolic expendi u es pe
se, bu a he ene gy ha is no gained. Las ly, he cos s o g ow h a e he esul o deduc ing he s anda d
me abolic a e, he cos s o cilia y ac i i y, and he cos s o diges ion and abso p ion o he o al me abolic
a e. The cos s o g ow h can be up o 34 % o he o al me abolic expendi u e and is basically he emnan
ene gy in es ed in he syn hesis o deposi ion o any kind o issue: so issues (including s o age issue),
byssus and shell.
7.3 Fac o s a ec ing he me abolic a e
7.3.1 Body size. Allome y
The ela ionship be ween body size and me abolic a e has been he subjec o s udy since he undamen al
allome ic ela ionship es ablished o mammals and bi ds was ex ended o include a wide ange o
in e eb a es, including molluscs (Hemmingsen, 1960; Zeu hen, 1947, 1953; on Be alan y, 1957). The
b oad in aspeci ic a iabili y o he allome ic mass exponen s o me abolic a e is a biological phenomenon
no ye ully unde s ood (e.g., Glazie , 2018; Ha on e al., 2019; Escala, 2022; Whi e e al., 2022). Wi hin
speci ic axonomic g oups, R–me abolic a e– o en a ies closely wi h M–body mass–, ollowing a powe
unc ion ha can be desc ibed as:
R=aMb
whe e ais he scaling coe icien (o p opo ionali y cons an ) and bis he scaling exponen (o loga i hmic
24 Gene al in oduc ion
slope). Du ing he la e 1800s and ea ly 1900s, many biologis s claimed ha b was uni e sally 2/3, he so-called
‘su ace law’, based on he idea ha me abolic esou ces, was es and hea a e exchanged ac oss o ganismal
su aces ollowing simple Euclidean geome y (Sa us and Rameaux, 1839; Glazie , 2014). This belie was
ini ially suppo ed in a ious bi ds and mammals (Glazie , 2014), bu a ound 1930s, se e al analyses o
in e speci ic me abolic scaling caused Kleibe and o he scien is s o claim ha a 3/4 exponen was uni e sal
o nea ly so. The ela ionship be ween body size and me abolic a e is s ill a sou ce o discussion conside ing
ha e en hougha easonable a ia ion bo h wi hin and among axa is acknowledged o b alue, i is unknown
i hese a ia ions a e de ia ions om he so-called gene al “¾-powe law”, o whe he he e is no such law
(Agu e and Whea ley, 2004). As explained be o e, he ¾-powe law assumes a scaling exponen o 0.75 o
i ually all o ganisms (e.g., B own e al., 2004), despi e he ac i i y o me abolic le el, gi ing he imp ession
o a common unde lying mechanis ic o igin (Sa age e al., 2004). Howe e , due o he b oad assump ions
o he law and he ample amoun o examples in which he b alue de ia es om 0.75 (see Glazie , 2005), i
has su e ed ha sh c i icism (e.g., Bokma, 2004; Sua ez e al., 2004; Glazie , 2005; Mulle -Landau e al., 2006;
Whi e e al., 2007; Glazie , 2008; Glazie , 2009; Glazie , 2010; Whi e, 2011; Ca ey e al., 2013), and i seems o
be no longe accep able (Glazie , 2022b).
The a ia ion in he me abolic scaling exponen is ela ed o ecological (ex insic) and biological/endogenous
ac o s (in insic). In insic e ec s include hose exe ed by (i) di e ences in body- empe a u e egula ion
s a egies (i.e., endo he mic s. ec o he mic animals) (Glazie , 2010; Whi e e al., 2006, 2019; Bigman e al.,
2021), (ii) ac i i y le el (Glazie , 2005, 2008, 2009, 2010, 2014; Whi e e al., 2007), (iii) li e cycle s ages (Glazie ,
2005; Glazie e al., 2015), (i ) sex (Glazie , 2005; Mo e e al., 2022), ( ) gene ic s ains (Ke ola and Ko iaho,
2012; Ma ho e al., 2013; Ma oo e al., 2019) and ( i) cellula g ow h modes (Kozlowski e al., 2003; Glazie ,
2022a). Ex insic ac o s, on he o he hand, include empe a u e, pH, salini y, ligh in ensi y, p eda o s,
pa asi es, a ailabili y o esou ces as well as die , habi a o ecological li es yle (Lo eg o e, 2000; Glazie ,
2005, 2006, 2014, 2018, 2020; McKechnie e al., 2006; Jeyasingh, 2007; Killen e al., 2010; McFee e s e al.,
2011; Glazie e al., 2011, 2020; Ma sden e a., 2012; Whi e and Kea ney, 2013; Ca ey and Sigwa , 2014;
Londono e al., 2015; Pequeno e al., 2017; Bushue e al., 2018; Fossen e al., 2019; Rubalcaba e al., 2020;
Gjoni e al., 2024).
The e ec s o he ecological and endogenous ac o s a ec ing me abolic scaling is p obably he consequence
o pheno ypic plas ici y coming o ei he biological egula ion o na u al selec ion (Glazie , 2022b). In ac ,
biological scaling is mo e and mo e pe cei ed as pheno ypically plas ic and e olu iona ily plian nowadays,
a he han physically o de elopmen ally cons ained (e.g., Ha e, 2002). As an answe o he accep ance o
he me abolic scaling di e si y, many mul i-mechanis ic models ha e been p oposed o explain i (see Glazie ,
2018 o e iew). Howe e , only he me abolic-le el bounda ies (MLB) hypo hesis p oposed by Glazie (2005;
2010, 2014) seems o explain no only mos o he a ia ion among axa bu also amongs physiological s a es.

Gene al in oduc ion 25
The MLB hypo hesis desc ibes how he obse ed alues o b o en all be ween he heo ized bounda y alues
o 0.667 and 1. I explains how b a ies when supply exceeds me abolic demand and when me abolic demand
exceeds supply. The luc ua ion o he scaling exponen be ween hose end alues migh depend on me abolic
a e, ac i i y and ecological ac o s (Glazie , 2010).
7.3.2 Physiological s a us
Cos s o main enance and g ow h change depending on he physiological s a us ha can in u n a y in a
sho , medium o long e m acco ding o acclima iza ion p ocesses. Con inuous changes in en i onmen al
condi ions like empe a u e, oxygen a ailabili y, salini y and wa e low a es in luence eeding e iciency
and ene gy expendi u e du ing ood acquisi ion, diges ion and assimila ion (Widdows and Bayne, 1971).
Fo ins ance, op imal empe a u es enhance enzyma ic ac i i ies in ol ed in p o ein syn hesis, educing he
ene gy equi ed o hese p ocesses (Hochachka and Some o, 2002), while hypoxic condi ions may inc ease
he ene gy cos s o p o ein syn hesis as he indi iduals swi ch o less e icien anae obic pa hways (De Zwaan
and Wijsman, 1976). All hose ac o s also ha e an impac on ood a ailabili y and nu i ional quali y, upon
which he cos s o ood acquisi ion undamen ally depend on (e.g., Bayne and Wo al, 1980). Fluc ua ions
in die composi ion also a ec he diges ion and assimila ion e iciency, as well as enzyme p oduc ion and
ac i i y (Iba ola e al., 1998a,b, 1999, 2000; K eege and Newell, 2001). In ac , adequa e and consis en
ood supply ensu es ha bi al es ha e he necessa y esou ces o e icien p o ein p oduc ion, educing
he me abolic cos s associa ed wi h p o ein syn hesis (Hawkins e al., 1985). Howe e , ni ogen misma ches
be ween ood and body issues mus be compensa ed by physiological mechanisms o homeos a ic nu ien
egula ion associa ed o p o ein biosyn hesis and hyd olysis u no e a es in di e en issues (A anz e al,
2023). Exposu e o pollu an s and pa hogen p esence can also inc ease p o ein u no e a es as bi al es
epai damaged p o eins and main ain cellula homeos asis (Hochachka and Some o, 2002; I anina e al.,
2010).
Adap a ions in he longe - e m in ol e seasonal changes ha happen concu en ly wi h ood a ailabili y. The
way an o ganism is con on ed wi h he seasonali y does no only depend on he ange in en i onmen al
dynamics, bu also on he physiological esponsi eness o he o ganism o hese condi ions. Fo example, a
physiological esponse (i.e., change in he inges ion a e) o an inc ease in ood concen a ion will be smalle
i his change occu s wi hin he ange o he unc ional esponse o he o ganism han i i occu s ou side o i .
In u e dependency o seasonali y and he concomi an ood a ailabili y he e is game ogenesis. In ac , i is
commonplace o obse e ha o mos ma ine and es ua ine in e eb a es game ogenesis is cyclical, wi h
cycles occu ing wi h an annual, mon hly o luna pe iodici y, and ound in pola , empe a e and in opical
species (Giese, 1959; Moo e, 1972). The ep oduc i e cycle also makes he cos s o g ow h a y, as ene gy
s o age in he o m o glycogen o lipids luc ua es depending on he ep oduc i e s age, wi h inc eased
26 Gene al in oduc ion
s o age be o e spawning (Be helin e al., 2000). Rep oduc i e cycles can in luence p o ein u no e a es, wi h
inc eased demands o p o ein syn hesis du ing game ogenesis and spawning (Gabbo , 1983). Fu he mo e,
he ene gy cos o ep oduc ion a ies wi h he s age o game ogenesis, wi h signi ican ene gy di e ed
om soma ic g ow h du ing spawning (Bayne, 1976). Du ing he p e- ep oduc i e s age, bi al es p ima ily
alloca e ene gy owa ds soma ic g ow h and shell o ma ion. Ene gy expendi u e is ela i ely low since less
ene gy is di e ed o ep oduc i e p ocesses (Bayne and Wo all, 1980). Du ing game ogenesis, bi al es begin
o alloca e signi ican ene gy owa ds he de elopmen o ep oduc i e issues. This shi esul s in a dec ease
in he ene gy a ailable o soma ic g ow h (Bayne, 1976). The spawning s age is cha ac e ized by he elease
o game es, which is ene ge ically demanding. This s age o en sees he highes di e sion o ene gy away
om soma ic g ow h owa ds ep oduc i e e o , lea ing e y li le o g ow h (Bayne and Newell, 1983).
Following spawning, bi al es en e a eco e y phase whe e ene gy alloca ion shi s back owa ds soma ic
g ow h and main enance, al hough eco e y o deple ed ene gy ese es is a p io i y (Gabbo , 1975).
7.3.3 Geno ype
Co ela ions be ween allozyme mul ilocus he e ozygosi y and i ness- ela ed cha ac e s in bi al e molluscs
ha e been unde s udy o decades (e.g., Koehn and Shumway, 1982; Fol z and Zou os, 1984; Koehn and
Ga ney, 1984; Zou os and Fol z, 1987; Gen ili and Beaumon , 1988; Koehn e al., 1988; Zou os e al., 1988;
Hawkins e al., 1989; Volckae and Zou os, 1989; Ga ney e al., 1990; Beaumon , 1991). When es ing
he easons o such co ela ion, inconsis encies we e ound, which lead o wo hypo hesis: he “di ec
o e dominance” hypo hesis (Koehn and Shumway, 1982; Mi on, 1993) poin ed a he enzymes as he di ec
esponsible o he co ela ion and he “associa i e o e dominance” hypo hesis (Oh a, 1971; Zou os e al., 1980)
pos ula ed he allozymes o only be indica o s o he gene ic condi ion esponsible o he co ela ion. La e ,
da a ob ained om s udies on DNA ma ke s a ou ed he associa i e o e dominance hypo hesis (Bie ne e al.,
1998, 2000; Col man e al., 1998; Coulson e al., 1998; Pogson and Fe olden, 1998). Independen o he cause
o he he e ozygosi y, he e ozygous indi iduals would na u ally exp ess a wide basal ange o e ec i e
p o eins, allowing he a oidance o new enzyme p oduc ion in he ace o changes in he en i onmen . Which
means ha di e en he e ozygosi y le els could ul ima ely be linked o di e en geno ypes wi h a lowe o
highe e iciency in he p o ein u no e . In his con ex , s udies conside ing di e ences in p o ein u no e
abili y sugges i as an impo an dis inc ea u e be ween di e en ially g owing indi iduals (Meye and
Manahan, 2010; Hedgecock e al., 2007; Hawkins and Bayne, 1992; Hawkins e al., 1986, 1997;; Wang e al.,
2018; Xie e al., 2020; Zhang e al., 2021). Mo eo e , some bi al e geno ypes a e mo e e icien han o he s a e
in con e ing (i) nu ien s in o p o eins (To o e al., 2004) and (ii) inges ed ood in o biomass, wi h op imized
mechanisms o diges ion and assimila ion, allowing hem o suppo apid issue g ow h (Filguei a e al.,
Gene al in oduc ion 27
2015). In ac , selec i e b eeding o as g ow h can enhance ai s such as mo e e icien nu ien abso p ion
and as e issue g ow h (Ve caeme and Langdon, 2005).
Howe e , in e -indi idual di e ences in o he p ocesses migh be esponsible o he me abolic cos s
di e ences in he g owing pheno ypes. Fo ins ance, Saa ed a e al., (2017) and P ie o e al., (2019) ound
in clams (R. philippina um) and mussels (M. gallop o incialis), espec i ely, a di e en ial gene exp ession in
genes ela ed o he immune sys em. Slow g owing indi iduals showed o e exp ession o genes in ol ed in
immune and de ence ypically exp essed in esponse o di e en s ess ypes ( empe a u e, salini y, me al
exposu e o bac e ia).
7.3.4 Fa y acid composi ion and ROS p oduc ion
Besides ATP p oduc ion, mi ochond ia a e in ol ed in a ious signal ansduc ion pa hways and many o he
ac i i ies in he cell (e.g., Kas anio is e al., 2017; San ulli e al., 2015; Pede sen, 1999; P asad, 2011; Pa appa e
al., 2011; Mis y e al., 2019). Howe e , e en in good condi ions, he elec on- anspo chain localized in
mi ochond ial memb anes is he majo cellula si e whe e oxygen is educed, being he main sou ce o eac i e
oxygen species (ROS) gene a ion in he cell. ROS a e he e o e a colla e al damage o he no mal me abolism
in he cell, a ou ine and necessa y p ocess ha is hence ine i able. In consequence, ROS p oduc ion is also
di ec ly p opo ional o cell ac i i y (Tamu a e al., 2020). Taking in o accoun hei high eac i i y, hese ROS
can ini ia e ee- adical p ocesses and cause he des uc ion o memb ane lipids, p o eins, and damage o
mi ochond ial DNA (K yla o e al., 2018). In ac , he accumula ion o damages caused by hese ee adicals
has been held accoun able o he dec ease in physiological unc ions ha ul ima ely leads o he aging and
dea h o he o ganism (Bu eme e al., 2010; Pamplona e al., 2011), which is known as he ee adical heo y
(Ha man, 1956). In bi al es, i has been ecen ly p o en he in e se co ela ion be ween ROS p oduc ion and
li espan (Is omina e al., 2023).
Acco ding o a ecen iewpoin , he cha ac e is ics o he a y acids in mi ochond ial memb anes may
in luence he a e o oxida i e damage in cells, and hus li espan (Hulbe and Else, 1999; Ba ja, 2002; Pamplona
e al., 2002; Hulbe e al., 2007). This co ela ion has also been demons a ed in a ious bi al e species
(Mun o and Blie , 2012; Rod íguez e al., 2019; Ung a i e al., 2016; Is omina e al., 2023). A highe cellula
edox homeos asis is associa ed wi h lowe le els o accumula ed mac omolecula damage, bu no necessa ily
wi h g ea e an ioxidan capaci ies no speci ic ac i i ies (Ung a i e al., 2016), which means ei he a lowe
ROS p oduc ion o less damage. The lipid composi ion o he cell memb ane migh also a ec he me abolic
expendi u es. In he oys e C. gigas, o ins ance, a posi i e signi ican co ela ion has been desc ibed be ween
he s anda d me abolism and he deg ee o phospholipid unsa u a ion in he memb anes (Pe ne e al., 2006,
2007, 2008). This sugges ha a lowe unsa u a ion le el in he memb anes allows o a lowe p o on leakage,
28 Gene al in oduc ion
u ning he me abolism in o a mo e e icien one. Enhanced memb ane and mi ochond ial e iciency can
lead o be e g ow h pe o mance, as mo e ene gy is a ailable o biosyn he ic p ocesses and less is los as
hea o used in main enance me abolism (Pö ne e al., 1999).
Oxida i e damage may be posi i ely ela ed o g ow h a e, due o he highe a e o ROS p oduc ion ha can
accompany g ea e cellula ac i i y. Fo example, ansgenic mice ha g ow as due o o e exp ession o
g ow h ho mone p oduce mo e ROS and ha e a g ea e incidence o lipid pe oxida ion (Rollo e al. 1996).
Simila ly, ele a ed g ow h a es ha e been eco ded as causing bo h a educ ion (Alonso-Al a ez e al., 2007)
and an inc ease (De Block and S oks, 2008) in an ioxidan de ences; hese opposi e ends we e none heless
bo h in e p e ed as indica ing g ea e oxida i e damage. I has been sugges ed ha oxida i e s ess migh
play a key ole as a cons ain on, and cos o , g ow h (Schan z e al., 1999; Monaghan e al., 2009) and i
has been measu ed in plan s (Zhang e al., 2016), cap i e inches (Alonso-Al a ez e al., 2006), wild alpine
ma mo s (Cos an ini e al., 2012) and ba n swallows (Cos an ini, 2014). Ye inconsis en pa e ns ha e been
epo ed o he ela ionship o g ow h wi h oxida i e s ess. Enhanced g ow h ha e been linked o highe
an ioxidan le els bu inc eased oxida i e damage in co ids (Salomons, 2009), sheep (Nussey e al. 2009),
scallops (Gue a e al., 2012), coal i s (S ie e al., 2014). Reduced le els o an ioxidan s ha e been ela ed
o g ow h in g ea i s (Kilgas e al., 2010), and bo h aised and educed an ioxidan le els in coho salmon
(Legga e al., 2007; Alm o h e al., 2012), bu o he s udies ha e ound no e ec (Rosa e al., 2008; La combe
e al., 2010; Geige e al., 2011).
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60 Gene al in oduc ion
Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes 67
a ion. Howe e , i a be e unde s anding o he g owing pa e ns is pu sued, esea ch should be done on he
implica ions o hose physiological di e ences a o he biological o ganisa ion le els.
As s a ed abo e, a ia ion in he g ow h o mussels has implica ions o bo h indi idual i ness and popula ion
dynamics. Comp ehending such a ia ion would be aluable o conse a ion and managemen and, he e o e,
wouldhelp imp o eaquacul u e p oduc ion(Kendall and Fox, 2002). He ewe ackle he indi idual a ia ion in
he g ow h o mussels om a mul idisciplina y app oach o ob ain a holis ic unde s anding o he o ganiza ion
and unc ion o he g owing pa e ns. The wo k aims o es ablish a connec ion be ween he physiological
pe o mances o he di e en g owing p o iles, and he issue s uc u e and cellula ac i i y o he wo main
o gans in ol ed in ene gy acquisi ion and p ocessing.
2 Ma e ials and me hods
2.1 Collec ion o mussel seeds and expe imen al se up
Mussel seeds, My ilus gallop o incialis, we e collec ed in Feb ua y 2020 om monolaye mussel beds g owing
in a ocky in e idal a ea loca ed in Iba angelu (Biscay, Spain, 43°24’ N; 2°40’ W). Mussels we e ans e ed
o he labo a o y in ai -exposed we con aine s a ambien empe a u e.
A he labo a o y, he shell leng h o all he indi iduals was measu ed wi h elec onic calipe s and 300
homogeneously sized indi iduals (shell leng h o 10.98 ±0.52 mm) we e so ed o expe imen s and placed
in a ank (50 L) a cons an seawa e salini y (33 PSU) and empe a u e (18 °C). The selec ed seeds we e
ea ed in he labo a o y du ing a 3-mon h pe iod unde a cons an ood supply ha consis ed o a suspension
o cul u ed algae Isoch ysis galbana (T-Iso) cons an ly dosed a 20,000 cells
·
mL
-1
. The concen a ion was
main ained s able by equen ly checking wi h a Coul e Mul isize 3 and homogenei y ensu ed wi h ai
ci cula ion. Du ing he ea ing pe iod, he anks we e cleaned up and seawa e - enewed wice a week. When
cleaned, mussels we e sepa a ed om one ano he by gen ly cu ing he byssus o a oid in e -indi idual
compe i ion o ood.
The i s week o he ea ing pe iod, he clea ance a e and he oxygen consump ion was de e mined in 20
andomly selec ed indi iduals. Those same indi iduals we e hen dissec ed o his ological analysis. The
emaining se o mussel seeds was main ained o h ee mon hs. A e his pe iod, he la ges 40 ( as -g owe s
– F), he 40 medium-sized mussels (in e media e g owe s – I) and he smalles 40 (slow-g owe s – S) we e
selec ed o be acclima ized unde wo di e en ood- a ions o wo weeks. Hal o he mussels (n = 20 o
each g owing condi ion) we e ed wi h a high a ion (50,000 cells
·
mL
-1
) and he o he hal wi h a low a ion
(10,000 cells ·mL-1).

68 Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes
A e heacclima ion pe iod, 10indi iduals om eachg oup abo ewe e used o measu e he maincomponen s
o he ene gy balance (clea ance a e –CR– and ou ine me abolic a e –RMR–). Once he physiological
measu emen s we e comple ed, whole animal lesh ( o he smalles indi iduals) and a c oss sec ion including
man le, gills and diges i e gland ( o he medium-size and la ges mussels) we e ex ac ed o his ological
examina ion. The gills o 10 addi ional mussels om each o hose six g oups we e ozen in liquid ni ogen
and s o ed a - 80 °C o biochemical analysis.
Figu e 1. Shell-leng h dis ibu ion o he mussels upon a i al o he labo a o y (ini ial size) and a e
h ee mon hs ( inal size). The shaded a eas delimi he size ange o he selec ed F, I and S mussels; hei
co esponding shell-leng hs (mm) and li e weigh s (g) (mean ±s anda d de ia ion) a e indica ed.
2.2 Biome y
The shell-leng hs and li e weigh s o indi idual mussels we e measu ed once e e y wo weeks using 0.05 mm
accu acy calipe s and a 0.01 mg accu acy balance.
2.3 Physiological pa ame e s
2.3.1 Clea ance a e (CR: L ·h-1)
Clea ance a e was measu ed by placing he mussels in expe imen al glass bo les o 250 mL wi h ounded
edges, he low a es o which we e adjus ed o ob ain a educ ion o 15–30 % on he pa icle concen a ion
Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes 69
compa ed wi h he con ol chambe . Samples o wa e in he ou low o indi idual and con ol chambe s
we e aken e e y hou du ing 11–12 h. Thus, he
CR
o each indi idual was calcula ed as he mean alue
o 11–12 de e mina ions du ing he whole day, and acco ding o he exp ession p oposed by Hild e h and
C isp (1976):
CR =F·((Ci−C0)/Ci)
whe e
F
is he low a e (L
·
h
-1
),
Ci
is he pa icle concen a ion in he con ol ou low and
C0
he pa icle
concen a ion in he ou low o he expe imen al chambe . Pa icle concen a ions we e de e mined wi h a
Coun e Coul e Z1.
2.3.2 Me abolic expendi u e (RMR: mL O2·h-1)
Rou ine me abolic a e was assessed by measu ing oxygen consump ion. Mussels we e emo ed om eeding
chambe s and in oduced in o espi ome e s o a ound 50 mL sealed wi h LDO oxygen p obes connec ed
o oxime e s (HATCH HQ40d). Ra es o oxygen consump ion we e compu ed om he decline in oxygen
concen a ion in he chambe s egis e ed du ing 3–4 h, o un il alues dec eased 20–30 % o ini ial baseline,
e e y 5–10 min. A con ol chambe was used o check he s abili y o he oxygen concen a ion.
2.3.3 Size s anda diza ion o physiological a es
CR and RMR we e s anda dised o a common li e weigh o 1 g, acco ding o he exp ession:
YST D = (1/WEXP )b·YEXP
in which
YST D
and
YEXP
ep esen , espec i ely, s anda d and expe imen al physiological a es and
WEXP
ep esen s heexpe imen al li eweigh o heindi idual. The powe aluesused o scale physiological
a es o body weigh (b) we e 0.58 (Bayne and Hawkins, 1997) o CR and 0.724 (Bayne e al., 1973) o RMR.
2.4 Gill su ace-a ea (GA: mm2·g-1)
Pho og aphs o he gill o 20 mussels we e aken wi h a digi al came a and he su ace a ea o he gills om
each indi idual was calcula ed using ImageJ so wa e (Na ional Ins i u es o Heal h). As a means o ensu e
co ec sizing, millime ic pape was placed unde he mussel when aking he pho og aph. Da a shown
co espond o one side o he demib anch. Gill a eas we e s anda dised o an equi alen o 1 g li e-weigh
mussel acco ding o he o mula:
GAST D = (1/WEXP )b·GAEXP
70 Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes
whe e
GAST D
and
GAEXP
ep esen he s anda dized and expe imen al gill a eas, espec i ely, and
WEXP
is he expe imen al li e weigh o he mussel. The powe unc ion used o scale gill a ea o li e weigh
was 0.66 (Vahl, 1973; Hawkins and Bayne, 1992; Jones e al., 1992).
2.5 His ology
The whole o ganisms o c oss sec ions (n = 10 pe expe imen al g oup) we e ixed in seawa e wi h 4
% o maldehyde, dehyd a ed in an e hanol ba h se ies, pa a in-embedded using a Leica ASP3005 issue
p ocesso and sec ioned a 5 wi h a Leica RM2125RTS mic o ome. Pa a in sec ions we e s ained wi h
wo di e en s aining p ocedu es. On he one hand, hema oxylin-eosin (H/E) s aining was used o analyze
he diges i e gland, gills and man le. On he o he hand, oluidine-eosin s aining was employed o be e
disc imina e basophilic cells in he diges i e gland (Blanco-Rayón e al., 2019).
2.5.1 Diges i e gland assessmen
The diges i e issue a io (CTD), he changes in olume densi y o basophilic cells (V BAS) and he a ophy
o he epi helium o he diges i e al eoli we e measu ed.
CTD and
V BAS
we e quan i ied h ough s e eology, by coun ing h ee andomly selec ed ields in each slide
a 40×objec i e ( inal magni ica ion 400×) and employing a d awing ube a ached o a ligh mic oscope. A
simpli ied e sion o he Weibel g a icule mul ipu pose es sys em M-168 (Weibel, 1989) was used o eco d
he hi s on basophilic cells (b), diges i e cells (d), di e icula lumens (l) and in e s i ial connec i e issue (c).
CTD a io was calcula ed as CTD = c/(b + d + l).
V BAS
was compu ed ollowing Delesse’s p inciple (Weibel,
1989), as
V BAS
/VEP, whe e
V BAS
is he olume o basophilic cells and VEP he olume o diges i e gland
epi helium.
Following Kim e al. (2006), a g ading om 0 o 4 was used o calcula e he a ophy index o he diges i e
al eoli. In ha classi ica ion, 0 means no mal diges i e di e icula wi h nea ly occluded lumen; 1 means
co-occu ence o no mal and pa ially a ophied ubules o epi helium hickness g ea e han one-hal o
no mal; 2 means diges i e epi helium hickness hal o no mal; 3 means signi ican ly a ophied ubules wi h
diges i e epi helium less han hal as hick as no mal, and 4 means ha diges i e epi helium is ex emely hin
and nea ly all ubules a e a ec ed.
2.5.2 Adipog anula cell densi y
The adipog anula (ADG) cell densi y was es ima ed as desc ibed by Bignell e al. (2008) using a g ading
sys em, whe e 0 means no ADG cells appa en wi hin esicula connec i e issue, 1 means ADG cells can be
seen bu hey appea o be sca ce, 2 means ADG cells appea sca e ed h oughou man le issue, 3 means
Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes 71
he e is a ma ked inc ease in he abundance o ADG cells and some a eas may no appea o show absolu e
consis ency, and 4 means ADG cells can be seen o cons i u e he majo i y o connec i e issue olume.
2.5.3 Gill s uc u e
To assess he gill s uc u e a g ading sys em was designed based on he on al and la e o- on al cilia densi y
and epi helium o ganiza ion (Table 1). No mal cilia densi y in mos lamella and well-o ganized epi helium
was g aded wi h he highes sco e. When a e age cilia densi y was less han no mal in mos lamella, bu
epi helium was s ill well o ganized, he sco ing lowe ed o one. The sco ing was he lowes when a e age
cilia densi y was less han no mal in nea ly all lamella and he epi helium showed an e iden diso ganiza ion.
Table 1. Semi-quan i a i e scale o gill s uc u e assessmen .
Sco e Desc ip ion
0F on al and la e o- on al cilia densi y is low, and cell damage and a
diso ganized epi helium is e iden
1F on al and la e o- on al cilia densi y is low bu he epi helium is
well o ganized
2F on al and la e o- on al cilia densi y is high and he epi helium is
well o ganized
2.6 Biochemical de e mina ions in he gill
Gills o 10 mussels om each o he six expe imen al g oups we e indi idually homogenised in 0.05 M
po assium phospha e bu e (pH 7.0). The homogena e was cen i uged a 10,000 g o 20 min a 4 °C and he
supe na an s we e s o ed a - 80 °C un il analysis. The gill samples we e analysed o glu a hione S- ans e ase
(GST), ca alase (CAT) and cy och ome c oxidase (COX) enzymes. All enzyme ac i i ies we e measu ed in
96-well pla es using a mic opla e eade (TECAN In ini e 200), analysed using Magellan so wa e (TECAN)
and we e exp essed as a unc ion o he p o ein concen a ion in he samples. The p o ein concen a ion
was de e mined in iplica e acco ding o B ad o d’s me hod adap ed o a mic opla e and using
γ
-bo ine
globulins as s anda d (Guilhe mino e al., 1996).
CAT ac i i y was measu ed as deg ada ion o hyd ogen pe oxide (H
2
O
2
, Fluka 95302) media ed by CAT
a 240 nm (Claibo ne, 1985). GST ac i i y was measu ed as he o ma ion a e o he conjuga ed subs a e
chlo odini obenzene-glu a hione (CDNB-GSH) a 340 nm, acco ding o Habig e al. 1974. When measu ing
COX ac i i y, in b ie , isola ion and assay condi ions we e as ollows: homogeniza ion bu e : 25 mM
po assium phospha e, pH 7.2, 10
µg/ml
PMSF, 2
µg/ml
ap o inin; assay: 20 mM po assium phospha e, pH
7.0, 16
µM
educed cy och ome c(II), 0.45 mM n-dodecyl-b-d-mal oside, 2
µg/ml
an imycin A; acquisi ion
wa eleng h: 550 nm.
72 Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes
2.7 S a is ical analysis
Da a was e alua ed i s o no mali y and homoscedas ici y by means o Shapi o-Wilk and Le ene’s es ,
espec i ely. In hose cases whe e no mali y was no ollowed, da a we e loga i hmically ans o med a e
which no mali y was held. Signi ican e ec s exe ed by g ow h-condi ion (F, I o S) and ood a ion (high o
low) on physiological and his ological measu emen s we e analyzed employing a wo-way ANOVA. As a pos
hoc Tukey (homogenei y o a iances) o Games-Howell (no homogenei y o a iances) es s we e applied.
Semi-quan i a i ely ga he ed da a was analyzed h ough non-pa ame ic es s. Fo K uskal-Wallis, Dunn’s
es was applied as pos hoc. S a is ical analyses we e pe o med using IBM SPSS S a is ics 25. Co a iance
analysis (ANCOVA; Za , 2010) was used o es he signi icance o di e ences be ween eg ession coe icien s
o he di e en g ow h a es.
3 Resul s
3.1 G ow h a e o as and slow g owe s
In e -indi idual di e ences in he g ow h a es we e e iden enough a e 3 mon hs as o easily selec as ,
in e media e and slow g owe s. F indi iduals we e 3.5 imes hea ie han S indi iduals we e, and hei shell
leng h was almos 70 % la ge han S mussels shells (Fig. 1). Indeed, i he g ow h a es (mm·day
-1
) o he
selec ed mussels a e compu ed by adjus ing linea eg ession models o he a ia ions o he mean alues o
shell leng hs wi h ime, he ollowing equa ions a ise:
Fas g owe s:
0.163 (±0.002) x ime (days) + 10.979 (±0.057), F = 8899.1, p < 0.001
In e media e g owe s:
0.110 (±0.001) x ime (days) + 10.979 (±0.036), F = 9218.2, p < 0.001
Slow g owe s:
0.052 (±0.001) x ime (days) + 10.979 (±0.038), F = 1817.9, p < 0.001
Unde main enance condi ions, as g owe s g ew an a e age o 0.163 mm·
-1
, in e media e g owe s 0.110
mm·
-1
and slow g owe s 0.052 mm·
-1
. Analysis o co a iance e ealed signi ican di e ences o he slopes
(slope es : F alue = 1066.038, d = 1026, p < 0.05), and mul iple compa ison among slopes e ealed ha
he h ee o hem we e s a is ically di e en om one ano he (bF s. bS: q = 79.972, p < 0.05; bF s. bI: q =
38.619, p < 0.05; bS s. bI: q = 40.678, p < 0.05).

Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes 73
3.2 Physiological componen s o he ene gy balance
3.2.1 Clea ance a e (CR: L ·h-1 ·g-1)
Fas -g owing indi iduals a ained signi ican ly 2 imes highe CR alues han hei slow-g owing coun e pa s
did(0.429 ±0.19 L·h
-1
·g
-1
s. 0.216±0.12L ·h
-1
·g
-1
, espec i ely), whileI indi iduals displayed in e media e
alues (0.321 ±0.15 L ·h
-1
·g
-1
) no di e en o hose o F and S mussels (Fig. 2). Fo bo h ood a ions,
he h ee g ow h-condi ion g oups ollowed a qui e simila pa e n. CR alues we e signi ican ly 2 imes
highe in he mussels ed wi h he low-concen a ed a ion (0.411 ±0.16 L ·h
-1
·g
-1
) when compa ed o he
mussels ed he high ood a ion (0.233 ±0.15 L ·h
-1
·g
-1
). Acco dingly, he wo-way ANOVA showed in Fig.
2 indica es ha bo h g ow h condi ion and a ion, bu no he in e ac ion, exe ed a signi ican e ec on he
CR o he mussels. The mean CR o mussels eco ded du ing he i s week o he expe imen is shown in he
igu e o compa a i e pu poses. Al hough no a emp o s a is ical es ing has been made, he main enance
o mussels in he labo a o y unde he condi ion o con inuous eeding exe ed a posi i e e ec upon he CR
in F an I mussels, bu no S mussels.
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1
CR (L · h-1)
IS F I S
Low High
F
Ini ial
Figu e 2. Clea ance a e (L ·h
-1
·g
-1
) o as (F: da k g ey), in e media e (I: ligh g ey) and slow (S: whi e)
g owing mussels o low-concen a ed (maize yellow) and high-concen a ed (blue) a ions. The clea ance
a e om he ini ial de e mina ion is also depic ed. In e als indica e s anda d de ia ion. On he op, he
wo-way ac o ANOVA es ing signi ican e ec s o g ow h condi ion (F, I o S) and a ion (Low o High) is
shown.
74 Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes
3.2.2 Rou ine me abolic a e (RMR: mL O2·h-1 ·g-1)
Mean alues o ou ine me abolic a e a e plo ed in Fig. 3. The oxygen consump ion o mussels was ound o
dec ease sha ply du ing he ea ing pe iod. The mean RMR alue was 0.09 ±0.017 mL O
2
·h
-1
·g
-1
du ing
he i s week a he labo a o y and ebled ha o he mean oxygen consump ion eco ded o selec ed F,
I and S mussels: 0.03 ±0.005 mL O
2
·h
-1
·g
-1
. The wo- ac o ANOVA indica es ha nei he he g ow h
condi ion no he ood a ion ac o s exe ed any signi ican e ec on he RMR.
0.00
0.02
0.04
0.06
0.08
0.10
0.12
Media
VO2(mL· h-1 ·g-1)
Ini ial IS F I S
Low High
F
Figu e 3. Oxygen consump ion (mL O
2·
h
-1·
g
-1
) o as (F: da k g ey), medium (I: ligh g ey) and slow (S: whi e)
g owing mussels o low-concen a ed (maize yellow) and high-concen a ed (shappi e blue) a ions. The
oxygen consump ion om he ini ial de e mina ion is also depic ed. In e als indica e s anda d de ia ion.
On he op, he wo-way ac o ANOVA es ing signi ican e ec s o g ow h condi ion (F, I o S) and a ion
(Low o High) is shown.
3.3 Gill su ace-a ea (GA: mm2·g-1)
Mean alues (±SD) o he gill su ace-a ea and he wo-way ac o ANOVA a e shown in Fig. 4. The wo-way
ANOVA indica es ha i espec i e o he a ion, he e a e di e ences among he gill su ace-a ea alues o
he g owing g oups. Tukey es e ealed ha F mussels had signi ican ly 40 % la ge gill su ace-a ea han
S mussels (p < 0.001): a e age alue o F g owe s is a ound 70 mm
2
·g
-1
, whe eas ha o S mussels abou
40 mm
2
·g
-1
. The alue o in e media e g owe s alls down o a mid- alue o a ound 56 mm
2
·g
-1
, which is
signi ican ly di e en om he alue o S mussels (p < 0.001), bu no om ha o F mussels (p = 0.077),
acco ding o pos hoc es s.
Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes 75
Gill a ea (mm2· g-1)
0
20
40
60
80
100
120
.
F
I
S
blanc
F
I
S
IS F I S
Low High
F
Figu e 4. Gill su ace-a ea (mm
2
·g
-1
) o as (F: da k g ey), in e media e (I: ligh g ey) and slow (S: whi e)
g owing mussels o low-concen a ed (maize yellow) and high-concen a ed (shappi e blue) a ions. In e als
indica e s anda d de ia ion. On he op, he wo-way ANOVA es ing signi ican e ec s o g ow h condi ion
(F, I o S) and a ion (Low o High) is shown.
3.4 His ological analysis o he diges i e gland
The esul s o he s e eological analysis o he diges i e gland o F, I and S mussels ed low and high ood
concen a ions a e compiled in Table 2, oge he wi h a summa y o he wo- ac o analysis o a iance. The
ini ial alues o each pa ame e a e also shown.
Table 2. Tissue-le el bioma ke s measu ed in as (F), medium (I) and slow (S) g owing mussels ed low and
high concen a ed ood a ions. CTD a io: Connec i e o Diges i e a io;
V BAS
: basophilic cell olume
densi y. Mean alues (±SD) a e p esen ed oge he wi h a summa y o wo- ac o ANOVA es ing signi ican
e ec s o g ow h condi ion and expe imen al ood- a ion. N = 10 each expe imen al g oup. Ini ial alues a e
shown on he le .
Tissue-le el Ini ial G ow h Low concen a ion High concen a ion Sou ce o in e ac ion
bioma ke s g oup (10,000 cells·mL-1) (50,000 cells·mL-1)
Mean (±SD) Mean (±SD) G ow h condi ion Ra ion In e ac ion
CTD a io 0.071 (±0.07) F0.163 (±0.12) 0.173 (±0.11) DF = 2 DF = 1 DF = 2
I0.344 (±0.21) 0.119 (±0.08) F = 34.41 F = 11.34 F = 8.48
S0.638 (±0.61) 0.399 (±0.26) p = 0.000 p = 0.001 p = 0.000
V BAS 0.213 (±0.06) F0.351 (±0.07) 0.241 (±0.06) DF = 2 DF = 1 DF = 2
I0.232 (±0.07) 0.288 (±0.07) F = 19.79 F = 3.67 F = 13.72
S0.401 (±0.12) 0.366 (±0.15) p = 0.000 p = 0.057 p = 0.000
76 Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes
3.4.1 Connec i e- o-diges i e (CTD) a io o he diges i e gland
G ow h condi ion, ood a ion and he in e ac ion e m exe ed signi ican e ec s on he CTD a io. Mean
CTD in S mussels (0.518 ±0.44) was almos 3 imes highe han ha in as (0.168 ±0.11) and in e media e
(0.232 ±0.14) g owe s (Fig. 5: A,B), being ha di e ence signi ican . The mussels ed low concen a ed a ion
a ained app oxima ely 1.5 imes highe CTD alues (0.382 ±0.31) han mussels ed high ood a ion (0.230
±0.15). Howe e , a ion a ec ed he CTD alues o bo h I and S mussels (Table 3) bu no F mussels, hus
esul ing in a signi ican in e ac ion.
3.4.2 Volume densi y o basophilic cells (V BAS)
G ow h condi ion signi ican ly a ec ed
V BAS
:pos hoc Tukey es showed ha S indi iduals had signi ican ly
lowe alues han F and I g owe s (S s. F: p = 0.000; S s. I: p = 0.000), being his las wo s a is ically equal o
each o he (F s. I: p = 0.089). Al hough he e is an upwa d end o he mean
V BAS
alue as he ood a ion
dec eases, he di e ences be ween a ions did no achie e he signi icance (p = 0.057). The in e ac ion e m
was ound o be signi ican .
3.4.3 A ophy index o diges i e al eoli
The mean alues o he a ophy index o he diges i e al eoli a e p esen ed in Fig. 6A, along wi h a summa y
o he K–W es . The es indica es he exis ence o signi ican di e ences in he a ophy index be ween
mussels o di e en g ow h-condi ion: slow-g owing mussels had signi ican ly ewe adipog anula cells
han as and in e media e g owe s did (Dunn’s es esul s: F s. S: p = 0.000; I s. S: p = 0.016; F s. I: p =
0.176) (Fig. 5: C,D). No e ec was exe ed by he a ion ac o .
3.5 His ological analysis o he gill
In Table 3, he mean alues o he semi-quan i a i e analysis o he gill appea ance a e shown. G ow h
ca ego y exe ed a signi ican e ec on gill s uc u e index, whe e slow g owe s had a lowe on al and la e o-
on al cilia densi y and a diso ganized s uc u e o he epi helium when compa ed o as and in e media e
g owe s (Dunn’s es esul s: S s. F: p = 0.000; S s. I: p = 0.004; F s. I: p = 0.325) (Fig. 5: E,F). No signi ican
di e ences we e ound be ween he gill appea ances o mussels ed unde di e en a ions. Mo eo e , he
ini ial alue ob ained is close o ha o F and I mussels han o ha o S indi iduals.
Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes 83
The mo phome ic pa ame e s included in he his ological analysis e lec he diges i e po en ial o he
di e en ially g owing o ganisms. In S mussels, he diges i e di e icula we e e iden ly educed in numbe ,
and appea ed sca e ed and su ounded by ample a eas o connec i e issue. A high CTD alue indica es a loss
o in eg i y o he diges i e gland, which has been linked, among o he s, o poo nu i i e s a us (Mújica e al.,
2015). Ac ually, a a low ood a ion, he mean CTD alue was signi ican ly highe han a a high ood a ion.
A lowe p opo ion o diges i e di e icula means a lowe p opo ion o e ec i e issue o p ocess ood. The
low numbe o diges i e di e icula ha S mussels ha e appea o display a high le el o a ophy ypically
cha ac e ized by an ex eme hinning o he diges i e ubules, whe e he diges i e cells a e o e ly agmen ed.
Degene a ion o diges i e cells has been epo ed in se e al mollusk species subjec ed o en i onmen al s ess
(e.g., Syasina e al., 1997), and bo h a ophy and changes in he mo phology o he diges i e al eoli cons i u e a
non-speci ic esponse o s ess ul en i onmen al condi ions (Beni o e al., 2019; Kim e al., 2006). Rega ding
he cell ype composi ion o he di e icula, S mussels showed a signi ican ly highe densi y o basophilic cells.
Unde good physiological condi ions, he diges i e cells ou numbe he basophilic cells, which is he case o
F and I mussels in his s udy unde bo h ood a ions. In S mussels, con e sely, he ela i e occu ence o
basophilic cells is appa en ly augmen ed due o diges i e cell loss, a condi ion ha is ypical when mussels a e
subdued o s ess ul si ua ions (So o e al., 2002; Zaldiba e al., 2008). The e o e, e en hough S mussels ha e
no been subdued o any s ess, and hey ha e been kep unde he same condi ions ha F g owe s, hey s ill
possess degene a ion ai s ha esemble hose seen in heal hy animals expe imen ally o na u ally s essed.
Compa ed o slow g owe s, as g owe s display a be e -equipped diges i e issue o p ocess ood al oge he .
The inhe en di e ences be ween g owing g oups a e so demons a ed, suppo ing he physiological da a.
Unde s anding he p ocess o in e -indi idual g ow h a e di e en ia ion equi es compa ing he ini ial
alues and hose eco ded h ee mon hs la e , once he size-di e en ia ion occu ed, as sugges ed by Fuen es-
San os e al. (2018). Ini ial alues o gill appea ance a e among he highes sco es, whe eas diges i e issue
a ophy, CTD and
V BAS
a e among he lowes , hus indica ing an op imal ini ial condi ion. Indeed, gonadal
de elopmen was obse ed in he samples aken o he ini ial de e mina ion, which esul ed in a massi e
spawning e en a e a ew days in he labo a o y. A e labo a o y condi ioning, mussels educed oxygen
consump ion, indica ing a gene al imp o emen o he ene gy balance, a educ ion ha could be linked o he
loss o gonadal issue. I canno be disca ded as well a highe RMR a he beginning due o he acclima ion
o he labo a o y. Howe e , only F and I mussels inc eased hei CR alues. His ological analysis e ealed
ha while F mussels main ained ela i ely simila alues o he ini ial ones, S mussels ha e gill and diges i e
issues ha a some poin s a ed de e io a ing. Ac ually, no only soma ic g ow h was no ably diminished,
bu also he accumula ion o ene gy ese es: while in almos all F mussels adipog anula issue was obse ed
in he man le (and e en be ween he diges i e di e icula), S mussels did no show such accumula ion. In ac ,
he nea absence o adipog anula issue in S mussels was u e ly independen o he a ion, which goes along

84 Chap e 1: Di e en ial issue de elopmen comp omising g ow h pheno ypes
wi h he a o emen ioned idea ha no e en a conside able inc ease in ood concen a ion is su icien o
S mussels o make up o hei de e io a ed issues. Al hough mo e s udies should be pe o med o de ail
he unde lying causes, he loss o unc ional diges i e capaci y in S mussels could be he consequence o he
p e iously discussed cons ain in he il e ing ac i i y o , al e na i ely, could s em om a cell-damage in he
diges i e gland simila o ha obse ed in he gill.
Fo he in e media e g owe s ha show he beha iou o he bulk o he popula ion, a end is appa en :
when mussels a e ed a low ood a ion, I indi iduals emain hal way be ween he alues displayed by F
and S mussels; whe eas a a high ood a ion I mussels almos ma ch he alues a ained by F g owe s. In
some pa ame e s, ha unalike beha iou is e lec ed s a is ically as an in e ac ion. I he in e -indi idual
di e ences eco ded s emmed jus om he S g owe s su e ing a de e io a ion p ocess, F and I g owe s
should be expec ed o display simila pe o mances and o ha e a simila appea ance unde he mic oscope.
Howe e , his is no he case. This may indica e ha unde condi ions o high ood a ailabili y, ood inges ion
o I mussels would no be comp omised by hei lowe il a ion abili y. Hence, hey would be e en able o
p ocess and accumula e as many ese es as hei F g owing coun e pa s. I also b ings o h he highe
capaci y ha some mussels ha e o de elop as F mussels e en a low ood a ions.
The his ological and biochemical cha ac e iza ion in his s udy complemen s he physiological da a ha
poin s a di e ences in he ood-acquisi ion a es and me abolic cos s as de e minan s o in e -indi idual
g ow h a iabili y. The s uc u al and unc ional di e ences ound in S mussels sugges ha hei degene a ed
issues o damaged cells impede he p ope acquisi ion, diges ion and abso p ion o ood. This esul s, as a
consequence, in he inabili y o ace any nu i ional e en . On he con a y, F mussels s and ou o hei
plas ici y since, by keeping hei his ological and biochemical pa ame e s i ually cons an , hey a e able o
ob ain ene gy in he mos e icien way unde any a ion.
This s udy se es as a s a ing poin o ield expe imen s es ing he issue and cellula o ganiza ion o
he di e en g owing p o iles in na u e, including he e ec s ha en i onmen al condi ions may impose.
Fu he mo e, g ow h a iabili y in na u e is a majo a ge o de eloping e icien aquacul u e sys ems, and
unde s anding he popula ion dynamics will be ele an o such de elopmen s o happen.
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ja
92 Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el
Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el 99
2 Ma e ials and me hods
2.1 Collec ion o mussels and expe imen al se up
2.1.1 Season and idal- egime expe imen
Two samplings we e made o collec M. gallop o incialis mussels om he shel e ed ocky sho e o Plen zia
(Biscay, Spain, 43º24’ N; 2º56’ W) (Fig. 1), coinciding wi h he au umn (No embe 2021) and sp ing (May
2022) seasons. Wa e empe a u e was a ound 15.5 ºC in bo h seasons and he phy oplank on concen a ion
simila (Bilbao e al., 2021). In each sampling, mussels we e collec ed a low ide (sp ing ides) om he
in e idal (n = 30) and sub idal (n = 30) subpopula ions, co e ing he b oades size- ange possible: 21.6 – 67.0
mm and 22.4 – 65 mm o in e idal and sub idal ide egimes in No embe ; 20.6 – 68.3 mm and 21.8 – 66.0
mm o in e idal and sub idal mussels in May. The e o e, ou di e en expe imen al g oups a ose om he
combina ion o he idal egime (sub idal –S– s. in e idal –I–) and sampling da e (No embe –N– s. May
–M–): SN,IN,SMand IM.
Figu e 1. Shel e ed sampling poin in he Bay o Plen zia in Biscay (No h o Spain).
Mussels we e ans e ed o he labo a o y in ai -exposed we con aine s. On bo h occasions, he p ocedu e
ollowed iden ical p o ocols: in e idal and sub idal mussels we e placed in wo di e en anks (50 L) a
cons an seawa e salini y (33 PSU) and empe a u e (16 ºC). The nex day upon a i al, he ou ine oxygen
consump ion o each indi idual was measu ed, while he s anda d oxygen consump ion was eco ded a e 7

100 Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el
days o as ing. This pe iod was es ablished o be su icien o mussels o minimize any ene gy cos de i ed
om diges ion p ocesses (P ie o e al., 2018).
2.1.2 Acclima ion expe imen
To unde s and he e ec s ha acclima ion o labo a o y condi ions migh ha e on he me abolism o bo h
idal egimes, all mussels collec ed in No embe we e kep in he labo a o y o a pe iod o 2 mon hs
indi idualized in independen chambe s. Two anks (50 L) we e used o sub idal and in e idal mussels,
espec i ely, main ained unde cons an seawa e salini y (33 PSU) and empe a u e (16 ºC). The seawa e
was pump di ec ly om a 12,000 L ese oi o na u al seawa e ha is il e ed h ough a biological il e
and h ee subsequen ibe glass il e s (100, 10 and 1 µm) be o e going in o he eci cula ing wa e sys em
in he labo a o y. Cons an ood was supplied in he o m o a combina ion o own-cul u ed Isoch ysis
galbana s ain BMCC1 mic oalgae (Basque Mic oalgae Cul u e Collec ion om Uni e si y o he Basque
Coun y), and a comme cial mix u e (Shell ish Die 1800®) o i e ma ine mic oalgae (Isoch ysis sp., Pa lo a
sp., Te aselmis sp., Thalassiosi a weiss logii and Thalassiosi a pseudonana) cons an ly dosed a 20000 pa
·
mL
-1
.
The concen a ion was kep s able by equen ly checking wi h a Coul e Mul isize 3 and homogenei y
ensu ed wi h ai ci cula ion. The anks we e cleaned and seawa e enewed wice a week. No mo ali y
e en s we e eco ded du ing he acclima ion pe iod. A e he 2-mon h acclima ion pe iod o con inuous
imme sion and eeding in he labo a o y, ou ine and s anda d me abolic a es we e again measu ed. Fo
each idal egime, wo di e en da a se s we e ob ained: an ini ial de e mina ion co esponding o he ield
condi ions (F) and a inal de e mina ion a e main enance in he labo a o y (L). Consequen ly, ou di e en
expe imen al g oups we e ob ained in his second expe imen : SF,IF,SL, and IL.
2.2 Oxygen consump ion
2.2.1 Rou ine oxygen consump ion (VO2R: mL O2·h-1)
Mussels we e in oduced in o chambe s anging om 50 o 250 ml (acco ding o mussel size) sealed wi h
LDO oxygen p obes connec ed o oxyme e s (HATCH HQ40d) o he de e mina ion o ou ine oxygen
consump ion. The oxygen consump ion a es we e calcula ed om he dec ease in oxygen concen a ion in
he chambe s eco ded du ing 3-4 h, o un il he alues dec eased 20-30 % o he ini ial baseline, e e y 5-10
minu es. A con ol chambe was used o check he s abili y o he oxygen concen a ion.
2.2.2 S anda d oxygen consump ion (VO2S: mL O2·h-1)
S anda d oxygen consump ion was likewise eco ded, excep o he 7-day as ing pe iod ha mussels we e
subdued o be o e measu emen s we e made.
Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el 101
2.3 Gill su ace-a ea (GA: mm2·g-1)
Gill su ace-a ea measu emen s we e only eco ded o he mussels collec ed in May, as he mussels collec ed
in No embe may no e lec ield alues a e wo mon hs o acclima ion in he labo a o y. A e he
physiological expe imen s we e concluded, all indi iduals we e ca e ully dissec ed. A pho og aph o he
in e nal issues was aken wi h a digi al came a and he su ace-a ea o he gills o each indi idual was
calcula ed using ImageJ so wa e (Ab àmo e al., 2004). A ule was placed nex o he mussel when aking
he pho og aph o size co ec ion. The da a shown co espond o one side o he demib anch.
2.4 Shell dimensions
Biome y and shell su ace-a ea we e calcula ed o all 30 mussels o each idal egime in bo h expe imen s.
In he case o he acclima ion expe imen , bo h measu emen s we e aken on a i al in he labo a o y and
a e 2 mon hs o main enance. The an e io -pos e io (leng h), do so- en al (heigh ) and la e al axis (wid h)
o he shell we e measu ed o he nea es 0.01 mm using digi al dial calipe s. The shell su ace-a ea (mm
2
) was
ob ained applying a o mula esembling an ellipsoid-like shape p oposed by Reime and Tedeng en (1996):
SA =L·(H2+W2)0.5·0.5π
whe e L, H and Wa e espec i ely he leng h (mm), wid h (mm) and heigh (mm).
2.5 Condi ion index (CI)
A e bo h samplings, once physiological measu emen s we e comple ed, he whole lesh o each animal was
dissec ed and desicca ed (24 h s. 100 ºC) o ob ain he lesh d y weigh (FDW: mg). The d y weigh o he shell
(SDW: mg) was ob ained a e he lesh esidues we e ca e ully emo ed om he su ace o he comple ely
ai -d ied shell. The shells we e weighed on a 0.01 mg accu acy balance, jus as he li e weigh o he en i e
animal. Condi ion index (CI) was compu ed acco ding o Da enpo and Chen (1987):
CI =FDW
TDW
whe e TDW ep esen s he o al d y weigh o he mussel compu ed as FDW + SDW.
2.6 S a is ical analysis
Da a we e e alua ed o no mali y and homoscedas ici y using Shapi o-Wilk and Le ene es s, espec i ely,
p io o da a analysis. No mal dis ibu ion o he esiduals was checked by No mal P-P plo s and he
independence o he obse a ions es ed by Du bin-Wa son es s.
102 Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el
Linea o dina y leas squa es eg ession analyses we e pe o med o de e mine he alues o he scaling
exponen s (b) and he coe icien s (a) o each eg ession. Reg essions we e compu ed wi h log- ans o med
da a o ou ine and s anda d oxygen consump ion (
VO2R
and
VO2S
), li e weigh , gill su ace-a ea shell
leng h, shell su ace-a ea and shell d y weigh . No -loga i hmically ans o med da a o shell wid h, shell
heigh and shell leng h we e also i ed o linea eg essions. Signi ican di e ences in scaling exponen s and
coe icien s be ween eg essions co esponding o each expe imen al g oup we e es ed using co a iance
p ocedu es (ANCOVA) desc ibed by Za (1999); b ie ly, i he null hypo hesis (
H0
: equal slopes
b1
=
b2
=
b3
...
=
bk
) was ejec ed, mul iple compa ison - es was pe o med o de e mine he signi ican di e ences be ween
each pai o slopes. I
H0
was accep ed, a common slope (
bc
) was compu ed and he null hypo hesis o equal
in e cep s (
a1
=
a2
=
a3
... =
ak
) was subsequen ly es ed. I in e cep s we e no di e en , a common in e cep
(
ac
) and common eg ession we e compu ed. Mul iple compa ison - es was pe o med o de e mine he
signi ican di e ences be ween each pai o ele a ions, in case hey we e di e en .
Da a esul ing om each expe imen was also assessed by mul iple eg ession analysis (a e obse a ion
independence and no mali y o esiduals we e checked) o sequen ially iden i y he explana o y a iables
ha we e mos closely associa ed wi h ou ine oxygen consump ion and s anda d oxygen consump ion
(dependen a iables). Fo he seasonali y expe imen , he explana o y a iables we e li e weigh (nume ic),
season (dummy a iable; May = 0, No embe = 1), ide (dummy a iable; sub idal = 0, in e idal = 1), 2-way
in e ac ions (li e weigh x season; li e weigh x ide; season x ide) and 3-way in e ac ion. Fo he acclima ion
expe imen , he explana o y a iables we e li e weigh (nume ic), ime (dummy a iable; Field = 0, Labo a o y
= 1), ide (dummy a iable; sub idal = 0, in e idal = 1), 2-way in e ac ions (li e weigh x ime; li e weigh x
ide; ime x ide) and 3-way in e ac ion.
The e ec o season and ide ac o s on shell su ace-a ea and condi ion index was analyzed wi h wo-way
ac o ANOVA. S a is ical analyzes we e pe o med using IBM SPSS S a is ics o Windows, Ve sion 28.0
(IBM Co p., 2021).
3 Resul s
3.1 Season and idal- egime expe imen
3.1.1 Rou ine oxygen consump ion (VO2R)
The da a o ou ine oxygen consump ion o each expe imen al g oup plo ed as a unc ion o hei espec i e
li e weigh can be ound in Fig. 2A. The esul ing equa ions a e summa ised in Fig. 2A on he op igh .
S a is ical compa isons be ween he ou eg ession lines showed ha he slopes di e ed om each o he (Fig.
2A). The allome ic exponen o he sub idal mussels was consis en ly highe han he allome ic exponen o
Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el 103
he in e idal ones, no wi hs anding he mon h. Howe e , he slope o he in e idal popula ion in No embe
was signi ican ly he lowes compa ed o he o he h ee.
The gene al equa ion ela ing ou ine oxygen consump ion wi h li e weigh (W) and ide in he mul iple
eg ession analysis was he ollowing (mean alue ±SD):
Replacing he dummy a iables, he ollowing eg ession models a ose o sub idal (0) and in e idal (1)
mussels aking oge he he alues o No embe and May:
Sub idal mussels: Log VO2= 0.875 (±0.045) log W - 1.733 (±0.054)
In e idal mussels: Log VO2= 0.670 (±0.056) log W - 1.552 (±0.068)
The eg ession analysis o he model ob ained he highes s a is ical signi icance (
R2
= 0.829, F = 186.426
and p < 0.001).
3.1.2 S anda d oxygen consump ion (VO2S)
Da a on s anda d oxygen consump ion o each expe imen al g oup plo ed as a unc ion o hei espec i e
li e weigh can be ound in Fig. 2B. On he op igh o Fig. 2B, he esul ing equa ions o such eg essions a e
shown. Fo
VO2S
, no signi ican di e ences we e ound be ween slopes, he e o e a common mass exponen
(
bc
= 0.644) was compu ed. Howe e , mass-speci ic s anda d oxygen consump ion was signi ican ly lowe in
in e idal mussels and, he e o e, ANCOVA showed signi ican di e ences in in e cep s be ween ide le els
(Fig. 2B - a ecomp.).
3.1.3 Shell dimensions
Wid h s. leng h. The indi idual shell wid hs o each mussel g oup ha e been plo ed in Fig. 3A as a unc ion
o hei espec i e shell leng hs. The esul ing equa ions a e shown on he op igh o Fig. 3A. No signi ican
di e ences we e ound among slopes and a common allome ic exponen (
bc
) o 0.393 was ob ained (Fig. 3A,
bo om igh ). Con e sely, ele a ions we e signi ican ly highe in in e idal mussels, ega dless o he season
(Fig. 3A, bo om igh ).
Heigh s. leng h. The indi idual shell heigh s o each mussel g oup ha e been plo ed in Fig. 3B as a unc ion
o he espec i e shell leng hs. No signi ican di e ences we e ound among slopes o ele a ions, gi ing ise
o a common eg ession (
R2
= 0.959; p < 0.001; F = 2687.46) wi h an allome ic exponen (
bcommon
) o 0.479
(±0.009) and a common ele a ion (
acommon
) o 4.539 (±0.457). The common eg ession exponen alues a e
shown on he bo om igh able o Fig. 3B.
104 Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el
Figu e 2. Reg ession lines o he allome ic ela ionships o he o m Y = a
·Xb
. (A) Log- ans o med ou ine
oxygen consump ion s. log- ans o med weigh ; (B) log- ans o med s anda d oxygen consump ion s. log-
ans o med weigh . On he op igh o each igu e, he allome ic ela ionship is shown acco ding o he
exp ession: Y = a
·LWb
, whe e LW is li e weigh . In case o a common b- alue, he ecompu ed a- alues
a e also shown (a
ecomp.
). On he bo om igh , ANCOVA and pos hoc es s. Sha ed le e s (a, b o c) indica e
no signi ican di e ences (p < 0.05). Pu ple and o ange symbols dis inguish ide le els (sub idal, in e idal),
ci cles and iangles seasons (No embe , May).
SN
: pu ple ci cles;
IN
: o ange ci cles;
SM
: pu ple iangles;
IM: o ange iangles.
SDW s. leng h. The indi idual shell d y weigh s o each mussel g oup ha e been plo ed in Fig. 4A as a
unc ion o hei espec i e shell leng hs. The esul ing equa ions a e shown on he op igh o Fig. 4A.
No signi ican di e ences we e ound among slopes and a common allome ic exponen (b
common
) o 2.531
was ob ained (Fig. 4A, bo om igh ). Con e sely, ele a ions we e signi ican ly highe in in e idal mussels,
ega dless o he season (Fig. 4A, bo om igh ).

Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el 105
Figu e 3. Reg ession lines o he allome ic ela ionships o he o m Y = bX - a. (A) Shell wid h (mm) s.
Shell leng h (mm); (B) Shell heigh (mm) s. Shell leng h (mm). On he op igh o each igu e, he allome ic
ela ionship o he shell dimension agains indi idual leng h is shown. In case o a common b- alue, he
ecompu ed a- alues a e also shown (a
ecomp.
). On he bo om igh , ANCOVA and pos hoc es s. Sha ed le e s
(a,b o c) indica e no signi ican di e ences (p < 0.05). Pu ple and o ange symbols dis inguish ide le els
(Sub idal, In e idal), ci cles and iangles seasons (No embe , May).
SN
: pu ple ci cles;
IN
: o ange ci cles;
SM: pu ple iangles; IM: o ange iangles.
SDW s. su ace-a ea. The indi idual shell d y weigh s o each mussel g oup ha e been plo ed in Fig. 4B as a
unc ion o hei espec i e shell su ace-a eas. The b- alue co esponds o he e ec ha size exe s on he
ela ionship be ween he wo a iables, whe eas he a- alue ep esen wha could be conside ed he densi y
o he shell. The esul ing equa ions a e shown on he op igh o Fig. 4B. Each slope di e ed signi ican ly
om each o he (Fig. 4B, bo om igh ), being he di e ences be ween mussel g oups smalle as he size
inc eases. Also he in e cep s indica e ha he densi y o he shell is i ually he same in he in e idal mussels
106 Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el
ega dless o he season ( o a common shell su ace-a ea o 3.3 mm
2
: he a- alue o
IM
is 0.777 and o
IN
is 0.703). Howe e , he shell densi y o sub idal indi iduals inc eases o e a 30 % in May compa ed o
No embe ( o a common shell su ace-a ea o 3.3 mm2: he a- alue o SMis 0.916 and o SNis 0.636).
Figu e 4. Reg ession lines o he allome ic ela ionships o he o m Y = a
·Xb
. (A) Log- ans o med
shell d y weigh (SDW) s. log- ans o med shell leng h; (B) log- ans o med shell d y weigh (SDW) s. log-
ans o med shell su ace-a ea. On he op igh o each igu e, he allome ic ela ionship is shown acco ding
o he exp ession Y = a
·
LW
b
, whe e LW is li e weigh . In case o a common b- alue, he ecompu ed a- alues
(a
ecomp.
)a e also shown. On he bo om igh , ANCOVA and pos hoc es s. Sha ed le e s (a, b o c) indica e
no signi ican di e ences (p < 0.05). Pu ple and o ange symbols dis inguish ide le els (sub idal, in e idal),
ci cles and iangles seasons (No embe , May).
SN
: pu ple ci cles;
IN
: o ange ci cles;
SM
: pu ple iangles;
IM: o ange iangles.
Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el 107
3.1.4 Condi ion index (CI)
Sub idal mussels om bo h seasons had a ound 30 % highe CI (Fig. 5), acco ding o he Tukey es . The
wo-way ANOVA showed ide le el as he only ac o signi ican ly a ec ing CI alues (Fig. 5, op igh ).
3.1.5 Gill su ace-a ea (GA: mm2·g-1)
Figu e 6 shows he ela ionship be ween gill su ace-a ea and shell leng h in sub idal and in e idal mussels.
The ANCOVA analysis showed no di e ences be ween slopes ( = 0.103, d = 1, 54; p > 0.05), wi h a b
common
alue o 1.955. Howe e , he in e cep o in e idal mussels was highe compa ed o he sub idal mussels ( =
3.125, d = 1, 54; p < 0.001).
Figu e 5. CI o sub idal and in e idal mussels o No embe and May. Sha ed le e s indica e absence o
s a is ical di e ences. On he op, he wo-way ac o ANOVA es ing signi ican e ec s o season (No embe
s. May) and ide le el (sub idal s. in e idal).
3.2 Acclima ion expe imen
3.2.1 Rou ine oxygen consump ion (VO2R)
Rou ine oxygen consump ions o each mussel g oup a e plo ed as a unc ion o hei espec i e li e weigh
in Fig. 7A and he esul ing equa ions a e summa ised on he bo om igh o he igu e. The slopes o
ou ine oxygen consump ion and li e weigh di e ed om each o he : in e idal mussels had lowe allome ic
exponen s, ega dless o whe he mussels we e acclima ed o no o labo a o y condi ions. Mul iple eg ession
analysis showed ha li e weigh and ide explained 82 % o he a ia ion in ou ine oxygen consump ion.
The esul ing gene al equa ion was he ollowing (mean alue ±SD):
108 Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el
Replacing he dummy a iables, he ollowing eg ession models a ose o sub idal (0) and in e idal (1)
mussels:
Sub idal mussels: Log VO2= 0.866 (±0.047) log W - 1.788 (±0.050)
In e idal mussels: Log VO2= 0.615 (±0.058) log W - 2.022 (±0.067)
The eg ession analysis o he model ob ained he highes s a is ical signi icance (R
2
= 0.820, F = 171.944 and
p < 0.001).
3.2.2 S anda d oxygen consump ion (VO2S)
The s anda d oxygen consump ion da a o each expe imen al g oup plo ed as a unc ion o hei espec i e
li e weigh can be ound in Fig. 7B. On he op igh o Fig. 7B, he esul ing equa ions o such eg essions
a e shown. Fo VO
2S
, he eg ession slopes we e no signi ican ly di e en b
c
= 0.662), bu he in e cep s
di e ed be ween he ide le els, wi h lowe alues o in e idal mussels (Fig. 7B, bo om igh ).
Figu e 6. Reg ession lines o he allome ic ela ionships o he o m Y = a
·
X
b
o gill su ace-a ea agains
shell leng h. On he op igh , he allome ic ela ionship o he gill su ace-a ea agains indi idual leng h
is shown. On he bo om igh , ANCOVA and pos hoc es s. Because a common b- alue was accep ed, he
ecompu ed a- alues a
ecomp.
a e also shown. Sha ed le e s (a, b o c) indica e no signi ican di e ences (p <
0.05). Pu ple and o ange symbols indica e alues o sub idal and in e idal mussels, espec i ely.
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Chap e 2: Me abolic scaling: cons i u i e adap a ion o ide le el 115
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ja

Chap e 3
Tide le el shapes he g ow h pheno ypes o My ilus gallop o incialis
unde ield ea ing condi ions
Ma y ocas de San Es eban, As u ias (1903) – Joaquín So olla
122 Chap e 3: Tidel le el shapes g ow h- a e pheno ypes
Resumen
Las di e encias de i adas de la e iciencia de los mecanismos isiológicos in oluc ados en la adquisición de
ene gía son una de las causas de las di e encias in e -indi iduales en asa de c ecimien o bajo condiciones de
labo a o io enmejillones. También en ellabo a o io, las asas deme abolismo más bajasson el ac o cla e pa a
la apa ición del eno ipo de c ecimien o ápido cuando la disponibilidad de comida es baja. Ningún es udio ha
in en ado analiza cómo se desa ollan los di e en es eno ipos bajo condiciones de campo compa ables, pe o
que implican di e en es escena ios ó icos. Dos g upos de 300 mejillones (12.16
±
1.10 mm cada uno) ue on
colocados en dos cajas ancladas al espigón a < 1 y 2.5 me os sob e la línea de ma ea: in e ma eal bajo (L) y
al o (H). T as 6 meses, se ob u ie on eno ipos de c ecimien o ápido (F), in e medio (I) y len o (S) en cada uno
de los ni eles ma eales, que ue on empleados pa a expe imen os de alimen ación y la medición del balance
ene gé ico, así como el á ea b anquial, el índice de es uc u a b anquial y el peso seco de la concha. Bajo
ambos egímenes ma eales, los mejillones S mos a on una densidad cilia meno en b anquias y conchas más
densas que los F. En L, los mejillones S casi alcanza on las abilidades de adquisición de comida y abso ción de
los F, pe o eduje on su dis ibución de ene gía hacia el c ecimien o somá ico, incluso a expensas de educi
su á ea b anquial, en a as de o os eque imien os ene gé icos, como conchas más pesadas, c ecimien o
gonadal o ac i idad an ioxidan e. En H, las di e encias en asa de c ecimien o se explican con el modelo de
adquisición de ene gía, pe o sin es a acompañado de di e encias en á ea b anquial. Es os esul ados no es án
en co espondencia con es udios p e ios que abajan con condiciones es ic i as, los cuales sugie en una
capacidad mayo de los F pa a educi su asa me abólica. Los bene icios de in e i en un á ea b anquial
mayo no compensan las des en ajas que ello supone en el campo.
Labu pena
Muskuilue an, banakoen a eko hazkun za- asa ezbe din asunak azal zen di a ene gia lo penean pa e
ha zen du en isiologia-mekanismoen e izien zia-desbe din asunen a abe a, labo a egi baldin ze an. Bai a
labo a egian, me abolismo- asa baxuagoak gakoak di a hazkun za azka eko eno ipoa age dadin jana i
esku aga i asun baxupean. Ike ke a ba e e ez du az e u zelan ga a zen di en eno ipo ezbe dinak balizko
egoe a o iko ezbe dinak di uz en landa-egoe a alde aga ie an. 300 muskuiludun bi mul zo (12.16
±
1.10 mm bakoi zak) sa u zi en ola u-ho ma a aingu a u ako bi ku xa an, ma ea-le o ik < 1 e a 2.5
me o a a: ma ea eko baxua (L) e a al ua (H). Sei hilabe e ge oago, ma ea eko maila bakoi zean hazkun za
azka eko (F), a eko (I) e a baxuko (S) eno ipoak lo u zi en, elikadu a espe imen uak e a ene gia-balan zea
neu zeko e abili zi enak, bai a b ankia-azale a, b ankia egi u a en indizea e a masko a en pisu leho a
neu zeko e e. Ma ea eko maila bakoi zean, S muskuiluek b ankie ako zilio-den si a e baxuagoa e a
masko lodiagoak age u zi uz en. L egoe an, S muskuiluek ia lo u zi uz en F muskuiluen jana i-esku a ze
Chap e 3: Tidel le el shapes g ow h- a e pheno ypes 123
e a xu gapen gai asunak, baina hazkun za soma ikoa i ene gia gu xiago eslei zen dio e, b ankia-azale a
mu iz ea en kon u a, bes e ene gia-eska ien alde, esa e ako, masko pisu suagoak, gonada-hazkun za edo
ak ibi a e an ioxida zailea. H egoe an, hazkun za- asa ezbe din asunak azal zen di a jana i esku aga i asun
modeloa en a abe a, b ankia-azale a ekin pa eka u a ez zegoena. Emai za hauek ez da oz ba egoe a
mu iz ailee an egindako ike ke ekin, F muskuiluek me abolismoa mu iz eko du en gai asuna azpima a u
du enak. B ankia-azale an inbe i zeak daka zan aban ailak ez du e konpen sa zen landa egoe an daka zan
desaban ailekin.
Abs ac
Di e ences de i ing om he e iciency o he physiological mechanisms in ol ed in he ene gy acquisi ion
a e one o he unde lying causes o in e -indi idual g ow h- a e di e ences unde labo a o y condi ions in
mussels. Also in he labo a o y, lowe me abolic a es a e he key ac o o he appea ance o he as g owing
pheno ype unde low ood a ailabili y. No s udy has a emp o analyse how he di e en pheno ypes de elop
unde compa able ield condi ions wi h ye di e en ophic scena ios. Two se s o 300 mussels (12.16
±
1.10 mm, each) we e placed in wo cages ancho ed o he b eakwa e a < 1 and 2.5 me es abo e he ide line:
low (L) and high (H) in e idal. A e 6 mon hs, as (F), in e media e (I) and slow (S) g owing pheno ypes
we e ob ained in each ide le el, which we e used o eeding expe imen s and he measu emen o he ene gy
balance, as well as he gill su ace-a ea, gill s uc u e index, and shell d y weigh . Unde bo h idal heigh s, S
g owe s we e ound o ha e lowe gill cilia densi y and dense shells han F g owe s. In L, S mussels almos
caugh up he ood acquisi ion and abso p ion abili ies o F, bu hey educe he ene gy alloca ion o soma ic
g ow h, e en a he expense o educing hei gill su ace-a ea, o he sake o o he ene ge ic eques s, such
as hea ie shells, gonadal g ow h o an ioxidan ac i i y. In H, g ow h a e di e ences a e explained by
he ene gy acquisi ion model no coupled wi h di e ences in gill su ace-a eas. These esul s a e no in
co espondence wi h p e ious s udies wo king wi h es ic i e condi ions, which sugges ed a highe capaci y
o as g owe s o educe hei me abolic a e. The bene i s o in es ing in gill su ace-a ea do no make up
o he disad an ages ha i implies in he ield.
124 Chap e 3: Tidel le el shapes g ow h- a e pheno ypes
Tide le el shapes he g ow h pheno ypes o My ilus gallop o incialis unde
ield ea ing condi ions
1 In oduc ion
The empe a e shel wa e s o he No heas A lan ic Ocean, in which he sou he n egion o he Bay o
Biscay is included, a e widely dispe sed wi h popula ions o he Medi e anean mussel (M. gallop o incialis)
(Ga mendia e al., 2011; Ma igómez e al., 2007; Ma ínez-Pi a e al., 2012). Mos o he s udies conduc ed
in his egion ha e been ocused on he cha ac e iza ion o ep oduc i e cycles (i.e., Ga mendia e al., 2010;
O iz-Za agoi ia e al., 2011; Azpei ia e al., 2017) o in he use o mussels as bioma ke s o en i onmen al
pollu ion (F anco e al., 2002; Ma igómez e al., 2004; Izagi e and Ma igómez, 2009; Jimeno-Rome o e al.,
2009; Solaun e al., 2013). Howe e , he g owing pa e ns and i s implica ions ha e no been he ocal poin o
he s udies pe o med wi h mussels in his a ea. Azpei ia e al. (2016, 2018) did analyse he g ow h pa e ns o
M. gallop o incialis in he Bay o Biscay, bu wi h mussels cul u ed in he open ocean. In he p esen s udy, he
use o cages ancho ed o a b eakwa e allowed he analysis o mussel g ow h unde ield condi ions in he
es ua y a wo di e en idal egimes, on he basis o a homogenously sized popula ion o mussel spa .
Na u al popula ions o M. gallop o incialis in he Bay o Biscay expe ience sho - e m idal luc ua ions in ood
a ailabili y and composi ion. The ae ial exposu e has he mos no iceable impac on he in e idal zone, which
es ic s he ime a ailable o ood consump ion, while o cing he use o me abolic ene gy on adjus ing
he esponses agains hypoxia, desicca ion and empe a u e ex emes (Fi zge ald e al., 2012; Leeuwis and
Gampe l, 2022). Also ide- and wind-d i en wa e mo emen s cause he esuspension o bo om sedimen s
ha p omo e he inc emen o pa icle concen a ion and he dilu ion o he a ailable phy oplank on (Bayne,
1993). The abili y o bi al es o con ol ood-p ocessing a es – ei he by ejec ing poo e quali y pa icles o
by changing clea ance a es – de e mines how hey a e impac ed by such a ia ions in pa icle concen a ion
and quali y (Thompson and Bayne, 1974; Bayne e al., 1989; Hawkins e al., 1996; Na a o e al., 1994, 1996;
Na a o and Widdows, 1997).
P ecisely he di e ences ha de i e om he e iciency o he physiological mechanisms in ol ed in he
ene gy acquisi ion (wa e pumping, pa icle cap u e and e en ion, o ganic pa icle selec ion, and pa icle
hyd olysis and abso p ion) a e one o he unde lying causes o in e -indi idual g ow h- a e di e ences.
This di e en ial capaci y is conside ed wi hin he acquisi ion model p oposed by Bayne e al., 1999, ha
condensed he esul s o s udies on he di e en ial g ow h in h ee explana o y, ye no -mu ually exclusi e,
models. Besides he acquisi ion model, wo o he models migh also explain he in e -indi idual g ow h a e
di e ences in bi al es. The me abolic e iciency model holds ha he e iciency o ene gy in es men in he
Gene al discussion 227
In he p esen s udy, bo h in mussels and oys e s, and ei he unde labo a o y o ield condi ions, eeding
a e and me abolic e iciency showed up as he mos impo an ac o s in he de elopmen o a as g owing
pheno ype, which has been ound o be acili a ed by a highe capaci y o acqui e ood ha does no imply
a highe me abolic expendi u e (Chap e s 1, 3 and 5). In o he wo ds, in all he condi ions s udied, as
g ow h was achie ed by a combina ion o he acquisi ion model and me abolic e iciency model (sensu Bayne,
1999). Inna e in e -indi idual di e ences in he abili y o acqui e and p ocess ood had been shown on
many occasions. The s udies by Tamayo e al. (2011, 2013, 2014, 2015, 2016) and P ie o e al. (2018, 2019,
2020
a,b
) se led he idea ha in e -indi idual di e ences in eeding abili ies we e de e mined by he gill
su ace-a ea. Unde labo a o y (Chap e 1) and ield condi ions a he low in e idal (Chap e 3) we ound
ha slow g owing mussels displayed a smalle gill su ace-a ea han as g owing mussels in mos scena ios,
which indica es a educed ene gy alloca ion owa ds he il e ing s uc u es. Unde high in e idal ield
condi ions hough, no such a pa e n was ound, since bo h as and slow g owing indi iduals showed simila
gill su ace-a eas (Chap e 3). This indica es ha he plas ici y o he gill-su ace a ea in ela ion o g ow h
a e does no seem o be as s aigh o wa d o ob ious as p e iously hough . We ha e demons a ed ha
unde labo a o y condi ions, when he po en ially nega i e ac o s ha may a ec he gill a e aken ou o he
equa ion (high empe a u es, desicca ion, oxygen dep i a ion), he indi iduals wi h su plus ene gy end o
in es in his issue, as i is ad an ageous o a be e ood acquisi ion. The e o e, he gill becomes a key o gan
o di e en ial g ow h pheno ypes o de elop. Howe e , in na u e, he ene gy is no in es ed o de elop
his o gan, since he ene gy disad an ages ha a la ge exposed su ace could b ing abou migh exceed he
bene i s.
One o he ou comes o he p esen esea ch has been o del e in o his idea ha size- ela ed in e -indi idual
di e ences in ood acquisi ion a e p o usely in e connec ed wi h co esponding di e ences in he gill, albei
p o iding mo e dimension o he well-es ablished idea ha he gill su ace-a ea is one o he majo d i e s
o he de elopmen o di e en g owing pheno ypes. In ac , despi e he ecognised impo ance o he gill in
he esea ch-con ex o in e -indi idual g ow h- a es, he e was a knowledge-gap p e en ing he conduc o
an in eg a ed analysis o he g ow h assessmen . The deep analysis pe o med o he gill s uc u e a issue
le el e ealed que comple a la ele ancia de la b anquia en la pa e de adquisicion del modelo, no es el a ea
sino su uncionalidad p o ided wi h addi ional in o ma ion ha has been so a o e looked in his ype o
analysis. Ademas hemos desa ollado es e indice que puede usa se como he amien a en u u os esea ch
de eloped he gill-s uc u e index as a good indica o o he densi y o la e al (d i e s o he wa e low) and
la e o- on al cilia (in cha ge o pa icle cap u e and anspo ing). Thus, he gill s uc u e index ep esen s
he densi y and obus ness o he gill cilia y equipmen .
Al hough li le in o ma ion is a ailable, i appea s ha he size o he gill possesses some plas ici y, as he e is
e idence o al e a ion in he ela i e size o his o gan in esponse o en i onmen al a ia ion (Tendeng en e

228 Gene al discussion
al., 1990; Honkoop e al., 2003; Du e e e al., 2017; Capelle e al., 2021). Howe e , he e is no in o ma ion
ega ding he possibili y o modi ying he densi y o gill cilia in esponse o al e a ions o en i onmen al
condi ions. We ound ha nei he he seasonal ac o no he idal le el a ec he gill s uc u e index (Chap e
4), which is only di e en be ween as and slow g owing indi iduals, ein o cing he no ion ha cilia
densi y is a de e mining ac o in endogenous di e ences in g ow h a e. The e o e, his ological e idence
epo ed he ein con i ms a clea ela ionship be ween cilia densi y and g ow h a e: slow g owing indi iduals
consis en ly showed less cilia and a poo e epi helial s uc u e han as g owe s did in hei gills. This seems
o be ela ed as well o a highe cellula damage ha may impede he building o he cilia y mesh. This
ela ionship seems o be a egula pa e n in mussels (bo h unde labo a o y –Chap e 1–, and ield condi ions
–Chap e s 3 and 4–), and oys e s (Chap e 5), which con i ms ha he mo pho- unc ional dispa i y o he
gills is ubiqui ous and endogenous o he g owing pheno ypes.
The unc ioning o he diges i e and abso p i e o gans cons i u es a second ac o ha can po en ially
shape he di e ences in he ood p ocessing be ween as and slow g owe indi iduals, hus comple ing he
physiological basis o he acquisi ion model. In his s udy, a e he analysis o he p opo ion o issues and
a ophy in he diges i e gland i has been p o ed ha supe imposed o he na u al a ia ions in he indexes,
he e was a s ong di e ence be ween as and slow g owing mussels: slow g owe s had mo e a ophied
diges i e ubules han as g owing mussels in bo h seasons and ide le els (Chap e 4). Those di e ences we e
e en mo e in ense be ween as and slow g owing mussels ea ed in he labo a o y (Chap e 1). Diges i e
ubules we e e iden ly a ophied and educed in numbe , appea ing sca e ed and su ounded by ample a eas
o connec i e issue in slow g owe s, which means a lowe p opo ion o e ec i e issue o p ocess ood.
These indings pa e he way o u he esea ch and new esea ch lines o de ail he unde lying causes o he
in e -indi idual di e ences in diges i e capaci y. Fo ins ance, o unde s and i he loss o unc ional diges i e
capaci y in slow g owing mussels is he consequence o he p e iously discussed cons ain in he il e ing
ac i i y o , al e na i ely, could s em om a cell-damage in he diges i e gland simila o ha obse ed in
he gill. E en mo e so when, in con as o mussels, no di e ences we e ound in oys e s (Chap e 5). The
di e ences in g ow h a e be ween as and slow g owing oys e s we e much smalle han in mussels. In ac ,
he oys e s analysed in Chap e 5 we e 1 yea -old adul s, du ing he cou se o which as g owe s g ew wo
imes mo e in leng h han slow g owe s. Con as ingly, he mussels analysed in Chap e s 1, 3 and 4, we e
ju eniles ha de eloped e en la ge di e ences in leng h in a much sho e pe iod o ime o only 3 (in he
labo a o y – Chap e 1), 6 and 12 mon hs (in he ield – Chap e s 3 and 4). Thus, i migh no be disca ded
ha a he han in e -speci ic di e ences alone, such a dispa i y o esul s be ween mussels and oys e could
e lec he di e ences in he g ow h a e gap be ween as and slow g owing indi iduals.
Ano he essen ial componen o he physiological basis o di e ences in g ow h pheno ypes po en ial is
me abolic e iciency. As a o emen ioned, he de elopmen o highe clea ance and abso p ion a es in as
Gene al discussion 229
indi iduals did no esul in highe ou ine me abolic a es, indica ing ha as indi iduals ha e a highe
me abolic e iciency. Unde di e en ood concen a ions, as g owe s wi h highe eeding a es showed
a 30 % highe COX ac i i y in hei gills, hence indica ing highe mi ochond ial ac i i y. Ye hei oxygen
consump ion alues we e he same o hose ob ained by slow g owe s. On he one hand, COX ac i i y was
only measu ed in he gills, and i is only ep esen a i e o he mi ochond ial espi a ion, whe eas he oxygen
consump ion is an es ima ion ha akes in o accoun all he issues o he indi idual. On he o he hand, lack
o conco dance be ween VO
2
and COX ac i i y migh indica e ha la ge amoun s o oxygen molecules in
slow g owe s a e no coupled o ae obic mi ochond ial espi a ion and ATP syn hesis. Since his would be
indica i e o a lowe oxida i e capaci y o mi ochond ia, i would explain pe se he in e -indi idual di e ences
in me abolic e iciency. Those oxygen molecules could be u ilely los in he de imen al p oduc ion o eac i e
oxygen species (ROS). In ac , a highe ROS p oduc ion in slow g owing indi iduals would be consis en
wi h he ac ha hei an ioxidan enzyme ac i i ies (ca alase and glu a hione S- ans e ase) in he gill a e
wo imes highe han in as g owing mussels. Fu he mo e, bo h an ioxidan ac i i ies inc eased e en
mo e unde low ood a ions, whe e a highe cilia y bea ing is demanded. A po en ial a enue o u he
in es iga ion would be o di ec ly analyse ATP p oduc ion h ough he use o his ochemis y echniques on
ATPase enzymes. An examina ion o he ene gy balances associa ed wi h cellula and mi ochond ial ene gy
u ilisa ion would also be a aluable addi ion o he esea ch.
As e idence o his lack o acquisi ion and me abolic e iciency in slow g owe s, i has been demons a ed in
Chap e 1 unde iden ical labo a o y condi ions ha he accumula ion o ese es in he o m o adipog anula
cells a e signi ican ly limi ed in slow g owe s, since he accumula ion o ene gy ese es is di ec ly co ela ed
o he clea ance a e. Fu he mo e, he adipog anula cells con o m a s o age issue cha ac e ised by an
abundan p o ein syn hesis, which necessi a es a high ATP p oduc ion o be employed o cellula wo k. This
p oduc ion may be less e icien in slow g owe s due o he p esumably lowe oxida i e capaci y o hei
mi ochond ia, as p e iously discussed.
To u he elabo a e he me abolic e iciency model is undamen al o conside he di e ences in ene gy
equi emen s o he immune sys em be ween di e en ially g owing pheno ypes. A couple o s udies (Saa ed a
e al., 2017; P ie o e al., 2019) ha e add essed he di e en ial gene ic exp ession in indi iduals selec ed as as
and slow g owe s unde labo a o y condi ions. Those s udies showed ha genes in ol ed in he immune
esponse we e o e -exp essed in slow g owing indi iduals, sugges ing a highe ac i i y o he immune
sys em. The cha ac e is ics o he immuni y o he di e en g owing pheno ypes ha e been analysed in
oys e s in he p esen s udy (Chap e 5), leading o he conclusion ha slow g owing indi iduals possess he
same cell concen a ion wi h ye less iabili y. This implies he need o inc easing he haema opoiesis. This
da ase indica es ha slow g owe s likely equi e a highe me abolic demand in he main enance o hei
immune sys em, a highe in es men o assimila ed ene gy in keeping he immune unc ion. Fu he mo e,
230 Gene al discussion
al hough no signi ican , he haemocy es o slow g owing oys e s displayed a highe p oduc ion o ROS,
which implies highe cos s o g ow h and ha would be cohe en wi h he p e iously men ioned lowe COX
and highe an ioxidan ac i i ies in he gills o slow g owing indi iduals o M. gallop o incialis (Chap e 1).
ROS p oduc ion in he haemocy es is subjec o la ge in e -indi idual a iabili y, al hough u he esea ch is
needed as we only measu ed i in iploid indi iduals (Chap e 5). S ill s ongly sugges s ha he e iciency
o he immunological ole o haemocy es is a plas ic-enough physiological ai ha may con ibu e o
in e -indi idual di e ences in g ow h capaci y.
When di e ences in he po en ial o he immune sys em a e conside ed in he con ex o g ow h dispa i ies,
one may ponde he possibili y ha slow g ow h is simply he consequence o o ganisms being unheal hy.
In his s udy, he seg ega ion o as and slow g owing o ganisms in he ield allowed he de elopmen o
he g owing pheno ypes unde na u al condi ions ha include he p esence o pa asi es, among many o he
en i onmen al haza ds. We ound ha as g owing mussels ha e a highe pa asi ic load han slow g owing
indi iduals, which ca ego ically ejec s he possibili y o in e -indi idual g ow h a e di e ences being ela ed
o di e en ial heal h s a us. A g ea e ood acquisi ion pe uni o ime and a la ge clea ance a ea (i.e.,
la ge gills) una oidably implies a highe exposu e o he en i onmen by as g owe s, since, indeed, hey
do no hing bu inc ease he p obabili y o pa asi e encoun e and subsequen in ec ion (Chap e 4). Ye a
g ea e pa asi ic load does no p e en hem om ob aining he highes alues o SFG and g ow h a es.
This can only mean ha as g owe s ha e high ole ance o pa asi ic in ec ion, ein o cing he no ion ha
hei immune sys em is mo e capable. The opposi e is ound in slow g owe s, which, as a consequence o
hei less-e ec i e o gans, dec ease hei ood consump ion and abso p ion, educing in exchange hei
exposu e o he en i onmen . Fo ui ously, a lowe exposu e migh p o ec hem agains pa asi ic in ec ion,
no only minimising he pa asi ic in ensi ies, bu also limi ing he ophic esou ces a ailable o pa asi es.
Fu he mo e, gi en ha he immune sys em o slow g owe s seems o be conside ably less obus and less
e ec i e, such limi a ion in pa asi e loading highly likely inc eases hei chances o su i al.
Thus a , i has become qui e clea ha di e ences in g ow h a e a e based on dis inc i e ea u es conce ning
he di e en le els o biological o ganisa ion, which explain in dep h he acquisi ion and he me abolic
e iciency models. Ac ually, he comp ehensi e in e p e a ion o ou da a sugges s ha bo h models a e
inex icably linked by a p ima y cause ha is ela ed o genuine di e ences be ween indi iduals. Less e icien
mi ochond ia in he gills o slow g owe s would lead o a lowe ae obic ATP syn hesis in he cells and a highe
p oduc ion o eac i e oxygen species, which could cause cell damage in he gill. This a ec s he s uc u e o
he o gan disabling i s po en ial o de elop a su icien ly capable cilia y ne wo k o p ope ood acquisi ion.
As a esul , he animal is unable o ob ain enough ene gy om he en i onmen , leading o a educed g ow h
a e. In addi ion, his consubs an ial na u e o he acquisi ion and me abolic e iciency models seems o occu
in any o he es ed condi ions in he labo a o y and in he ield; along seasons (gonadal de elopmen ), and a
Gene al discussion 231
di e en idal le els. Howe e , in he ield, he si ua ion becomes mo e complex and he cons ain s on he
speci ic me abolic e iciencies o slow g owe s may necessi a e speci ic adap a ions a ec ing bo h ene gy
acquisi ion and ene gy edis ibu ion ha equi es a ca e ul case-by-case analysis.
As p e iously s a ed, in labo a o y condi ions whe e animals we e p o ided wi h a es ic ed amoun o ood,
as g owe s de eloped by means o an enhanced capaci y o minimise s anda d ene gy expendi u e (Tamayo
e al., 2016; P ie o e al., 2018). Ou indings ha e demons a ed ha his ene gy sa e pheno ype does no
occu in na u al condi ions wi h ophic limi a ion (high in e idal), mos p obably because in he ield he e
a e nume ous o he ac o s besides ood ha equi e high ene gy le els o main enance. Cos ly p ocesses
such as soma ic main enance and epai , ep oduc ion, and g ow h compe e o esou ces and when ene gy
is no a i s highes i is impossible o maximise alloca ion o hem all, so ade-o s mus happen. Hence, he
hi d model o ene gy edis ibu ion (i.e., alloca ion model) may also be implica ed in he de elopmen o he
di e se g ow h pheno ypes, aiding in he unde s anding o in e -indi idual g ow h a e a iabili y.
The pano ama o he mussels ea ed a low in e idal analysed in May (Chap e s 3 and 4) di ec ly con on s
us wi h his possibili y. This is he only case wi h no clea beha iou o acquisi ion and me abolic e iciency
models, as in ac bo h as and slow g owe s il e ed simila ly and ob ained no di e en SFG alues. This
can only indica e ha in slow g owe s a subs an ial pa o he assimila ed ene gy would be in es ed in issue
p oduc ion ha is ei he eleased o he en i onmen (game e o byssus p oduc ion) o apped in he shell.
Shell g ow h has been demons a ed o be a plas ic componen in mussels since shell densi y and shape was
ound o change along seasons and ide le els (Chap e 2). In spi e o he a iabili y o his mo phological ai ,
no di e ences we e obse ed be ween he shell ai s o as and slow g owing mussels (Chap e 4), al hough
he e is an in insic allome ic di icul y when analysing such a ibu es. The only di e ences in shell we e
ound no in hei mo phology bu in hei composi ion be ween he shells o as and slow g owing oys e s in
Chap e 5. Fas g owing oys e s showed a much highe accumula ion o o ganic ma e in hei shells, which
migh in ac indica e a highe ene gy in es men . S ill, i should be no ed ha oys e and mussel shells a e
di e en in hei a ibu es. Oys e shells a e much mo e i egula , much oughe o ugged, and co uga ed
compa ed o mussel shells, which a e mo e uni o m, smoo h and possess a mo e o ganised in e nal s uc u e.
Di e en ial shell cha ac e is ics a e likely ela ed wi h hei biology, as while mussels a e a ached o ocks
using byssus h eads, oys e s a e cemen ed o ha d subs a es using hei own shell ma e ial as cemen and
hey need o adjus he shell-shape o he a ailable space in he complex h ee-dimensional la ice o he oys e
bed. In addi ion, oys e shells a e gene ally mo e agile and p one o ac u e han mussel shells, which may
equi e g ea e ene gy in es men s in hei egene a ion. This p ocess necessi a es highe equencies o
pe ios acum p oduc ion (solely composed o o ganic ma e ) and p obably bene i s om he accumula ion
o highe o ganic ma e pe cen age in he laye s o he o ganic ma ix ha se e as a basis o he deposi ion
232 Gene al discussion
o calcium ca bona e c ys als in he shell (Wa abe, 1984; Falini e al., 1996; Choi and Kim, 2000). Fu he
esea ch would be in e es ing o analyse i his di e ence in o ganic ma e p oduc ion happens also in
mussels and, consequen ly, a di e en ene gy in es men .
Gonadal de elopmen and spawning a e submi ed o endoc ine con ol in bi al es (see Osada and Ma sumo o
2016, o e iew). The his ological analysis desc ibed in Chap e 4 has shown he exis ence o clea di e ences
in he in ensi y o ollicle a esia be ween as and slow g owing mussels. Highe a esia le els in as g owe s
indica e ha hey a e able o eco e a subs an ial pa o hei gonadal in es men . A esia is conside ed o be
a esponse o un a ou able en i onmen al condi ions, a physiological egula o y mechanism con olling he
numbe o oocy es obespawned (Benninge , 2017)andallowing he ealloca ion o ene gy om ep oduc ion
owa ds soma ic g ow h, de ence and epai mechanisms o ensu e su i al (Gagné e al., 2011, Vazquez e
al., 2021). By elimina ing non- iable oocy es, ( u ning on a esia p ocesses), mussels can edi ec ene gy
and esou ces o main aining heal hie oocy es o o he physiological unc ions, con ibu ing o gene al
ene gy e iciency (Gus a sson e al., 2019). Al hough excessi e a esia can lead o a signi ican educ ion in he
o e all ep oduc i e ou pu (Pé ez e al., 2015), i also ensu es ha only he mos iable oocy es a e e ained,
enhancing he likelihood o success ul e ilisa ion and o sp ing su i al (Lowe e al., 2015). In ou s udy
(Chap e 4), ollicula a esia le els and he di e ences in a esia le els be ween as and slow g owing mussels
we e ound o be highe a he high in e idal cage, i.e., a he mos ene ge ically cons aining en i onmen .
Besides a ec ing he gonadal/soma ic issue in es men a io, a esia in ensi y p obably a ec s he pace o
gonadal de elopmen . Fo ins ance, gi en he educed capaci y o eabso b gonadal issue in slow g owing
indi iduals, he sca ce su plus ene gy assimila ed by hese o ganismswould be p e e en ially alloca ed owa ds
gonadal p oduc ion, hus accele a ing game e p oduc ion and spawning. Indeed, he his ological analysis o
he game e de elopmen al s ages (Chap e 4) appea o suppo he idea ha slow g owe s a high ide le el
display an ea lie ep oduc ion iming han as g owe s. P io i ising he alloca ion o ene gy in o gonadal
de elopmen o ces slow g owing indi iduals o elease game es o e a sho e pe iod o ime and ea lie in
he season. The sho ening o ep oduc i e ime migh pe haps be bene icial o slow g owing indi iduals
since i migh po en ially allow conse a ion o ene gy o physiological de ences o longe pe iods o ime.
The di e ences in a esia le els be ween di e en ially g owing pheno ypes du ing he ep oduc i e pe iod
eco ded in his s udy s ongly suppo he possibili y ha a esia p ocesses egula ing gonadal/soma ic
alloca ion o ene gy migh be a de e mining ac o in he occu ence o in e -indi idual di e ences in g ow h
a e. Beninge (2017) has indica ed ha “a esia is a widesp ead, ye seldom iden i ied phenomenon in ma ine
bi al es, which p obably a ec s p e ious and cu en da a on ecundi y and ep oduc i e e o bo h in wild
and cul u e popula ions” and has conside ed o be an exci ing ield o u u e esea ch.
In No embe , a bo h idal le els, as and slow g owing mussels di e ge signi ican ly in h ee physiological
ai s: condi ion index, gill s uc u e index and s anda d me abolic a e. Fas g owing mussel specimens

Gene al discussion 233
ha e highe le els o hese h ee pa ame e s han hei slow g owing coun e pa s, a di e ence ha was
much mo e p onounced in he low in e idal. These esul s show ha unde highly s ess ul en i onmen al
ci cums ances caused by low ood a ailabili y and high p esence o pa asi es, as g ow h is linked no only o
he main enance o a high cilia-densi y in he gill bu also o he possession o a highe s anda d me abolic
expendi u e. Since he mussels a e a es ing ep oduc i e pe iod and ha e ele a ed in ensi ies o pa asi e
in ec ion, i seems likely ha he inc eased s anda d me abolic a e displayed by as g owing specimens
ep esen s an ex a ene gy in es men in he main enance o a mo e e ec i e o ac i e immune sys em,
meaning app op ia e a es o haemocy e syn hesis and main enance. In ac , he need o a highe ene gy
in es men in de ence mechanisms o igh pa asi e loading impedes he occu ence o he ene gy sa e
pheno ype ha i does eme ge unde asep ic labo a o y ea ing condi ions. To pu i b ie ly, a highe gill
s uc u e index gua an ees a g ea e and mo e e icien ood acquisi ion (i.e., enhanced acquisi ion and
me abolic e iciency models), allowing he gain o an ene gy su plus ha can be edi ec ed owa ds e icien
de ence p ocesses (alloca ion model). Consequen ly, in his ins ance, he skil ully wo en assembly o he h ee
ene ge ic models wo king oge he p edic ably shapes he de elopmen o he di e en g owing pheno ypes.
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236 Gene al discussion
Conclusions
1.
The gill su ace-a ea is a key ac o o he de elopmen o in e -indi idual g ow h a e di e ences
unde labo a o y ea ing condi ions. The ela ionship be ween gill-su ace a ea and g ow h a e unde
ield ea ing condi ions is no as s ong as in he labo a o y, and is no as decisi e o he de elopmen
o he di e en g ow h pheno ypes.
2.
A clea ela ionship be ween cilia densi y and g ow h a e is con i med, he pheno ypes wi h he lowes
g ow h a es always display less cilia and a poo e epi helial s uc u e han hose wi h he highes
g ow h a es. This ac o is in e e y ci cums ance and wi hou excep ion di e en in as and slow
g owe s, se ing up as a pi o al ac o in he de elopmen o he g owing pheno ypes. Tha could be
ela ed o a highe cellula damage ha may impede he building o he cilia y mesh.
3.
The acquisi ion and me abolic e iciency models a e in insically linked by a p imo dial cause
in ol ing he educed mi ochond ial oxida i e capaci y o slow g owe s, esul ing in an inc eased
ROS p oduc ion and p o oking me abolic damage. This would cause s uc u al damage o he gill
weakening i s capaci y o ood acquisi ion, esul ing in educed ene gy inco po a ion.
4.
The slow g owing pheno ype has a lowe capaci y o diges ion and/o abso p ion han he as g owing
pheno ype, ega dless o he ood a ion: less p opo ion o e ec i e diges i e issue in hei diges i e
gland, as well as highe a ophy in he diges i e ubules. Wi hou he limi a ion in ood acquisi ion a
high ood a ion, his di e ence could be c ucial o he de elopmen o he g owing pheno ypes, in
which ha ing a be e -de eloped il a ion mechanism does no imply a unc ional ad an age.
5.
The na u al en i onmen makes he allome ic ela ionship o he me abolism change. A cause-e ec
ela ionship be ween habi a s and scaling exponen s can be es ablished, demons a ing ha di e en
s anda disa ion alues o me abolic a e need o be used when wo king wi h popula ions o di e en
habi a s. Fo in e idal mussels he scaling exponen is always a ound 2/3 (0.66), whe eas sub idal
mussels inc ease he scaling exponen om 0.64 o 0.87 when ac i i y is de eloped.
6.
Unde es ic i e ophic condi ions in he ield (high in e idal), as g owe s did no de elop h ough
a lowe ed s anda d me abolic a e (ene gy sa e s), bu h ough inc eased acquisi ion and he me abolic
e iciency models. Howe e , in he ield, hose wo models a e complemen ed by he alloca ion model
when shaping he di e en g ow h pheno ypes. The ene gy alloca ion ma e ialises in he un es ained
game e elease o slow g owe s and a much highe capaci y o as g owe s o game e eabso p ion.
The eabso p ion allows as g owe s no o was e he ene gy in es ed in such an expensi e issue and
o edi ec i o soma ic g ow h.