Spatiotemporal and gender-specific parasitism in two species of gobiid fish

This is a sel -a chi ed e sion o an o iginal a icle. This e sion may di e om he o iginal in pagina ion and ypog aphic de ails. Au ho (s): Ti le: Yea : Ve sion: Copy igh : Righ s: Righ s u l: Please ci e he o iginal e sion: CC BY 4.0 h ps://c ea i ecommons.o g/licenses/by/4.0/ 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 | 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 | 6115 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 | 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 | 6117 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 | 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 REFERENCES Ande sson, M. (1994). Sexual selec ion. P ince on, NJ: P ince on Uni e si y P ess. Bagge, A. 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