125
Ea ing con es be ween na i e and non-indigenous bi al e
species: es ima ing cap u e e iciencies and clea ance a es
using na u al ses on
Sa a Cab al1, F ede ico Ca alho1, Joana P. C. C uz1, Joshua Heumülle 1, Jose M. F. Baba o2,
Luc A. Comeau3, Paula Chainho1,4 , Ana C. B i o1,5
1 MARE—Ma ine and En i onmen al Science Cen e, ARNET—Aqua ic Resea ch Ne wo k, Faculdade de Ciências, Uni e sidade de Lisboa, 1749-016 Lisboa, Po ugal
2 Ins i u o de In es igaciones Ma inas CSIC, Edua do Cabello 6, 36208 Vigo, Spain
3 Fishe ies and Oceans Canada, Gul Fishe ies Cen e, P.O. Box 5030, Monc on, E1C 9B6 New B unswick, Canada
4 Escola Supe io de Tecnologia, Ins i u o Poli écnico de Se úbal, 2914-508 Se úbal, Po ugal
5 Depa amen o de Biologia Vege al, Faculdade de Ciências, Uni e sidade de Lisboa, 1749-016 Lisboa, Po ugal
Co esponding au ho : Sa a Cab al (sdcab [email p o ec ed])
Copy igh : This is an open access a icle
dis ibu ed unde he e ms o he CC0 Public
Domain Dedica ion.
Resea ch A icle
Abs ac
Despi e he bu geoning numbe o non-indigenous species (NIS) in wo ldwide coas al ecosys ems,
he quan i ica ion o hei di ec impac s on na i e communi ies emains la gely unexplo ed. This is
pa icula ly ue conce ning eeding compe i ion in sympa ic il e - eeding bi al es. In his s udy, ou aim
was o ill a gap o knowledge on he po en ial ophic compe i ion be ween na i e and non-indigenous
bi al es, namely by ocusing on h ee species ha co-occu in Po uguese es ua ine sys ems: he na i e
cockle (Ce as ode ma edule) and Po uguese oys e (Magallana angula a) and he non-indigenous Manila
clam (Rudi apes philippina um). The speci ic objec i es we e o i) es ima e hei cap u e e iciency
(≈ pa icle e en ion e iciency; CE); ii) assess hei clea ance a es (CR); and iii) p o ide a science-based
suppo o sui able managemen measu es ega ding NIS. Expe imen s we e conduc ed in bo h ield
and labo a o y condi ions using he na u al ses on p esen in he seawa e . The CE was highe o he
la ge size classes (8–14 μm) o pa icles measu ed ( anging om 4–14 μm), ega dless o he species.
While he indi idual CRs we e no signi ican ly di e en among species, he CR pe g am o ash- ee d y
body issue weigh was signi ican ly highe o he na i e cockle, sugges ing ha he NIS does no hold
a compe i i e ad an age in clea ing suspended pa icles. Howe e , he Manila clam migh be limi ing
ood sou ces a ailabili y o he na i e species since he e is an o e lap o hei ecological niches.
Key wo ds: Ce as ode ma edule, Magallana angula a, Po ugal, e en ion e iciency, Rudi apes
philippina um
In oduc ion
Biological in asions a e conside ed one o he main h ea s o he ma ine en i on-
men , being a key d i e o biodi e si y change (Ruiz e al. 1999; S e a is e al.
2005; Zo i a e al. 2013; Jimenez e al. 2018). Non-indigenous species (NIS) ha e
become ubiqui ous ac oss coas al ecosys ems such as es ua ies, bays, and coas al
lagoons (Ruiz e al. 2009), since hese a e shel e ed zones p esen ing a high le el
o an h opogenic p essu e and ac i i ies (Ruiz e al. 2000). The ad e se impac s o
NIS a e mul iple and in e disciplina y anging om economic (a ec ing ishe ies,
Academic edi o :
Tammy Robinson-Smy he
Recei ed:
30 Janua y 2025
Accep ed:
25 Ma ch 2025
Published:
7 Oc obe 2025
Ci a ion: Cab al S, Ca alho F, C uz
JPC, Heumülle J, Baba o JMF,
Comeau LA, Chainho P, B i o AC
(2025) Ea ing con es be ween na i e
and non-indigenous bi al e species:
es ima ing cap u e e iciencies and
clea ance a es using na u al ses on.
In: Anas ácio P, Ribei o F, Chainho P
(Eds) In asions in Aqua ic Sys ems.
NeoBio a 102: 125–150. h ps://doi.
o g/10.3897/neobio a.102.148326
NeoBio a 102: 125–150 (2025)
DOI: 10.3897/neobio a.102.148326
Ad ancing esea ch on alien species and biological in asions
A pee - e iewed open-access jou nal
NeoBio a
126
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
aquacul u e, and ou ism sec o s, among o he s; Galil e al. 2014) o ecologi-
cal (including single species in e ac ions, popula ion declines, local ex inc ions,
changes in communi y composi ion, and e ec s on en i e ecosys em p ocesses and
unc ions; Ka sane akis e al. 2014; An on e al. 2019).
Despi e he g owing knowledge abou NIS impac s, his in o ma ion is no ye
p ope ly add essed unde he Eu opean Union legal amewo ks o he p o ec-
ion and managemen o ma ine and eshwa e ecosys ems. Al hough empo al
occu ence, abundance and spa ial dis ibu ion o NIS a e indica o s (desc ip o
D2) used o assess he En i onmen al S a us (ES) o ma ine wa e s unde he
Ma ine S a egy F amewo k Di ec i e (MSFD 2008), no speci ic consensual ools
o measu e he magni ude o bioin asion impac s ha e been o mally adop ed ye .
Likewise, he indices p oposed o assess he Ecological Quali y S a us (EQS) in
ansi ional and coas al wa e s unde he Wa e F amewo k Di ec i e (WFD 2000)
do no add ess impac s o NIS (Zaiko and Daunys 2015).
One o he po en ial ecological haza ds posed by he in oduc ion o NIS ha
should be conside ed in assessmen ools and by decision make s is he displacemen
o na i e species (T uhla e al. 2014). This can occu due o nume ous easons such
as es ic ed mobili y when compe ing o space a ailabili y (Shinen and Mo gan
2009), di ec p eda ion (Ba ini e al. 2021), pa asi ism and diseases (S ige -Pou-
eau and Thouzeau 2015) o a high po en ial o ood compe i ion be ween na i e
and NIS (Comeau e al. 2015; Nielsen e al. 2017; Sonie 2017; Rod igues e al.
2023). Clea ance a e measu emen s (CR; de ined as he olume o wa e clea ed o
pa icles pe uni o ime) may o e insigh in o he po en ial ophic compe i ion
be ween suspension- eeding bi al es. An ex ensi e CR li e a u e spanning ac oss
decades (Møhlenbe g and Riisgå d 1978; Iglesias e al. 1998; T oos e al. 2009;
Yu e al. 2017) e ealed he sensi i i y o CR alues o se e al ac o s, such as em-
pe a u e (Pe ne e al. 2008; C an o d e al. 2011), salini y (Casas e al. 2018), dis-
inc i e expe imen al se -ups (Riisgå d 2001), ood quan i y and quali y (Na a o
and Iglesias 1993), and con amina ion le el a sampling si es (Widdows 2001). To
da e, hese expe imen s ha e been conduc ed p ima ily unde labo a o y condi ions
(Møhlenbe g and Riisgå d 1978, 1979; Denis e al. 1999; Nakamu a 2001; Hau e
e al. 2003; T oos e al. 2009; Joyce e al. 2019) o using a i icial die s (Na a o
and Widdows 1997; Pe e sen e al. 2004; Pascoe e al. 2009; Nagasoe e al. 2011;
Tamayo e al. 2013). Ne e heless, i is ecognized ha labo a o y CR esul s may
de ia e om in si u measu emen s (C an o d 2001; Pe e sen e al. 2004; Cla ie
and Chau aud 2010; Rosa e al. 2018). The e o e, di e en species should be com-
pa ed wi hin he same ophic compe i ion s udy (T oos e al. 2009), wi h he
animals main ained unde he same expe imen al condi ions and p e e ably g azing
on all he di e si y o ses on na u ally a ailable in he seawa e .
No wi hs anding he as esea ch unde aken ocusing on CR, some e ms (e.g.
il a ion a e, e en ion e iciency, pumping a e, cap u e e iciency) ha e been
in e changeably used (Rosa e al. 2018; S ee es e al. 2022), leading o con usion.
The e m e en ion e iciency is mos ly used o e e o he p opo ion o pa icles
ha encoun e he gill ilamen s and a e clea ed om he wa e , being essen ial o
de e mine i be o e measu ing a bi al e’s CR (C an o d e al. 2016). Following
he ecommenda ion o Rosa e al. (2018), ‘ e en ion e iciency’ will he ea e be
deno ed as cap u e e iciency (CE). This is because he numbe o pa icles ha a e
e ained by he gill can only be accu a ely de e mined i in i o di ec app oaches
a e used (Shime a and Juma s 1991; Wa d e al. 1998; Rosa e al. 2018).
127
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
The non-indigenous Manila clam Rudi apes philippina um is a bi al e na i e o
he Indo-Paci ic Ocean ha was i s ly epo ed in Po ugal in 1984 o aquacul-
u e pu poses (Ruano and Sob al 2000). I s p esence h oughou Eu opean coun-
ies has been ecognized o a ec biogeochemical cycles and mac oalgal g ow h
(Ba oli e al. 2001) as well as causing a educ ion in bo h densi y and spa ial
dis ibu ion a ea o na i e bi al es (P ano i e al. 2006, ICES 2008). Fu he mo e,
Maia e al. (2025) sugges ed ha R. philippina um holds a compe i i e ad an age
when compa ed wi h na i e sympa ic species, no only due o i s apid g ow h
and ea ly sexual ma u i y, bu also because o i s b oad die and lexibili y in eed-
ing on mul iple ood sou ces acco ding o hei a ailabili y in he wa e column.
The pu pose o he p esen s udy was o assess he po en ial ophic compe i ion
be ween na i e and non-indigenous bi al es eeding on na u al pa icles. The speci ic
objec i es we e o i) compa e he CE o wo na i e species ( he cockle Ce as ode ma
edule and he Po uguese oys e Magallana angula a) and one non-indigenous spe-
cies ( he Manila clam R. philippina um); ii) es ima e hei CR unde ield and
labo a o y condi ions; and iii) p o ide a science-based suppo o compe en au-
ho i ies and egula o s o sui able managemen measu es ega ding NIS.
Me hods
Expe imen al design
To es ima e he Cap u e E iciency (CE) and he Clea ance Ra e (CR), a o al o
14 expe imen s (se en in he ield and se en in he labo a o y; Fig. 1) we e con-
duc ed wi h h ee species o bi al es: he na i e common cockle (Ce as ode ma
edule) and Po uguese oys e (Magallana angula a) and he non-indigenous Manila
clam (Rudi apes philippina um).
The ield expe imen s ook place be ween Sep embe 20 h and Oc obe 11 h, 2018,
in an oys e aquacul u e a m loca ed in he Sado es ua y (Se úbal, Po ugal). This
si e is known o i s wide a iabili y o in-si u en i onmen al pa ame e s, such as em-
pe a u e and salini y (AQUASADO 2022). Thus, o educe he in luence o hese
luc ua ing a iables, he expe imen s we e also eplica ed in he labo a o y, whe e
condi ions a e inhe en ly mo e s able. These expe imen s we e conduc ed be ween
he 5 h and he 21s o Decembe 2018 a he MARE-ULisboa (Lisboa, Po ugal).
Field expe imen s
Wild specimens o C. edule and R. philippina um we e collec ed in an in e -
idal a ea o he Sado es ua y (38°32.01'N, 8°46.85'W), while M. angula a
indi iduals we e ob ained di ec ly om he aquacul u e a m whe e he ex-
pe imen s occu ed. A se o 12 incuba o s (wi h a maximum olume o 1.2 L
each) we e placed on a mobile pla o m (Fig. 2). A single specimen o one o
he selec ed species was placed in each incuba o and h ee emp y incuba o s
we e used as a con ol. Incuba o s we e dis ibu ed andomly o e he expe i-
men pla o m and an ai pump was a ached o he wall o each incuba o o
homogenize he wa e inside hem and minimize sedimen a ion o pa icles.
Th ee eplica es o each species we e used pe expe imen . The pla o m was
lowe ed o main ain he incuba o s pe manen ly imme sed and a e 48 hou s
o acclima iza ion he expe imen began by gen ly aising he pla o m wi h
128
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Figu e 1. Diag am o he wa e samples ( olume and imings) collec ed in he ield and labo a o y expe imen s o he h ee bi al e
species (C. edule, M. angula a and R. philippina um).
Figu e 2. Expe imen al se -up o he ield expe imen s, conduc ed in he Sado es ua y (Se úbal, Po ugal), using a mobile pla o m wi h
incuba o s o h ee bi al e species (C. edule, M. angula a and R. philippina um) and con ols.
he incuba o s un il all we e isola ed ou o he wa e column. Wa e empe a-
u e and salini y we e con inuously moni o ed wi h wo logge s HOBO U24
Conduc i i y (U24-002-C): one was posi ioned nea he mobile pla o m and
he o he one u he away a a ixed poin in he wa e canal (Table 1).
129
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Each expe imen was conduc ed o 90 minu es, wi h wa e samples being col-
lec ed om each incuba o e e y 15 minu es, including a sample a T0 ( ime o
s a ) and ano he a T (end ime). A o al o 45 mL o wa e was collec ed om
each incuba o a each ime, p ese ed wi h 1% Lugol’s Solu ion (Me ck 109261)
and subsequen ly s o ed in he da k a oom empe a u e un il u he pa icle
measu emen s. In addi ion, 15 mL o wa e we e collec ed om each incuba o
a T0 o measu e u bidi y wi h a Lo ibond in a ed u bidime e TB 210 IR
(Table 1), as a p oxy o he a ailable ses on load. Unpublished da a measu ed a
he same loca ion e ealed a high co ela ion be ween u bidi y and suspended
pa icula e ma e (SPM; See Suppl. ma e ial 1); deno ing ha he a e age SPM
du ing ield expe imen s was 38.35 mg L-1.
Labo a o y expe imen s
The ield expe imen s we e eplica ed in he labo a o y using seawa e collec ed
in he Sado es ua y. Simila ly, specimens o C. edule and R. philippina um we e
collec ed in an in e idal a ea o he Sado es ua y (38°32.01'N, 8°46.85'W),
while M. angula a indi iduals we e ob ained di ec ly om he aquacul u e
a m whe e he ield expe imen s occu ed. A e wa ds, all animals we e ans-
po ed cooled wi h icepacks o MARE-ULisboa, whe e hey we e main ained
pe manen ly imme sed o 48 hou s in an aqua ium o acclima e. A con inu-
ous na u al seawa e low was main ained in he aqua ium o ensu e adequa e
physico-chemical condi ions and ood supply.
The labo a o y expe imen s used 15 incuba o s (wi h a maximum olume o 1.2
L each) placed inside an aqua ium (wi h 200 L o olume) wi h seawa e (Fig. 3).
Fou specimens o each o he selec ed species (C. edule, M. angula a and R. philip-
pina um) we e placed in ou indi idual ae a ed incuba o s and h ee emp y ae a ed
incuba o s we e used as con ol. Incuba o s we e andomly dis ibu ed inside he
aqua ium. Wa e empe a u e and salini y (Table 1) we e con inuously moni o ed
wi h one logge HOBO U24 Conduc i i y (U24-002-C), while dissol ed oxygen
and pH alues we e eco ded daily wi h a mul ipa ame ic p obe YSI EXO2. Addi-
ionally, he concen a ion o ammonia was also moni o ed by spec opho ome y
o gua an ee ha i was always low.
Samples o 45 mL we e aken e e y 15 minu es om each incuba o , o a o al
o 60 minu es du ing each expe imen , including a sample a T0 ( ime o s a ) and
ano he a T (end ime). These samples we e p ese ed wi h 1% Lugol’s Solu ion
(Me ck 109261) and s o ed in he da k a oom empe a u e un il subsequen
pa icle measu emen s. In addi ion, 15 mL o wa e we e also collec ed om each
incuba o du ing T0 ( ime o s a ) o measu e he u bidi y wi h a Lo ibond
in a ed u bidime e TB 210 IR (Table 1) wi h he aim o e i ying he a ailabili y
o pa icles. Acco ding o he co ela ion be ween u bidi y and SPM (See Suppl.
ma e ial 1), he a e age SPM du ing he labo a o y expe imen s was 11.33 mg L-1.
Table 1. En i onmen al condi ions du ing ield and labo a o y expe imen s.
Expe imen Da e Tempe a u e
(min. – max. (°C))
Salini y
(min. – max.)
Tu bidi y
(mean ± s.d. (NTU))
Field Sep embe o
Oc obe 2018
13–20 21–25 30.88 ± 21.35
Labo a o y Decembe 2018 15–20 22–25 6.32 ± 3.01
130
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Val ome y
In bo h expe imen s, al e opening mo emen s o he bi al es we e eco ded ol-
lowing a me hodology desc ibed in Nagai e al. (2006) and Comeau e al. (2012).
Each bi al e specimen had a coa ed Hall elemen senso (HW-300a, Asahi Kasei,
Japan) glued o one al e and a magne a ached o he o he al e (di ec ly in he
opposi e posi ion o he Hall senso ), c ea ing a magne ic ield (Fig. 4). This mag-
ne ic ield was eco ded as ou pu ol age by s ain eco ding de ices (DC 104R,
Tokyo Sokki Kenkyujo Co., Japan) and a e wa ds con e ed in o al e opening
dis ance. These measu emen s allowed he iden i ica ion o specimens ha we e
comple ely and consis en ly closed du ing he expe imen s and hus, undoub edly
no in e ac ing wi h hei en i onmen . These specimens we e disca ded om he
expe imen s as hey we e p esumably s essed by he manipula ions. This app oach
minimized he po en ial unde es ima ion o CR.
Es ima ion o he Condi ion Index (CI)
A he end o he expe imen s, all bi al es we e placed in sepa a e plas ic bags, p e-
se ed in a eeze a -20 °C and s o ed o u u e analysis. La e , all specimens we e
p ocessed in he labo a o y: he bi al e shells we e i s measu ed and hen he
so body was sepa a ed om he shell wi h a scalpel and weeze s, and bo h pa s
we e d ied a 60 °C o 72 hou s, o ob ain he d y weigh . Las ly, he d y mea
Figu e 3. Expe imen al se -up o he labo a o y expe imen s, conduc ed a he MARE-ULisboa
(Lisboa, Po ugal), using an aqua ium wi h incuba o s o he h ee bi al e species (C. edule,
M. angula a and R. philippina um).
131
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
was bu n in a mu le u nace un il weigh s abiliza ion a 500 °C, o es ima e he
ashes’ weigh . The Condi ion Index (CI) was calcula ed acco ding o he ollowing
o mula adap ed om Walne and Mann (1975):
The mean shell leng h, mean ash- ee d y weigh (AFDW) o he body issue
and mean condi ion index (CI) o each species used in ield and labo a o y expe -
imen s a e summa ized in Table 2.
Taking in o conside a ion ha he mean ash- ee d y weigh (AFDW) o he
body issue o he specimens a ied g ea ly be ween ield and labo a o y expe i-
men s, da a we e analysed sepa a ely o each expe imen ype.
Es ima ion o Cap u e E iciency (CE) and Clea ance Ra es (CR)
The pa icle coun and pa icle size dis ibu ion we e de e mined using a PAMAS
lase pa icle coun e (model S4031 GO) con aining an HCB-LD-50/50 ligh -sca -
e ing senso . Pa icles we e coun ed using he ligh blocking p inciple: when he
cell is 100% illumina ed by lase ligh , he pa icle blocks ligh , and cas s a shadow
on a pho ode ec o . The pa icle size is de e mined by he amoun o blocked ligh .
Con ol incuba o s we e also analysed o iden i y any educ ion in pa icles due o
bo om deposi ion and adjus acco dingly he incuba o s wi h bi al e specimens
by sub ac ing his decline in pa icle concen a ion. Fu he mo e, hese con ols
we e also used o cha ac e ize he na u al ses on p esen in each expe imen . Fo all
expe imen s, he PAMAS used an ini ial olume o 15 mL o each wa e sample,
in which pa icles we e coun ed in 1 mL o seawa e .
The PAMAS was ini ially se o de e mine 33 classes o sizes anging om 1 o
150 μm o p o ide a e y di e en ia ed analysis o he sizes. Howe e , he ac ual
ange moni o ed o de e mine bo h CEs and CRs was se be ween 4 and 14 μm
due o he ollowing: 1) he highes e en ion e iciency alues o bi al es a e
a ained o pa icles wi h 4 μm and abo e (Møhlenbe g and Riisgå d 1978; C an-
o d e al. 2016); and 2) mos o he pa icles ound in he seawa e we e wi hin
his size ange. O he wise, i he numbe o pa icles o a speci ic size is educed,
Figu e 4. A diag am o an oys e wi h a Hall elemen senso a ached o a al e and a small magne
a ached o he opposi e al e B hall elemen senso glued o he al e o a R. philippina um specimen.
132
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
inco ec in e p e a ions may be d awn, since he pa icles migh no be cap u ed
due o i s size o simply because hei a ailabili y in he na u al seawa e is oo low
o be e ec i ely cap u ed.
The es ima ion o CE and CR o all species and bo h ield and labo a o y
expe imen s ollowed he s a ic me hod desc ibed by C an o d e al. (2016). A sus-
pension eede pumping a a cons an a e and wi hou wa e enewal will emo e
pa icles a a a e ha declines exponen ially (Coughlan 1969). Consequen ly, he
PAMAS can be used o measu e he slope o he na u al loga i hm o pa icle
concen a ion decline o e ime (λ), aking in o conside a ion ha o all mea-
su emen s, his decline should be linea o e ime in o de o ensu e he cons an
pumping a e assump ion (C an o d e al. 2016).
The CE was es ima ed o each indi idual and each pa icle size acco ding o he
ollowing equa ion adap ed om C an o d e al. (2016):
whe e λsample, size ep esen s he slope o he linea eg ession be ween he pa icle
concen a ion ( ans o med in na u al loga i hm) and he elapsed ime o a gi en
pa icle size class in he sample; λcon ol, size is he slope o he linea eg ession be ween
he pa icle concen a ion ( ans o med in na u al loga i hm) and he elapsed ime
o he same pa icle size class in he con ol (all con ols we e a e aged o each
sampling da e); and λsample, a e age is he a e age o he λsample, size ac oss all pa icle
size classes o each indi idual. This s anda diza ion by he a e age alue ac oss all
pa icle size classes allowed o minimize he e ec o po en ial measu emen e o s
om a single pa icle size class coun . The esul ing CE alues ange om 0 o 1,
ep esen ing pa icles sizes ha a e no cap u ed and cap u ed a maximum e i-
ciency, espec i ely. Ne e heless, a e aging pa icles ac oss size classes, a he han
using he maximum, may lead o CE alues exceeding 1. Suppl. ma e ial 2 depic s
an example o how some componen s o he CE o mula we e es ima ed o each
specimen. Subsequen ly, he mean CE o each pa icle size was es ima ed o each
species, by a e aging all he indi iduals CE. See Table 3 o he sample sizes pe
species and ype o expe imen included in he CE es ima ion.
CR was es ima ed o each specimen, acco ding o he equa ion adap ed om
Casas e al. (2018):
Table 2. Mean (± SD) shell leng h (mm), ash- ee d y body issue weigh (AFDW; g) and condi ion
index (%) o bo h ield and labo a o y expe imen s o h ee bi al e species (C. edule, M. angula a
and R. philippina um).
Expe imen Species Mean shell leng h
(mm)
Mean AFDW o
body (g)
Mean Condi ion
Index (%)
Field C. edule 31.30 ± 1.39 0.55 ± 0.24 9.61 ± 4.92
M. angula a 85.17 ± 6.91 3.82 ± 1.55 7.60 ± 2.58
R. philippina um 43.57 ± 2.07 1.51 ± 0.79 10.43 ± 4.25
Labo a o y C. edule 29.50 ± 1.66 0.18 ± 0.02 4.12 ± 0.61
M. angula a 91.11 ± 4.93 1.41 ± 0.20 3.16 ± 0.70
R. philippina um 47.09 ± 1.79 0.50 ± 0.06 4.59 ± 0.51
133
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
whe e λsample ep esen s he slope o he linea eg ession be ween he pa icle con-
cen a ion ( ans o med in na u al loga i hm) and he elapsed ime in he sam-
ple; λcon ol is he slope o he linea eg ession be ween he pa icle concen a ion
( ans o med in na u al loga i hm) and he elapsed ime in he con ol (all con ols
we e a e aged o each sampling da e); and V is he olume o seawa e in each
incuba o (1.2 L). Wi h he aim o educing he weigh o po en ial ou lie s on
he es ima es o he CR, he app oach o Casas e al. (2018) was ollowed. This
me hod in eg a es he pa icle concen a ion alues eco ded h oughou he mul-
iple sampling imes, ins ead o using only da a om he beginning and he end o
he expe imen s. Addi ionally, only linea eg essions wi h 2 > 0.90 we e selec ed
o he subsequen analyses. Suppl. ma e ial 3 depic s an example o how he CR
was es ima ed o each specimen and Table 3 desc ibes he numbe o bi al es pe
species and ype o expe imen included in he CR es ima ion.
Las ly, since he s udied bi al e species ha e disc epan sizes, CR absolu e alues
a e only ep esen a i e when compa ing esul s be ween indi iduals o he same
species. Hence, ollowing he CR es ima ions, hese alues we e di ided by he
ash- ee d y weigh (AFDW) o he body issue o he espec i e specimen o be
compa able be ween he di e en species.
S a is ical analysis
The Shapi o-Wilk’s and Le ene’s es s we e used o assess he no mali y o esiduals
and he homogenei y o a iances, espec i ely. To es o di e ences in CE alues
be ween species and ac oss pa icle size classes a Pe mu a ional Analysis o Va iance
(PERMANOVA; Ande son e al. 2008) was conduc ed o each expe imen ype
( ield and labo a o y) wi h B ay-Cu is simila i y ma ices and 9999 pe mu a ions.
This analysis was pe o med on PRIMER® 7 (Cla ke and Go ley 2015), using a
wo-way ixed-e ec c ossed design (Fac o s: species; pa icle size).
A e wa ds, K uskal–Wallis es s we e used o compa e he mean di e ences in
CR be ween species, bo h o ield and labo a o y esul s. All compa isons we e pe -
o med o CR (L h-1 ind-1) and CR (L h-1 g-1 AFDW). Dunn’s pos hoc es s we e
used o pai wise compa isons be ween g oups. Apa om he PERMANOVA,
all he analyses we e pe o med in R e sion 4.4.1 (RS udio e sion 2024.12.0).
Resul s
In spi e o gene ally simila mean shell leng h ac oss expe imen s (wi hin each
species), he mean AFDW o body issue was always highe in ield expe imen s,
ega dless o he species (Table 2). Conside ing his ou come, no di ec compa i-
sons be ween ield and labo a o y expe imen s we e pe o med in his pape .
A he onse o he expe imen s, he a e age concen a ion o pa icles p es-
en in he seawa e was es ima ed o each pa icle size (Fig. 5). Pa icle con-
cen a ions in he ield we e on a e age 6 o 11 imes highe han in he lab-
o a o y. The maximum a e age numbe o pa icles pe ml we e eco ded o
he size classes o 4–5 μm (12805.12 pa icles ml-1 and 2202.87 pa icles ml-1
o ield and labo a o y, espec i ely), whe eas he minimum was obse ed o
pa icles wi hin he size class o 13–14 μm (1940.39 pa icles ml-1 and 190.69
pa icles ml-1 o ield and labo a o y, espec i ely).
140
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Consequen ly, go e ning en i ies and egula o s should be cau ious when es ab-
lishing new a eas o bi al e aquacul u e p oduc ion and ensu e ha da a on CE
and CR o bo h na i e and NIS a e aken in o accoun since he e is an o e lap
o hei ecological niches. Besides, conside ing ha he indi iduals used in hese
expe imen s we e ep esen a i e o he exploi able popula ions (since hei shell
leng hs we e all abo e he minimum ma ke ing size), his in o ma ion should also
be conside ed when managing NIS and na i e species’ s ocks.
Conclusion
In conclusion, ou esul s indica e ha C. edule, M. angula a and R. philippina um
ha e simila cap u e e iciencies o he size classes o pa icles measu ed in his
s udy ( anging om 4–14 μm). Mo eo e , R. philippina um did no p esen a com-
pe i i e ad an age in clea ing suspended pa icles when compa ed wi h he na i es
M. angula a and C. edule, wi h he la e e ealing o be he mos e icien species
on a issue weigh basis. The e o e, he in asion success o R. philippina um may
be explained by o he biological cha ac e is ics o ad an ages in ecological in e -
ac ions such as ep oduc i e a es, space compe i ion o o e lapping niche spaces.
I is highly ecommended ha u u e s udies ocus on hese aspec s in o de o
p o ide he ull ex en o he po en ial impac s o NIS on na i e species. No wi h-
s anding, NIS may s ill jeopa dize he en i e ecosys em, by exe ing an addi ional
p essu e on i s ca ying capaci y. Finally, his s udy p o ides an impo an baseline
con ibu ion o he managemen o NIS by de e mining cap u e e iciencies and
clea ance a es es ima ed exclusi ely wi h na u al seawa e depic ing a mo e accu-
a e ep esen a ion o he p ocesses ha occu in he en i onmen .
Acknowledgemen s
A special hank you o A onso Fe ei a, Filipa A onso, Inês A onso, Inês Teodo o,
Isabel Ca doso, Ma ga ida Raposo, Ma ion Co e , Ped o Coelho, Ped o Gomes,
Ped o M. Oli ei a, Te esa Camelo and Thomas Goulding, o assis ing us du ing
he expe imen s. Thanks a e also due o Ramón Filguei a o he aluable sugges-
ions. This s udy bene i ed om discussions wi hin he Wo king G oup on In o-
duc ions and T ans e s o Ma ine O ganisms (WGITMO) unde he In e na ional
Council o he Explo a ion o he Seas (ICES). Finally, he au ho s g a e ully
acknowledge he sugges ions o he e iewe s ha imp o ed he manusc ip .
Addi ional in o ma ion
Con lic o in e es
The au ho s ha e decla ed ha no compe ing in e es s exis .
E hical s a emen
No e hical s a emen was epo ed.
Funding
This wo k was suppo ed by he Po uguese Founda ion o Science and Technology (FCT), h ough he
g an s SFRH/BD/145746/2019 (h ps://doi.o g/10.54499/SFRH/BD/145746/2019), 2020.06325.
BD (h ps://doi.o g/10.54499/2020.06325.BD), UI/BD/151399/2021, CEECIND/00095/2017,
141
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
2020.01797.CEECIND, UIDB/04292/2020 (h ps://doi.o g/10.54499/UIDB/04292/2020), and
he Associa e Labo a o y ARNET (h ps://doi.o g/10.54499/LA/P/0069/2020). Addi ionally, his
wo k was also unded by he MAR2020 p ojec s AQUASADO (MAR-02.01.01-FEAMP-0051) and
NIPOGES (MAR-01.03.02-FEAMP-0013) and by he Eu opean Union’s In e eg A lan ic p ojec
COCKLES (EAPA_458/2016).
Au ho con ibu ions
Concep ualiza ion: PC, ACB. Fo mal analysis: SC, ACB. Funding acquisi ion: PC, ACB. In es iga-
ion: JH, PC, SC, FC, JPCC, JMFB, LAC, ACB. Me hodology: JMFB, JPCC, FC, SC, JH, LAC,
ACB. P ojec adminis a ion: ACB. Resou ces: JMFB, LAC, PC. Supe ision: ACB, PC. W i ing -
o iginal d a : SC. W i ing - e iew and edi ing: ACB, JMFB, FC, PC, JH, JPCC, LAC.
Au ho ORCIDs
Sa a Cab al h ps://o cid.o g/0000-0002-7302-4105
F ede ico Ca alho h ps://o cid.o g/0000-0003-2909-0604
Paula Chainho h ps://o cid.o g/0000-0002-3539-9942
Da a a ailabili y
All o he da a ha suppo he indings o his s udy a e a ailable in he main ex o Supplemen a y
In o ma ion.
Re e ences
Ande son MJ, Go ley RN, Cla ke KR (2008) PERMANOVA + o PRIMER: Guide o So wa e
and S a is ical Me hods. PRIMER-E, Plymou h, UK. h ps://lea ninghub.p ime -e.com/books/
pe mano a- o -p ime -guide- o-so wa e-and-s a is ical-me hods
An on A, Ge aldi NR, Lo elock CE, Apos olaki ET, Benne S, Ceb ian J, K ause-Jensen D, Ma bà
N, Ma ine o P, Pandol i JM, San ana-Ga con J, Dua e CM (2019) Global ecological impac s
o ma ine exo ic species. Na u e Ecology & E olu ion 3: 787–800. h ps://doi.o g/10.1038/
s41559-019-0851-0
AQUASADO (2022) Rela ó io Final - P omo e a AQUAcul u a sus en á el no es uá io do SADO.
A akawa H, Yaoi a T, Koike T, Mo inaga T (1998) Size o suspended pa icles caugh by Manila
clam, Rudi apes philippina um. Oceanog aphic Li e a u e Re iew 7: 1179. h ps://www.in ona.
pl// esou ce/bwme a1.elemen .else ie -cb215dc -ae08-324 -b0b7-119e8ecb9c46
Ba illé L, P ou J, Hé al M, Raze D (1997) E ec s o high na u al ses on concen a ions on he eed-
ing, selec ion, and abso p ion o he oys e C assos ea gigas (Thunbe g). Jou nal o Expe imen al
Ma ine Biology and Ecology 212: 149–172. h ps://doi.o g/10.1016/S0022-0981(96)02756-6
Ba JM, Mun oe D, Rose JM, Cal o L, Cheng KM, Baye S, K eege D (2023) Seasonal Feeding
Beha io o Aquacul u e Eas e n Oys e s (C assos ea i ginica) in he Mid-A lan ic. Es ua ies and
Coas s 1: 1–16. h ps://doi.o g/10.1007/s12237-023-01293-9
Ba oli M, Nizzoli D, Via oli P, Tu olla E, Cas aldelli G, Fano EA, Rossi R (2001) Impac o Tapes
philippina um a ming on nu ien dynamics and ben hic espi a ion in he Sacca di Go o.
Hyd obiologia 455: 203–212. h ps://doi.o g/10.1023/A:1011910422400
Ba ini N, Giache i CB, Cas o KL, Bo olus A, Schwind E (2021) New in asi e p eda o educes
he abundance o na i e p ey in a cold- empe a e ma ine ouling communi y. Aqua ic Conse a-
ion 31: 2842–2854. h ps://doi.o g/10.1002/aqc.3681
Bayne BL, Hawkins AJS, Na a o E, Iglesias IP (1989) E ec s o ses on concen a ion on eeding,
diges ion and g ow h in he mussel My ilus edulis. Ma ine Ecology P og ess Se ies 55: 47–54.
h ps://doi.o g/10.3354/meps055047
142
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
B icelj VM, Malou RE (1984) In luence o algal and suspended sedimen concen a ions on he
eeding physiology o he ha d clam Me cena ia me cena ia. Ma ine Biology 84: 155–165.
h ps://doi.o g/10.1007/BF00393000
B i o AC, Pe ei a H, Picado A, C uz J, Ce eja R, Biguino B, Chainho P, Nascimen o Â, Ca alho F,
Cab al S, San os C, Palma C, Bo ges C, Dias JM (2023) Inc eased oys e aquacul u e in he Sado
Es ua y (Po ugal): How o ensu e ecosys em sus ainabili y? The Science o he To al En i on-
men 855: 158898. h ps://doi.o g/10.1016/j.sci o en .2022.158898
Cab al S, Ca alho F, Gaspa M, Ramajal J, Sá E, San os C, Sil a G, Sousa A, Cos a JL, Chainho P
(2020) Non-indigenous species in so -sedimen s: A e some es ua ies mo e in aded han o he s?
Ecological Indica o s 110: 105640. h ps://doi.o g/10.1016/j.ecolind.2019.105640
Ca deccia A, Ma chini A, Occhipin i-Amb ogi A, Galil B, Gollasch S, Minchin D, Na ščius A,
Olenin S, Oja ee H (2018) Assessing biological in asions in Eu opean Seas: Biological ai s o
he mos widesp ead non-indigenous species. Es ua ine, Coas al and Shel Science 201: 17–28.
h ps://doi.o g/10.1016/j.ecss.2016.02.014
Casas SM, La aud R, La Pey e MK, Comeau LA, Filguei a R, La Pey e JF (2018) Quan i ying salin-
i y and season e ec s on eas e n oys e clea ance and oxygen consump ion a es. Ma ine Biology
165: 1–13. h ps://doi.o g/10.1007/s00227-018-3351-x
Chiesa S, Lucen ini L, F ei as R, Ma zano FN, B eda S, Figuei a E, Caill-Milly N, He be RJH,
Soa es AMVM, A gese E (2017) A his o y o in asion: COI phylogeny o Manila clam Ru-
di apes philippina um in Eu ope. Fishe ies Resea ch 186: 25–35. h ps://doi.o g/10.1016/j. ish-
es.2016.07.024
Cla ke KR, Go ley RN (2015) PRIMER 7: Use manual/ u o ial. PRIMER-E L d., Plymou h, UK.
Cla ie J, Chau aud L (2010) Biodeposi p oduc ion by B ac echlamys exillum (bi al e: Pec in-
idae) in a opical lagoon. Jou nal o Sea Resea ch 64: 231–240. h ps://doi.o g/10.1016/j.
sea es.2010.03.001
Comeau LA, May and É, Malle A (2012) Win e quiescence and sp ing awakening o he Eas e n
oys e C assos ea i ginica a i s no he nmos dis ibu ion limi . Ma ine Biology 159: 2269–
2279. h ps://doi.o g/10.1007/s00227-012-2012-8
Comeau LA, Filguei a R, Guyonde T, Sonie R (2015) The impac o in asi e unica es on he de-
mand o phy oplank on in longline mussel a ms. Aquacul u e (Ams e dam, Ne he lands) 441:
95–105. h ps://doi.o g/10.1016/j.aquacul u e.2015.02.018
Co eia MJ, Chainho P, Goulding T, Ca alho F, Cab al S, Fe ei a FG, Vasconcelos L (2025) Pa -
icipa o y ac ion esea ch suppo ing adap i e go e nance o Manila clam ishe ies. Ma ine Policy
174: 106605. h ps://doi.o g/10.1016/j.ma pol.2025.106605
Coughlan J (1969) The es ima ion o il e ing a e om he clea ance o suspensions. Ma ine Biology
2: 356–358. h ps://doi.o g/10.1007/BF00355716
C an o d PJ (2001) E alua ing he “ eliabili y” o il a ion a e measu emen s in bi al es. Ma ine
Ecology P og ess Se ies 215: 303–305. h ps://doi.o g/10.3354/meps215303
C an o d PJ (2019) Magni ude and ex en o wa e cla i ica ion se ices p o ided by bi al e sus-
pension eeding. In: Smaal A, Fe ei a J, G an J, Pe e sen JSØ (Eds) Goods and Se ices o
Ma ine Bi al es. Sp inge In e na ional Publishing, 119–141. h ps://doi.o g/10.1007/978-3-
319-96776-9_8
C an o d PJ, E an Wa d J, Shumway SE (2011) Bi al e il e eeding: a iabili y and limi s o he
aquacul u e bio il e . In: Shumway SE (Ed.) Shell ish Aquacul u e and he En i onmen . John
Wiley & Sons, Inc., Ox o d, 81–124. h ps://doi.o g/10.1002/9780470960967.ch4
C an o d PJ, S ohmeie T, Filguei a R, S and Ø (2016) Po en ial me hodological in luences on
he de e mina ion o pa icle e en ion e iciency by suspension eede s: My ilus edulis and Ciona
in es inalis. Aqua ic Biology 25: 61–73. h ps://doi.o g/10.3354/ab00660
143
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Denis L, Allio E, G zebyk D (1999) Clea ance a e esponses o Medi e anean mussels, My ilus
gallop o incialis, o a ia ions in he low, wa e empe a u e, ood quali y and quan i y. Aqua ic
Li ing Resou ces 12: 279–288. h ps://doi.o g/10.1016/S0990-7440(00)86639-5
Despacho n.° 26/DG/2024, July 24 h (2024) Despacho n.° 26/DG/2024, July 24 h. h ps://www.dg m.
p /documen s/20143/84407/ _2796510_1.pd /43cb5 d6-b3ac- 068-87b9-6b189057052d
Dias E, Chainho P, Ba ocas-Dias C, Adão H (2019) Food sou ces o he non-indigenous bi al e
Rudi apes philippina um (Adams & Ree e, 1850) and ophic niche o e lap wi h na i e species.
Aqua ic In asions 14: 638–655. h ps://doi.o g/10.3391/ai.2019.14.4.05
Fe nandes S, Sob al P, an Du en L (2007) Clea ance a es o Ce as ode ma edule unde inc eas-
ing cu en eloci y. Con inen al Shel Resea ch 27: 1104–1115. h ps://doi.o g/10.1016/j.
cs .2006.08.010
Galil BS, Ma chini A, Occhipin i-Amb ogi A, Minchin D, Na ščius A, Oja ee H, Olenin S
(2014) In e na ional a i als: Widesp ead bioin asions in Eu opean Seas. E hology Ecology and
E olu ion 26: 152–171. h ps://doi.o g/10.1080/03949370.2014.897651
Galimany E, F eeman CJ, Lun J, Domingos A, Sacks P, Wal e s L (2017) Feeding compe i ion
be ween he na i e oys e C assos ea i ginica and he in asi e mussel My ella cha uana. Ma ine
Ecology P og ess Se ies 564: 57–66. h ps://doi.o g/10.3354/meps11976
Goulle que P, He al M, Deslous-Paoli JM, P ou J, Ga nie J, Raze D, Bo om hana a W (1989)
Ecophysiologie e bilan éne gé ique de la palou de japonaise d’éle age Rudi apes philippina um.
Jou nal o Expe imen al Ma ine Biology and Ecology 132: 85–108. h ps://doi.o g/10.1016/0022-
0981(89)90217-7
G ay MW, Pin on D, Canes elli A, Dix N, Ma cum P, Kimb o D, G izzle R (2022) Beyond esi-
dence ime: Quan i ying ac o s ha d i e he spa ially explici il a ion se ices o an abundan
na i e oys e popula ion. Es ua ies and Coas s 45: 1343–1360. h ps://doi.o g/10.1007/s12237-
021-01017-x
Hau e J, Hu e A, Pal adeau H, Nou y M, Penisson C, Ma in JLY, Boud y P (2003) Feeding and
espi a o y ime ac i i ies in he cupped oys e s C assos ea gigas, C assos ea angula a and hei
hyb ids. Aquacul u e (Ams e dam, Ne he lands) 218: 539–551. h ps://doi.o g/10.1016/S0044-
8486(02)00493-3
Ha en DS, Mo ales-Alamo R (1970) Fil a ion o pa icles om suspension by he Ame ican oys e
C assos ea i ginica. The Biological Bulle in 139: 248–264. h ps://doi.o g/10.2307/1540081
ICES (2008) Repo o he Wo king G oup on In oduc ion and T ans e s o Ma ine O ganisms
(WGITMO). Copenhagen, Denma k. h ps://co e.ac.uk/ eade /225939220
Iglesias JIP, Na a o E, Al a ez-Jo na E, A men ina I (1992) Feeding, pa icle selec ion and ab-
so p ion in cockles Ce as ode ma edule (L.) exposed o a iable condi ions o ood concen a ion
and quali y. Jou nal o Expe imen al Ma ine Biology and Ecology 162: 177–198. h ps://doi.
o g/10.1016/0022-0981(92)90200-T
Iglesias JIP, U u ia MB, Na a o E, Al a ez-Jo na P, La e xea X, Boug ie S, He al M (1996) Va i-
abili y o eeding p ocesses in he cockle Ce as ode ma edule (L.) in esponse o changes in ses-
on concen a ion and composi ion. Jou nal o Expe imen al Ma ine Biology and Ecology 197:
121–143. h ps://doi.o g/10.1016/0022-0981(95)00149-2
Iglesias JIP, U u ia MB, Na a o E, Iba ola I (1998) Measu ing eeding and abso p ion in suspen-
sion- eeding bi al es: An app aisal o he biodeposi ion me hod. Jou nal o Expe imen al Ma ine
Biology and Ecology 219: 71–86. h ps://doi.o g/10.1016/S0022-0981(97)00175-5
INE (2023) Es a ís icas da Pesca: 2022. Lisboa.
Jiang W, Coppola F, Jiang Z, F ei as R, Mao Y, Tan Z, Fang J, Fang J, Zhang Y (2023) A ood-web
model as a ool o he ecosys em-le el managemen o bi al es in an A lan ic coas al lagoon.
Ma ine En i onmen al Resea ch 190: 106117. h ps://doi.o g/10.1016/j.ma en es.2023.106117
144
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Jimenez H, Keppel E, Chang AL, Ruiz GM (2018) In asions in Ma ine Communi ies: Con as -
ing Species Richness and Communi y Composi ion Ac oss Habi a s and Salini y. Es ua ies and
Coas s 41: 484–494. h ps://doi.o g/10.1007/s12237-017-0292-4
Jø gensen CB (1989) Wa e p ocessing in cilia y eede s, wi h special e e ence o he bi al e il e
pump. Compa a i e Biochemis y and Physiology. Pa A, Physiology 94: 383–394. h ps://doi.
o g/10.1016/0300-9629(89)90562-8
Joyce PWS, K eg ing LT, Dick JTA (2019) Rela i e impac s o he in asi e Paci ic oys e , C assos ea
gigas, o e he na i e blue mussel, My ilus edulis, a e media ed by low eloci y and ood concen-
a ion. NeoBio a 45: 19–37. h ps://doi.o g/10.3897/neobio a.45.33116
Ka lsson Ö, Jonsson PR, La sson AI (2003) Do la ge ses on pa icles con ibu e o he die o he bi-
al e Ce as ode ma edule? Ma ine Ecology P og ess Se ies 261: 161–173. h ps://doi.o g/10.3354/
meps261161
Ka sane akis S, Wallen inus I, Zene os A, Leppäkoski E, Çina ME, Oz ü k B, G abowski M, Go-
lani D, Ca doso AC (2014) Impac s o in asi e alien ma ine species on ecosys em se ices and
biodi e si y: A pan-Eu opean e iew. Aqua ic In asions 9: 391–423. h ps://doi.o g/10.3391/
ai.2014.9.4.01
Kiø boe T, Møhlenbe g F (1981) Pa icle Selec ion in Suspension-Feeding Bi al es. Ma ine Ecology
P og ess Se ies 5: 291–296. h ps://doi.o g/10.3354/meps005291
Koo BJ, Seo J (2020) Fil a ion a es o he manila clam, Rudi apes philippina um, in idal la s
wi h di e en hyd og aphic egimes. PLoS ONE 15: e0228873. h ps://doi.o g/10.1371/jou nal.
pone.0228873
Langdon CJ, Newell RIE (1990) U iliza ion o de i us and bac e ia as ood sou ces by wo bi al e
suspension- eede s, he oys e C assos ea i ginica and he mussel Geukensia demissa. Ma ine
Ecology P og ess Se ies 58: 299–310. h ps://doi.o g/10.3354/meps058299
Maia F, Gaspa MB, Ba oso CM (2025) Compa a i e s udy o Rudi apes philippina um and Ru-
di apes decussa us in Ria de A ei o, Po ugal: In asi e species managemen and ma ine esou ce
conse a ion. Es ua ine, Coas al and Shel Science 314: 109123. h ps://doi.o g/10.1016/j.
ecss.2025.109123
Ma he s NF (1974) Some compa a i e aspec s o il e - eeding in Os ea edulis L. and C assos ea
angula a (Lam.) (Mollusca: Bi al ia). The Jou nal o Molluscan S udies 41: 89–97. h ps://doi.
o g/10.1093/ox o djou nals.mollus.a065265
Møhlenbe g F, Riisgå d HU (1978) E iciency o pa icle e en ion in 13 species o suspension eed-
ing bi al es. Ophelia 17: 239–246. h ps://doi.o g/10.1080/00785326.1978.10425487
Møhlenbe g F, Riisgå d HU (1979) Fil a ion Ra e, Using a New Indi ec Technique, in Thi een
Species o Suspension-Feeding Bi al es. Ma ine Biology 54: 143–147. h ps://doi.o g/10.1007/
BF00386593
Mou a P, Ga aule LL, Vasconcelos P, Chainho P, Cos a JL, Gaspa MB (2017) Age and g ow h o
a highly success ul in asi e species: The manila clam Rudi apes philippina um (Adams & Ree e,
1850) in he Tagus Es ua y (Po ugal). Aqua ic In asions 12: 133–146. h ps://doi.o g/10.3391/
ai.2017.12.2.02
MSFD (2008) MSFD 2008/56/EC. Di ec i e 2008/56/EC o he Eu opean pa liamen and o he
council o 17 June 2008 es ablishing a amewo k o communi y ac ion in he ield o ma-
ine en i onmen al policy (Ma ine S a egy F amewo k Di ec i e). h p://da a.eu opa.eu/eli/
di /2008/56/oj
Nagai K, Honjo T, Go J, Yamashi a H, Oh SJ (2006) De ec ing he shell ish kille He e ocapsa
ci cula isquama (Dinophyceae) by measu ing bi al e al e ac i i y wi h a Hall elemen senso .
Aquacul u e (Ams e dam, Ne he lands) 255: 395–401. h ps://doi.o g/10.1016/j.aquacul-
u e.2005.12.018
145
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Nagasoe S, Suzuki K, Yu imo o T, Fuseya R, Fukao T, Yama ogi T, Kimo o K, Maeno Y (2011)
Clea ance e ec s o he paci ic oys e C assos ea gigas on he ish-killing algae Cha onella ma ina
and Cha onella an iqua. Aqua ic Biology 11: 201–211. h ps://doi.o g/10.3354/ab00295
Nakamu a Y (2001) Fil a ion a es o he Manila clam, Rudi apes philippina um: Dependence on
p ey i ems including bac e ia and picocyanobac e ia. Jou nal o Expe imen al Ma ine Biology
and Ecology 266: 181–192. h ps://doi.o g/10.1016/S0022-0981(01)00354-9
Na a o E, Iglesias JIP (1993) In aunal il e - eeding bi al es and he physiological esponse o sho -
e m luc ua ions in ood a ailabili y and composi ion. In: Dame RF (Ed.) Bi al e Fil e Feede s.
Heidelbe g: Sp inge , Be lin, 25–56. h ps://doi.o g/10.1007/978-3-642-78353-1_2
Na a o JM, Widdows J (1997) Feeding physiology o Ce as ode ma edule in esponse o a wide ange
o ses on concen a ions. Ma ine Ecology P og ess Se ies 152: 175–186. h ps://doi.o g/10.3354/
meps152175
Na a o E, Iglesias JIP, O ega MM (1992) Na u al sedimen as a ood sou ce o he cockle Ce -
as ode ma edule (L.): E ec o a iable pa icle concen a ion on eeding, diges ion and he scope
o g ow h. Jou nal o Expe imen al Ma ine Biology and Ecology 156: 69–87. h ps://doi.
o g/10.1016/0022-0981(92)90017-5
Nielsen M, Hansen BW, Vismann B (2017) Feeding ai s o he Eu opean la oys e , Os ea edu-
lis, and he in asi e Paci ic oys e , C assos ea gigas. Ma ine Biology 164: 1–10. h ps://doi.
o g/10.1007/s00227-016-3041-5
Nilin J, Pes ana JLT, Fe ei a NG, Lou ei o S, Cos a-Lo u o LV, Soa es AM (2012) Physiological
esponses o he Eu opean cockle Ce as ode ma edule (Bi al ia: Ca didae) as indica o s o coas al
lagoon pollu ion. The Science o he To al En i onmen 435: 44–52. h ps://doi.o g/10.1016/j.
sci o en .2012.06.107
NIPOGES (2022) Rela ó io Final - Es ado a ual das populações de amêijoa-japonesa da Ria de
A ei o, lagoa de Óbidos e es uá ios do Tejo e Sado – Bases cien í icas pa a uma ges ão sus en á el
do ecu so.
Ong EZ, B i a M, Moens T, Van Colen C (2017) Physiological esponses o ocean acidi ica ion
and wa ming syne gis ically educe condi ion o he common cockle Ce as ode ma edule. Ma ine
En i onmen al Resea ch 130: 38–47. h ps://doi.o g/10.1016/j.ma en es.2017.07.001
Pascoe PL, Pa y HE, Hawkins AJS (2009) Obse a ions on he measu emen and in e p e a ion
o clea ance a e a ia ions in suspension- eeding bi al e shell ish. Aqua ic Biology 6: 181–190.
h ps://doi.o g/10.3354/ab00123
Pe ne F, T emblay R, Redjah I, Sé igny JM, Gione C (2008) Physiological and biochemical ai s
co ela e wi h di e ences in g ow h a e and empe a u e adap a ion among g oups o he eas -
e n oys e C assos ea i ginica. The Jou nal o Expe imen al Biology 211: 969–977. h ps://doi.
o g/10.1242/jeb.014639
Pe e sen JK, Boug ie S, Smaal AC, Ga en P, Robe S, La sen JEN, B ummelhuis E (2004) In e -
calib a ion o mussel My ilus edulis clea ance a e measu emen s. Ma ine Ecology P og ess Se ies
267: 187–194. h ps://doi.o g/10.3354/meps267187
P ano i F, F anceschini G, Casale M, Zucche a M, To icelli P, Gio ana di O (2006) An ecological
imbalance induced by a non-na i e species: The Manila clam in he Venice Lagoon. Biological
In asions 8: 595–609. h ps://doi.o g/10.1007/s10530-005-1602-5
P ins TC, Smaal AC, Pouwe AJ (1991) Selec i e inges ion o phy oplank on by he bi al es My ilus
edulis L. and Ce as ode ma edule (L.). Hyd ological Bulle in 25: 93–100. h ps://doi.o g/10.1007/
BF02259595
Rahman MA, Hende son S, Mille -Ezzy PA, Li XX, Qin JG (2020) Analysis o he seasonal impac
o h ee ma ine bi al es on ses on pa icles in wa e column. Jou nal o Expe imen al Ma ine
Biology and Ecology 522: 151251. h ps://doi.o g/10.1016/j.jembe.2019.151251
146
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Ramajal J, Pica d D, Cos a JL, Ca alho FB, Gaspa MB, Chainho P (2016) Amêijoa-japonesa, uma
no a ealidade no es uá io do Rio Tejo: Pesca e p essão social e impac o socio-económico. En e
Rios e Ma es: um Pa imónio de Ambien es, His ó ias e Sabe es. Tomo V da Rede B asPo .
Riisgå d HU (2001) On measu emen o il a ion a es in bi al es— he s ony oad o eliable
da a: Re iew and in e p e a ion. Ma ine Ecology P og ess Se ies 211: 275–291. h ps://doi.
o g/10.3354/meps211275
Rod igues N, Ribei o D, Miyahi a IC, Po ugal SGM, San os LN, Ne es RAF (2023) Do eeding
esponses o a non-na i e bi al e ou pe o m he na i e one in a coas al lagoon? A possible expla-
na ion o he in asion success o he da k alse mussel My ilopsis leucophaea a. Pee J 11: e15848.
h ps://doi.o g/10.7717/pee j.15848
Rosa M, Wa d JE, Shumway SE (2018) Selec i e Cap u e and Inges ion o Pa icles by Suspen-
sion-Feeding Bi al e Molluscs: A Re iew. Jou nal o Shell ish Resea ch 37: 727–746. h ps://doi.
o g/10.2983/035.037.0405
Ruano F, Sob al DV (2000) Ma ine non-indigenous species – cu en si ua ion in Po ugal. In:
Rod igues L, Reino L, Godinho LO, F ei as H (Eds) P oceedings o he 1s Symposium on Non-
indigenous Species: In oduc ion, Causes and Consequences. Liga pa a a P o ecção da Na u eza,
Lisboa, Po ugal, 58–63.
Ruiz GM, Fo ono P, Hines AH, G osholz ED (1999) Non-indigenous species as s esso s in es-
ua ine and ma ine communi ies: Assessing in asion impac s and in e ac ions. Limnology and
Oceanog aphy 44: 950–972. h ps://doi.o g/10.4319/lo.1999.44.3_pa _2.0950
Ruiz GM, Fo ono PW, Ca l on JT, Wonham MJ, Hines AH (2000) In asion o Coas al Ma ine
Communi ies in No h Ame ica: Appa en Pa e ns, P ocesses, and Biases. Annual Re iew o
Ecology and Sys ema ics 31: 481–531. h ps://doi.o g/10.1146/annu e .ecolsys.31.1.481
Ruiz GM, F ees one AL, Fo ono PW, Simkanin C (2009) Habi a Dis ibu ion and He e ogenei y
in Ma ine In asion Dynamics: he Impo ance o Ha d Subs a e and A i icial S uc u e. In:
Wahl M (Ed.) Ma ine Ha d Bo om Communi ies. Sp inge -Ve lag, Be lin, 321–332. h ps://
doi.o g/10.1007/b76710_23
Shime a J, Juma s PA (1991) Physical mechanisms and a es o pa icle cap u e by suspension- eed-
e s. Oceanog aphy and Ma ine Biology 29: 191–257.
Shinen JS, Mo gan SG (2009) Mechanisms o in asion esis ance: Compe i ion among in e idal
mussels p omo es es ablishmen o in asi e species and displacemen o na i e species. Ma ine
Ecology P og ess Se ies 383: 187–197. h ps://doi.o g/10.3354/meps07982
Smaal AC, an Du en LA (2019) Bi al e Aquacul u e Ca ying Capaci y: Concep s and Assess-
men ools. In: Smaal A, Fe ei a J, G an J, Pe e sen J, S and Ø (Eds) Goods and Se ices o
Ma ine Bi al es. Sp inge In e na ional Publishing, 451–483. h ps://doi.o g/10.1007/978-3-
319-96776-9_23
Smaal AC, Vonck APMA, Bakke M (1997) Seasonal a ia ion in physiological ene ge ics o My ilus
edulis and Ce as ode ma edule o di e en size classes. Jou nal o he Ma ine Biological Associa ion
o he Uni ed Kingdom 77: 817–838. h ps://doi.o g/10.1017/S0025315400036213
Sob al P, Widdows J (1997) In luence o hypoxia and anoxia on he physiological esponses o he
clam Rudi apes decussa us om sou he n Po ugal. Ma ine Biology 127: 455–461. h ps://doi.
o g/10.1007/s002270050033
Sob al P, Widdows J (2000) E ec s o inc easing cu en eloci y, u bidi y and pa icle-size selec ion
on he eeding ac i i y and scope o g ow h o Rudi apes decussa us om Ria Fo mosa, sou h-
e n Po ugal. Jou nal o Expe imen al Ma ine Biology and Ecology 245: 111–125. h ps://doi.
o g/10.1016/S0022-0981(99)00154-9
Sonie R (2017) Rôle nu i ionnel du picophy oplanc on pou les bi al es d’éle age. PHD Thesis.
Uni e si é du Québec à Rimouski (Rimouski). h ps://semapho e.uqa .ca/id/ep in /1359/
147
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
S ee es L, Vimond C, S ohmeie T, Casas S, S and Ø, Comeau LA, Filguei a R (2022) Rela ionship
be ween pumping a e and pa icle cap u e e iciency in h ee species o bi al es. Ma ine Ecology
P og ess Se ies 691: 55–68. h ps://doi.o g/10.3354/meps14063
S ege J, Bošnjak M, Belmake J, Galil BS, Zuschin M, Albano PG (2022) Non-indigenous molluscs
in he Eas e n Medi e anean ha e dis inc ai s and canno eplace his o ic ecosys em unc ion-
ing. Global Ecology and Biogeog aphy 31: 89–102. h ps://doi.o g/10.1111/geb.13415
S en on-Dozey JME, B own AC (1992) Clea ance and e en ion e iciency o na u al suspended pa -
icles by he ock-pool bi al e Vene upis co uga us in ela ion o idal a ailabili y. Ma ine Ecology
P og ess Se ies 82: 175–186. h ps://doi.o g/10.3354/meps082175
S en on-Dozey JME, B own AC (1994) Sho - e m changes in he ene gy balance o Vene upis co -
uga us (Bi al ia) in ela ion o idal a ailabili y o na u al suspended pa icles. Ma ine Ecology
P og ess Se ies 103: 57–64. h ps://doi.o g/10.3354/meps103057
S ige -Pou eau V, Thouzeau G (2015) Ma ine Species In oduced on he F ench Channel-A lan ic
Coas s: A Re iew o Main Biological In asions and Impac s. Open Jou nal o Ecology 5: 227–
257. h ps://doi.o g/10.4236/oje.2015.55019
S e a is N, Zene os A, Papa hanassiou E (2005) Globalisa ion in ma ine ecosys ems: The s o y o
non-indigenous ma ine species ac oss Eu opean seas. Oceanog aphy and Ma ine Biology - an
Annual Re iew 43: 419–453. h ps://doi.o g/10.1201/9781420037449.ch8
S ohmeie T, S and Ø, Alunno-B uscia M, Duinke A, C an o d PJ (2012) Va iabili y in pa icle
e en ion e iciency by he mussel My ilus edulis. Jou nal o Expe imen al Ma ine Biology and
Ecology 412: 96–102. h ps://doi.o g/10.1016/j.jembe.2011.11.006
S ua V, Klumpp DW (1984) E idence o ood- esou ce pa i ioning by kelp-bed il e eede s.
Ma ine Ecology P og ess Se ies 16: 27–37. h ps://doi.o g/10.3354/meps016027
Tamayo D, Iba ola I, Na a o E (2013) The mal dependence o clea ance and me abolic a es in
slow- and as -g owing spa s o manila clam Rudi apes philippina um. Jou nal o Compa a i e
Physiology. B, Biochemical, Sys emic, and En i onmen al Physiology 183: 893–904. h ps://doi.
o g/10.1007/s00360-013-0764-1
T oos K, S amhuis EJ, an Du en LA, Wol WJ (2009) Feeding cu en cha ac e is ics o h ee mo -
phologically di e en bi al e suspension eede s, C assos ea gigas, My ilus edulis and Ce as ode ma
edule, in ela ion o ood compe i ion. Ma ine Biology 156: 355–372. h ps://doi.o g/10.1007/
s00227-008-1088-7
T uhla AM, Dodd JA, Ald idge DC (2014) Di e en ial lea -li e p ocessing by na i e (Gam-
ma us pulex) and in asi e (Dike ogamma us illosus) eshwa e c us aceans unde en i onmen al
ex emes. Aqua ic Conse a ion 24: 56–65. h ps://doi.o g/10.1002/aqc.2375
U u ia MB, Iglesias JIP, Na a o E (1997) Feeding beha iou o Ce as ode ma edule in a u bid
en i onmen : Physiological adap a ions and de i ed bene i . Hyd obiologia 355: 173–180.
h ps://doi.o g/10.1023/A:1003050700881
Walne PR, Mann R (1975) G ow h and biochemical composi ion in Os ea edulis and C assos ea
gigas. In: Ba nes H (Ed.) Nin h Eu opean ma ine biology symposium. Abe deen Uni e si y P ess
Sco land, Uni ed Kingdom, 587–607.
Wa d JE, San o d LP, Newell RIE, MacDonald BA (1998) A new explana ion o pa icle cap u e in
suspension- eeding bi al e molluscs. Limnology and Oceanog aphy 43: 741–752. h ps://doi.
o g/10.4319/lo.1998.43.5.0741
Widdows J (2001) Bi al e clea ance a es: Inaccu a e measu emen s o inaccu a e e iews and mis ep-
esen a ion. Ma ine Ecology P og ess Se ies 221: 303–305. h ps://doi.o g/10.3354/meps221303
Widdows J, Na a o JM (2007) In luence o cu en speed on clea ance a e, algal cell deple ion in he
wa e column and esuspension o biodeposi s o cockles (Ce as ode ma edule). Jou nal o Expe -
imen al Ma ine Biology and Ecology 343: 44–51. h ps://doi.o g/10.1016/j.jembe.2006.11.011
148
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
WFD (2000) WFD, 2000/60/EC. Di ec i e 2000/60/EC o he Eu opean Pa liamen o he Coun-
cil o 23 Oc obe 2000 es ablishing a amewo k o communi y ac ion in he ield o wa e policy
(Wa e F amewo k Di ec i e). h p://da a.eu opa.eu/eli/di /2000/60/oj
Yu Z, Zhou Y, Qi Z, Luo P, Hu C (2017) Tempo al dynamics in clea ance a e o he Po uguese
oys e C assos ea angula a cul i a ed in Dapeng Co e, sou he n China. Aquacul u e (Ams e dam,
Ne he lands) 479: 824–828. h ps://doi.o g/10.1016/j.aquacul u e.2017.07.030
Zaiko A, Daunys D (2015) In asi e ecosys em enginee s and bio ic indices: Gi ing a w ong imp es-
sion o wa e quali y imp o emen ? Ecological Indica o s 52: 292–299. h ps://doi.o g/10.1016/j.
ecolind.2014.12.023
Zo i a I, Solaun O, Bo ja A, F anco J, Muxika I, Pascual M (2013) Spa ial dis ibu ion and empo al
ends o so -bo om ma ine ben hic alien species collec ed du ing he pe iod 1989-2008 in he
Ne ión es ua y (sou heas e n Bay o Biscay). Jou nal o Sea Resea ch 83: 104–110. h ps://doi.
o g/10.1016/j.sea es.2013.04.009
Supplemen a y ma e ial 1
Rela ionship be ween he Suspended Pa icula e Ma e (SPM) and he u bidi y
o he ield expe imen s si e (an aquacul u e a m loca ed in he Sado es ua y,
Se úbal, Po ugal)
Au ho s: Sa a Cab al, F ede ico Ca alho, Joana P. C. C uz, Joshua Heumülle , Jose M. F. Baba o,
Luc A. Comeau, Paula Chainho, Ana C. B i o
Da a ype: pd
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License (h p://openda a-
commons.o g/licenses/odbl/1.0/). The Open Da abase License (ODbL) is a license ag eemen
in ended o allow use s o eely sha e, modi y, and use his Da ase while main aining his same
eedom o o he s, p o ided ha he o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.102.148326.suppl1
Supplemen a y ma e ial 2
Rep esen a ion o a single incuba o wi h a bi al e ac i ely il e ing
Au ho s: Sa a Cab al, F ede ico Ca alho, Joana P. C. C uz, Joshua Heumülle , Jose M. F. Baba o,
Luc A. Comeau, Paula Chainho, Ana C. B i o
Da a ype: pd
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License (h p://openda a-
commons.o g/licenses/odbl/1.0/). The Open Da abase License (ODbL) is a license ag eemen
in ended o allow use s o eely sha e, modi y, and use his Da ase while main aining his same
eedom o o he s, p o ided ha he o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.102.148326.suppl2
149
NeoBio a 102: 125–150 (2025), DOI: 10.3897/neobio a.102.148326
Sa a Cab al e al.: Es ima ing cap u e e iciencies and clea ance a es o h ee bi al e species
Supplemen a y ma e ial 3
Rep esen a ion o bo h a sample wi h bi al e (g een) and he con ol (g ey) o (A)
he decline in he numbe o pa icles o e he expe imen ime and (B) he linea
eg ession be ween he pa icle concen a ion ( ans o med in na u al loga i hm)
and he elapsed ime
Au ho s: Sa a Cab al, F ede ico Ca alho, Joana P. C. C uz, Joshua Heumülle , Jose M. F. Baba o,
Luc A. Comeau, Paula Chainho, Ana C. B i o
Da a ype: pd
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License (h p://openda a-
commons.o g/licenses/odbl/1.0/). The Open Da abase License (ODbL) is a license ag eemen
in ended o allow use s o eely sha e, modi y, and use his Da ase while main aining his same
eedom o o he s, p o ided ha he o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.102.148326.suppl3
Supplemen a y ma e ial 4
PERMANOVA analysis esul s on cap u e e iciency (CE) o h ee bi al e species
(C. edule, M. angula a and R. philippina um)
Au ho s: Sa a Cab al, F ede ico Ca alho, Joana P. C. C uz, Joshua Heumülle , Jose M. F. Baba o,
Luc A. Comeau, Paula Chainho, Ana C. B i o
Da a ype: pd
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License (h p://openda a-
commons.o g/licenses/odbl/1.0/). The Open Da abase License (ODbL) is a license ag eemen
in ended o allow use s o eely sha e, modi y, and use his Da ase while main aining his same
eedom o o he s, p o ided ha he o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.102.148326.suppl4
Supplemen a y ma e ial 5
PERMANOVA Pai -wise es o de ec di e ences on CE be ween pa icle sizes o ield
expe imen s o h ee bi al e species (C. edule, M. angula a and R. philippina um)
Au ho s: Sa a Cab al, F ede ico Ca alho, Joana P. C. C uz, Joshua Heumülle , Jose M. F. Baba o,
Luc A. Comeau, Paula Chainho, Ana C. B i o
Da a ype: pd
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License (h p://openda a-
commons.o g/licenses/odbl/1.0/). The Open Da abase License (ODbL) is a license ag eemen
in ended o allow use s o eely sha e, modi y, and use his Da ase while main aining his same
eedom o o he s, p o ided ha he o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.102.148326.suppl5
