151
Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
species li ing in sympa y
Ma ia Yu. Tkachenko1, Michal Hnilička1,2 , Michal Janáč1, Yu iy K ach1,3 , Lukáš Ve ešník1,
Ma ké a Ond ačko á1
1 Ins i u eo Ve eb a eBiologyo heCzechAcademyo Sciences,K ě ná8,60300B no,CzechRepublic
2 Depa men o Bo anyandZoology,Facul yo Science,Masa ykUni e si y,Ko lářská2,61137,B no,CzechRepublic
3 Ins i u eo Ma ineBiology,Na ionalAcademyo Scienceso Uk aine,37I alyiskaS .,65048Odesa,Uk aine
Co espondingau ho :Ma ké aOnd ačko á(ond acko[email p o ec ed])
Copy igh : © Ma ia Yu. Tkachenko e al.
This is an open access a icle dis ibu ed unde
e ms o he C ea i e Commons A ibu ion
License (A ibu ion 4.0 In e na ional – CC BY 4.0).
Resea ch A icle
Abs ac
Non-na i e species ha e he po en ial o al e hos communi y s uc u e, which, in u n, may a ec
pa asi e ansmission, di e si y and dis ibu ion, pa icula ly when he in oduced hos is ecologically
o phylogene ically ela ed o i s na i e hos (s). In his s udy, we examine whe he he in oduc ion o a
compe en non-na i e ish hos shi s pa asi e load and communi y composi ion in na i e ish species.
Speci ically, we ocus on wo Eupe ca ian species: he na i e Eu asian pe ch (Pe ca lu ia ilis) and he
non-na i e pumpkinseed sun ish (Lepomis gibbosus), which was in oduced in o Eu ope om No h
Ame ica. Ou esul s show ha he pa asi e communi y o na i e pe ch co-occu ing wi h non-na i e
pumpkinseed (sympa ic popula ions) di e signi ican ly om hose o pe ch inhabi ing si es una -
ec ed by pumpkinseed in oduc ion (allopa ic popula ions). Mo eo e , sympa ic pe ch popula ions
exhibi signi ican ly highe pa asi e abundance, in acommuni y ichness and dominance, along wi h
lowe equi abili y, compa ed o allopa ic popula ions. These indings sugges ha he in oduc ion o
pumpkinseed may ha e con ibu ed o shi s in bo h pa asi e abundance and di e si y in na i e ish
hos s. Addi ionally, ou s udy indica es a po en ial pa asi e spillback o he ema ode Bucephalus poly-
mo phus and spill-o e o he Asian in asi e pa asi ic copepod Neoe gasilus japonicus, bo h associa ed
wi h pumpkinseed es ablishmen in he s udy a ea. The success ul inclusion o non-na i e ish species
in o he li e cycles o se e al independen ly in oduced and un ela ed in asi e pa asi es unde sco es
he impo ance o in oduced hos s in d i ing changes wi hin local pa asi e communi ies.
Key wo ds: F eshwa e ish, pa asi e communi y, pe ch, pumpkinseed, species in oduc ion, spill-back
In oduc ion
The in oduc ion o non-na i e eshwa e ish species has inc eased signi ican ly ac oss
he wo ld o e he pas ew decades, leading o nega i e socio-economic, ecological
and e olu iona y impac s on local biodi e si y (Hulme 2009; Vi ule e al. 2009; Go-
zlan e al. 2010; Cuche ousse and Olden 2011). Local ecosys ems may be a ec ed by
in asi e species h ough a ange o mechanisms, including p eda ion, compe i ion o
ood and space, hyb idisa ion, al e a ions in ophic ela ionships and modi ica ion o
biochemical cycles (Leunda 2010; Cuche ousse and Olden 2011). The success o an
in asi e species may also be pa ially linked o pa asi es and pa hogens. Fo example,
in oduced species can gain an ad an age o e na i e species due o he absence o hei
Academic edi o : Filipe Ribei o
Recei ed:
30 Janua y 2025
Accep ed:
16 Ap il 2025
Published:
7 Oc obe 2025
Ci a ion: Tkachenko MYu, Hnilička
M, Janáč M, K ach Yu, Ve ešník
L, Ond ačko á M (2025) Shi in
pa asi e load in na i e and non-
na i e Eupe ca ian ish species
li ing in sympa y. In: Anas ácio P,
Ribei o F, Chainho P (Eds) In asions
in Aqua ic Sys ems. NeoBio a 102:
151–171. h ps://doi.o g/10.3897/
neobio a.102.148301
NeoBio a 102: 151–171 (2025)
DOI: 10.3897/neobio a.102.148301
Ad ancing esea ch on alien species and biological in asions
A pee - e iewed open-access jou nal
NeoBio a
152
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
na u al pa asi es ( he so-called enemy elease hypo hesis; Keane and C awley (2002))
o h ough he in oduc ion o in asi e pa asi es o pa hogens ha a e mo e ha m ul
o na i e compe i o s (Lymbe y e al. 2014). While he ole o pa asi es in he success
o in asi e species is widely ecognised (e.g. To chin e al. (2003); P en e e al. (2004);
Dunn (2009)), he impac o in asi e species on pa asi e communi ies in na i e hos s
has ecei ed less a en ion (Hohenadle e al. 2019).
Non-na i e species can al e local pa asi e communi ies h ough he in oduc ion
o non-na i e pa asi es capable o pa asi ising local hos s o by in e ac ing wi h na-
i e pa asi e species. New pa asi e species co-in oduced o he in aded ecosys em
may ei he be hos -speci ic and emain pa o he pa asi ic auna o hei o iginal
hos (Lymbe y e al. 2014) o hey may in ec na i e species (Ta aschewski 2006),
po en ially esul ing in subsequen changes o local pa asi e di e si y. Fo example,
he in oduc ion o Eu asian pe ch (Pe ca lu ia ilis; Eupe ca ia, Pe cidae) in o A i-
can lakes led o he co-in oduc ion o se e al ces odes ha la e became es ablished
in na i e ish popula ions (Loke and Ho kin 2015). In F ance, monogenean pa -
asi es o he in asi e common nase (Chond os oma nasus) in ec ed he h ea ened
na i e sou h-wes Eu opean nase (Pa achond os oma oxos oma) a si es whe e he
wo species co-occu ed (Šimko á e al. 2012). Following a success ul in oduc ion,
he e o e, non-na i e pa asi e species may be expec ed o ansmi om he in asi e
species o na i e hos s, ypically hose ha a e ecologically simila o axonomically
close (Mack e al. 2000). This has led o he concep o “pa asi e spill-o e ” (Clea e-
land e al. 2002; P en e e al. 2004), which sugges s ha non-na i e pa asi es can
in ec na i e hos species in in aded habi a s, hus accele a ing hei ange expansion
(Galli e al. 2005). Fu he mo e, hese in e ac ions may bene i he in oduced hos
i he pa asi e nega i ely a ec s i s new hos (Tompkins e al. 2003).
Howe e , in e ac ions be ween non-na i e hos s and local pa asi e auna appea
o occu mo e equen ly han he abo e-men ioned spill-o e (Kelly e al. 2009).
In his con ex , Kelly e al. (2009) in oduced he concep o “pa asi e spill-back”,
which sugges s ha , when a non-indigenous species se es as a compe en hos o
a na i e pa asi e, he p esence o he addi ional hos can ampli y disease impac s on
na i e species, a ec ing bo h indi idual hos s and en i e popula ions. Fo example,
in Ge man i e s a ec ed by he in asion o Pon o-Caspian species (gobiids and
amphipods), local ish species exhibi ed highe in ec ion a es by he nema ode Ra-
phidasca is acus, which success ully used Pon o-Caspian gobies as pa a enic hos s,
compa ed o i e s ha had no been in aded (Hohenadle e al. 2019). A speci ic
case o pa asi e spill-back is he hypo hesis o “in asional mel down” (Simbe lo
and on Holle 1999), which p oposes ha mul iple species simul aneously colo-
nising a new en i onmen can enhance each o he ’s chances o in asion. Ce ain
ecological ela ionships ha may de elop amongs in asi e species, such as p eda-
o -p ey in e ac ions, symbiosis and pa asi ism, could acili a e he es ablishmen
o in ade pa asi es, e en i he pa asi es we e in oduced h ough o he ec o s
(Ta aschewski 2006; Emde e al. 2014). This is pa icula ly ele an o pa asi es
wi h complex li e cycles as hei in asion success depends on he a ailabili y o sui -
able in e media e hos s. In e es ingly, in asional mel down may also occu wi hin
pa asi e-pa asi e ela ionships, as exempli ied by he eel nema ode Anguillicola c as-
sus, which escapes he hos ’s immune esponse by in ading he cys o ano he in a-
si e pa asi e, he acan hocephalan Pompho hynchus lae is (Hohenadle e al. 2018).
Non-na i e species can also al e local pa asi e communi ies h ough he “dilu-
ion e ec ”. In his case, i hey a e no compe en hos s o he acqui ed pa asi es,
153
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
non-na i e species may ac as pa asi e sinks, o dilu ion agen s, educing pa asi e
p e alence in local popula ions (Keesing e al. 2006; Gend on and Ma cogliese
2017). Non-na i e species can also dis up pa asi e ansmission pa hways. Fo
example, ish can dec ease he p e alence o ema odes in na i e ish popula ions
by p eying on he pa asi e’s in e media e hos s, such as snails (Poulin and Mouil-
lo 2003). Addi ionally, na i e specialis pa asi es may decline i non-na i e hos s
eplace na i e hos s, pa icula ly when he non-na i e species a e unsui able hos s,
po en ially leading o he ex inc ion o ce ain na i e pa asi e species (Hohenadle
e al. 2019). This can esul in he homogenisa ion o pa asi e communi ies, a-
ou ing gene alis pa asi es (Dunn 2009). Finally, changes in hos a ailabili y and
communi y s uc u e can shi compe i i e dynamics amongs pa asi e species,
o example, when a di e se na i e hos communi y is supplan ed by a dominan
non-na i e species, ollowing which pa asi e di e si y is educed, p omo ing he
dominance o a ew gene alis pa asi e species (Gend on e al. 2012).
Aqua ic ecosys ems a e highly ulne able o he in oduc ion o non-na i e spe-
cies, whe he as hos s, such as ish, molluscs o c us aceans (Bódis e al. 2012) o
hei associa ed pa asi es (Esposi o e al. 2023). Fu he mo e, he in oduc ion
o species in o eshwa e ecosys ems can ha e nume ous impac s on na i e com-
muni ies and on ecosys em unc ioning (Ha el e al. 2015). The Eu asian pe ch
is a widely dis ibu ed p eda o y eshwa e species (S epien and Haponski 2015)
inhabi ing bo h len ic and lo ic wa e bodies (Ba uš and Oli a 1995). I equen ly
co-occu s wi h he non-na i e pumpkinseed sun ish (Lepomis gibbosus; Eupe ca ia,
Cen a chidae), a No h Ame ican eshwa e species (Sco and C ossman 1973)
in oduced in o Eu ope as an o namen al ish in he la e 19 h cen u y which has
had nega i e impac s on local ecosys ems (Soes e al. 2011). The pumpkinseed is
now widesp ead ac oss many Eu opean coun ies and was added o he lis o In-
asi e Species o Union Conce n in 2019 (Eu opean Commission 2019).
In i s na i e No h Ame ican ange, he pumpkinseed commonly occu s sym-
pa ically wi h he yellow pe ch (Pe ca la escens), a sis e species o he Eu asian
pe ch (Colle e and Bana escu 1977; Shche bukha 1993), wi h bo h species sha -
ing simila habi a and ood p e e ences (Sun and Ha ey 1986; Runciman and
Lea 2009). Despi e millions o yea s o isola ion, he pa asi e assemblages o hese
wo pe ch species, composed o non-hos -speci ic pa asi es, a e no andom, bu
con ain key componen s ha a e p edic able a he con inen al scale (Ca ney and
Dick 1999). As a esul , pumpkinseed in Eu ope sha e se e al common pa asi es
wi h he Eu asian pe ch, such as he ces odes T iaenopho us nodulosus and Bo h-
ioces us cla iceps and he nema ode Camallanus lacus is (Ca ney and Dick 1999;
Masson e al. 2015; Ond ačko á e al. 2019a; K ach e al. 2021a).
Building on p esen knowledge o he sympa ic occu ence o hese wo Eupe ca -
ian ish species, his s udy aims o e alua e po en ial changes in pa asi e communi ies
be ween popula ions whe e ei he pe ch o pumpkinseed li e wi hou hei Eupe ca -
ian ela i e (allopa ic si es) and popula ions whe e bo h species co-exis (sympa ic
si es). In doing so, we: 1) compa e he abundance and species di e si y o pa asi e
communi ies o assess he abili y o non-na i e pumpkinseed o acqui e local pa asi e
species, 2) e alua e he simila i y o pa asi e communi ies be ween sympa ic and allo-
pa ic popula ions in bo h hos species and iden i y pa asi e species ha signi ican ly
con ibu e o shi s in he pa asi e communi y o pe ch and 3) ocus on pa asi e spe-
cies sha ed be ween he pe ch and pumpkinseed and discuss hei ele ance in he
con ex o po en ial pa asi e spill-back, spill-o e , dilu ion o in asional mel down.
154
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Ma e ial and me hods
Fish and pa asi e sampling
Fish we e collec ed om eigh small len ic wa e bodies (oxbows and sand pi s) in he
lowe Mo a a Ri e Basin in he Czech Republic, h ee si es ha ing allopa ic popu-
la ions o pe ch and o pumpkinseed (six si es in o al) and wo si es ha ing sympa -
ic popula ions o bo h species (Table 1). Fish we e collec ed using elec o ishing gea
(SEN, a Bednář R., Olomouc, Czech Republic; equency 75–85 Hz; maximum ou -
pu 225/300 V) o seine ne s (7 m long, 1 cm mesh size), depending on habi a ype.
A e collec ion, he ish we e anspo ed ali e in ae a ed i e wa e o he acili ies a
he Ins i u e o Ve eb a e Biology, whe e hey we e placed in ou doo anks, sepa a ed
by ish species and locali y. Fi een ish pe species we e collec ed o each si e (75 pe ch
and 75 pumpkinseed in o al) and examined o pa asi es (Table 1). Following humane
dispa ch, s anda d leng h (SL, mm) was measu ed o each ish, a e which he ins,
skin, gills, gill co e s, eyes, muscle and in e nal o gans (in es ine, li e , spleen, hea ,
kidney, gonads) we e inspec ed o he p esence o pa asi es. All ish we e dissec ed
wi hin h ee days o sampling o ensu e maximum pa asi e eco e y (K ach e al. 2016).
Table 1. Lis o si es sampled o pa asi e communi ies o na i e Eu opean pe ch Pe ca lu ia ilis and non-na i e pumpkinseed sun ish
Lepomis gibbosus in he Basin o he lowe Mo a a Ri e , Czech Republic, showing numbe o ish dissec ed (n), ish s anda d leng h (SL
in mm (mean, ange)), pa asi e p e alence (%), o al abundance o pa asi es and pa asi e species ichness.
Locali y name Coo dina es Fish species n Fish SL Pa asi e
p e alence
Pa asi e
abundance
Pa asi e species
ichness
Sympa ic si es
Babice oxbow 49.117968, 17.488028 P. lu ia ilis 15 69 (61-98) 100 209 12
L. gibbosus 15 74 (63-81) 100 532 9
U Jezu sandpi 49.131407, 17.510408 P. lu ia ilis 15 71 (63-79) 100 358 18
L. gibbosus 15 75 (65-82) 100 989 10
Allopa ic si es
Deda a sandpi 48.633176, 16.959805 P. lu ia ilis 15 71 (56-114) 100 123 10
Kanada oxbow 49.102925, 17.492513 P. lu ia ilis 15 71 (63-76) 100 129 11
Penne oxbow 49.156364, 17.511674 P. lu ia ilis 15 71 (66-87) 93 118 11
Dyje oxbow D3 48.684344, 16.916031 L. gibbosus 15 68 (52-84) 100 6623 4
Dyje oxbow D6 48.717369, 16.888908 L. gibbosus 15 59 (55-64) 100 97 5
Pohansko oxbow 48.725360, 16.890936 L. gibbosus 15 60 (53-70) 100 285 8
Pa asi e p ocessing
Non-me azoan pa asi es we e examined ali e unde ligh mic oscopy and hei p es-
ence/absence eco ded. Numbe s o Ich hyoph hi ius mul i iliis and De mocys idium
we e eco ded. Me azoan pa asi es we e collec ed, coun ed and p ese ed o species
iden i ica ion. Monogeneans and myxospo eans we e p ese ed in GAP (glyce -
ine-ammonium-pic a e) and p epa ed as semi-pe manen slides (Malmbe g 1970),
while ces odes, ema odes, acan hocephalans and nema odes we e p ese ed in ho
4% o maldehyde. P io o species iden i ica ion, ces odes and ema odes we e
s ained wi h i on ace ic ca mine, dehyd a ed in e hanol o inc easing concen a ion
and moun ed in Canada balsam as pe manen slides (Geo gie e al. 1986; C ibb
and B ay 2010). Acan hocephalans we e p essed be ween wo slides and p ese ed
in 70% e hanol. Bo h p ese ed acan hocephalans and nema odes we e moun ed
in glyce ol as empo a y slides o ligh mic oscopy. C us aceans and bi al es we e
155
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
p ese ed in 4% o maldehyde and iden i ied unde ligh mic oscopy. All p ese ed
pa asi es we e iden i ied o species le el, o o he lowes possible axonomic le el
when species-le el iden i ica ion was no easible. An Olympus BX53 ligh mic o-
scope (Olympus Op ical Co., Hambu g, Ge many) equipped wi h phase-con as ,
di e en ial (Noma ski) in e e ence con as and image analysis so wa e (CellSens
S anda d digi al image analysis package; Olympus Op ical Co., Hambu g, Ge ma-
ny) was used o species iden i ica ion. Iden i ica ion ollowed he keys o Baue
(1987), Be e ley-Bu on (1984), Mo a ec (2013) and Suda iko e al. (2002).
A subsample o la al ces odes (Bo h iocephalidae, P o eocephalidae) and ema-
odes (Diplos omum), o which species iden i ica ion could no be de e mined mo -
phologically, was p ese ed in 96% e hanol o u he molecula analysis. Subsequen -
ly, DNA was ex ac ed using he In iso b® Spin Fo ensic Ki (STRATEC Molecula ,
Ge many) ollowing he s anda d p o ocol. Fo Diplos omum me ace ca iae, he o -
wa d p ime BD1 (5′-GTCGTAACAAGGTTTCCGTA-3′) and e e se p ime 4S
(5′-TCTAGATGCGTTCGAA(G/A)TGTCGATG-3′) (Bowles e al. 1993) we e used
o ob ain he ITS1 pa ial sequence, wi h an annealing empe a u e o 58 °C (PCR
de ails in Dudli e al. (2024)), while he o wa d p ime 18S9F and e e se p ime
18S637R (Moszczynska e al. 2009) we e employed o ob ain he 18S pa ial sequence
o he la al ces odes (Bo h iocephalidae, P o eocephalidae). The PCR eac ion mix
con ained 4 μl o ex ac ed DNA, 0.3 μl o each p ime (10 μM), 2 μl o bu e A,
0.2 μl o dNTPs (10 mM), 0.2 μl o MgCl2 (25 mM), 0.5 U/μl o Taq polyme ase
and ddH2O up o a o al olume o 10 μl. PCR was pe o med using he KAPA2G
Robus Ho S a PCR Ki (Kapabiosys ems, USA) in a Mas e cycle ep g adien S
he mocycle (Eppendo , Ge many) wi h he ollowing empe a u e p o ile: 95 °C
o 2 min, 33 cycles o 95 °C o 30 s, 58 °C o 30 s and 72 °C o 5 min, wi h a inal
ex ension a 72 °C o 5 min. All PCR p oduc s we e pu i ied using an ExoSAP-IT
Ki (A yme ix Inc., San a Cla a, USA) ollowing he manu ac u e ’s p o ocol. PCR
p oduc s we e comme cially sequenced a Eu o ins Genomics Ge many GmbH. The
sequences we e checked and aligned using Geneious® .9.0.5 and compa ed wi h he
NCBI da abase using BLASTn o assess sequence simila i y. Simila i y 99.8–100%
and 99.5–100% o ITS/18S and COI, espec i ely, was applied o pe o m species
assignmen . Newly-gene a ed sequences we e submi ed o GenBank unde he acces-
sion numbe s: PV402115, PV402120-1, PV402623, PV402631 and PV402405-6.
Da a analysis
Only hose pa asi es ha could be coun ed we e used o quan i a i e analysis
(i.e. kine oplas ids and cilia es, excep Ich hyoph hi ius mul i iliis, we e excluded
om he analysis), while all pa asi e axa we e included in he quali a i e analy-
sis. Non-na i e pa asi es included species co-in oduced wi h pumpkinseed om
No h Ame ica (acco ding o Ho man (1999)) and species in oduced his o ically
o he s udy a ea om Asia by o he ec o s. Acqui ed pa asi es included bo h Eu o-
pean (Mo a ec 2001) and Asian species (Wielgoss e al. 2008; Konečný e al. 2018;
Ond ačko á e al. 2025) in ec ing pumpkinseed and Asian species in ec ing pe ch.
Pa asi e load was exp essed in e ms o p e alence, in ensi y o in ec ion and abun-
dance, calcula ed ollowing Bush e al. (1997). Mean abundance was calcula ed as
he a e age numbe o pa asi es pe hos in each locali y, in ensi y o in ec ion as
he a e age numbe o pa asi es pe in ec ed hos s and p e alence as he pe cen age
o in ec ed hos s. Di e ences be ween pa asi e communi ies we e analysed a bo h
156
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
he in acommuni y le el (pa asi es ound on a single hos ) and componen com-
muni y le el (pa asi es ound in a hos popula ion) (Bush e al. 1997).
Analysis a he in acommuni y le el was conduc ed using gene alised linea
mixed models (GLMM), which we e used o compa e pa asi e abundance (nega-
i e binomial dis ibu ion) and in acommuni y species ichness (Poisson dis ibu-
ion) be ween species (pe ch/pumpkinseed) and be ween ype o popula ion (allo-
pa ic/sympa ic), wi h si e as a andom ac o . The same app oach was applied o
compa e he abundance and ichness o acqui ed pa asi es, wi h he excep ion o
compa isons be ween acqui ed pa asi es in sympa ic and allopa ic popula ions o
pe ch, whe e he low incidence o acqui ed pa asi es made es ing o di e ences in
abundance poin less. Ins ead, we es ed o di e ences in p e alence using GLMM
wi h a Be noulli dis ibu ion.
Di e ences in pa asi e di e si y a he componen communi y le el we e as-
sessed using h ee di e si y indices, i.e. he Shannon-Wiene index (H), which in-
dica es a e age niche wid h; he dominance index (D), which exp esses he ex en
o which a ew species domina e he communi y; and he equi abili y index (J),
which measu es he e enness wi h which indi iduals a e dis ibu ed amongs he
axa p esen (Magu an 2004). Pe mu a ion es s (1000 pe mu a ions) we e used
o compa e di e si y indices be ween g oups (hos species, allopa ic/sympa ic
locali ies). All di e si y analyses we e pe o med using PAST so wa e (PAlaeon o-
logicalSTa is ics, .3.22; Hamme e al. (2001)).
Di e ences in pa asi e communi y composi ion be ween sympa ic and allo-
pa ic popula ions in bo h hos species we e es ed using pe mu a ional mul i a -
ia e analysis o a iance (PERMANOVA; Ande son (2001)) and isualised using
non-me ic mul idimensional scaling (NMDS). Bo h NMDS and PERMANOVA
we e conduc ed sepa a ely on wo dis ance ma ices, i.e. a ma ix based on Jacca d
dis ances (bina y) and one based on B ay-Cu is dis ances (quan i a i e, abundance
da a ou h- oo ans o med), wi h PERMANOVA based on 999 pe mu a ions.
All s a is ical analyses we e pe o med using R .4.3.1 (R Co e Team 2023), wi h
he MASS (Venables and Ripley 2002), lme4 (Ba es e al. 2015), lm es (Zeileis
and Ho ho n 2002) and egan (Oksanen e al. 2022) packages.
Resul s
Pa asi e communi y composi ion in na i e and in oduced hos s
All pumpkinseed and all, bu one pe ch we e in ec ed wi h a leas one pa asi e axon.
In o al, 38 pa asi e axa we e ound, 31 in ec ing pe ch and 18 in ec ing pumpkin-
seed (Table 2). Th ee pa asi e species co-in oduced wi h pumpkinseed om No h
Ame ica, he monogeneans Onchocleidus dispa and O. similis and he ema ode
Pos hodiplos omum cen a chi, we e ound solely on hei na u al hos , ep esen ing
85% o all pumpkinseed pa asi es. Th ee addi ional species, A. c assus, Neoe gasilus
japonicus and Sinanodon a woodiana, we e in oduced o he s udy a ea om Asia,
con ibu ing 5% and 10% o he pa asi e communi ies o pe ch and pumpkin-
seed, espec i ely. T ema ode me ace ca iae domina ed he pa asi e communi ies o
bo h hos species, ep esen ing 55% o me azoan pa asi es in pe ch (nine species)
and 75% in pumpkinseed ( ou species). The maximum in ensi y o in ec ion in
pumpkinseed was by me ace ca iae o P. cen a chidae (up o 1111 pa asi es pe ish),
whe eas in pe ch, i was me ace ca iae o B. polymo phus (up o 33 pa asi es).
157
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Table 2. Lis o pa asi e species ound in Eu asian pe ch Pe ca lu ia ilis and pumpkinseed Lepomis gibbosus in len ic wa e bodies in he
basin o he lowe Mo a a Ri e .
Pe ca lu ia ilis Lepomis gibbosus
ALLOPATRIC SYMPATRIC ALLOPATRIC SYMPATRIC
P e alence Abundance P e alence Abundance P e alence Abundance P e alence Abundance
Opis hocon a
Ich hyospo ea De mocys idium spp. 15.6% 0.4
Exca a a
Kine oplas ida C yp obiidae spp. 3.3% 3.3%
SAR
Oligohymenopho ea Apiosoma spp. 33.3% 56.7%
Cap iniana piscium 3.3%
Epis ylis spp. 2.2%
Scyphidia spp. 15.6% 20.0%
T ichodinidae spp. 40.0% 63.6% 13.3%
Ich hyoph hi ius mul i iliis 3.3% 0.03 15.6% 0.8
Animalia
Myxospo ea Myxospo idia sp. (muscle) 13.3% 0.3
Monogenea Onchocleidus dispa 57.8% 20.1
Onchocleidus similis 20.0% 0.6 50.0% 10.0
T ema oda Bucephalus polymo phus 100% 6.5 76.7% 14.6
Rhipidoco yle campanula 2.2% 0.02
Diplos omum
pseudospa haceum
26.7% 0.3 3.3% 0.03
Diplos omum sp. Lineage 3
sensu Fal ýnko á e al. 2022
6.7% 0.07
Tylodelphys cla a a 46.7% 3.3 6.7% 0.13
Clinos omum complana um 51.1% 2.4 26.7% 0.4
Cya hoco yle p ussica 3.3% 0.03
Holos ephanus cobi idis 3.3% 0.03
Holos ephanus luhei 10.0% 0.1
Me o chis xan hosomus 3.3% 0.03
Pos hodiplos omum cen a chi 88.9% 131.8 16.7% 0.2
Ces oda Bo h ioces us cla iceps 6.7% 0.1
P o eocephalus pe cae 4.4% 0.1 23.3% 0.5
T iaenopho us nodulosus 11.1% 0.1 8.9% 0.3
Valipo a campylanc is o a 6.7% 0.1
Nema oda Anguillicola c assus 4.4% 0.2 13.3% 0.4 20.0% 0.5
Camallanus unca us 26.7% 0.8
Philome a ob u ans 15.6% 0.5
Philome a sp. 2.2% 0.02
Schulmanela pe uschewskii 8.9% 0.3 6.7% 0.07
Acan hocephala Acan hocephalus lucii 11.1% 0.3 3.3% 0.03
Pompho hynchus lae is 3.3% 0.3
Bi al ia Sinanodon a woodiana 23.3% 0.4 26.7% 1.2 3.3% 0.07
C us acea E gasilus sieboldi 57.8% 1.4 50.0% 4.4 3.3% 0.03
Neoe gasilus japonicus 6.7% 0.07 60.0% 24.7
Pa ae gasilus longidigi us 23.3% 0.8
B anchiu a A gulus oliaceus 6.7% 0.1 3.3% 0.03 13.3% 0.2 3.3% 0.03
Nine pa asi e species we e ound in bo h pe ch and pumpkinseed hos s, i.e. he
cilia es Ich hyoph hi ius mul i iliis; he la al ema odes Bucephalus polymo phus
and Tylodelphys cla a a; he la al ces ode T iaenopho us nodulosus; he la al nema-
ode A. c assus, bi al e glochidia o S. woodiana, he copepods E gasilus sieboldi and
N. japonicus and he b anchiu an A gulus oliaceus (Fig. 1). Addi ionally, ep esen-
a i es o he T ichodinidae and C yp obiidae amilies we e ound in bo h hos s,
al hough species iden i ica ion was no pe o med (Table 2).
158
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Pa asi e abundance and di e si y in na i e and in oduced hos s
Mean pa asi e abundance di e ed signi ican ly be ween hos species (GLMM,
Z = 5.931, p < 0.001), being en imes highe in pumpkinseed (113.6 ± 233.1 S.D.)
compa ed o pe ch (10.6 ± 8.8). Pa asi e in acommuni y species ichness anged om
1–10 in pe ch and 1–7 in pumpkinseed, wi h signi ican ly highe species ichness in
pe ch (3.9 ± 1.9) han pumpkinseed (2.8 ± 1.2) (GLMM, Z = 3.849, p < 0.001).
Pa asi e di e si y indices di e ed signi ican ly be ween na i e and non-na i e
hos s (pe mu a ion es s, p < 0.0001 o all compa isons). Bo h he Shannon di-
e si y index and equi abili y we e highe in pe ch han pumpkinseed (Shannon
di e si y index: pe ch H = 2.524, pumpkinseed H = 1.099; equi abili y: pe ch J =
0.735, pumpkinseed J = 0.380), while dominance was lowe in pe ch (D = 0.118)
han pumpkinseed (D = 0.509).
Allopa ic s. sympa ic popula ions
Pa asi e abundance was signi ican ly highe in sympa ic han allopa ic pe ch
popula ions (GLMM: Z = 4.081, p < 0.001), bu did no di e in pumpkinseed
popula ions (GLMM, Z = 0.195, p = 0.846; Fig. 2A). Simila ly, in acommuni y
ichness was signi ican ly highe in sympa ic han allopa ic pe ch popula ions
(GLMM, Z = 3.206, p < 0.001), while no di e ences we e ound in pumpkin-
seed popula ions (GLMM, Z = 0.174, p = 0.862; Fig. 2B). Howe e , sympa ic
pumpkinseed popula ions we e pa asi ised by a signi ican ly highe abundance o
acqui ed pa asi es (including bo h Eu opean and Asian species) han allopa ic
popula ions (GLMM, Z = 2.864, p = 0.004). Pe ch om sympa ic popula ions
hos ed acqui ed pa asi es signi ican ly mo e o en han hose om allopa ic pop-
ula ions (GLMM, d = 1, 73, P = 0.001).
Figu e 1. P opo ion o me azoan pa asi e axa in in acommuni ies o na i e Eu opean pe ch Pe ca lu ia ilis and non-na i e pumpkinseed
Lepomis gibbosus examined a eigh locali ies: 1) wi h sympa ic occu ence o pe ch and pumpkinseed: A = U Jezu, B = Babice; 2) wi h al-
lopa ic pe ch: C = Deda a, D = Kanada, E = Penne; and 3) wi h allopa ic pumpkinseed: F = Pohansko, G = Oxbow D3, H = Oxbow D6.
159
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Pa asi e species ichness was highe in sympa ic han allopa ic popula ions o
bo h species (18 and 13 in pe ch, 13 and 9 in pumpkinseed), despi e jus wo sym-
pa ic si es being compa ed o h ee allopa ic si es. While Shannon di e si y did no
di e in pe ch (H = 1.905 and 1.781 o allopa ic and sympa ic popula ions), i was
signi ican ly highe in sympa ic (H = 1.173) compa ed wi h allopa ic (H = 0.527)
pumpkinseed popula ions. In pumpkinseed, equi abili y was highe in sympa ic
(J = 0.458) compa ed o allopa ic popula ions (J = 0.240), while dominance was
highe in allopa ic popula ions (D = 0.736) compa ed o sympa ic (D = 0.361;
p < 0.001 o all compa isons). In con as , signi ican ly lowe dominance (D = 0.210;
p = 0.01) and highe equi abili y (J = 0.743; p < 0.001) we e obse ed in allopa ic
popula ions compa ed o sympa ic ones in pe ch (D = 0.244; J = 0.616).
The composi ion o pa asi e communi ies in bo h pe ch and pumpkinseed di -
e ed signi ican ly be ween sympa ic and allopa ic popula ions. This was con-
i med o bo h Jacca d (Fig. 3A) and B ay-Cu is (Fig. 3B) dis ance ma ices
(PERMANOVA, d = 1, 73, P = 0.001 o all analyses).
Discussion
In his s udy, we es ed whe he he in oduc ion o a compe en non-na i e ish
hos , he pumpkinseed, migh shi he pa asi e load and communi y composi ion
o na i e ish species, such as he Eu asian pe ch. We ound ha he pa asi e com-
muni ies o na i e pe ch co-occu ing wi h non-na i e pumpkinseed a sympa ic
si es di e ed signi ican ly om hose o pe ch a allopa ic si es, which we e no in-
luenced by he in oduc ion o pumpkinseed. Speci ically, pa asi e communi ies o
pe ch popula ions li ing in sympa y wi h pumpkinseed exhibi ed signi ican ly high-
e pa asi e abundance, in acommuni y ichness and dominance, along wi h lowe
equi abili y compa ed o hose in allopa ic popula ions. These indings sugges ha
he in oduc ion o pumpkinseed may ha e con ibu ed o shi s in pa asi e abun-
dance, di e si y and communi y composi ion in he na i e ish species.
Figu e 2. Pa asi e abundance (A) and in acommuni y species ichness (B) in sympa ic and allopa ic popula ions o in oduced pumpkinseed
Lepomis gibbosus (g een ba s) and na i e Eu opean pe ch Pe ca lu ia ilis (blue ba s) in small len ic wa e bodies in he lowe Mo a a Ri e Basin. Pa -
asi e abundance is exp essed wi h a loga i hmic scale. Ho izon al line: median, box: in e qua ile ange, whiske s: non-ou lie ange, poin s: ou lie s.
166
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Bowles J, Hope M, Tiu WU, Liu XS, McManus DP (1993) Nuclea and mi ochond ial gene ic
ma ke s highly conse ed be ween Chinese and Philippine Schis osoma japonicum. Ac a T opica
55(4): 217–229. h ps://doi.o g/10.1016/0001-706X(93)90079-Q
Bush AO, La e y KD, Lo z JM, Shos ak AW (1997) Pa asi ology Mee s Ecology on I s Own
Te ms: Ma golis e al. Re isi ed. The Jou nal o Pa asi ology 83(4): 575–583. h ps://doi.
o g/10.2307/3284227
Ca ney JP, Dick TA (1999) En e ic helmin hs o pe ch (Pe ca lu ia ilis L.) and yellow pe ch (Pe ca
la escens Mi chill): S ochas ic o p edic able assemblages? The Jou nal o Pa asi ology 85(5):
785–795. h ps://doi.o g/10.2307/3285812
Clea eland S, Hess GR, Dobson AP, Lauen o h MK, McCallum HI, Robe s MG, Wood o e R
(2002) The ole o pa hogens in biological conse a ion. In: Hudson PJ, Rizzoli A, G en ell BT,
Hees e beek H, Dobson AP (Eds) The ecology o wildli e diseases. Ox o d Uni e si y P ess,
Ox o d, 139–150. h ps://doi.o g/10.1093/oso/9780198506201.003.0008
Colle e BB, Bana escu P (1977) Sys ema ics and zoogeog aphy o he ishes o he amily Pe cidae.
Jou nal o he Fishe ies Resea ch Boa d o Canada 34(10): 1450–1463. h ps://doi.o g/10.1139/
77-209
C ibb TH, B ay RA (2010) Gu wash, body soak, blende and hea - ixa ion: App oaches o he
e ec i e collec ion, ixa ion and p ese a ion o ema odes o ishes. Sys ema ic Pa asi ology
76(1): 1–7. h ps://doi.o g/10.1007/s11230-010-9229-z
Cuche ousse J, Olden JD (2011) Ecological impac s o non-na i e eshwa e ishes. Fishe ies
(Be hesda, Md.) 36(5): 215–230. h ps://doi.o g/10.1080/03632415.2011.574578
Douda K, V ílek M, Sla ík O, Reicha d M (2012) The ole o hos speci ici y in explaining he in-
asion success o he eshwa e mussel Anodon a woodiana in Eu ope. Biological In asions 14(1):
127–137. h ps://doi.o g/10.1007/s10530-011-9989-7
Dudli I, K ach Y, Tkachenko MY, Naza uk K, Ond ačko á M (2024) Compa a i e analysis o pa asi e
load on ecen ly es ablished in asi e pumpkinseed Lepomis gibbosus (Ac inop e ygii: Cen a chidae)
in Eu ope. Ac a Pa asi ologica 69(1): 819–830. h ps://doi.o g/10.1007/s11686-024-00794-2
Dunn AM (2009) Pa asi es and biological in asions. Ad ances in Pa asi ology 68: 161–184.
h ps://doi.o g/10.1016/S0065-308X(08)00607-6
Emde S, Kochmann J, Kuhn T, Pla h M, Klimpel S (2014) Ge ing wha is se ed? Feeding ecology
in luencing pa asi e-hos in e ac ions in in asi e ound goby Neogobius melanos omus. PLoS ONE
9(10): e109971. h ps://doi.o g/10.1371/jou nal.pone.0109971
Esposi o A, Foa a J, Quilichini Y (2023) Pa asi ic Helmin hs and F eshwa e Fish In oduc ion in
Eu ope: A Sys ema ic Re iew o Dynamic In e ac ions. Fishes 8(9): 450. h ps://doi.o g/10.3390/
ishes8090450
Eu opean Commission (2019) Commission implemen ing egula ion (EU) 2019/1262 o 25 July
2019 amending Implemen ing Regula ion (EU) 2016/1141 o upda e he lis o in asi e alien
species o Union conce n. O icial Jou nal o he Eu opean Union L199: 1–4. h ps://eu -lex.
eu opa.eu/eli/ eg_impl/2019/1262/oj/eng
Fal ýnko á A, Kudlai O, Pan oja C, Yako le a G, Lebede a, D (2022) Ano he plea o ‘bes p ac ice’
in molecula app oaches o ema ode sys ema ics: Diplos omum sp. clade Q iden i ied as Diplos o-
mum bae i Dubois, 1937 in Eu ope. Pa asi ology 149: 503–518. h ps://doi.o g/10.1017/
S0031182021002092
Fobe E, Fox MG, Ridgway M, Copp GH (2011) Hea ed compe i ion: How clima e change
will a ec non-na i e pumpkinseed Lepomis gibbosus and na i e pe ch Pe ca lu ia ilis in e ac-
ions in he UK. Jou nal o Fish Biology 79(6): 1592–1607. h ps://doi.o g/10.1111/j.1095-
8649.2011.03083.x
F anco á K, Ond ačko á M, Polačik M, Ju ajda P (2011) Pa asi e auna o na i e and non-na i e
popula ions o Neogobius melanos omus (Pallas, 1814) (Gobiidae) in he longi udinal p o ile o he
167
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Danube Ri e . Jou nal o Applied Ich hyology 27(3): 879–886. h ps://doi.o g/10.1111/j.1439-
0426.2010.01582.x
Galli P, S e ani F, Benzoni F, Zullini A (2005) In oduc ion o alien hos –pa asi e complexes in a
na u al en i onmen and he symbio a concep . Hyd obiologia 548(1): 293–299. h ps://doi.
o g/10.1007/s10750-005-3645-0
Gend on AD, Ma cogliese DJ (2017) Enigma ic decline o a common ish pa asi e (Diplos omum
spp.) in he S . Law ence Ri e : E idence o a dilu ion e ec induced by he in asi e ound
goby. In e na ional Jou nal o Pa asi ology. Pa asi es and Wildli e 6(3): 402–411. h ps://doi.
o g/10.1016/j.ijppaw.2017.04.002
Gend on AD, Ma cogliese DJ, Thomas M (2012) In asi e species a e less pa asi ized han na i e
compe i o s, bu o how long? The case o he ound goby in he G ea Lakes-S . Law ence Basin.
Biological In asions 14(2): 367–384. h ps://doi.o g/10.1007/s10530-011-0083-y
Geo gie B, Bise ko V, Geno T (1986) In o o s aining me hod o ces odes wi h i on ace oca -
mine. Helmin hologia 23: 279–281. [Co pus ID: 90795915]
Gozlan RE, B i on JR, Cowx I, Copp GH (2010) Cu en knowledge on non-na i e eshwa e
ish in oduc ions. Jou nal o Fish Biology 76(4): 751–786. h ps://doi.o g/10.1111/j.1095-
8649.2010.02566.x
Halme oja A, Val onen ET, Koskenniemi E (2000) Pe ch (Pe ca lu ia ilis L.) pa asi es e lec ecosys-
em condi ions: A compa ison o a na u al lake and wo acidic ese oi s in Finland. In e na ional
Jou nal o Pa asi ology 30(14): 1437–1444. h ps://doi.o g/10.1016/S0020-7519(00)00115-6
Hamme Ø, Ha pe DAT, Ryan PD (2001) PAST: Paleon ological s a is ics so wa e package o
educa ion and da a analysis. Palaeon ologia Elec onica 4(1): 1–9. h p://palaeo-elec onica.
o g/2001_1/pas /issue1_01.h m
Ha el JE, Ko alenko KE, Thomaz SM, Amal i ano S, Ka s LB (2015) Aqua ic in asi e species:
Challenges o he u u e. Hyd obiologia 750(1): 147–170. h ps://doi.o g/10.1007/s10750-
014-2166-0
Hnilička M, Janáč M, Palupo á E, Tkachenko M, Ho ká P, Jando á K, Holubo á K, Ju ajda P,
Ond ačko á M (2024) S able iso ope analysis e eals ish ju eniles as a empo al main e-
sou ce consumed by in asi e pumpkinseed (Lepomis gibbosus). Hyd obiologia 852: 2409–2426.
h ps://doi.o g/10.1007/s10750-024-05658-4
Ho man GL (1999) Pa asi es o No h Ame ican eshwa e ishes. Co nell Uni e si y P ess, I haca.
h ps://doi.o g/10.7591/9781501735059
Hohenadle MAA, Honka KI, Emde S, Klimpel S, Su es B (2018) Fi s e idence o a possible
in asional mel down among in asi e ish pa asi es. Scien i ic Repo s 8(1): 15085. h ps://doi.
o g/10.1038/s41598-018-33445-4
Hohenadle MAA, Nache M, F eese M, Pohlmann JD, Hanel R, Su es B (2019) How Pon o-Cas-
pian in ade s a ec local pa asi e communi ies o na i e ish. Pa asi ology Resea ch 118(9):
2543–2555. h ps://doi.o g/10.1007/s00436-019-06399-3
Hube V, Geis J (2019) Rep oduc ion success o he in asi e Sinanodon a woodiana (Lea 1834) in e-
la ion o na i e mussel species. Biological In asions 21(11): 3451–3465. h ps://doi.o g/10.1007/
s10530-019-02060-3
Hulme PE (2009) T ade, anspo and ouble: Managing in asi e species pa hways in an e a
o globaliza ion. Jou nal o Applied Ecology 46(1): 10–18. h ps://doi.o g/10.1111/j.1365-
2664.2008.01600.x
Innal D, S a escu-Bedi an MM (2022) A e iew o cu en knowledge on pa asi es o nonindig-
enous ish species in he inland wa e s o Tü kiye. T ansyl anian Re iew o Sys ema ical and
Ecological Resea ch 24(1): 55–74. h ps://doi.o g/10.2478/ se -2022-0004
Keane RM, C awley MJ (2002) Exo ic plan in asions and he enemy elease hypo hesis. T ends
Ecology and E olu ion 17(4): 164–170. h ps://doi.o g/10.1016/S0169-5347(02)02499-0
168
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Keesing F, Hol RD, Os eld RS (2006) E ec s o species di e si y on disease isk. Ecology Le e s
9(4): 485–498. h ps://doi.o g/10.1111/j.1461-0248.2006.00885.x
Kelly DW, Pa e son RA, Townsend CR, Poulin R, Tompkins DM (2009) Pa asi e spillback: A neglec -
ed concep in in asion ecology? Ecology 90(8): 2047–2056. h ps://doi.o g/10.1890/08-1085.1
Kennedy CR (2001) In e speci ic in e ac ions be ween la al digeneans in he eyes o pe ch, Pe ca
lu ia ilis. Pa asi ology 122(S1): S13–S22. h ps://doi.o g/10.1017/S0031182000016851
Kołodziej-Sobocińska M, B zeziński M, Niemczynowicz A, Zalewski A (2018) High pa asi e in ec-
ion le el in non-na i e in asi e species: I is jus a ma e o ime. Ecog aphy 41(8): 1283–1294.
h ps://doi.o g/10.1111/ecog.03362
Konečný A, Popa OP, Ba áko á V, Douda K, B yja J, Smi h C, Popa LO, Reicha d M (2018) Mod-
elling he in asion his o y o Sinanodon a woodiana in Eu ope: T acking he ou es o a seden-
a y aqua ic in ade wi h mobile pa asi ic la ae. E olu iona y Applica ions 11(10): 1975–1989.
h ps://doi.o g/10.1111/e a.12700
Kuzmano a D, Chunchuko a M, Ki in M (2019) Helmin hs and helmin h communi ies o pe ch
(Pe ca lu ia ilis, Linnaeus, 1758) as bioindica o s o ecosys em condi ion o he Ma i sa Ri e .
Scien i ic Pape s-Se ies D-Animal Science 62(1): 463–468. h ps:// esea ch.ebsco.com/c/ 27ojl/
iewe /pd / ng dm7q ? ou e=de ails
K ach Y, Mie zejewska K (2011) Non-indigenous ben hic ishes as new hos s o Bucephalus poly-
mo phus Bae , 1827 (Digenea: Bucephalidae) in he Vis ula Ri e basin, Poland. Knowledge and
Managemen o Aqua ic Ecosys ems 400(400): 2. h ps://doi.o g/10.1051/kmae/2010034
K ach Y, Ond ačko á M, Janáč M, Ju ajda P (2016) Me hodological issues a ec ing he s udy o
ish pa asi es. I. Du a ion o li e ish s o age p io o dissec ion. Diseases o Aqua ic O ganisms
119(2): 107–115. h ps://doi.o g/10.3354/dao02990
K ach Y, Ju ajda P, B yjo á A, T ichko a T, Ribei o F, Přik ylo á I, Ond ačko á M (2017) Eu opean
dis ibu ion o me ace ca iae o he No h Ame ican digenean Pos hodiplos omum c . minimum
cen a chi (S igei o mes: Diplos omidae). Pa asi ology In e na ional 66: 635–642. h ps://doi.
o g/10.1016/j.pa in .2017.06.003
K ach Y, Tkachenko M, Ba áko á V, Zięba G, Ond ačko á M (2021a) The ole o he non-in-
digenous pumpkinseed Lepomis gibbosus (Ac inop e ygii: Cen a chidae) in he li e cycle o Bo-
h iocephalus cla iceps (Ces oda: Bo h iocephalidae) in Eu ope. Pa asi ology Resea ch 120(9):
3163–3171. h ps://doi.o g/10.1007/s00436-021-07268-8
K ach Y, Tkachenko M, Sei e o á M, Ond ačko á M (2021b) Insigh s in o he di e si y, dis ibu-
ion and phylogeny o h ee e gasilid copepods (Hexanauplia: E gasilidae) in len ic wa e bodies
o he Mo a a i e basin, Czech Republic. Limnologica 91: 125922. h ps://doi.o g/10.1016/j.
limno.2021.125922
K ach Y, Tkachenko M, Ba áko á V, Ku sokon Y, Janáč M, Demchenko V, Ond ačko á M (2023)
Pa asi e communi ies and gene ic s uc u e o non-na i e pumpkinseed, Lepomis gibbosus, in
di e en Black Sea d ainages o Uk aine. Knowledge and Managemen o Aqua ic Ecosys ems
424(424): 1. h ps://doi.o g/10.1051/kmae/2022023
K ach Y, Tkachenko M, Gianne o D, Míč R, Ba áko á V, Ağdama S, Saç G, Özuluğ M, Ta kan AS,
Ond ačko á M (2024) Low gene ic and pa asi e di e si y o in asi e pumpkinseed Lepomis gibbosus
(Cen a chidae) expanding in Tü kiye. Di e si y 16(5): 272. h ps://doi.o g/10.3390/d16050272
Leunda PM (2010) Impac s o non-na i e ishes on Ibe ian eshwa e ich hyo auna: Cu en knowl-
edge and gaps. Aqua ic In asions 5(3): 239–262. h ps://doi.o g/10.3391/ai.2010.5.3.03
Loke ES, Ho kin BV (2015) Pa asi ology: A concep ual app oach. CRC P ess, 1–550. h ps://doi.
o g/10.1201/9780429258695
Lucký Z, Na á il S (1984) Pa asi ic diseases o he pe ch (Pe ca lu ia ilis) in de en ion ese oi s
o he Mo a a i e basin. Ac a Ve e ina ia B no 53(1–2): 81–90. h ps://doi.o g/10.2754/
a b198453010081
169
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Lymbe y AJ, Mo ine M, Kanani HG, Bea y SJ, Mo gan DL (2014) Co-in ade s: The e ec s o
alien pa asi es on na i e hos s. In e na ional Jou nal o Pa asi ology. Pa asi es and Wildli e 3(2):
171–177. h ps://doi.o g/10.1016/j.ijppaw.2014.04.002
Mack RN, Simbe lo D, Lonsdale WM, E ans H, Clou M, Bazzaz FA (2000) Bio ic in asions:
Causes, epidemiology, global consequences, and con ol. Ecological Applica ions 10(3): 689–710.
h ps://doi.o g/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
Magu an AE (2004) Measu ing Biological Di e si y. Blackwell Publishing, Ox o d, 1–256.
Malmbe g G (1970) The exc e o y sys ems and he ma ginal hooks as a basis o sys ema -
ics o Gy odac ylus (T ema oda, Monogenea). A ki ü Zoologie 23: 1–235. [Co pus ID:
53523534]
Masson G, Vanacke M, Fox MG, Beisel J-N (2015) Impac o he ces ode T iaenopho us nodulo-
sus on he exo ic Lepomis gibbosus and he au och honous Pe ca lu ia ilis. Pa asi ology 142(6):
745–755. h ps://doi.o g/10.1017/S0031182014001826
Mo a ec F (2001) Checklis o he me azoan pa asi es o ishes o he Czech Republic and he Slo ak
Republic. P ague. Academia (Ca acas): 1–169.
Mo a ec F (2013) Pa asi ic nema odes o eshwa e ishes o Eu ope, Re ised 2nd edn. Academia,
P ague, 1–601.
Mo ozińska-Gogol J (2013) Pa asi e communi ies o Eu opean pe ch, Pe ca lu ia ilis L. (Ac inop e-
ygii: Pe ci o mes: Pe cidae) om lake Łebsko (Cen al Coas , Poland). Annals o Pa asi ology
59(2): 89–98.
Moszczynska A, Locke S, McLaughlin JD, Ma cogliese D, C ease T (2009) De elopmen o p ime s
o he mi ochond ial cy och ome c oxidase I gene in digene ic ema odes (Pla yhelmin hes)
illus a es he challenge o ba coding pa asi ic helmin hs. Molecula Ecology Resou ces 9(s1):
75–82. h ps://doi.o g/10.1111/j.1755-0998.2009.02634.x
Mühlegge JM, Ji sa F, Konecny R, Sa mann H, F ank C (2012) Bucephalus polymo phus Bae ,
1827-a new ish pa asi e in Aus ia? Wiene Klinische Wochensch i 121(S3): 50–52.
h ps://doi.o g/10.1007/s00508-009-1236-1
Oksanen J, Simpson G, Blanche F, Kind R, Legend e P, Minchin P, O’Ha a R, Solymos P, S e ens
M, Szoecs E, Wagne H, Ba bou M, Bedwa d M, Bolke B, Bo ca d D, Ca alho G, Chi ico M,
De Cace es M, Du and S, E angelis a H, Fi zJohn R, F iendly M, Fu neaux B, Hannigan G, Hill
M, Lah i L, McGlinn D, Ouelle e M, Ribei o Cunha E, Smi h T, S ie A, Te B aak C, Weedon
J (2022) egan: Communi y Ecology Package. R package e sion 2.6-4. h ps://CRAN.R-p ojec .
o g/package= egan
Ond ačko á M, Hudco á I, Dá ido á M, Adámek Z, Kašný M, Ju ajda P (2015a) Non-na i e gobies
acili a e he ansmission o Bucephalus polymo phus (T ema oda). Pa asi es & Vec o s 8(1): 382.
h ps://doi.o g/10.1186/s13071-015-0999-7
Ond ačko á M, Valo á Z, Hudco á I, Michálko á V, Šimko á A, Bo che ding J, Ju ajda P (2015b)
Tempo al e ec s on hos -pa asi e associa ions in ou na u alized goby species li ing in sympa y.
Hyd obiologia 746(1): 233–243. h ps://doi.o g/10.1007/s10750-014-1967-5
Ond ačko á M, K ach Y, Ma ens A, Ju ajda P (2019a) Limi ed pa asi e acquisi ion by non-na i e
Lepomis gibbosus (Ac inop e ygii: Cen a chidae) a wo ponds in he Uppe Rhine basin, Ge ma-
ny. Jou nal o Helmin hology 93(4): 453–460. h ps://doi.o g/10.1017/S0022149X18000469
Ond ačko á M, Vše ičko á L, Adámek Z, Kopeček L, Ju ajda P (2019b) Ecological plas ici y o
ubenose goby, a small in ade in Sou h Mo a ian wa e s. Hyd obiologia 829(1): 217–235.
h ps://doi.o g/10.1007/s10750-018-3833-3
Ond ačko á M, Ba áko á V, K ach Y, B yjo á A, T ichko a T, Ribei o F, Ca assou L, Ma ens
A, Masson G, Zechmeis e T, Ju ajda P (2021a) Pa asi e in ec ion e lec s hos gene ic di e -
si y among non-na i e popula ions o pumpkinseed sun ish in Eu ope. Hyd obiologia 848(9):
2169–2187. h ps://doi.o g/10.1007/s10750-020-04410-y
170
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
Ond ačko á M, Janáč M, Bo che ding J, G abowska J, Ba áko á V, Ju ajda P (2021b) Non-na i e
gobies sha e p edominan ly imma u e pa asi es wi h local ish hos s. Jou nal o Ve eb a e Biology
70(4): 21050. h ps://doi.o g/10.25225/j b.21050
Ond ačko á M, Tkachenko M, Ba áko á V, B yjo á A, Janáč M, Zięba G, Py zanowski K, K ach
Y (2023) Popula ion gene ic s uc u e, pa asi e in ec ion and soma ic condi ion o pumpkinseed
Lepomis gibbosus (Ac inop e ygii: Cen a chidae) in he Ode i e basin. Jou nal o Fish Biology
102(2): 426–442. h ps://doi.o g/10.1111/j b.15273
Ond ačko á M, Tkachenko MY, Ve ešník L, H onek J, Janáč M (2025) Dis ibu ion and hos ange
o a highly in asi e pa asi ic copepod Neoe gasilus japonicus (Ha ada, 1930). Hyd obiologia 852:
2221–2239. h ps://doi.o g/10.1007/s10750-024-05577-4
Piasecki W, Falandysz M (1994) P elimina y su ey on pa asi e auna o pumpkinseed sun ish. Ac a
Ich hyologica e Pisca o ia 24(1): 87–100. h ps://doi.o g/10.3750/AIP1994.24.1.07
Poulin R (2008) E olu iona y Ecology o Pa asi es. P ince on Uni e si y P ess, New Yo k, 1–360.
h ps://doi.o g/10.1515/9781400840809
Poulin R, Mouillo D (2003) Pa asi e specializa ion om a phylogene ic pe spec i e: A new index
o hos speci ici y. Pa asi ology 126(5): 473–480. h ps://doi.o g/10.1017/S0031182003002993
P en e J, MacNeil C, Dick JTA, Dunn AM (2004) Roles o pa asi es in animal in asions. T ends in
Ecology & E olu ion 19(7): 385–390. h ps://doi.o g/10.1016/j. ee.2004.05.002
R Co e Team (2023) R: A Language and En i onmen o S a is ical Compu ing. R Founda ion o
S a is ical Compu ing, Vienna, Aus ia. h ps://www.R-p ojec .o g/
Runciman JB, Lea BR (2009) A e iew o yellow pe ch (Pe ca la escens), mallmou h bass (Mic op-
e us dolomieu), la gemou h bass (Mic op e us salmoides), pumpkinseed (Lepomis gibbosus), wall-
eye (Sande i eus) and no he n pike (Esox lucius) dis ibu ions in B i ish Columbia. Canadian
Manusc ip Repo o Fishe ies and Aqua ic Sciences No. 2882. Fishe ies and Oceans Canada
Science B anch, Paci ic Region Paci ic Biological S a ion, Nanaimo, 1–141. h ps://publica ions.
gc.ca/collec ions/collec ion_2010/mpo-d o/Fs97-4-2882-eng.pd
Sasal P, Mo and S, Guégan JF (1997) De e minan s o pa asi e species ichness in Medi e anean
ma ine ish. Ma ine Ecology P og ess Se ies 149: 61–71. h ps://doi.o g/10.3354/meps149061
Sco WB, C ossman EJ (1973) F eshwa e ishes o Canada. Bulle in - Fishe ies Resea ch Boa d o
Canada 184: 1–966. h ps://publica ions.gc.ca/si e/eng/9.870340/publica ion.h ml
Shche bukha AY (1993) On he ela ionships be ween ossil and ecen axa o he genus Pe ca
(Os eich hyes, Pe cidae). Ves nik Zoologii 4: 39–40. [In Russian]
Shuke o a S, Ki in D, Hanzelo á V (2010) Endohelmin h communi ies o he pe ch, Pe ca lu i-
a ilis (Pe ci o mes, Pe cidae) om S eba na Biosphe e Rese e, Bulga ia. Helmin hologia 47(2):
99–104. h ps://doi.o g/10.2478/s11687-010-0016-9
Simbe lo D, on Holle B (1999) Posi i e in e ac ions o nonindigenous species: In asional mel -
down? Biological In asions 1(1): 21–32. h ps://doi.o g/10.1023/A:1010086329619
Šimko á A, Na á ilo á P, Dá ido á M, Ond ačko á M, Sinama M, Chappaz R, Gilles A, Cos edoa
C (2012) Does in asi e Chond os oma nasus shi he pa asi e communi y s uc u e o endem-
ic Pa achond os oma oxos oma in sympa ic zones? Pa asi es & Vec o s 5(1): 200. h ps://doi.
o g/10.1186/1756-3305-5-200
Šlapanský L, Ju ajda P, Janáč M (2016) Ea ly li e s ages o exo ic gobiids as new hos s o unionid
glochidia. F eshwa e Biology 61(6): 979–990. h ps://doi.o g/10.1111/ wb.12761
Sobecka E, Słomińska M (2007) Species ichness, di e si y and speci ici y o he pa asi es o b eam
Ab amis b ama (L.) and pe ch Pe ca lu ia ilis L. in he es ua y o he Od a Ri e , Poland.
Helmin hologia 44(4): 188–192. h ps://doi.o g/10.2478/s11687-007-0030-8
Soes DM, Cooke SJ, an Klee HH, B oeckx PB, Veen lie P (2011) A isk analysis o sun ishes
(Cen a chidae) and pygmy sun ishes (Elassoma idae) in he Ne he lands. Final epo . Bu eau
Waa denbu g B , Culembo g, 1–110.
171
NeoBio a 102: 151–171 (2025), DOI: 10.3897/neobio a.102.148301
Ma ia Yu. Tkachenko e al.: Shi in pa asi e load in na i e and non-na i e Eupe ca ian ish
S epien CA, Haponski AE (2015) Taxonomy, dis ibu ion, and e olu ion o he Pe cidae. In: Biology and
cul u e o Pe cid ishes. Sp inge , Ne he lands, 3–60. h ps://doi.o g/10.1007/978-94-017-7227-3_1
S oyano B, Mu a chie Y, Panko P, Geo gie BB (2017a) Helmin h pa asi es in he alien Lepomis
gibbosus (L.) (Cen a chidae) om he Lake A anaso sko we lands, Bulga ia: Su ey o species and
s uc u e o helmin h communi ies. Ac a Zoologica Bulga ica 69(4): 555–574.
S oyano B, Geo gie a S, Panko P, Kudlai O, Kos adino a A, Geo gie BB (2017b) Mo phology
and molecules e eal he alien Pos hodiplos omum cen a chi Ho man, 1958 as he hi d species o
Pos hodiplos omum Dubois, 1936 (Digenea: Diplos omidae) in Eu ope. Sys ema ic Pa asi ology
94(1): 1–20. h ps://doi.o g/10.1007/s11230-016-9680-6
Suda iko VE, Shigin AA, Ku ochkin YuV, Lomakin VV, S enko RP, Yu lo a NI (2002) Me ace ca i-
ae o ema odes pa asi es o eshwa e hyd obion s in Cen al Russia. Nauka, Moscow, 1–298.
[In Russian]
Sun J, Ha ey HH (1986) Popula ion dynamics o yellow pe ch (Pe ca la escens) and pumpkinseed
(Lepomis gibbosus) in wo acid-s essed lakes. Wa e , Ai , and Soil Pollu ion 30(3–4): 611–617.
h ps://doi.o g/10.1007/BF00303324
Su ha J, Unge P, Palm HW (2022) Fish pa asi e communi y o h ee lakes wi h di e en o-
phic s a us in Mecklenbu g-Wes e n Pome ania, Ge many. Ac a Pa asi ologica 67(1): 340–350.
h ps://doi.o g/10.1007/s11686-021-00465-6
Székely C (1994) Pa a enic hos s o he pa asi ic nema ode Anguillicola c assus in Lake Bala on,
Hunga y. Diseases o Aqua ic O ganisms 18: 11–20. h ps://doi.o g/10.3354/dao018011
Ta aschewski H (2006) Hos s and pa asi es as aliens. Jou nal o Helmin hology 80(2): 99–128.
h ps://doi.o g/10.1079/JOH2006364
Thomas K, Olle ie F (1992) Pa a enic hos s o he swimbladde nema ode Anguillicola c assus.
Diseases o Aqua ic O ganisms 13: 165–174. h ps://doi.o g/10.3354/dao013165
Tompkins DM, Whi e AR, Boo s M (2003) Ecological eplacemen o na i e ed squi els by
in asi e g eys d i en by disease. Ecology Le e s 6(3): 189–196. h ps://doi.o g/10.1046/j.1461-
0248.2003.00417.x
To chin ME, La e y KD, Dobson AP, McKenzie VJ, Ku is AM (2003) In oduced species and hei
missing pa asi es. Na u e 421(6923): 628–629. h ps://doi.o g/10.1038/na u e01346
Val onen ET, Holmes JC, A onen J, Rau alah i I (2003) Pa asi e communi ies as indica o s o e-
co e y om pollu ion: Pa asi es o oach (Ru ilus u ilus) and pe ch (Pe ca lu ia ilis) in Cen al
Finland. Pa asi ology 126(7): S43–S52. h ps://doi.o g/10.1017/S0031182003003494
Venables WN, Ripley BD (2002) Mode n Applied S a is ics wi h S. Fou h Edi ion. Sp inge , New
Yo k. h ps://doi.o g/10.1007/978-0-387-21706-2
Vi ule JRS, F ei e CA, Simbe lo D (2009) In oduc ion o nonna i e eshwa e ish can ce ainly
be bad. Fish and Fishe ies 10(1): 98–108. h ps://doi.o g/10.1111/j.1467-2979.2008.00312.x
Vi as Muñoz JC, S aaks G, Knop K (2017) The eye luke Tylodelphys cla a a a ec s p ey de ec ion
and in aspeci ic compe i ion o Eu opean pe ch (Pe ca lu ia ilis). Pa asi ology Resea ch 116(9):
2561–2567. h ps://doi.o g/10.1007/s00436-017-5564-1
Wielgoss S, Ta aschewski H, Meye A, Wi h T (2008) Popula ion s uc u e o he pa asi ic nem-
a ode Anguillicola c assus, an in ade o declining No h A lan ic eel s ocks. Molecula Ecology
17(15): 3478–3495. h ps://doi.o g/10.1111/j.1365-294X.2008.03855.x
Wie zbicka J, Wie zbicki K, Piasecki W, Smie ana P (2005) A compa a i e s udy on he pa asi e
auna o pe ch, Pe ca lu ia ilis L., collec ed om a eshwa e coas al lake b ackish-wa e Bal ic
Sea and he in e connec ing canal. Wiadomosci Pa azy ologiczne 51(4): 295–302.
WoRMS (2025) Wo ld Regis e o Ma ine Species. h ps://www.ma inespecies.o g a VLIZ.
h ps://doi.o g/10.14284/170 [Accessed 2025-01-21]
Zeileis A, Ho ho n T (2002) Diagnos ic Checking in Reg ession Rela ionships. R News 2(3): 7–10.
h ps://CRAN.R-p ojec .o g/doc/Rnews/
