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Spa io empo al and gende -speci ic pa asi ism in wo species o gobiid ish
© 2018 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Published e sion
Ka onen, Anssi; Linds öm, Kai
Ka onen, A., & Linds öm, K. (2018). Spa io empo al and gende -speci ic pa asi ism in wo
species o gobiid ish. Ecology and E olu ion, 8(12), 6114-6123.
h ps://doi.o g/10.1002/ece3.4151
2018
6114
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Ecology and E olu ion. 2018;8:6114–6123.
www.ecole ol.o g
1 | INTRODUCTION
Pa asi ism is a po en sou ce o selec ion in na u al hos popula ions
and has ecen ly been sugges ed o play a ole in p ocesses such
as main enance o sexual ep oduc ion (Jokela, Dybdahl, & Li ely,
2009; King, Delph, Jokela, & Li ely, 2009) and di e gence o hos
popula ions (Eizagui e, Lenz, Kalbe, & Milinski, 2012; Ka onen &
Seehausen, 2012). Indeed, se e al pa asi e axa impai hos condi ion
h ough deple ion o esou ces, issue damage, and manipula ion o
hos beha io (Ba be , Hoa e, & K ause, 2000; Ba be & S ensson,
2003; Ha e & Milinski, 2016; Jokela, Taskinen, Mu ikainen, & Kopp,
2005; Ka onen, Seppälä, & Val onen 2004a; Moo e, 2002; Seppälä,
Lilje oos, Ka onen, & Jokela, 2008) and hus ha e se e e implica-
ions o hos i ness. The isk o pa asi ism is o en s uc u ed bo h
spa ially and empo ally because o spa ial agg ega ion o in ec ed
indi iduals and pa asi e in e media e hos s (Bye s, Blakeslee, Linde ,
Coope , & Magui e, 2008; Fal ýnko á, Val onen, & Ka onen, 2008;
Jokela & Li ely, 1995; Ka onen, Cheng, & Val onen, 2005), and
Recei ed: 5 Feb ua y 2018
|
Re ised: 3 Ap il 2018
|
Accep ed: 9 Ap il 2018
DOI: 10.1002/ece3.4151
ORIGINAL RESEARCH
Spa io empo al and gende - speci ic pa asi ism in wo species
o gobiid ish
Anssi Ka onen1 | Kai Linds öm2
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s use, dis ibu ion and ep oduc ion in any medium,
p o ided he o iginal wo k is p ope ly ci ed.
© 2018 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
1Uni e si y o Jy askyla, Depa men o
Biological and En i onmen al Science,
Jy askyla, Finland
2Åbo Akademi Uni e si y En i onmen al and
Ma ine Biology, Tu ku, Finland
Co espondence
Anssi Ka onen, Depa men o Biological
and En i onmen al Science, Uni e si y o
Jy askyla, Jy askyla, Finland.
Email: anssi. [email p o ec ed]
Funding in o ma ion
The s udy was suppo ed by he Academy
o Finland (g an s #292736 and #310632
o AK).
Abs ac
Pa asi ism is conside ed a majo selec i e o ce in na u al hos popula ions. In ec ions
can dec ease hos condi ion and igou , and po en ially in luence, o example, hos
popula ion dynamics and beha io such as ma e choice. We s udied pa asi e in ec-
ions o wo common ma ine ish species, he sand goby (Poma oschis us minu us) and
he common goby (Poma oschis us mic ops), in he b ackish wa e No he n Bal ic
Sea. We we e pa icula ly in e es ed in he occu ence o pa asi e axa loca ed in
cen al senso y o gans, such as eyes, po en ially a ec ing ish beha io and ma e
choice. We ound ha bo h ish species ha bo ed pa asi e communi ies domina ed
by axa ansmi ed o ish h ough aqua ic in e eb a es. In ec ions also showed
signi ican spa io empo al a ia ion. T ema odes in he eyes we e e y ew in some
loca ions, bu in ec ion le els we e highe among emales han males, sugges ing di -
e ences in exposu e o esis ance be ween he sexes. To es be ween hese hy-
po heses, we expe imen ally exposed male and emale sand gobies o in ec ion wi h
he eye luke Diplos omum pseudospa haceum. These ials showed ha he ish be-
came eadily in ec ed and emales had highe pa asi e numbe s, suppo ing highe
suscep ibili y o emales. Eye luke in ec ions also caused high ca a ac in ensi ies
among he ish in he wild. Ou esul s demons a e he po en ial o hese pa asi es
o in luence hos condi ion and isual abili ies, which may ha e signi ican implica-
ions o su i al and ma e choice in goby popula ions.
KEYWORDS
hos –pa asi e in e ac ion, ma e choice, pa asi e communi y, sexual selec ion, i ulence
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KARVONEN ANd LINdSTRÖM
seasonal changes in elease o pa asi e in ec i e s ages (Ka onen,
Seppälä, & Val onen 2004b; Taskinen, Val onen, & Mäkelä, 1994).
Consequen ly, he impac o pa asi es can also a y among hos
popula ions and, i pe sis en , such di e ences can po en ially c e-
a e di e en selec ion p essu es o hos indi iduals li ing in hese
popula ions (Ka onen & Seehausen, 2012).
Se e al hos species o pa asi es exp ess seconda y sexual
cha ac e is ics h ough which hey can ad e ise hei igou , as
well as esis ance o pa asi es (Hamil on & Zuk, 1982). O en hese
signals a e isually pe cei ed o namen s such as long ails o b igh
colo a ion, and commonly displayed by males. Fo example, he
connec ion be ween he exp ession o sexual o namen s and pa a-
si ism has been demons a ed in many species o bi ds (Hõ ak, O s,
Vellau, Spo iswoode, & Pape Mølle , 2001; McG aw & Hill, 2000;
Thompson, Hillga h, Leu, & McClu e, 1997) and ish (Ba be , A no ,
B ai hwai e, And ew, & Hun ing o d, 2001; Houde & To io, 1992;
Maan, an de Spoel, Jimenez, an Alphen, & Seehausen, 2006).
O e all, cu en e idence s ongly sugges s ha male sexual o na-
men s could signal esis ance o pa asi ism. Howe e , educ ion in
hos ision could impai he abili y o indi iduals o pe cei e sexual
signals. Fo example, i has been shown in cichlid ishes ha isually
pe cei ed sexual signals ad e ised h ough male colo a ion can be
blu ed because o inc eased wa e u bidi y, esul ing in hyb id-
iza ion o species ollowing he elaxa ion o colo - based sexual se-
lec ion (Seehausen, an Alphen, & Wi e, 1997). Simila ly, pa asi es
ound in he key senso y o gans, such as he eyes, could impai hos
ision and he abili y o pe cei e isual cues om po en ial ma es
(Ka onen & Seehausen, 2012). In species whe e sexual selec ion
is based on males displaying seconda y sexual cha ac e is ics, he
abili y o emales o judge male quali y when in ec ed wi h such
pa asi es could be comp omised. Howe e , while ma ing decisions
a e known o be in luenced by gene al condi ion (Co on, Small,
& Pomiankowski, 2006) and also pa asi e in ec ions (Lopez, 1999;
Mazzi, 2004; P ennig & Tinsley, 2002; Poulin & Vicke y, 1996) o he
choosie sex, he po en ial o pa asi es di ec ly in e e ing wi h sex-
ual selec ion ope a ing h ough isual signals pe cei ed by emales
has emained i ually unexplo ed. He e, we explo e pa asi ism and
pa icula ly he in ec ions in he eyes o gobiid ishes whe e emales
ac i ely choose males based on seconda y sexual cha ac e is ics.
Gobies (Gobiidae) a e abundan ish species li ing in ma ine and
b ackish wa e habi a s a ound he wo ld. Fi e species o gobies in-
habi he Bal ic Sea, wo o which, he sand goby (Poma oschis us
minu us, Pallas 1770) and he common goby (Poma oschis us mic ops,
K øye 1838), a e he mos common. Du ing he ep oduc i e pe-
iod in ea ly summe , males build nes s whe e hey a ac emales o
spawn using seconda y sexual ai s. In he sand goby, o ins ance,
hese include a b igh blue spo on he i s do sal in and he size o
he in i sel , as well as speci ic cou ship beha io (Fo sg en, 1992;
Linds öm, S . Ma y, & Pampoulie, 2006). Also, he size o he nes
is one o he key de e minan s o ep oduc i e success o a male
because he mos ecund emales canno lay all hei eggs in small
nes s (Linds öm, 1992). All hese cha ac e is ics o male quali y a e
pe cei ed isually by emales.
P e ious s udies ha e shown ha gobies also ha bo a di e se
pa asi e auna. Fo example, Bal ic gobies can hos ou o 22 spe-
cies o pa asi es depending on he hos species and sampling ime
(Zande , 2003). Fu he , Zande (2005) epo ed ha he pa asi e
communi ies we e o en mos di e se in au umn wi h e y ew spe-
cies p esen in he sp ing. S udies ha e also epo ed highe pa asi e
in ec ion among wild- caugh emale sand gobies compa ed o males
(Van Damme & Olle ie , 1994), sugges ing highe exposu e and/o
suscep ibili y o emales. Finally, beha io al ials ha e shown ha
in ec ion o male sand gobies wi h mac opa asi es in he body ca i y
and on he ins and skin did no a ec male dominance o emale
ma e choice (Ba be , 2002). Howe e , Ba be (2002) also ound ha
in ec ion in ensi y o Gy odac ylus monogeneans had a nega i e e -
ec on he de elopmen o he do sal in size, a po en ial seconda y
sexual ai o he sand goby.
We explo ed pa asi e in ec ions o he sand goby and he com-
mon goby in he Bal ic Sea by conduc ing a eplica ed sampling cam-
paign o male and emale ish o cap u e spa io empo al a ia ion
and possible gende di e ences in pa asi ism. We we e pa icula ly
in e es ed in a ia ion in in ec ion o pa asi es inhabi ing senso y
o gans o ish ha could show he po en ial o pa asi e- induced
changes in condi ions o sexual selec ion and ma e choice among
he sampling loca ions. Simila ly, in ec ions could in luence o e -
win e su i al o he ish and esul in lowe in ec ion le els in he
ea ly summe . Fu he mo e, o explain pa e ns o in ec ion o he
pa asi es in he wild, we exposed male and emale sand gobies o
con olled expe imen al in ec ion om ema ode eye lukes in he
labo a o y. Di e ences in he abundance o hese pa asi es be ween
male and emale ish unde simila le el o exposu e would be consis-
en wi h he idea o di e ences in suscep ibili y be ween he sexes.
2 | MATERIALS AND METHODS
2.1 | Sampling o gobies
Sand gobies and common gobies we e sampled om h ee loca-
ions in he p oximi y o he T ä minne Zoological s a ion, sou he n
Finland. The i s loca ion was nex o he s a ion ( e e ed he e o as
“S a ion”; 59°50′41″N, 23°14′58″E), he second ca. 500 m om he
S a ion (Långholmen; 59°50′48″N, 23°15′12″E), and he hi d a -
he ou o he sea ca. 4 km om he S a ion (Va gskä ; 59°49′24″N,
23°08′38″E). All loca ions had a bo om subs a e o sand o so
mud wi h li le o no ege a ion. Sampling was conduc ed h ee
imes, June 2014, June 2015, and Oc obe 2015, o cap u e bo h
spa ial and empo al a ia ion in in ec ions. A each loca ion, gobies
we e caugh om a dep h o 0.5–1 m using a seine ne . Howe e ,
sampling campaigns a some o he loca ions we e unsuccess ul a
imes (Table 1) due o comple e absence o ish. Fish we e b ough
ali e o he labo a o y, eu hanized, sexed, measu ed o leng h
(mm), and inspec ed esh o in ec ions on ins ( igh pec o al in),
gills, eyes, and in e nal o gans unde a mic oscope. Pa asi es we e
iden i ied a genus o species le el when possible. P e alence (p o-
po ion o ish in ec ed, %) and mean abundance (mean pa asi e
6116
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KARVONEN ANd LINdSTRÖM
TABLE1 P e alence (% ish in ec ed) and mean abundance (numbe o pa asi es pe ish ± SE) o he pa asi e axa de ec ed in sand gobies cap u ed om h ee loca ions in he No he n
Bal ic Sea in June 2014–Oc obe 2015
Pa asi e
June 2014 June 2015 Oc obe 2015
S a ion
n = 29
Långholmen
n = 30
Va gskä
n = 31
S a ion
n = 30
Långholmen
n = 30
Va gskä
n = 30
S a ion
n = 0
Långholmen
n = 6
Va gskä
n = 14
T ichodina sp. 90
11.2 ± 3.4
86.7
2.9 ± 0.4
67.7
2.6 ± 0.9
96.7
24.6 ± 6.6
96.7
14.0 ± 2.8
66.7
5.6 ± 1.8
16.7
0.2 ± 0.2
57.1
1.7 ± 0.7
Gy odac ylus sp. 0.0 10
0.1 ± 0.1
0.0 10
0.1 ± 0.1
3.3
0.03 ± 0.03
10
0.1 ± 0.1
0.0 57.1
0.9 ± 0.4
Diplos omum spp. 0.0 6.7
0.07 ± 0.05
3.2
0.03 ± 0.03
26.7
0.4 ± 0.1
23.3
0.2 ± 0.1
30
0.4 ± 0.1
16.7
0.2 ± 0.2
78.6
2.8 ± 11.3
Diplos omum bae i 3.4
0.07 ± 0.07
0.0 0.0 6.7
0.07 ± 0.05
3.3
0.03 ± 0.03
0.0 0.0 21.4
0.4 ± 0.2
Apa emon sp. 31
0.4 ± 0.1
33.3
0.8 ± 0.3
9.7
0.1 ± 0.1
40
1.0 ± 0.3
30
0.5 ± 0.2
40
0.9 ± 0.3
16.7
0.2 ± 0.2
64.3
2.9 ± 1.6
C yp oco yle sp. 56
0.9 ± 0.2
80
2.9 ± 0.5
80.6
5.6 ± 1.0
50
1.2 ± 0.3
26.7
0.5 ± 0.2
70
6.2 ± 1.6
0.0 71.4
2.2 ± 0.5
Sphae os omum sp. 0.0 6.7
0.07 ± 0.05
0.0 0.0 0.0 0.0 0.0 0.0
P o eocephalus sp. 13.8
0.2 ± 0.1
13.3
0.1 ± 0.1
6.5
0.1 ± 0.1
3.3
0.03 ± 0.03
3.3
0.03 ± 0.03
3.3
0.03 ± 0.03
0.0 0.0
Camallanus lacus is 3.4
0.03 ± 0.03
3.3
0.07 ± 0.07
0.0 0.0 0.0 0.0 0.0 0.0
Uniden i ied nema ode 10.3
0.1 ± 0.1
16.7
0.2 ± 0.1
16.1
0.2 ± 0.1
6.7
0.07 ± 0.05
0.0 6.7
0.07 ± 0.05
0.0 7.1
0.07 ± 0.07
Echino hynchus gadii 6.9
0.1 ± 0.1
0.0 0.0 0.0 0.0 0.0 0.0 0.0
Neoechino hynchus u ili 6.9
0.07 ± 0.05
0.0 6.5
0.2 ± 0.1
0.0 6.7
0.1 ± 0.1
6.7
0.1 ± 0.1
0.0 0.0
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KARVONEN ANd LINdSTRÖM
numbe pe ish) we e calcula ed o each pa asi e axa. In addi ion,
ish eye lenses we e s udied be o e dissec ion o co e age o ca a-
ac s caused by Diplos omum spp. eye lukes using sli - lamp (Kowa
SL- 15) mic oscopy (Ka onen e al., 2004a). Ca a ac s we e sco ed
as 10%, 20%,…,100% co e age o he lens a ea, which co ela es
wi h he dele e ious e ec s o he pa asi es on ish (Ka onen &
Seppälä, 2008; Seppälä, Ka onen, & Val onen, 2005) and hus p o-
ides an indi ec measu e o pa asi e- induced e ec s on he hos .
Di e ences in o al pa asi e abundance be ween he loca ions and
sampling imes we e analyzed using GLMs wi h nega i e binomial
dis ibu ion and log link unc ion. Abundances o he pa asi e axa
T ichodina sp. and Gy odac ylus sp. (see Resul s) we e excluded om
he analyses as hey we e s udied only om one pec o al in.
2.2 | Expe imen al exposu e
Expe imen al exposu e o sand gobies (Figu e 1) was conduc ed in
h ee con aine s each wi h 6 l o wa e (16°C) aken om he Bal ic
Sea, con inuous ae a ion, and 10 ish ( i e emales and i e males)
cap u ed 1 week ea lie om he Va gskä sampling loca ion, o al-
ing 30 ish (mean leng h: 48.0 ± 2.0 mm [ emales], 53.5 ± 1.9 mm
[males]). Be o e he expe imen , he ish had been housed in ep-
lica ed la ge s ock aqua ia supplied wi h a con inuous low o esh
seawa e and ed wi h li e mysiid sh imp and ozen Chi onomidae
la ae ad libi um. In addi ion o he h ee exposu e con aine s, one
con aine wi h 10 ish and an e en sex a io se ed as he unexposed
con ol. This was used o eco d possible in ec ions esul ing om
pa asi e in ec i e s ages p esen in he wa e , i any, and hose ha
had aken place ecen ly in he wild be o e he ish we e caugh ,
which could no be sepa a ed om hose esul ing om he expe i-
men al exposu e (see below). Each o he h ee in ec ion con aine s
hen ecei ed a o al dose o 750 D. pseudospa haceum ce ca iae (75
ce ca iae pe ish) ha had been eleased by i e in ec ed Lymnaea
s agnalis snails collec ed om Lake Vuojä i, Cen al Finland. No e
ha he e is no de ec able popula ion gene ic s uc u e in hese
pa asi es ac oss Finland (Louhi, Ka onen, Rells ab, & Jokela, 2010),
which is why pa asi e o igin was unlikely o a ec he esul s. The
snails we e allowed o p oduce ce ca iae o 2 h in 2 dl o wa e
(20°C). Suspensions o he snails we e hen combined, and he ce -
ca ial densi y was es ima ed by aking en 1 ml samples. Wa e in
he con aine s was egula ly mixed du ing he i s hou o expo-
su e o ensu e equal exposu e o all indi iduals o he pa asi e. The
ish we e main ained in hese condi ions o 18 h , which is su i-
cien ime o he pa asi es o each he eye lenses in a small ish
(Louhi, Sundbe g, Jokela, & Ka onen, 2015). The e was no mo ali y
o ish du ing o a e he exposu e. All ish we e hen eu hanized
and s udied o he numbe o pa asi es in he eye lenses. Olde
in ec ions o igina ing om he wild and hose o igina ing om he
expe imen al exposu e could be dis inguished based on he size o
he pa asi e me ace ca iae. All expe imen al p ocedu es we e in ac-
co dance wi h he e hical s anda ds o he Finnish Regional S a e
Adminis a i e Agency and conduc ed unde license (License code:
ESAVI/4706/04.10.07/2015). Da a we e analyzed using ANCOVA
wi h ish sex as a ixed ac o and con aine as a andom ac o o
accoun o dependency among ish exposed in he same con aine .
Fish leng h was used as a co a ia e. All analyses we e conduc ed
using SPSS 24 s a is ical package.
3 | RESULTS
In o al, 12 pa asi e axa we e de ec ed among he 200 sand gobies
and 168 common gobies examined, including i e ema odes, wo
nema odes, wo acan hocephalans, one ces ode, one monogenean,
and one p o ozoan (Table 1, Table 2). All pa asi e axa we e obse ed
in bo h ish species, excep o he acan hocephalan Echino hynchus
gadii, which was obse ed only in he sand goby. The mean numbe
o pa asi e axa pe ish was signi ican ly highe in he sand goby
(2.23 ± 0.1, all numbe s indica e mean ± SE, ange 0–7) han in he
common goby (1.78 ± 0.1, ange 0–4) ( es : 354 = 3.76, p < .001;
loca ions and sampling imes combined). In bo h ish species, he
p o ozoan T ichodina sp. was he mos p e alen and abundan pa a-
si e axa wi h p e alence anging be ween 16.7% and 96.7% in he
sand goby and 0%–100% in he common goby, depending on he
loca ion and sampling ime (Table 1, Table 2). Among he mac opa a-
si es, ema odes C yp oco yle sp., Apa emon sp., and Diplos omum
spp. we e mos commonly obse ed. Mean o al pa asi e abun-
dance was signi ican ly highe in he common goby compa ed o
he sand goby (GLM: Wald = 11.76, p < .001; sampling loca ions
combined) while his depended on he sampling ime (Wald = 30.65,
p < .001 (sampling ime); Wald = 32.86, p < .001 (species × sampling
ime); Figu e 2). The e we e also signi ican di e ences in pa asi e
abundance among he loca ions so ha Långholmen and Va gskä
loca ions had he highes pa asi e abundances (GLM: Wald = 14.25,
p = .001; sampling imes combined) while his again depended on
he ish species (Wald = 28.01, p < .001 (species); Wald = 32.63,
p < .001 (species × sampling loca ion); Figu e 2).
To al pa asi e abundance was no di e en be ween males and e-
males in ei he ish species (Wald = 1.05, p = .305 (sex); Wald = 1.98,
p = .159 (species × sex); imma u e ish excluded, sampling loca ions
FIGURE1 Female sand gobies (Poma oschis us minu us).
Pho og aph by Kai Linds öm

6118
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KARVONEN ANd LINdSTRÖM
and sampling imes combined). Howe e , a mo e de ailed analysis
o he in ec ions o Diplos omum eye luke in Va gskä showed ha
emales ha bo ed signi ican ly highe abundances o hese pa asi es
compa ed o males (GLM: Wald = 4.94, p = .026 (sex); Wald = 30.64,
p < .001 (sampling ime); Figu e 3a). In ec ions o eye lukes also
caused signi ican ca a ac co e age in he eye lenses o sand go-
bies. Ca a ac co e age inc eased wi h pa asi e abundance so ha
he co e age apidly app oached 100% when he e was mo e han
one pa asi e pe lens. The ela ionship was cap u ed by a s eep as-
ymp o ic cu e (Figu e 4). Howe e , he e was no di e ence in ca -
a ac s caused by a gi en pa asi e abundance be ween he male and
emale sand gobies ( es on esidual ca a ac co e age om he
nonlinea eg ession: 36 = 0.228, p = .821). While his sugges s sim-
ila suscep ibili y o pa asi e- in lic ed damage be ween he sexes,
eyes o emale sand gobies in Va gskä ne e heless showed highe
a e age ca a ac s han males because o hei highe pa asi e abun-
dances ( es : 82 = 2.082, p = .040). No ca a ac s we e obse ed in
unin ec ed eye lenses.
Expe imen al exposu e o sand gobies om Va gskä o D. pseu-
dospa haceum in ec ion indica ed ha all ish became eadily in ec ed
wi h he pa asi e. The mean pa asi e abundance pe ish inc eased
wi h body size (ANCOVA: F1,23 = 15.60, p < .001) and anged om
43.0 ± 6.0 o 52.6 ± 5.8 depending on he con aine (F2,2.1 = 4.06,
FIGURE2 Es ima ed mean o al pa asi e abundance (±SE) in
sand gobies and common gobies cap u ed a h ee sampling imes
(a, sampling loca ions combined) and om h ee sampling loca ions
(b, sampling imes combined) in he No he n Bal ic Sea. Es ima es
a e om GLM models. Numbe s o ish s udied a e indica ed in
Table 1
0
5
10
15
20
25
June 2014 June 2015 Oc obe 2015
Numbe o pa asi es
Sampling ime
Sand goby Common goby
0
2
4
6
8
10
12
14
16
18
S a ion Långholmen Va gskä
Numbe o pa asi es
Sampling loca ion
Sand goby Common goby
(a)
(b)
FIGURE3 Mean abundance o Diplos omum spp. eye lukes
(±SE) in emale and male sand gobies cap u ed om Va gskä
a h ee sampling imes (a). Es ima ed mean abundance o
D. pseudospa haceum eye lukes (±SE) om he ANCOVA model
in emale and male sand gobies exposed o expe imen al pa asi e
in ec ion in h ee con aine s in he labo a o y (b)
0
1
2
3
4
5
6
7
8
June 2014 June 2015 Oc obe 2015
Numbe o pa asi es
Sampling ime
Females Males
0
10
20
30
40
50
60
70
80
123
Numbe o pa asi es
Con aine
FemalesMales
(a)
(b)
FIGURE4 Rela ionship be ween he abundance o
Diplos omum spp. eye lukes and he co e age o pa asi e-
induced ca a ac s in eye lenses o sand gobies (da a pooled
ac oss sampling loca ions and sampling imes). Black line
shows he i o he nonlinea eg ession model [ca a ac
co e age = 90.4 + −111.1*exp(−0.76*pa asi es), R2 = .41, F3,35 = 72.5,
p < .0001]
Numbe o pa asi es in he lens
121086420
Ca a ac co e age o he lens a ea (%
)
100
80
60
40
20
0
|
6119
KARVONEN ANd LINdSTRÖM
p = .193 (con aine ); Figu e 3b). Simila ly o he ield da a (see abo e),
he e was a signi ican di e ence in pa asi e abundance be ween
he sexes so ha emales we e mo e hea ily in ec ed (F1,3.0 = 10.56,
p = .047 (sex); F2,23 = 0.58, p = .568 (sex × con aine ); Figu e 3b). This
sugges s highe suscep ibili y o emales o in ec ion. New o ecen
in ec ions we e no de ec ed among he 10 unexposed con ol ish
indica ing ha he e was no na u al exposu e om he wa e du ing
he expe imen and ha he ish had no been ecen ly in ec ed in
he wild. Fou o he 30 exposed ish and one o he 10 con ol ish
ha bo ed ully de eloped Diplos omum me ace ca iae, likely as a e-
sul o in ec ion in he wild in he p e ious summe .
4 | DISCUSSION
Spa ial and empo al a ia ion in pa asi ism can ha e signi ican
implica ions o hos popula ions by unde lying a iabili y in in lu-
ence o pa asi es on he condi ion and ep oduc ion o indi iduals
(Le e e e al., 2009; Tompkins, Dunn, Smi h, & Tel e , 2011; Wood
e al., 2007). This is pa icula ly clea wi h in ec ions ha can cause
de imen al e ec s on he hos s, such as hose loca ed in he cen al
senso y o gans. Mo eo e , hos s species in which such e ec s can
come abou al eady a low pa asi e numbe s may su e he mos
no able consequences. We examined pa asi e in ec ions o wo spe-
cies o gobiid ishes in he No he n Bal ic Sea. We sco ed he en i e
mac opa asi e communi y in hese ishes and speci ically a ge ed
eye lukes o he genus Diplos omum ha a e known o cause loss
o ision in se e al ish species, wi h he e ec s likely being mos
p ominen in smalle ish species wi h he smalles eye lenses. We
ound signi ican spa io empo al a ia ion in in ec ions as well as di -
e ences be ween he ish species so ha he common gobies we e
mo e hea ily in ec ed in mos cases. While he e was no e ec o
hos sex on he in ec ions o e all, emale sand gobies we e mo e
hea ily in ec ed wi h eye lukes a he sampling loca ion wi h he
highes in ec ion. An expe imen al exposu e o he ish indica ed
ha he di e ence be ween he sexes was a leas pa ly explained
by he highe suscep ibili y o emales o in ec ion.
Spa io empo al a ia ion in pa asi ism is a common ea u e o
mos hos –pa asi e in e ac ions, including pa asi ic in ec ions o
ish in eshwa e (Ma cogliese, Gend on, Plan e, Fou nie , & Cy ,
2006; de Roij & MacColl, 2012) and in sea (G u e , 1998; Sikkel,
Neme h, McCammon, & Williams, 2009). We ound ha pa asi e
in ec ions o he wo goby species ollowed simila pa e ns. Fi s ,
in ec ion abundances we e clea ly di e en be ween he loca ions,
pa icula ly in he common goby, and mainly d i en by he ema-
ode C yp oco yle sp. This could e lec , o example, spa ial a ia ion
in in ec ion p e alence in he i s in e media e snail hos s o he
pa asi e, which is commonly obse ed also in o he ema ode sys-
ems (Fal ýnko á e al., 2008; Jokela & Li ely, 1995). Second, wi h
ew excep ions, di ec ly ansmi ed pa asi es (T ichodina sp. and
Gy odac ylus sp.) we e clea ly mo e p e alen in he ea ly summe
compa ed o au umn, e lec ing he empe a u e- d i en eplica ion
o hese pa asi es (Bagge & Val onen, 1999; Halme oja, Val onen,
& Taskinen, 1992; Koski aa a, Val onen, & P os , 1991; Rin amäki-
Kinnunen & Val onen, 1997). Thi d, ophically ansmi ed pa asi es
(ces odes, nema odes, and acan hocephalans) showed spo adic oc-
cu ence a low numbe s, sugges ing ha he gobies unlikely a e he
p ima y ish hos s o hese pa asi es in his sys em. Fou h, many o
he la al ema odes, pa icula ly in sand gobies om he Va gskä
loca ion wi h he highes in ec ion, ended o be mo e abundan
in au umn compa ed o ea ly summe (Table 1). This well e lec s
he ypical accumula ion o ema odes in hei in e media e hos s
du ing summe mon hs (Fal ýnko á, Ka onen, & Val onen, 2011;
Ka onen, Hudson, Seppälä, & Val onen, 2004; Ka onen e al.,
2004a,b). The lowe abundance in he ea ly summe is also consis-
en wi h he idea ha he mos hea ily in ec ed indi iduals may
be los om he popula ion du ing win e , while ou da a we e oo
ew o es his p ope ly. Fo example, Diplos omum in ec ions and
ca a ac s compa able o his s udy in he eye lenses a e known o
cause se ious i ness consequences in ish (C owden & B oom, 1980;
Ka onen & Seppälä, 2008; Seppälä e al., 2005), suppo ing a possi-
bili y o pa asi e- d i en popula ion e ec s (Ma cogliese, Compagna,
Be ge on, & McLaughlin, 2001). O e all, b oad lines o he spa ial
and empo al a ia ion o pa asi ism in his sys em a e in acco dance
wi h ea lie indings o pa asi e in ec ions in gobies in he Bal ic Sea
(Zande , 2003, 2005; Zande & Kes ing, 1998; Zande , S ohbach, &
G oenewold, 1993).
We also ound a dis inc di e ence be ween male and emale
sand gobies in he abundance o eye luke in ec ion so ha emales
we e mo e hea ily in ec ed bo h in he ield and in he expe imen-
al exposu e. This is in con as wi h he gene al pa e n o highe
in es a ion in males ac oss a ange o hos –pa asi e sys ems (Klein,
2004; Poulin, 1996), al hough ew s udies ha e epo ed highe pa -
asi e in ec ions also in emales, o example, in guppies (Richa ds,
an Oos e hou , & Cable, 2010; S ephenson, an Oos e hou ,
Mohammed, & Cable, 2015; Tadi i, Sco , & Fussmann, 2016), gobies
(Van Damme & Olle ie , 1994) and co al ee ish (Sikkel, Fulle , &
Hun e, 2000). One eason o he sex di e ence in his sys em could
be ha males and emales in he ield a e di e en ly exposed o he
pa asi e ce ca iae. Ou sampling ime in ea ly summe coincided
wi h he b eeding season o gobies (Hes hagen, 1977; Linds öm,
1998; Nyman, 1953) when males a e de ending nes s and eggs, and
emain mos ly s a iona y. On he o he hand, emales a e ac i ely
swimming a ound in sea ch o spawning and eeding oppo uni ies,
which could inc ease hei exposu e o he pa asi e ce ca iae (see
also Sikkel e al. (2000)). Howe e , ou exposu e expe imen showed
ha he sex di e ence in in ec ions is no me ely due o beha io al
di e ences, bu ha emales a e also mo e suscep ible o in ec ion
han males. This is in e es ing as i con adic s wi h he gene al end
o males being mo e suscep ible o pa asi e in ec ions because o
sex ho mones ha can supp ess immune unc ion (Klein, 2004).
The eason why such a sex- speci ic in ec ion pa e n was obse ed
only in Va gskä is cu en ly unclea , bu may be ela ed o di e -
ences be ween he habi a ypes. Fo example, he sampling si es
S a ion and Långholmen a e mo e shel e ed compa ed o he mo e
exposed Va gskä , al hough his would sugges lowe a he han
6120
|
KARVONEN ANd LINdSTRÖM
TABLE2 P e alence (% ish in ec ed) and mean abundance (numbe o pa asi es pe ish ± SE) o he pa asi e axa de ec ed in common gobies cap u ed om h ee loca ions in he
No he n Bal ic Sea in June 2014–Oc obe 2015
Pa asi e
June 2014 June 2015 Oc obe 2015
S a ion
n = 30
Långholmen
n = 24
Va gskä
n = 0
S a ion
n = 30
Långholmen
n = 30
Va gskä
n = 0
S a ion
n = 0
Långholmen
n = 24
Va gskä
n = 30
T ichodina sp. 100
18.0 ± 5.7
95.8
32 ± 0.5
96.7
16.8 ± 4.2
100
15.3 ± 2.9
0.0 60.0
0.9 ± 0.2
Gy odac ylus sp. 3.3
0.03 ± 0.03
50.0
0.7 ± 0.2
16.7
0.5 ± 0.3
3.3
0.03 ± 0.03
0.0 6.7
0.07 ± 0.05
Diplos omum spp. 0.0 0.0 3.3
0.03 ± 0.03
30.0
0.4 ± 0.1
83
0.1 ± 0.1
13.3
0.1 ± 0.1
Diplos omum bae i 0.0 0.0 0.0 3.3
0.03 ± 0.03
0.0 0.0
Apa emon sp. 3.3
0.07 ± 0.07
83
0.1 ± 0.1
30
0.3 ± 0.1
13.3
0.1 ± 0.1
83
0.1 ± 0.1
13.3
0.2 ± 0.1
C yp oco yle sp. 16.7
0.5 ± 0.4
58.3
2.0 ± 0.6
63.3
4.2 ± 1.4
76.6
13.1 ± 3.5
45.8
3.7 ± 1.3
73.3
3.9 ± 0.8
Sphae os omum sp. 3.3
0.03 ± 0.03
0.0 0.0 0.0 0.0 0.0
P o eocephalus sp. 3.3
0.03 ± 0.03
0.0 0.0 13.3
0.1 ± 0.1
0.0 3.3
0.03 ± 0.03
Camallanus lacus is 6.7
0.07 ± 0.05
0.0 0.0 0.0 0.0 0.0
Uniden i ied nema ode 6.7
0.07 ± 0.05
4.2
0.04 ± 0.04
0.0 3.3
0.03 ± 0.03
42
0.04 ± 0.04
0.0
Echino hynchus gadii 0.0 0.0 0.0 0.0 0.0 0.0
Neoechino hynchus u ili 0.0 4.2
0.04 ± 0.04
0.0 0.0 0.0 0.0
|
6121
KARVONEN ANd LINdSTRÖM
highe in ec ion in he la e . On he o he hand, he popula ion size
o seagulls, e ns, and me ganse ids, he de ini i e hos s o many
ema odes including Diplos omum, may be la ge a Va gskä han
he o he si es (Linds öm & Ran a, 1992). This could enhance pa a-
si e li e cycles locally (Ma cogliese e al., 2001). Howe e , de ails o
he di e ences in in ec ion p ocesses need u he wo k.
Ou da a also show ha jus one o wo wo ms in ec ing an eye
lens o small ish, such as gobies, can se e ely ha m he lens (i.e.,
ca a ac s co e ing he majo i y o lens we e o med a e y low in-
ec ion). This is because he size o he pa asi e me ace ca iae (and
he damage hey in lic pe lens olume) likely emain ela i ely con-
s an ega dless o he lens size, bu he size o he eye lens inc eases
wi h ish size. Thus, in la ge ish species, ca a ac co e age ypically
inc eases linea ly wi h he pa asi e abundance and ens o pa asi es
pe lens may be equi ed o high ca a ac in ensi ies (Ka onen &
Seppälä, 2008; Ka onen e al., 2004a), whe eas e en a low- le el in-
ec ion is likely o se e ely impai he ision o a small ish (see also
Owen, Ba be , and Ha (1993)). Du ing ma ing, emale sand gobies
isi se e al males (Fo sg en, 1997; Linds öm & Leh onen, 2013)
and base hei ma e choice on a ange o isual cues (Fo sg en, 1992;
Linds öm e al., 2006). As a consequence, a ac i e males each high
ma ing success compa ed o less a ac i e ones (Linds öm & Seppä,
1996) and his non andom dis ibu ion o ma ing success esul s in
sexual selec ion (Ande sson, 1994; Emlen & O ing, 1977). This p o-
cess, howe e , can be po en ially a ec ed by impai ed isual abili y o
emales. Fo example, dec eased wa e cla i y in e e es wi h isual
abili ies o emales and his has been in oked as an explana ion o
weakened sexual selec ion in u bid wa e s (Jä enpää & Linds öm,
2004; Seehausen e al., 1997). Simila ly, i he isual abili y o emales
was hampe ed by Diplos omum, his could a ec he way emales can
judge males and exp ess hei ma ing p e e ences, as hey would no
be able o de ec male ma ing signals. Consequen ly, ma ing sys ems
in a eas o high in ec ion isk o emales could become mo e andom
and esul in weakened sexual selec ion. Such a p ocess could easily
c ea e spa ial a ia ion in he in ensi y o sexual selec ion and may
con ibu e o p ese ing gene ic a ia ion in male seconda y sexual
ai s. Howe e , emale p e e ences a e also based on he quali y o
male pa en al ca e (Linds öm e al., 2006; Pampoulie, Linds öm, &
S . Ma y, 2004). Thus, i is possible ha emales in a eas o high in-
ec ion, on a e age, selec males exhibi ing lowe quali y ca e, which
hen esul s in lowe o sp ing p oduc ion. While ou da a a e sug-
ges i e o he po en ial o such pa asi e- induced changes in ma e
choice, hese ques ions need o be ackled expe imen ally.
To conclude, spa io empo al a ia ion in pa asi ism among pop-
ula ions, as well as ha be ween sexes, can de e mine o wha ex-
en hos popula ions su e i ness consequences o in ec ions in
e ms o dec eased su i al and ep oduc i e success. Se e al ea -
lie s udies ha e sugges ed ha sexual cha ac e is ics used in ma e
choice can ad e ise esis ance o an indi idual owa d pa asi e
in ec ions. Howe e , he al e na i e ha pa asi e in ec ions could
in luence his p ocess by impai ing he isual abili y o one sex o
pe cei e such cha ac e is ics is i ually unexplo ed. Ou da a show
he po en ial o such changes in ma e choice in small- sized ish such
as gobies, whe e isual abili ies o emales pe cei ing signals om
males could de e io a e a e y low in ec ion in ensi ies. Howe e ,
we also sugges ha such e ec s a e likely o be di e en among
hos popula ions expe iencing di e en le els o pa asi ism. O e all,
ela ionships be ween spa io empo al a ia ion in in ec ions,
gende - biased pa asi ism and ma e choice o m an in e es ing ield
o u he expe imen al esea ch.
ACKNOWLEDGMENTS
We hank T ä minne Zoological S a ion o logis ic suppo . Da id
Ma cogliese ga e aluable commen s on an ea lie d a .
CONFLICT OF INTEREST
The au ho s decla e ha hey ha e no con lic o in e es .
AUTHOR CONTRIBUTIONS
AK and KL concei ed, designed, and pe o med he expe imen s. AK
analyzed he da a. AK and KL w o e he manusc ip .
ORCID
Anssi Ka onen h p://o cid.o g/0000-0002-2731-3344
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