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In luence o body size and en i onmen al condi ions on pa asi e assemblages o he
black-spo ed c oake (P o onibea diacan hus) (Teleos ei: Sciaenidae) in no he n
Aus alia
© The Au ho (s), 2024. Published by Camb idge Uni e si y P ess
Published e sion
Po e , Megan; Ba on, Diane P.; Williams, Joel; Randall, Jo; O askainen, O so;
C ook, Da id A.; Shamsi, Shokoo eh
Po e , M., Ba on, D. P., Williams, J., Randall, J., O askainen, O., C ook, D. A., & Shamsi, S.
(2024). In luence o body size and en i onmen al condi ions on pa asi e assemblages o he
black-spo ed c oake (P o onibea diacan hus) (Teleos ei: Sciaenidae) in no he n Aus alia.
Pa asi ology, Ea ly online. h ps://doi.o g/10.1017/S0031182024001008
2024
Pa asi ology
camb idge.o g/pa
Resea ch A icle
Ci e his a icle: Po e M, Ba on DP, Williams
J, Randall J, O askainen O, C ook DA, Shamsi
S (2024). In luence o body size and
en i onmen al condi ions on pa asi e
assemblages o he black-spo ed c oake
(P o onibea diacan hus) (Teleos ei: Sciaenidae)
in no he n Aus alia. Pa asi ology 1–11.
h ps://doi.o g/10.1017/S0031182024001008
Recei ed: 23 May 2024
Re ised: 31 July 2024
Accep ed: 1 Augus 2024
Keywo ds:
body size; en i onmen ; ma ine ecosys ems;
pa asi es; P o onibea diacan hus; season
Co esponding au ho :
Megan Po e ;
Email: [email p o ec ed]
© The Au ho (s), 2024. Published by
Camb idge Uni e si y P ess. This is an Open
Access a icle, dis ibu ed unde he e ms o
he C ea i e Commons A ibu ion licence
(h p://c ea i ecommons.o g/licenses/by/4.0/),
which pe mi s un es ic ed e-use, dis ibu ion
and ep oduc ion, p o ided he o iginal a icle
is p ope ly ci ed.
In luence o body size and en i onmen al
condi ions on pa asi e assemblages o he
black-spo ed c oake (P o onibea diacan hus)
(Teleos ei: Sciaenidae) in no he n Aus alia
Megan Po e 1,2 , Diane P. Ba on1,2 , Joel Williams3, Jo Randall4,5,6,
O so O askainen7,8, Da id A. C ook4,9 and Shokoo eh Shamsi1,2
1
School o Ag icul u al, En i onmen al and Ve e ina y Sciences, Cha les S u Uni e si y, Wagga Wagga, NSW,
Aus alia;
2
Gulbali Ins i u e, Cha les S u Uni e si y, Wagga Wagga, NSW, Aus alia;
3
Ins i u e o Ma ine and
An a c ic S udies, Uni e si y o Tasmania, Hoba , TAS, Aus alia;
4
Resea ch Ins i u e o he En i onmen and
Li elihoods, Cha les Da win Uni e si y, Casua ina, NT, Aus alia;
5
Aus alian Ins i u e o Ma ine Science, A a u a
Timo Resea ch Facili y, Casua ina, NT, Aus alia;
6
Depa men o Indus y, Tou ism and T ade, No he n Te i o y
Go e nmen o Aus alia, Be imah, NT, Aus alia;
7
Depa men o Biological and En i onmen al Science,
Uni e si y o Jy äskylä, Jy äskylä, Finland;
8
O ganismal and E olu iona y Biology Resea ch P og amme, Facul y o
Biological and En i onmen al Sciences, Uni e si y o Helsinki, Helsinki, Finland and
9
Depa men o P ima y
Indus ies, Na ande a Fishe ies Cen e, Na ande a, NSW, Aus alia
Abs ac
The unc ioning and ichness o ma ine sys ems (and biological in e ac ions such as pa asi ism)
a e con inuously in luenced by a changing en i onmen . Using hie a chical modelling o species
communi ies (HMSC), he p esence and abundance o mul iple pa asi e species o he black-
spo ed c oake , P o onibea diacan hus (Sciaenidae), was modelled agains en i onmen al
measu es e lec ing seasonal change. P o onibea diacan hus we e collec ed in h ee seasons
ac oss 2019–2021 om ou loca ions wi hin he wa e s o he No he n Te i o y, Aus alia.
The leng h o P. diacan hus p o ed o ha e a s ong posi i e e ec on he abundance o pa asi e
axa and o e all pa asi ic assemblage o he sciaenid hos . This inding in oduces po en ial
implica ions o pa asi ism in he u u e as ish body size esponds o ishing p essu e and cli-
ma e changes. O he a ious en i onmen al ac o s measu ed du ing he opical seasons o
no he n Aus alia, wa e empe a u e and salini y changes we e shown as po en ial causal ac-
o s o he a iance in pa asi e p esence and abundance, wi h changes mos in luen ial on
ex e nal pa asi ic o ganisms. As en i onmen al ac o s like ocean empe a u e and salini y di -
ec ly a ec pa asi e–hos ela ionships, his s udy sugges s ha pa asi e assemblages and he eco-
logical unc ions ha hey pe o m a e likely o change conside ably o e he coming decades in
esponse o clima e change and i s p oceeding e ec s.
In oduc ion
Fish dis ibu ion, beha iou and physiology a e all a ec ed by clima ic and en i onmen al
ac o s, as well as biological in e ac ions including p eda ion and pa asi ism. Wi h he inc eas-
ing unp edic abili y o ma ine ecosys em unc ioning in e ol ing en i onmen al condi ions,
he e is a g owing need o de elop an unde s anding o he en i onmen al impac s on bo h
ish and hei pa asi e communi ies (Lõhmus and Bjö klund, 2015; Poloczanska e al., 2016;
Esbaugh, 2018). Pa asi ic o ganisms ha exploi ma ine hos s a e likely o be impac ed by a
changing clima e, bo h di ec ly h ough he changing ambien habi a , and indi ec ly ia
e ec s on hei hos s (Lõhmus and Bjö klund, 2015). Many pa asi es equi e in e media e
hos (s) o comple e hei li e cycle, which means ha impac s may be cumula i e along he
li e cycle (La e y, 2012). Pa asi es wi h li e cycles ha u ilize ee-swimming la al s ages
a e elian on bo h hos a ailabili y and sui able en i onmen al condi ions o de elopmen
and su i al (Poulin and Leung, 2011; Lehun e al., 2023).
Al hough he en i onmen al implica ions o a changing clima e on ma ine pa asi es and
hei ish hos s a e nume ous, he eac ions o pa asi es o habi a a iabili y a e no s aigh -
o wa d. Holmes (1990) p esen ed a summa y o he de e minan s o helmin h communi y
s uc u e in ma ine ishes, highligh ing he in e ac ions be ween a ious bio ic ( ish die
and physiology) and abio ic (en i onmen al) ac o s. Pa asi e in ec ion a es may inc ease
in esponse o mino ises in ocean empe a u e (Macnab and Ba be , 2012; Neube e al.,
2016; Klimpel e al., 2019; Bye s, 2021), whe eas o o he pa asi e axa, in ec ion a es decline
wi h inc easing empe a u e (Bye s, 2021). Al hough di icul o p edic , pa asi e ecology is
likely o change conside ably in esponse o clima e change and i s p oceeding e ec s, and
i clima e impac s con inue o in luence ma ine ecosys em p ocesses, some pa asi es will
ace subop imal ansmission condi ions and/o may soon ha e ewe hos s a ailable as a esul
o hos he mal p e e ence and hos beha iou al changes (Klimpel e al., 2019; Reynolds e al.,
2019; Bye s, 2021).
h ps://doi.o g/10.1017/S0031182024001008 Published online by Camb idge Uni e si y P ess
In addi ion o he sho - e m seasonal changes expe ienced in
opical and sub opical ma ine egions like no he n Aus alia,
subs an ial long- e m en i onmen al changes and ocean esponses
a e expec ed as a esul o clima e change (Koenigs ein e al., 2016).
Clima e models p edic u he wa ming, wi h ocean su aces su -
ounding Aus alia wa ming a a a e less han he global a e age
(CSIRO and Bu eau o Me eo ology, 2023c). P edic ions also
include inc eased s a i ica ion and acidi ica ion, s onge polewa d
cu en s, sea le el ise and al e ed s o m and ain all egimes
(Hobday e al., 2006; Poloczanska e al., 2007,2016;Bindo
e al., 2019; Ge ais e al., 2021). Hea y ain all e en s in
Aus alia ha e inc eased in in ensi y (CSIRO and Bu eau o
Me eo ology, 2023a), wi h egions su ounding he equa o like
he no h o Aus alia gene ally expe iencing we e yea s (CSIRO
and Bu eau o Me eo ology, 2023b). In addi ion o ain all changes,
he a e age sea-su ace empe a u e o Aus alia has also inc eased
by mo e han 1°C since 1900, including eigh o he en wa mes
yea s since 2010 (CSIRO and Bu eau o Me eo ology, 2023a).
Clima e change s udies p edic ha ocean wa ming will igge a
pola shi in he dis ibu ion o ma ine o ganisms, leading o
decline in ish species ichness in opical wa e s, along wi h
changes in sea-su ace empe a u es, salini y le els and he le els
o dissol ed oxygen (Ba ange and Pe y, 2009;Bindo e al.,
2019; Yang e al., 2023). In addi ion o popula ion mo emen s,
he physiology o se e al ma ine ish species has been s ongly
in luenced by empe a u e-d i en changes in ec ui men and
soma ic g ow h, wi h o e all educ ions in size eco ded in ep o-
duc i ely ac i e s ock (She idan and Bick o d, 2011; Lindma k
e al., 2022). The black-spo ed c oake P o onibea diacan hus
(Teleos ei: Sciaenidae) is a la ge ma ine ish species o conside able
alue o ec ea ional, adi ional and comme cial ishing sec o s o
no he n Aus alia (Phelan e al., 2008;Saunde se al., 2021), and
is one ma ine species likely o be impac ed by ocean wa ming, wi h
dis ibu ion shi s epo ed in se e al ma ine ish species (Jacups,
2010; Poloczanska e al., 2013;Zhange al., 2019;Ge aise al.,
2021). P o onibea diacan hus is dis ibu ed in he we –d y opics
o no he n Aus alia, occu ing h oughou he Indo-wes Paci ic
egion, including Papua New Guinea, and eaching om he
Pe sian Gul o Japan (B ay, 2022;Randalle al., 2023).
Inhabi ing he we –d y opics, P. diacan hus is o en exposed o
mino en i onmen al changes as a esul o he opical wea he
condi ions and seasonal changes, including changes o wa e qual-
i y, composi ion and mo emen . The monsoonal we season in
no he n Aus alia b ings signi ican ain all o e he mon hs
om Decembe o Ma ch, ypically esul ing in ele a ed eshwa e
un-o om i e sys ems in o nea sho e es ua ine and coas al
habi a s. The combina ion o eshwa e un-o , sedimen mixing
and idal lows du ing he we season o en leads o signi ican
changes in wa e empe a u e, salini y and chemical composi ion
o coas al ma ine wa e s (Ande son e al., 2011). The d y season,
ypically be ween Ap il and Augus , is a pe iod o negligible ain all
and low un-o o eshwa e in o he en i onmen . The ansi ion
pe iod om d y o we , e e ed o as he ‘build-up’season, occu s
be ween Sep embe and No embe , and is associa ed wi h ises in
empe a u e and humidi y, and inc easing ain all mainly om
i egula , non-monsoonal s o ms (Po e e al., 2023b).
As na u al componen s o ecological sys ems, pa asi ic o gan-
isms a e expec ed o eac o en i onmen al changes and he
subsequen beha iou al changes, heal h impac s and mo emen
pa e ns o hei hos s (Bye s, 2021). Wi h p e ious s udies high-
ligh ing he ichness o pa asi e in ec ion in P. diacan hus (Po e
e al., 2023a,2023b,2023c), he e is a need o unde s and he
po en ial clima e-induced p essu es ha his majo pa asi e–hos
sys em may ace. This s udy in es iga ed he pa asi es occu ing in
P. diacan hus popula ions o he no he n coas o Aus alia and
modelled he p esence and abundance o mul iple pa asi e axa
ela i e o en i onmen al a iables. The esul s o his s udy a e
discussed wi h espec o he impac s o en i onmen al change
on pa asi es, and how hese changes migh mani es as pa e ns
o pa asi e p e alence, abundance and di e si y. In unde s anding
how pa asi es espond o seasonal a iabili y, his s udy aims o
imp o e he capaci y o p edic how pa asi es (and hei impac s
on hos s) will espond o en i onmen al a ia ion in a changing
clima e.
Ma e ials and me hods
Fish and pa asi e collec ion
The ish and pa asi es included in his s udy a e as desc ibed in
Po e e al.(2023b). In b ie , 176 P. diacan hus we e collec ed
om ou coas al loca ions o he No he n Te i o y coas
(Fig. 1). The ish we e sampled om wo nea sho e loca ions in
p oximi y o he mou hs o he Daly Ri e and he Ma y Ri e
(Pe on Islands and Sampan C eek, espec i ely), and wo o sho e
loca ions o he Tiwi Islands (Cau ion Poin and Mi chell Poin ).
The si es chosen allowed compa ison be ween nea sho e and o -
sho e si es, wi h nea sho e loca ions ecei ing eshwa e ou low
in he we season, and hose o sho e mo e e lec i e o oceanic
condi ions wi h no eshwa e ou low nea by. Fish we e cap u ed
a hese si es du ing h ee seasonal sampling pe iods in
2019–2021 including: build-up (Oc obe –No embe 2019 and
2020), la e-we (Feb ua y–Ma ch 2020 and 2021) and mid-d y
(June–July 2019 and 2020), wi h monsoonal we season ain all
occu ing om Decembe o Ma ch, and he negligible ain all
du ing he d y season be ween Ap il and Augus . Pa asi es we e
collec ed om he gills and he gas oin es inal sys ems o each
ish and iden i ied o as low a axonomic le el as possible.
En i onmen al da a
A he ime o cap u e o ish, en i onmen al da a we e collec ed
a he wa e su ace and a he dep h o cap u e, which a ied
be ween 3 and 30 m, depending on he loca ion: Sampan C eek
3‒8 m, Cau ion Poin 10‒15 m, Pe on Islands 15‒25 m and
Mi chell Poin 20‒30 m. En i onmen al a iables measu ed
we e: dissol ed oxygen, wa e empe a u e, salini y, ammonia,
o al dissol ed ni ogen and o al dissol ed phospho us. Gi en
P. diacan hus is conside ed a deme sal species (B ay, 2022), he
measu es o dissol ed oxygen and wa e empe a u e om he
lowe pa o he wa e column we e used in he analyses.
Ammonia, o al dissol ed ni ogen, and o al dissol ed phos-
pho us we e examined as po en ial indica o s o eshwa e
ou low a he sampling si es.
Da a analysis
Summa y s a is ics o he pa asi e and en i onmen al da a we e
compiled o each loca ion by season o collec ion (Table 1).
Due o low sample sizes, da a ac oss he wo yea s we e g ouped
by season o collec ion. Fo each o he pa asi e axa, mean abun-
dance ( he o al numbe o indi iduals o a pa icula pa asi e pe
sample di ided by he o al numbe o hos s examined, including
unin ec ed hos s), and p e alence ( he numbe o hos s in ec ed
wi h a pa icula pa asi e di ided by he numbe o hos s exam-
ined, exp essed as a pe cen age) we e calcula ed (Bush e al.,
1997). The mean alues o each en i onmen al a iable we e
also calcula ed and compiled o each loca ion by season o collec-
ion (Table 2).
Fo he s a is ical analysis, he da a we e analysed using a join
species dis ibu ion model called hie a chical modelling o species
communi ies (HMSC; O askainen e al., 2017; O askainen and
2 Megan Po e e al.
h ps://doi.o g/10.1017/S0031182024001008 Published online by Camb idge Uni e si y P ess
Ab ego, 2020). The esponse da a used in he model comp ise he
abundance o pa asi e axa om he ish hos . Fo he analyses,
he indi idual ish we e used as sampling uni s and he coun
o each o he 11 pa asi e axa we e used as he esponse a iable.
To accoun o ze o-in la ion o some o he pa asi e axa,
a hu dle model was applied, i.e. one model o p esence–absence
o he axa, and ano he model o he abundance o axa condi-
ional on p esence. P obi eg ession was applied in he p esen-
ce–absence model, and linea eg ession o log ans o med
coun da a in he abundance condi ional on p esence model.
The coun da a we e ans o med by decla ing ze os as missing
da a, log- ans o ming, and hen scaling he da a o ze o mean
and uni a iance wi hin each axa. Fish collec ion yea and loca-
ion we e included as andom e ec s, and ish collec ion season,
ish leng h, ish sex and six en i onmen al a iables: dissol ed
oxygen, wa e empe a u e, salini y, ammonia, o al dissol ed
ni ogen and o al dissol ed phospho us, we e included as ixed
e ec s. As species ai s, he ca ego ical a iable o in e nal o
ex e nal pa asi es was also applied.
Bo h models we e i ed using he HMSC package om R
(Tikhono e al., 2020) assuming he de aul p io dis ibu ions
(O askainen and Ab ego, 2020). The pos e io dis ibu ion was
sampled using ou Ma ko chain Mon e Ca lo (MCMC) chains.
Each chain consis ed o 37 500 i e a ions, o which 12 500 i e a-
ions we e emo ed as bu n-in and he emaining hinned by
100 o esul in 250 pos e io samples pe chain, so he e we e
1000 pos e io samples in o al. The MCMC con e gence
diagnos ics we e examined h ough he po en ial scale educ ion
ac o s o he model pa ame e s (Gelman and Rubin, 1992).
Bo h he explana o y powe s and he p edic i e powe s
we e examined o each o he models, wi h measu es o he
species-speci ic AUC and Tju ’sR
2
(simila o R
2
, Tju , 2009)
examined o he p esence–absence model (Pea ce and Fe ie ,
2000), and R
2
measu ed o he abundance condi ional on he
p esence model. To compu e he explana o y powe , model p e-
dic ions we e made based on he models being i ed o all o
he da a. The p edic i e powe was compu ed by pe o ming a
i e- old c oss alida ion, in which he sampling uni s we e
assigned andomly o i e olds, and p edic ions o each old
we e based on he model ha was i ed o he da a on he emain-
ing ou olds.
To quan i y he d i e s o pa asi e axa ichness and abun-
dance, he explained a ia ion was pa i ioned among he ixed
and andom e ec s included in he model. To examine associa-
ions be ween pa asi e axa and en i onmen al a iables, pa asi e
esponses o he explana o y a iables we e measu ed, coun ing
he p opo ion o pa asi es showing posi i e o nega i e associa-
ions wi h a leas 95% pos e io p obabili y.
Resul s
All 176 ish we e in ec ed wi h a leas one pa asi e and a o al o
11 pa asi e axa we e iden i ied om he gills and he gas oin es-
inal sys em o use in he analysis (Table 1). Ex e nal pa asi es
included copepods, Le nan h opus pa ac ucia us Boxshall,
Be no , Ba on, Diggles, Yong, A kinson-Coyle & Hu son, 2020
(see Boxshall e al., 2020) and Caligus sp., and wo species o
monogeneans, Diplec anum imo can hus Po e , Ba on,
F ancis & Shamsi, 2023 and Diplec anum diacan hi Po e ,
Ba on, F ancis & Shamsi, 2023 (see Po e e al., 2023a), com-
bined as Diplec anum spp. due o he di icul y in dis inc ion
be ween he species a ime o dissec ion. O he in e nal pa asi es
Figu e 1. Collec ion si es o P o onibea diacan hus om no he n Aus alia. Map sou ced om he O ice o Resea ch Se ices and G adua e S udies, Spa ial Da a
Analysis Ne wo k (SPAN), Cha les S u Uni e si y, Wagga Wagga, Aus alia.
Pa asi ology 3
h ps://doi.o g/10.1017/S0031182024001008 Published online by Camb idge Uni e si y P ess
Table 1. P e alence and mean abundance o pa asi es om P o onibea diacan hus, ac oss seasons (Mid-d y, Build-up and La e-we ), and si es (Cau ion Poin , Mi chell Poin , Pe on Islands, Sampan C eek)
Mid-d y Build-up La e-we
Cau ion
Poin
Mi chell
Poin
Pe on
Islands
Sampan
C eek
Cau ion
Poin
Mi chell
Poin
Pe on
Islands
Sampan
C eek
Cau ion
Poin
Mi chell
Poin
Pe on
Islands
Sampan
C eek
Numbe o ish 19 10 17 18 7 10 10 20 16 20 20 9
Mean leng h (cm) 98.6 98.5 108.3 112.6 84.9 101.0 108.7 112.4 107.8 92.8 85.1 123.6
Pa asi e axa PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
PA
M
Copepoda
Caligus sp.
10.5 0.1 0.0 0.0 70.6 1.6 22.2 0.4 28.6 0.3 0.0 0.0 20.0 0.2 5.0 0.1 0.0 0.0 0.0 0.0 25.0 0.5 0.0 0.0
Le nan h opus sp. 78.9 2.1 100.0 6.7 52.9 2.9 83.3 3.9 71.4 3.1 100.0 5.7 100.0 4.2 95.0 12.9 93.8 7.9 70.0 2.6 90.0 2.6 100.0 8.4
Monogenea
Diplec anum spp.
100.0 834.1 100.0 1223.0 100.0 1204.2 100.0 1058.4 100.0 1262.7 100.0 2498.0 100.0 39.6 100.0 195.2 100.0 2658.8 100.0 829.0 100.0 544.0 100.0 3293.3
Nema oda
Cucullanidae
100.0 21.9 90.0 24.4 94.1 18.5 94.4 18.9 100.0 18.9 100.0 11.8 100.0 10.7 85.0 24.0 93.8 56.4 100.0 13.0 100.0 10.1 100.0 57.9
Asca ididae 5.3 0.1 0.0 0.0 0.0 0.0 27.8 0.4 0.0 0.0 0.0 0.0 10.0 0.2 15.0 0.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
O he Nema odes 26.3 0.3 10.0 0.1 23.5 0.4 11.1 0.1 0.0 0.0 10.0 0.3 10.0 0.1 20.0 0.3 0.0 0.0 0.0 0.0 10.0 0.3 0.0 0.0
Digenea
O ien odiplop oc odaeum sp.
100.0 21.5 100.0 39.1 100.0 49.8 83.3 6.9 100.0 19.4 100.0 38.3 100.0 26.4 85.0 13.1 100.0 32.3 90.0 13.8 100.0 23.8 88.9 19.3
S ephanos omum sp. 89.5 14.8 100.0 33.3 82.4 8.2 88.9 30.1 100.0 12.9 100.0 21.0 70.0 4.9 85.0 10.2 81.3 30.9 85.0 11.3 65.0 3.4 100.0 57.0
Pleo chis sp. 10.5 0.1 80.0 5.3 5.9 0.1 0.0 0.0 0.0 0.0 30.0 0.4 0.0 0.0 0.0 0.0 12.5 0.3 25.0 0.5 10.0 0.2 0.0 0.0
Hemiu idae 0.0 0.0 0.0 0.0 17.6 0.5 16.7 0.2 14.3 0.1 0.0 0.0 0.0 0.0 0.0 0.0 6.3 0.2 10.0 0.2 30.0 0.5 11.1 0.8
Opecoelidae 5.3 0.1 0.0 0.0 35.3 0.8 27.8 0.4 0.0 0.0 10.0 0.2 0.0 0.0 5.0 0.1 0.0 0.0 0.0 0.0 25.0 0.6 0.0 0.0
P e alence, exp essed as a pe cen age, is he numbe o hos s in ec ed wi h a pa icula pa asi e di ided by he numbe o hos s examined. Mean Abundance is exp essed as he o al numbe o indi iduals o a pa icula pa asi e pe sample di ided by he o al
numbe o hos s examined, including unin ec ed hos s.
4 Megan Po e e al.
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included in he analysis he e we e adul nema odes belonging o
he amilies Cucullanidae and Asca ididae, and a u he g oup o
nema odes no ye iden i ied bu classi ied as ‘O he Nema odes’
gi en hei simila i ies in mo phological cha ac e is ics and gene al
ecology. Adul digenean ema odes O ien odiplop oc odaeum sp.,
S ephanos omum sp., Pleo chis sp., and ep esen a i es om he
amilies Hemiu idae and Opecoelidae we e also included.
The en i onmen al a iables di e ed be ween loca ions based
on seasons (Table 2). The wa e empe a u e o he insho e loca-
ions o Pe on Islands and Sampan C eek di e ed om ha o he
o sho e loca ions, being lowe in he mid-d y, bu highe in
he build-up and la e-we . Salini y a he insho e loca ions in
he build-up was ma kedly lowe in he la e-we season, indica ing
a eshwa e in luence a hese si es. Le els o ammonia did no
exhibi a clea seasonal pa e n. Be ween seasons only, le els o
ni ogen and phospho us we e highe in he la e-we season
han in he mid-d y and build-up seasons.
The MCMC con e gence diagnos ics o he HMSC models we e
sa is ac o y, meaning ha he models we e adequa ely i ed o he
da a (O askainen and Ab ego, 2020). Namely, he po en ial scale
educ ion ac o s o he β-pa ame e s we e on a e age 1.002
(0.998‒1.013) o he p esence–absence model and 1.002
(0.997‒1.009) o he abundance condi ional on p esence model.
The p esence–absence models showed a good i o he da a, he
mean Tju R
2
(AUC) epo ed as 0.186 (0.861) o explana o y
powe , and 0.108 (0.693) p edic i e powe . The abundance condi ional
on he p esence model showed sa is ac o y model i , wi h he mean
R
2
alue being 0.407 o explana o y powe and 0.095 o p edic i e
powe . Diplec anum spp. (p e alence 100%) and Cucullanidae (p e a-
lence 96%), we e p esen in (almos ) all samples and he e o e no
conside ed in o ma i e o he p esence–absence model.
Fo he p esence–absence model he explana o y powe o
each species was low (Fig. 2A), sugges ing he a iables use in
he model only explain a small p opo ion o he a iance and
he e o e he dis ibu ion o pa asi e axa is mo e by andom
chance han by he en i onmen . Va iance pa i ion o e he
explana o y a iables included in he p esence–absence model
showed ha he p opo ion o he ixed e ec s o wa e empe a-
u e and season explained be ween 20 and 40% o a iance o
mos pa asi es, wi h salini y explaining he nex highes p opo -
ion be ween 10 and 20% (Fig. 2B). The explana o y powe o
he abundance condi ional on he p esence model (Fig. 2C)
showed ha i e pa asi e axa explained g ea e han 40% o a i-
ance, wi h he Diplec anum spp. and ‘O he Nema odes’explain-
ing he highes p opo ions o o e 60% o a iance. Ou o he
explained a iance o he abundance condi ional on he p esence
model, he ixed e ec s ha explained mos o he a iance
included salini y, wa e empe a u e, leng h and season
(Fig. 2D). Al hough s ill no eco ding he highes p opo ion o
explained a iance, he ixed e ec s o o al dissol ed ni ogen
and o al dissol ed phospho us we e much mo e co ela ed wi h
mos pa asi e axa in he abundance condi ional on he p esence
model, when compa ed wi h he p esence–absence model. Fo he
abundance o ex e nal pa asi es, season explained he mos a i-
ance o bo h Caligus sp. and Diplec anum spp. (Fig. 2D).
The be a plo o he p esence–absence model showed L. pa a-
c ucia us and Caligus sp. o ha e a nega i e esponse o he la e-
we season (Fig. 3A). In he be a plo o he p esence–absence
model, L. pa ac ucia us and he wo mos p e alen in e nal pa a-
si es (O ien odiplop oc odaeum sp. and S ephanos omum sp.)
showed inc easing occu ence p obabili y wi h inc easing wa e
empe a u e. In e es ingly, all bu S ephanos omum sp. had a
nega i e associa ion wi h salini y (Fig. 3A).
The be a plo o he abundance condi ional on he p esence
model demons a ed ha mo e han hal o all pa asi e axa a e
signi ican ly mo e abundan as ish leng h inc eases (Fig. 3B).
Table 2. Mean alues o en i onmen al measu es aken o seasons and si es
Mid-d y Build-up La e-we
Cau ion
Poin
Mi chell
Poin
Pe on
Islands
Sampan
C eek
Cau ion
Poin
Mi chell
Poin
Pe on
Islands
Sampan
C eek
Cau ion
Poin
Mi chell
Poin
Pe on
Islands
Sampan
C eek
Dissol ed oxygen (mg L
−1
) 6.4 6.2 6.5 6.8 7.5 7.8 5.6 6.0 6.0 6.0 5.8 6.6
Wa e empe a u e (°C) 26.3 26.9 23.8 25.0 29.9 29.6 31.2 30.9 29.9 29.9 30.6 30.2
Salini y ( om >2 m) 35.4 36.0 35.5 35.4 35.1 35.1 36.2 36.7 34.6 35.2 32.6 29.6
Ammonia 0.5 0.5 1.1 0.6 1.0 0.3 2.2 0.2 0.3 0.8 1.6 0.2
To al dissol ed ni ogen 4.4 10.2 10.2 6.5 13.1 5.6 5.5 4.4 7.1 10.2 9.6 11.0
To al dissol ed phospho us 0.3 0.3 0.3 0.4 0.3 0.4 0.2 0.3 0.3 0.4 0.5 0.7
Pa asi ology 5
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Diplec anum spp. abundance has a posi i e associa ion wi h many
en i onmen al a iables including bo h he mid-d y and he la e-
we seasons ( ela i e o he build-up season), dissol ed oxygen
and empe a u e, ammonia and o al dissol ed ni ogen
(Fig. 3B). The abundance o bo h L. pa ac ucia us and
Diplec anum spp. had a nega i e associa ion wi h o al dissol ed
phospho us. In all, i e pa asi e axa we e nega i ely associa ed
wi h o al dissol ed phospho us (Fig. 3B).
The p esence–absence model p edic s ha pa asi e ichness is
posi i ely co ela ed wi h ish leng h (Fig. 4A). Pa asi e species
ichness was ela i ely consis en as empe a u e changes,
howe e , he e was a d op in ichness a empe a u es be ween
27 and 28°C (Fig. 4B). This d op occu ed a only he one loca ion
and season a which his empe a u e was eco ded (Table 2), and
when ou pa asi e axa we e no p esen (Table 1). Species ich-
ness was highes when salini y le els we e low, wi h a d op
eco ded when salini y exceeded 36‰(Fig. 4C).
Discussion
The p esence and abundance o pa asi es we e signi ican ly in lu-
enced by he body size o P. diacan hus, wi h he e ec o body
Figu e 2. (A) Plo o explana o y powe o he p esence–absence model highligh ed h ough he Tju R
2
alues o he pa asi e species, (B) plo o a iance pa i ion
o e he explana o y a iables in he p esence–absence model, showing he p opo ion o a iance explained by bo h he andom e ec s and he ixed e ec s o
he pa asi e species, (C) plo o explana o y powe o he abundance condi ional on p esence model highligh ed h ough he R
2
alues o he pa asi e species,
(D) plo o a iance pa i ion o e he explana o y a iables in he abundance condi ional on p esence model, showing he p opo ion o a iance explained
by bo h he andom e ec s and he ixed e ec s o he pa asi e species. NB: Abb e ia ions o en i onmen al a iables ha e been used and include dissol ed
oxygen as (LowDO), wa e empe a u e as (LowTemp), ammonia as (NH), o al dissol ed ni ogen as (TDN) and o al dissol ed phospho us as (TDP).
6 Megan Po e e al.
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size on pa asi es p o ing he s onges ac o ac oss he seasons.
Posi i e associa ions be ween body size and pa asi e p esence
and abundance ha e been epo ed in nume ous p e ious s udies
and s ock analyses o ma ine ishes (Thoney, 1993; Je y e al.,
2013; Welch e al., 2015; Ba on e al., 2018; Taillebois e al.,
2017; Taillebois e al., 2021; Kouadio e al., 2023). S udies con i m
a gene al link be ween hos size and pa asi e ichness, howe e
he e is an ob ious need o conside ha his complex associa ion
is a om a simple linea ela ionship (Poulin e al., 2011). Hos
size co esponds closely o he size o habi a a ailable o pa asi ic
auna and is also co ela ed wi h hos li e span, meaning ha la -
ge hos s o e a la ge habi a pa ch and ea u e longe -li ed habi-
a s, he e o e ha bou ing iche pa asi e aunas (Poulin and
Mo and, 2004; Poulin e al., 2011). This is jus i ied wi h he
ma ked inc ease in pa asi e species ichness shown as he hos
size o P. diacan hus exceeds 100 cm. Food selec ion amongs
ishes is po en ially in luenced by bo h empe a u e and body
size (Coghlan e al., 2024), and as ish ma u e, changes in eeding
modes and die composi ion a e common, wi h P. diacan hus o
example known o ansi ion om small in e eb a es such as
c abs and p awns, o la ge p ey i ems like ish (Ba on, 2018).
This die a y change would ce ainly in luence he pa asi ic
auna o he ish hos , and gi en his occu s as a esul o ma u -
a ion, can u he suppo he associa ion be ween ish hos size
and pa asi e species ichness. S udies also sugges ha g ea e
abundances o pa asi es a e ound in o sho e ish communi ies
Figu e 3. (A) Be a plo o he species esponses o he explana o y a iables in he
p esence–absence model wi h a leas 95% pos e io p obabili y, (B) Be a plo o
he species esponses o he explana o y a iables in he abundance condi ional
on p esence model wi h a leas 95% pos e io p obabili y. NB: In 3A and 3B, he
ed and blue colou s indica e hose pa asi e axa–en i onmen al a iable pai s
wi h a leas 0.95 suppo o ei he a posi i e o nega i e associa ion, espec i ely.
I he e is no colou , he pa asi e axa p esence/absence o abundance condi ional
on p esence is deemed o no ha e an associa ion wi h he en i onmen al a iable,
i.e. he axa a e nei he posi i ely no nega i ely in luenced by he en i onmen al
a iable. Abb e ia ions o en i onmen al a iables a e as hose desc ibed in Fig. 2.
Figu e 4. G adien plo s o he ela ionships be ween: (A) Pa asi e species ichness
and ish leng h om all samples (cm), (B) Pa asi e species ichness and wa e em-
pe a u e (°C), (C) Pa asi e species ichness and salini y. NB: Pa asi e species ichness
is a e lec ion o he numbe o di e en pa asi e species ha a e known o in ec a
pa icula hos (o hos popula ion).
Pa asi ology 7
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when compa ed wi h hei ju enile coun e pa s nea sho e, sug-
ges ing ha ce ain pa asi es a e in ac accumula ed o e ime,
o ha he e is a po en ially g ea e numbe o in ec ed in e medi-
a e hos s o sho e (Thoney, 1993).
Changes in body size o ish in esponse o ocean wa ming a e
o en a ibu ed o he empe a u e-size ule (TSR), wi h
ec o he ms ea ed a wa me empe a u es de eloping as e bu
eaching smalle ul ima e body sizes (Ohlbe ge , 2013;
Lindma k e al., 2022). This inding has co ela ed wi h obse a-
ions o se e al comme cially exploi ed ma ine ish species
(Olsen e al., 2004; Ande sen e al., 2007; Baud on e al., 2014;
Rijn e al., 2017; Ikpewe e al., 2021; Woo on e al., 2022), wi h
nega i e size shi s impeding he main enance and eco e y o
exploi ed ma ine ish popula ions whose la ge indi iduals a e
ypically he mos ecund (Genne e al., 2010). Gi en ha educ-
ions in ish size ha e been obse ed as ecological esponses o
inc easing ocean empe a u es (She idan and Bick o d, 2011;
Audzijony e e al., 2020), i appea s likely ha clima e change
will ha e signi ican impac s on associa ions be ween pa asi es
and hei hos s in he u u e. Conside ing he impo an ole o
pa asi es in ma ine ood webs and ecosys em p ocesses (Timi
and Poulin, 2020; Po e e al., 2023b,2023c), he esul s highligh
he need o imp o e unde s anding o he seconda y e ec s o cli-
ma e change on hos pa asi e dynamics, and he po en ial u u e
implica ions o ma ine ecosys ems (Bye s, 2021).
To assess he po en ial e ec s o clima e change on pa asi e
communi ies, i is impo an o conside he b oad ma ine ecosys-
em impac s and adap a ions in hos biology ha also impac
pa asi es. The p esen s udy demons a es ha en i onmen al
a iables we e s ongly associa ed wi h pa asi e ichness and
abundance in P. diacan hus. The a iance in pa asi e p esence
and abundance can be pa ially explained by seasonal changes
in en i onmen al condi ions, which include wa e empe a u e,
salini y le els, and ni ogen and phospho us. The sho - e m sea-
sonal en i onmen al ac o s a ied be ween loca ions and seasons
in his s udy, wi h consis en ly wa me wa e empe a u es and
associa ed lowe le els o dissol ed oxygen du ing he la e-we
season and a Pe on Islands du ing he build-up season.
Oxygena ion s ess has been epo ed o inc ease pa asi e p e a-
lence and in ec ion success in ulne able hos s wi h e ec s seen
in bo h ish me abolic unc ion and physiology (Mikhee e al.,
2014; Poloczanska e al., 2016; Bye s, 2021; Sama as e al.,
2023). Rising global empe a u es lead o dec eased oxygen solu-
bili y in wa e (B ei bu g e al., 2018), and hus i is expec ed ha
he we season o no he n Aus alia will p oduce lowe wa e
oxygen le els in associa ion wi h wa me ocean empe a u es in
he u u e. In addi ion o oxygen nega i ely co a ying wi h em-
pe a u e, oxygen declines in es ua ies and nea sho e ma ine eco-
sys ems ha e also been caused by inc eased loadings o nu ien s
(B ei bu g e al., 2018). Nu ien le els o ni ogen and phos-
pho us we e highes a he nea sho e si es du ing he la e-we sea-
son when hese a eas o no he n Aus alia a e o en inunda ed
wi h s o mwa e and un-o om i e sys ems, loodplains
and ag icul u al land (P zeslawski e al., 2011). The le els o phos-
pho us in his s udy a e ela ed o wa e column u bidi y du ing
seasonal ou lows (Kämä i e al., 2020), and i is possible ha cli-
ma e change may b ing mo e equen , high le els o ou low.
These un-o e en s and changes in wa e composi ion (includ-
ing du ing idal mo emen s) cause c i ical dis u bance o he eco-
sys em, in luencing le els o ene gy and nu ien s, and a ec ing
he composi ion o ben hic o ganisms (Ande son e al., 2011).
I is impo an o ecognize ha di e en pa asi e species
espond di e en ly o en i onmen al changes, and as o whe he
pa asi e in ec ions inc ease o dec ease as a esul o clima e
changes will o en come down o he indi idual species a hand
(Mackenzie, 1999). Ex e nal pa asi es, such as he copepods and
monogeneans om his s udy, exhibi e y di e en mo phological
cha ac e is ics such as he na u e o hei egumen and hei size,
bo h o which a e highly in luen ial on he le el o sensi i i y ha
hese o ganisms e lec when aced wi h he su ounding changes
in ac o s like wa e empe a u e and salini y (Mölle , 1978). The
wo mos p e alen ex e nal pa asi es o his s udy, L. pa ac ucia us
and Diplec anum spp., demons a ed a nega i e associa ion wi h
salini y. Le nan h opus pa ac ucia us was also signi ican ly mo e
likely o be p esen du ing wa me condi ions, whe eas Caligus
sp. was mo e likely o be absen du ing he la e-we season when
he wa e empe a u e was a i s wa mes . Caligus sp. did no
show a signi ican associa ion wi h salini y, indica ing ha he pa a-
si es may no be as in luenced by changes in salini y as L. pa ac u-
cia us and Diplec anum spp. P e ious s udies ha e simila ly
desc ibed changes in ex e nal pa asi e abundance in wa me , saline
condi ions, wi h educed p esence a low salini ies (B icknell e al.,
2006;Callawaye al., 2012;Bye s,2021).
The de elopmen and di e si y o some pa asi e species
depends on he p esence o sui able in e media e hos s, in com-
bina ion wi h o he abio ic and bio ic ac o s (Klimpel e al.,
2019). In e nal pa asi es, such as he digeneans and nema odes
in he p esen s udy, may be bu e ed om di ec en i onmen al
a ia ion, bu may be a ec ed by he pa asi e’s eliance on an ea l-
ie hos (Neube e al., 2016; Bye s, 2021). Any en i onmen al
in luence on he in e nal pa asi e–hos sys em in he p esen
s udy may no be e lec i e o seasonal cycles bu ins ead o a
‘lag e ec ’due o he indi ec impac s on in e nal pa asi es o
hei dependence on in e media e hos s. Fo example, he signi i-
can ly lowe empe a u e du ing he p eceding mid-d y season
can a ec pa asi e in ec i i y, longe i y, and su i al o ansmis-
sion o ee-li ing s ages o in e nal pa asi es (Pie ock and
Ma cogliese, 2003; Lõhmus and Bjö klund, 2015) and may also
lowe he ac i i y o bo h in e media e hos s (molluscs, small
ishes and c us acea) and P. diacan hus (Lõhmus and
Bjö klund, 2015). This can ul ima ely esul in lowe ansmission
o la al digeneans (whose capsule is o en agile and delica e)
(Pie ock and Ma cogliese, 2003) be ween hos s, o om ege a-
ion, and he e o e lowe abundance o adul s ages in P. dia-
can hus du ing he build-up. Thus, i is impo an o u u e
esea ch o unde s and whe he changes in he dynamics o pa a-
si e assemblages’is a cumula i e e ec o e many seasons o
whe he changes a e uly e lec i e o wha occu s in each indi-
idual season. On he empo al scale o global clima e change,
o e all in luences on he in e nal pa asi e–hos sys ems may accu-
mula e and p esen somewha di e en ly o he in luences caused
by sho - e m seasonal en i onmen al a ia ion.
This s udy has shown ha seasonal en i onmen al a ia ion has an
impac on he abundance and dis ibu ion o pa asi es. The e ec s o
sho - e m seasonal en i onmen al a ia ion and ish hos size, p o-
ides a window in o he po en ial u u e o pa asi e–hos sys ems
when exposed o longe e m clima e a ia ion. As ocean empe a u es
con inue o wa m and he impac s o clima e change play ou ac oss
b oad-scale ecosys em p ocesses, changes in ophic s uc u e, ene gy
low and nu ien dynamics a e o be expec ed. Gi en he a ying ecol-
ogy o pa asi ic o ganisms, indi idual esponses o clima e changes a e
di icul o p edic . None heless, posi i e co ela ions be ween
P. diacan hus leng h and pa asi e assemblages –and he complex asso-
cia ions wi h en i onmen al a iables –sugges ha undamen al
shi s in pa asi e–hos dynamics o ma ine ishes a e likely unde a
changing clima e.
Supplemen a y ma e ial. The supplemen a y ma e ial o his a icle can
be ound a h ps://doi.o g/10.1017/S0031182024001008.
Da a a ailabili y s a emen . All da a p oduced o his s udy a e p o ided
in he manusc ip .
8 Megan Po e e al.
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