Pohybová Aktivita Nepůvodních Hlaváčovitých Ryb Disertační Práce

PŘÍRODOVĚDECKÁ FAKULTA

Pohybová aktivita nepůvodních hlaváčovitých ryb Disertační práce

Luděk Šlapanský

Vedoucí práce: Ing. Pavel Jurajda, Dr.

Ústav Botaniky a Zoologie

Brno 2019

Bibliografický záznam

Autor: Mgr. Luděk Šlapanský Přírodovědecká fakulta, Masarykova univerzita Ústav Botaniky a Zoologie

Název práce: Pohybová aktivita nepůvodních

hlaváčovitých ryb

Studijní program: Biologie

Studijní obor: Zoologie

Školitel: Ing. Pavel Jurajda, Dr. Ústav Biologie Obratlovců Akademie Věd České republiky, Květná 8, 603 65 Brno

Akademický rok: 2018/2019

Počet stran: 67+99

Klíčová slova: invazní druhy; hlaváč černoústý; pohybová aktivita

Bibliographic entry

Author: Mgr. Luděk Šlapanský Faculty of Science, Masaryk university Department of Botany and Zoology

Title of Dissertation: Movement activity of non-native Gobiids

Degree Programme: Biology

Field of Study: Zoology

Supervisor: Ing. Pavel Jurajda, Dr. Institute of the Vertebrate Biology, Czech Academy of Sciences, Květná 8, 603 65 Brno

Academic Year: 2018/2019

Number of Pages: 67+99

Keywords: invasion species; round goby; movement activity

Abstrakt

Činností člověka došlo a stále dochází k narušení nepřekonatelných biogeografických bariér. Výsledkem je strmě narůstající množství biologických invazí rostlin a živočichů, které se zejména v posledních dekádách dostává do centra zájmu odborné i laické veřejnosti. V této disertační práci jsem se zabýval dvěma druhy nepůvodních hlaváčovitých ryb původem z Ponto-Kaspické oblasti, konkrétně hlavačkou poloměsíčitou (Proterorhinus semilunaris, Heckel 1837) a především hlaváčem černoústým (Neogobius melanostomus, Pallas 1814), které pronikly do vod České republiky a mají potenciál stát se invazními. Zaměřil jsem se na mechanismy šíření těchto nepůvodních druhů v podmínkách českých řek, konkrétně na rychlost postupu invazní fronty, na roli vlastní pohybové aktivity v procesu šíření (tj. bez pomoci člověka) a na doposud málo prozkoumanou pohybovou aktivitu raných vývojových stádií hlaváčovitých ryb. Mimo to jsem také sledoval potenciální vliv rozšiřování hlaváčovitých ryb na původní ichtyofaunu a unioidní mlže. Zjistil jsem, že větší část populace hlaváče černoústého vykazuje relativně malou intenzitu pohybové aktivity v rámci dlouhého sledovaného období. Zbývající menší část populace se však vyznačovala vyšší intenzitou pohybové aktivity a v některých případech byla vzdálenost, kterou daný jedinec urazil, překvapivě velká (770 m za 26 dní). Tito „pionýři“ jsou pravděpodobně zodpovědní za poměrně rychlý posun invazní fronty v kolonizovaných řekách. Pasivní poproudý pohyb (drift) raných vývojových stádií následně slouží v řekách, jak ke stabilizování a posílení populací ve směru po proudu od nově kolonizovaného území, tak k vyplnění mezer mezi zdrojovou populací a pionýry, čímž výrazně přispívá k celému kolonizačnímu procesu. Tento způsob šíření po proudu nabývá na významu v případě náhodné či úmyslné introdukce do vzdálených oblastí, což dokumentuje zavlečení hlaváče černoústého do Labe lodní dopravou, kdy se nejbližší geneticky a morfologicky shodná populace nacházela v 600 km vzdáleném úseku Labe u Hamburku. Poznatky získané v této dizertační práci prokázaly, že nepůvodní hlaváčovité ryby dokáží v krátké době kolonizovat dlouhé úseky vodních toků a to buď za pomoci člověka, nebo své vlastní pohybové aktivity. Navzdory očekávání se však neprokázal

škodlivý vliv těchto druhů na původní ichtyofaunu a unioidní mlže, ačkoli není vyloučeno, že se škodlivé působení projeví až v delším časovém horizontu. Je proto důležité sledovat šíření a působení hlaváčovitých ryb na původní ekosystém i nadále.

Abstract

Human activity has been, and still is, breaking down previously insurmountable biogeographical barriers. As a result, there have been a steadily increasing number of plant and animal invasions. Particularly in recent decades, such biological invasions have become of particular interest, both within the scientific community and to the general public. In this dissertation thesis, I deal with two potentially invasive non-native gobiid fish species originating from the Ponto-Caspian region, the tubenose goby (Proterorhinus semilunaris, Heckel 1837) and, especially, the round goby (Neogobius melanostomus, Pallas 1814), which have now penetrated into Czech waters. This thesis focuses mainly on the mechanisms of spread employed by these non-native species in conditions specific to Czech rivers, especially the rate of invasion front progress, the role of natural movement activity in the spreading process (i.e. non-anthropogenic movement), and the rarely studied issue of gobiid early life stage movement activity. In addition, I examine the potential impact of gobiid expansion on native ichthyofauna and unionid molluscs. My long-term monitoring results suggest that the larger part of the round goby population displays a relatively low intensity of movement activity. However, a relatively small part of the population is characterised by an increased intensity of movement activity, with some individuals capable of travelling surprisingly large distances (e.g. 770m per 26 days). These “pioneers” are most likely responsible for the relatively rapid invasion front shifts observed in colonised rivers. Subsequently, passive downstream movement (drift) of early life stages in rivers acts both to stabilise and strengthen populations downstream of the newly colonised areas and to fill the gap between the source population and the pioneers; thereby greatly contributing to the entire colonisation process. The downstream spread of juveniles becomes particularly important in cases of accidental (or deliberate) introduction to distant areas, as documented by the transport of round goby into the River Elbe by shipping, the nearest genetically and morphologically identical population being located 600 kilometres downstream near Hamburg. The results presented in this dissertation thesis demonstrate that non-native gobiid fishes are able to colonise long stretches of river over a relatively short period, whether

by anthropogenic assistance or through their own movement activity. Unexpectedly, however, no harmful effects on native ichthyofauna and unionid molluscs have been recorded to date, though it is still possible that harmful impacts will be manifested over a longer time-scale. As such, it remains important that invasive gobiid fishes are continuously monitored for any negative impacts on the native ecosystem.

Poděkování

V následujících řádcích bych chtěl poděkovat všem, kteří se podíleli, byť jen krátkým komentářem nebo povzbudivým slovem na nelehkém procesu tvorby předkládané práce. Mé poděkování patří na prvním místě Pavlu Jurajdovi, který se mě ujal už jako studentského „potěru“ a i přes mé nelehké začátky byl tím nejlepším školitelem, jakého jsem si snad ani nezasloužil. Trpělivost, zázemí, cenné rady a odborné vedení, které mi za celé mé studium poskytl, jsem se snažil bez zbytku zužitkovat při tvorbě vědeckých publikací i při práci v terénu. Chtěl bych poděkovat Michalovi Janáčovi za pomoc při analýze dat a za jeho erudované rady při psaní publikací, včetně této práce. A především za konzultace nejen na vědecké téma, při kterých jsem si osvojil schopnost smysluplně argumentovat. Děkuji všem kolegům z Ústavu biologie obratlovců AV ČR za pomoc při sběru materiálu v terénu a za jejich přátelský a ochotný přístup, díky němuž jsem se mohl na každý výjezd za vzorky těšit. Děkuji zástupcům podniku Lesy České republiky a Moravského rybářského svazu, že nám umožnili vzorkování ve svých vodách. V neposlední řadě bych rád poděkoval svým rodičům za podporu a kladení otázek typu: „Kdy už to bude konečně napsané?“, čímž mě osobitě nutili práci opravdu napsat. A děkuji také svým kamarádům, kteří mi pomáhali překonávat krušné chvíle tím, že byli vždy nablízku.

Tato práce byla vypracována na Ústavu biologie obratlovců AV ČR, v.v.i. a jako součást projektů GAČR: ECIP P505/12/G112 a P505/11/1768.

Prohlášení

Prohlašuji, že jsem svoji disertační práci vypracoval samostatně s využitím informačních zdrojů, které jsou v práci citovány.

Brno 25. února 2019 ……………………………… Jméno Příjmení

Obsah

1. Předmluva ...... 12 2. Úvod ...... 13 2.1 Pohybová aktivita...... 13 2.2 Vymezení procesu invaze ...... 14 2.3 Invaze ve sladkovodních ekosystémech ...... 17 2.4 Dopady invazí na sladkovodní ekosystém ...... 19 2.5 Invaze hlaváčovitých ryb ...... 20 2.5.1 Rychlost „přirozeného“ šíření hlaváčů ...... 22 2.5.2 Vliv nepůvodních hlaváčů na původní ekosystém ... 25 2.6 Invaze hlaváčů do ČR ...... 27 2.6.1 Hlavačka poloměsíčitá ...... 27 2.6.2 Hlaváč černoústý ...... 30 3. Cíle práce ...... 32 4. Shrnutí jednotlivých publikací ...... 33 4.1 Publikace A ...... 33 4.2 Publikace B ...... 35 4.3 Publikace C ...... 37 4.4 Publikace D ...... 39 4.5 Publikace E ...... 40 5. Závěr ...... 42 6. Seznam použité literatury ...... 46 7. Přílohy ...... 68

1. Předmluva

Zvyšující se tempo šíření nepůvodních druhů a s ním spojené biologické invaze v současnosti nenechávají v klidu vědeckou ani laickou veřejnost. Pro účinnou ochranu původní biodiversity před potenciální nebo reálnou hrozbou invaze je třeba detailně porozumět mechanismu invazních procesů. Jednou z nejpodstatnějších složek, podmiňující úspěšné proniknutí nepůvodního či invazního druhu do nového ekosystému a udržení se v něm, je schopnost efektivně využívat veškeré složky pohybové aktivity. V disertační práci jsem se zaměřil na studium pohybové aktivity nepůvodních hlaváčovitých ryb, jež reprezentují rapidně se šířící invazní skupinu druhů. V úvodu popisuji pohybovou aktivitu v obecné rovině společně s její rolí v procesu invaze ve vodním prostředí, načež následně přecházím k cílové čeledi hlaváčovitých. Detailněji se pak věnuji mechanismům šíření a rozsahu vlastní pohybové aktivity hlaváčovitých ryb na různých stupních ontogenetického vývoje, především u hlaváče černoústého, který představuje rychle se šířící invazní druh. Zjištěné výsledky jsou obsaženy ve 4 publikacích (2 prvoautorské) vydaných v odborných periodikách s IF a jednom rukopise (prvoautorský) odeslaném k recenznímu řízení. V publikacích D a E byl použit materiál nasbíraný v průběhu magisterského studia, avšak zpracování a příprava publikací probíhala již v doktorském studiu. V závěru práce shrnuji a diskutuji výsledky předložených publikací společně s přehledem možných ochranných opatření bránících dalšímu šíření nepůvodních hlaváčovitých ryb. Je zde naznačeno i další možné směřováním výzkumu týkajícího se invaze nepůvodních hlaváčovitých ryb, který by nám o této problematice poskytl ucelený obraz. V příloze se nachází publikace vztahující se k tématu disertační práce, seznam mých příspěvků na zahraničních i domácích konferencích a přehled další publikační a výzkumné činnosti.

2. Úvod

2.1 Pohybová aktivita

Pohyb organismu, definovaný jako změna polohy celého těla v prostoru a čase, je esenciální složkou života. Mechanismy pohybu jsou značně diverzifikované napříč živočišnou říší. Mikroorganismy, rostliny nebo živočichové se pohybují různými způsoby (aktivně nebo pasivně), v různých časových a prostorových škálách. Pohyb obecně hraje klíčovou roli v určení budoucího osudu jedince, a tak se současně významně podílí i na struktuře a dynamice populací, společenstev a ekosystémů, včetně ovlivňování diversity a evolučních procesů (Bullock et al. 2002; Nathan et al. 2008; Clobert et al. 2012). Dynamika pohybové aktivity živočichů zahrnuje denní i sezónní využívání známé, prostorově omezené oblasti (domovský okrsek), kde jedinci vykonávají různé činnosti jako je získávání potravy, páření nebo péče o mláďata (Dingle 1996; Powell 2000; Lucas & Baras 2001). Pohyb za hranice domovského okrsku může vyústit v další specifické typy pohybové aktivity, které jsou běžně definovány pro skupiny organismů, i když je to samozřejmě jedinec, který se pohybuje (Begon et al. 2006). Pokud dochází k pravidelným synchronizovaným přesunům, obvykle většího množství jedinců konkrétních druhů, často ve specifickém vývojovém stádiu, mezi domovskými okrsky, jedná se o migraci. Termín migrace může být aplikován na pestrou škálu typů pohybu v různorodém prostorovém a časovém měřítku, což může zahrnovat například denní migrace planktonu, sezónní přesuny motýlů nebo hnízdní migrace ptáků na značné vzdálenosti (Begon et al. 2006; Milner-Gulland et al. 2011). Průzkumné cesty na větší vzdálenosti nebo jednosměrný pohyb organismu mimo současný domovský okrsek, při kterém se jedinec může eventuálně usadit v novém okrsku, představuje stručnou definici disperze (Nathan 2001; Dingle & Drake 2007). S povahou tohoto procesu souvisí celá řada konsekvencí, k nimž patří redukce příbuzenského křížení, únik z nepříznivých lokálních podmínek, únik před predátory a mnohé další (Lucas & Baras 2001; Bullock et al. 2002; Clobert et al. 2012).

Disperze má však ještě jeden významný důsledek, a to v podobě rozptylu druhů do oblastí, ve kterých nejsou původní, což může v krajních případech vyústit až v proces invaze (Nathan 2001).

2.2 Vymezení procesu invaze

Ještě než přikročím k problematice invazí v konkrétních příkladech, bude třeba alespoň částečného náhledu do teoretické roviny invazních procesů. Ačkoli se poznání biologických invazí neustále prohlubuje a mohlo by se zdát, že charakter invazního procesu je již jasně vymezen, existuje stále několik překážek k vytvoření obecně platné terminologie. Komplikace nastávají při určování pojmů s invazí spojených, které není mnohdy jednoduché jednoznačně definovat (Blackburn et al. 2011). Samotné vymezení pojmu invazní druh se může v detailech lišit mezi obory i mezi jednotlivými autory, díky absenci jednotného koncensu (Colautti & McIsaac 2004). Při popisování biologické invaze, respektive šíření invazního druhu, však panuje shoda v konkrétních fázích těchto procesů, které musí daný druh splňovat, aby byl označen jako invazní. První základní podmínkou je překonání geografické bariéry za přispění aktivity člověka (introdukovaný druh), případně vlastními silami, a kolonizace území, kde se daný druh dříve nevyskytoval (nepůvodní druh). Přitom musí být schopen přežít v podmínkách nového prostředí, kde vytvoří a udrží životaschopnou populaci bez zásahů člověka (naturalizovaný druh), která se po úspěšném usazení začne šířit, zpravidla velice rychle, do okolního ekosystému - v tom případě se označuje už jako invazní druh (Richardson et al. 2000; Pyšek et al. 2004). Tento přístup převládá především u autorů popisujících rostlinné invaze. U dalších autorů (především těch popisujících živočišné invaze) se k rychlému šíření jako podmínka invazivnosti přidává navíc negativní vliv na původní společenstva či celý ekosystém (Lodge & Shrader-Frechette 2003; Beck et al. 2008; Keller et al. 2011). I když pravdou zůstává fakt, že nepůvodní druh může mít škodlivý efekt na původní druhy v rozličných úrovních invazního procesu, označuje se obvykle jako invazní právě až po dosažení vysoké populační hustoty nebo rozsáhlém rozšíření areálu společně s významným působením na složky původního ekosystému (obr. 1) (Ricciardi et al. 2013).

Takovéto ohrožení však nemusí být bezprostředně rozpoznatelné, pokud druh prochází obdobím klidu, tzv. "lag fáze", během kterého se přizpůsobuje novým podmínkám prostředí a svoji populační hustotu zvyšuje jen velmi pozvolna nebo vůbec (Crooks 2005). Doba trvání období klidu je značně variabilní a podstatnou roli v něm hraje dostatečný přísun nových jedinců, který může celý proces invaze značně urychlit, obzvláště v případech příchodu geneticky odlišných jedinců, kteří zvyšují celkovou variabilitu a tím pádem i adaptabilitu na nové podmínky prostředí v rozrůstající se populaci nepůvodního druhu (Simberloff 2009; Keller & Taylor 2010). Na konci klidového období pak dochází k rapidnímu nárůstu populační hustoty v místě introdukce a rychlé kolonizaci dalších částí nově obsazeného ekosystému, čímž se jednoznačně naplňuje definice invazního druhu (Crooks & Soulé 1999). Invazním druhem navíc nemusí být vždy druh nepůvodní. Původní druhy mohou začít rapidně kolonizovat přilehlé oblasti v důsledku změn v jejich přirozeném prostředí (eutrofizace, globální oteplování, změny habitatu) zapříčiněných člověkem (Valéry et al. 2009) a způsobovat stejné problémy jako nepůvodní invazní druhy. Přeměna původního, nepůvodního či naturalizovaného druhu na druh invazní však může selhat na každé z dříve zmíněných úrovní. Pouze malá část z obrovského množství nepůvodních druhů (pravidlo deseti - Williamson & Fitter 1996) dospěje až do stavu, kdy začne představovat hrozbu pro původní ekosystém (Richardson & Pyšek 2006). Ačkoli i v tomto bodě může invaze uspět pouze krátkodobě. Existují názorné případy, jako například u lokálních invazních populací ropuchy obrovské (Freeland 1986) nebo u cichlidy druhu Cichlasoma urophtalmus (Trexler et al. 2000), kdy došlo k rychlému nárůstu populační hustoty následované jejím relativně brzkým zhroucením. Překročení nosné kapacity prostředí v důsledku změny lokálních podmínek (např. zvýšený predační tlak, vyčerpání zdrojů, rozvoj nemocí, atd.), tak často vede k ústálení populace na nižších hustotách v blízkosti rovnovážnému stavu nebo k jejímu úplnému vymizení (Simberloff & Gibbons 2004; Crooks 2005). S přihlédnutím k předcházejícím příkladům je vhodné zmínit, že označení druhu za invazní není vždy zcela vhodné. Scénář každé další invaze téhož druhu je totiž odlišný v mnoha parametrech, což vede ke vzniku nepřeberného množství možných výsledných stavů v závislosti na konkrétních podmínkách (Mollot et al. 2017). Druh invazní v jednom ekosystému tak nemusí uspět v jiném ekosystému i přes dostatečný počet

jedinců a vícenásoubnou introdukci. Ve většině situací se tak jeví jako vhodnější úžívání termínu 'invazní populace druhu', nežli pojem 'invazní druh' (Colautti & McIsaac 2004). Při určovaní invazivnosti, a tím pádem i potenciálního ohrožení pro ekosystém, je třeba sledovat (invazní) populace nepůvodního druhu velice důkladně, po delší dobu, ve všech fázích kolonizačního procesu vedoucího až k invazi. I málo významné a nepřímé efekty způsobené nepůvodními druhy, kterým není věnována dostatečná pozornost, totiž mohou vyústit ve významné strukturální a funkční změny v celém ekosystému (Simberloff 2011; Vilà et al. 2011).

Obrázek 1. Zjednodušené schéma invazního procesu (upraveno podle Lokwood et al. 2007).

2.3 Invaze ve sladkovodních ekosystémech

Se vzrůstajícími aktivitami člověka se zvyšuje i množství invazních druhů schopných překonávat geografické a další bariéry, dříve bránící jejich expanzi. Zjednodušené šíření nepůvodních a invazních druhů má za následek, že biologickými invazemi jsou v současnosti postiženy všechny typy ekosystémů (Sakai et al. 2001; Vilà et al. 2011). Nejčastěji ze všech jsou pak invazemi s negativními následky zasaženy ekosystémy sladkovodní (Ricciardi & Kipp 2008). K této zvýšené náchylnosti k invazím značně přispívá fakt, že se jedná o systémy s dobře vymezenými hranicemi, limitovanou diverzitou a s omezenou velikostí populací druhů, které je obývají. Řeky a jezera tak fungují jako izolované ostrovy, které jsou podstatně náchylnější k invazím díky evoluční naivitě lokální bioty (Ricciardi & MacIsaac 2011). Sladkovodní ekosystémy jsou navíc postiženy degradací svého přirozeného charakteru způsobeného lidskou činností, zejména znečišťováním, nadměrným využíváním, fragmentací, zničením a nahrazováním habitatu či manipulací s průtoky. K těmto faktorům se čím dál častěji připojuje i klimatická změna, která stojí za podstatnými změnami ve fungování vodních ekosystémů (Rahel & Olden 2008). Pod vlivem těchto faktorů se stávají sladkovodní ekosystémy ještě mnohem zranitelnější vůči pronikání nepůvodních druhů (Dudgeon et al. 2006; Vörösmarty et al. 2010; Havel et al. 2015). Hlavní podmínkou pro vznik invazních populací v takto narušených ekosystémech však stále v drtivé většině případů zůstává introdukce nepůvodního druhu člověkem. Tisíce nepůvodních druhů jsou přemísťovány prostřednictvím rozličných vektorů spojených s lidskou činností. Na jednom z předních míst mezi zprostředkovateli introdukce nepůvodních druhů do sladkých vod nalezneme vypouštění balastní vody ve vnitrozemských přístavech nebo v ústí velkých řek s brakickou vodou (Drake & Lodge 2004; Gollasch 2006). Význam nákladní lodní dopravy navíc umocňuje transport nepůvodních organismů na povrchu trupu nákladních lodí (Drake & Lodge 2007; Hulme 2009). Za účelem navýšení množství přepravovaného zboží se také započalo s propojováním izolovaných vodních ploch a jednotlivých povodí prostřednictvím sítě vnitrozemských vodních cest, jejichž prostřednictvím se otevírá přístupová cesta do nového prostředí řadě nepůvodních druhů. Tímto způsobem vznikly, tzv. „invazní

koridory“ jenž spojují dříve izolovaná povodí, za současného poskytování zdrojových populací invazních druhů při šíření do přilehlých vodních těles (Panov et al. 2009). Při tvorbě plavebních kanálů jsou navíc degradovány původní břehy a příbřežní habitaty, které jsou nahrazovány homogenizovanými strukturami nevhodnými pro původní druhy živočichů (Wolter 2001; Wolter & Arlinghaus 2003). Zájem člověka o kvalitní zdroje potravy také znamenal prudký rozvoj akvakultury vedoucí k záměrným introdukcím hospodářsky významných druhů ryb po celém světě. Ačkoli jsou nepůvodní druhy chovány v izolovaných objektech, téměř vždy dojde k jejich úniku z chovných zařízení do přilehlých vod a k potenciálnímu ohrožení původního ekosystému (Cook et al. 2008; Gozlan 2017). Násada cílových druhů ryb pro akvakulturu však poměrně často obsahuje také další nevítané pasažéry. Vynikajícím příkladem náhodné introdukce bylo neúmyslné zavlečení střevličky východní (Pseudorasbora parva) do Evropy s násadou amura bílého (Ctenopharyngodon idella) (Gozlan et al. 2010). S chovem ryb v akvakulturách bezprostředně souvisí i vysazování nepůvodních druhů do volných vod za účelem hospodářského, biomanipulačního (30% akvatických nepůvodních druhů v Evropě) nebo rekreačního využití (Gozlan 2017; Bobeldyk et al. 2015). Jako názorný příklad drastického dopadu záměrné introdukce na původní sladkovodní ekosystém nám může sloužit dramatické snížení biodiversity způsobené okounem nilským (Lates niloticus) v jezeře Viktoria (Witte et al. 1992). Sportovní rybáři jsou v přenosu nepůvodních druhů zainteresováni v menší míře. Vypouštění živočišných nástrah a nástražních ryb touto zájmovou skupinou je sice spíše lokálního významu, avšak zpřístupňuje cestu do jinak izolovaných vodních těles (Gozlan et al. 2010). Rovněž obchod s akvarijními a okrasnými živočichy zastupuje významný vektor pro šíření populací invazních druhů. Největší nebezpečí spočívá v jeho rozsahu a současně v minimální kontrole celého odvětví. Vypouštění akvarijních druhů ryb a živočichů společně s úniky z okrasných jezírek způsobilo, že jedna třetina nejhorších invazních druhů má původ z této zájmové činnosti (Padilla & Williams 2004; Bobeldyk et al. 2015). Alarmující skutečností stále zůstává fakt, že frekvence výskytu invazních populací nepůvodních druhů ve sladkých vodách po celém světě v posledních dekádách neustále

roste a má za následek často nenapravitelné škody na původním ekosystému (Ricciardi & MacIsaac 2000; Strayer 2010; Toussaint et al. 2018).

2.4 Dopady invazí na sladkovodní ekosystém

Dojde-li k proniknutí nepůvodního druhu do ekosystému za současného vzniku invazní populace, jsou unikátní zdroje a služby poskytované tímto ekosystémem ohroženy stejně jako biodiverzita původních druhů. Působení nepůvodních druhů má ekologický dopad na každé úrovni od genů až po celý ekosystém (Cucherousset & Olden 2011) a je realizováno především prostřednictvím soutěže o limitované zdroje s původními druhy nebo redukováním populace původních druhů přímou predací (Sakai et al. 2001; Gozlan 2008; Gallardo et al. 2016). Invazní ekosystémoví inženýři přeměňující obasazený habitat do zcela nové podoby, tímto způsobem spouští ekosystémové změny, které mohou přetrvat i mnoho let po vymizení tohoto invazního druhu (Strayer 2010). Současně se může invazní ekosystémvý inženýr podílet na tzv. „invasional meltdown“ procesu, při kterém jeho transformační činnost usnadňuje pronikání dalších populací invazních druhů do původního ekosystému (Simberloff & von Holle 1999). Slávička mnohotvárná (Dreissena polymorpha) narušila ekologické vazby v ekosystému Velkých Severoamerických jezer (MacIsaac 1996) a umožnila dramatický nárůst populace hlaváče černoústého (Neogobius melanostomus), různonožce Echinogammarus ischnus i dalších druhů (Ricciardi 2001). Nepůvodní druhy si do nového přostředí mohou přenést parazity a patogeny ze své domoviny. Nový patogen je častokrát schopen napáchat mnohonásobně větší škody v populacích původních druhů, nepřizpůsobených na exotickou infekci či parazita, než jeho původnímu hostiteli (Prenter et al. 2004; Crowl et al. 2008). Ztráta původního druhového bohatství může být zapříčiněna i hybridizací s nepůdními druhy (Huxel 1999; Kovach et al. 2015) a v neposlední řadě také narušením stávajících vztahů v potravních sítích (Cucherousset & Olden 2011). Interakce mezi invazními populacemi nepůvodních druhů a původními společenstvy nekončí nutně negativními interakcemi. Existuje poměrně velké množství případů, kdy nepůvodní druhy rozličnými způsoby podpořily druhy původní (Rodriguez 2006), což

můžeme označit pozitivní ekologický dopad. Ekonomický přínos introdukcí nepůvodních druhů není rovněž nutné zpochybňovat (Gozlan 2008). Nicméně, změny způsobené v dosavadním fungovaní těchto funkčních celků a výskyt zcela nových interakcí může vést k homogenizaci lokální bioty nebo až k nenávratné ztrátě mnohdy unikátních sladkovodních ekosystémů (Rahel 2002; Mollot et al. 2017).

2.5 Invaze hlaváčovitých ryb

Hlaváčovité ryby s více jak 2000 druhů, představují jednu z nejpočetnějších čeledí kostnatých ryb. Zástupci této čeledi (Gobiidae) jsou nejčastěji malé bentické ryby s velikostí nepřesahující 10 centimetrů obývající převážně mořské prostředí, v menším množství jsou zastoupeny druhy, obývají brakické a sladké vody (Nelson 1994). Typickým znakem hlaváčovitých ryb jsou břišní ploutve srostlé v přísavný terč, absence plynového měchýře a specifický způsob rozmnožovaní. Hlaváči jsou totiž řazeni mezi speleofilní druhy ryb, které k rozmnožování vyžadují dutiny mezi kameny nebo jiné podobné struktury (Miller 1986). K úspěchu hlaváčovitých ryb při kolonizaci nových areálů přispívá řada vlastností typických pro nejúspěšnější invazní druhy. Patří mezi ně vysoká plodnost doplněná o rodičovskou péči samců o jikry (zaručující reprodukční úspěšnost těchto ryb), dále pak fyziologická tolerance k široké škále přírodních faktorů, omnivorie, krátký generační čas a agresivní chování (Sakai et al. 2001; Marchetti et al. 2004; Havel et al. 2015). Díky těmto vlastnostem najdeme mezi hlaváči druhy, které značně rozšířily svůj původní areál výskytu. S invazemi ve sladkovodních ekosystémech jsou nejčastěji spojovány ryby z podčeledi Benthophilinae, konkrétně hlaváč Kesslerův (Pontikola kessleri), hlaváč dněsterský (Babka gymnotrachelus); hlaváč říční (Neogobius fluviatilis); hlavačka poloměsíčitá (Proterorhinus semilunaris) a především hlaváč černoústý (Neogobius melanostomus) (Copp et al. 2005; Roche et al. 2013), který bude v popředí zájmu i v rámci této disertační práce. Všechny vyjmenované druhy mají svůj původ v Ponto-Kaspické oblasti. A i když jejich areál původního výskytu zasahoval do dolních až středních částí velkých řek (Dunaj, Volha, Dněpr, Don) ústících do Černého, Kaspického nebo Azovského moře, 20

dlouho nedošlo k přirozenému šíření hlaváčů výše proti proudu těchto toků. Půdu pro budoucí expanzi připravilo až budování plavebních koridorů pro lodní dopravu a technické úpravy vodních toků usnadňující plavbu, které vytvořily volnou ekologickou niku v podobě pozměněných nebo zničených habitatů (Mollot et al. 2017). Řada těchto vodních cest vznikala již před desítkami až stovkami let (Rakauskas et al. 2016). Nicméně, primárním podmětem pro rozvoj invazí Ponto-Kaspických druhů byly geopolitické a socio-ekonomické změny, které probíhaly v několika vlnách až od 60 let 20. století, jež vedly k dalšímu rozvoji a zintenzivnění lodní dopravy, včetně budování nových plavebních kanálů, jako je například průplav Dunaj – Mohan – Rýn (Panov et al. 2009; Roche et al. 2013). V současnosti síť plavebních kanálů v Evropě přesahuje délku 28 000 kilometrů a propojuje 37 zemí (Panov et al. 2009). Tyto zásahy otevřely hlaváčům i dalším nepůvodním druhům z Ponto-Kaspické oblasti cestu do nových, dříve nedosažitelných oblastí prostřednictvím tří hlavních koridorů. Severní koridor propojil Černé a Azovské moře s Kaspickým přes kanál Don – Volha. Na Volhu posléze navazují vodní cesty umožňující propojení s Baltským a Bílým mořem. Centrální koridor spojil vodní cestou přes Dněpr – Pripyat – Bug – Vislu, Černé moře s Baltem. Jižní koridor propojil Černé moře se Severním mořem kanálem Dunaj – Mohan – Rýn (Copp et al. 2005; Panov et al. 2009). Mimo hlavní invazní koridory existuje v Evropě rozvětvená síť dalších vodních cest s pontenciálem zprostředkovávat invaze nepůvodních druhů; např. Panov et al. (2007) uvádí síť tvořenou 30 hlavními větvemi a více než 100 menších větví s 350 přístavy. Hlavním impulsem pro zvýšení zájmu o hlaváčovité ryby však bylo objevení hlaváče černoústého ve Velkých jezerech v Severní Americe v roce 1990 (Jude et al. 1992) a jeho následné rapidní rozšíření v celé oblasti s negativním dopadem na lokální společenstvo (Charlebois et al. 1997; Bronnehuber et al. 2011; Kornis et al. 2012). Ve stejnou dobu jako v Americe byl výskyt hlaváče černoústého potvrzen i v Baltském moři (Skóra & Stolarski 1993), kde se populace hlaváče začala rovněž rychle rozrůstat a šířit (Skóra & Sapota 2005). V obou případech je nasnadě způsob zavlečení hlaváče černoústého do nového prostředí. Lokalizace prvních jedinců hlaváčů uvnitř nebo v blízkosti říčních (vnitrozemských) přístavů jednoznačně indikují lodní dopravu jako hlavní vektor přesnosu (Charlebois 1997; Skóra & Sapota 2005; Wiesner 2005). Genetická data potvrdila, že na počátku těchto významných invazí bylo introdukováno

velké množsví jedinců hlaváče čenoústého (v menším počtu u hlavačky mramorované) během několika transportů z různých zdrojových oblastí (Dillon & Stepien 2001; Brown & Stepien 2009). Mechanismus transportu není zcela prostudován, nicméně jako nejpravděpodobnější se zdá být transport larev hlaváčovitých ryb v tancích na balastní vodu v nákladních lodích. Larvy hlaváčů se v době po soumraku přesouvají do horních vrstev vodního sloupce, kde se živí zooplanktonem. Nákladní lodě čerpající balastní vodu tak mohou načerpat tisíce „larválních“ jedinců, kteří jsou schopní přežít v podmínkách balastních nádrží po dlouhou dobu (Hayden & Miner 2009; Kornis et al. 2012). Wonham et al. (2000) uvádí, že hlaváčovité ryby jsou hojně zastoupeny ve společnstvech obývajících jeskyně a další habitaty s nedostatkem světla, což může představovat preadaptaci pro přepravu v balastních nádržích. Lodní doprava tak bezesporu představuje primární vektor šíření hlaváčovitých ryb. Náhodné introdukce lodní dopravou do nového ekosystému se týkají zejména toků, které mají pro tento typ přepravy vhodné podmínky (např. Dunaj – Mohan – Rýn) nebo velkých vodních ploch s hustou sítí lodní dopravy (Severo-Americká Velká jezera). Proniknutí hlaváčovitých ryb do menších splavných toků s nízkou intenzitou lodní přepravy touto cestou je mnohem méně pravděpodobné, přičemž nesplavné toky jsou zcela mimo dosah tohoto vektoru. I přesto jsou nesplavné toky kolonizovány hlaváčovitými rybami ve velkém rozsahu a až s překvapivou rychlostí, vezmeme-li v úvahu jejich morfologii (Miller 1986) a dříve popsané chování těchto ryb predikující omezenou pohyblivost (Ray & Corkum 2001; Brownscombe & Fox 2012). Nejpravděpodobnějším možným vysvětlením je šíření pomocí vlastní pohybové aktivity podpořené úmyslnými nebo náhodnými introdukcemi nesouvisejícími s nákladní lodní dopravou.

2.5.1 Rychlost „přirozeného“ šíření hlaváčů

Disperze hlaváčovitých ryb prostřednictvím přirozené pohybové aktivity stála dlouho mimo zájem výzkumníků (Landsman et al. 2011). Teprve až s pronikáním hlaváčů do nesplavných toků a menších přítoků vzrostla i pozornost věnovaná tomuto procesu, který můžeme označit jako sekundární fázi invaze (Poos et al. 2010; Bronnenhuber et al. 2011; Kornis et al. 2017). Naprostá většina studií zabývajících se touto fází invaze

Ponto-Kaspických hlaváčů je zaměřena na hlaváče černoústého, který vykazuje nejvyšší rychlost šíření společně s největším potenciálem ke škodlivému působení na původní ekosystémy. V teoretických odhadech i v empirických měřeních přirozené disperzní rychlosti (pohybové aktivity) hlaváčovitých se objevují značné rozdíly. V literatuře se můžeme setkat s rychlostí šíření v rozsahu od 0,5 km/rok (Bronnenhuber et al. 2011) přes 1-4 km/rok (Kornis et al. 2012) až po 17 km/rok (Brandner et al. 2013), kdy se rychlost šíření v těchto studiích většinou odvozuje od vzdálenosti, kterou hlaváči urazí během roku v nesplavných tocích od poslední známé lokality výskytu, přičemž se horní hranice rychlosti šíření zdá být příliš vysoká pro přirozenou disperzi. I když hlaváč je schopen krátkodobě vyvinout vysokou rychlost (při únikové reakci až 163 m/s-1; Tierney et al. 2011), udržení konstantního vysokého tempa je energeticky náročné a není proto reálné, aby hlaváč plaval takovou rychlostí po delší dobu. V případech rychlého „přirozeného“ protiproudého šíření je tak velice pravděpodobné, že do tohoto procesu alespoň částečně zasáhl člověk. Podporu pro toto tvrzení můžeme najít v modelu vytvořeném Brownscombe et al. (2012), který pracuje s introdukcemi prostřednictvím rybářů a predikuje následný rychlý posun invazní fronty (27 km/rok). Navíc bylo prokázáno, že i rekreační plavba (malé čluny) může zprostředkovat transport hlaváčů do dříve obtížně dostupných nebo naprosto izolovaných lokalit. Jikry hlaváčů nakladené na trup malých rekreačních člunů dokáží přežít dlouhou dobu mimo vodu. Hirsch et al. (2016a) prokázali, že líhnutí raných vývojových stádií proběhlo úspěšně u 95% jiker deponovaných mimo vodu po 24 hodin. Přejezdy rekreantů mezi lokalitami mohou vést k posunu invazní fronty prostřednictvím člověka a opět zkreslit reálnou rychlost přirozeného šíření. Za výhradně přirozeným posunem hranic stávajícího areálu stojí čelo invazní fronty tvořené pionýrskými jedinci a následně populacemi jejich potomků se stejnými specifickými vlastnostmi (fenotypem). V extrémních případech může nastat tzv. efekt olympijské vesnice, kdy se množí na invazní frontě pouze jedinci s nejlepší schopností disperze (Chuang & Peterson 2016). Nicméně, stejně jako u rychlosti šíření, ani v tomto případě nepanuje jednoznačná shoda v tom, jaké vlastnosti převládají v populaci pionýrských jedinců a rozdíly nalezneme jak v geograficky vzájemně vzdálených oblastech, tak i v jednotlivých povodích. Můžeme se tak setkat se studiemi, které

dokumentují jako nejvíce disperzní jedince v populaci velké dospělé ryby (Gutowsky & Fox 2011; Brandner et al. 2013). Jiné studie jako nositele invaze navrhují malé jedince (převážně samce), kteří byli vytlačeni při kompetici s teritoriálními velkými jedinci z vhodného prostředí a museli hledat teritorium na hranici jádrové oblasti výskytu nebo za ní (Ray & Corkum 2001; Brownscombe & Fox 2012; Massson et al. 2016). Ačkoli je v případě ryb závislost pohybové aktivity na pohlaví studována poměrně málo, je možné v obecné rovině tvrdit, že vyšší míru pohyblivosti u polygynních ryb vykazují samci (Hutchings & Gerber 2002; Gros et al. 2009). I v případě hlaváče černoústého byla laboratorně prokázána vyšší intenzita pohybové aktivity samců (Marentette et al. 2011), konečně i terénní výzkum přinesl podporu tomuto názoru (Corkum et al. 2004; Young et al. 2010; Thompson & Simon 2015). Navzdory těmto skutečnostem se v literatuře setkáváme i s opačným trendem, kdy se na invazní frontě vyskytovaly ve větších počtech samice, což může poukazovat na jejich zvýšenou pohybovou aktivitu (Brownscombe & Fox 2012; Brandner et al. 2013). Možným vysvětlením může být reprodukční chování a systém párování. U hlaváče černoústého teritoriální samec v době rozmnožování brání úkryt, do kterého několik samic postupně ukládá jikry, a o nakladenou snůškou pak samec pečuje do vylíhnutí jiker (Marentette et al. 2009). Zvýšená pohybová aktivita samic tak může mít původ ve vyhledání dominantních samců a jejich hnízd. V některých případech se proto můžeme setkat s poměrem pohlaví výrazně vychýleným ve prospěch samic (Bergstrom et al. 2008). V předešlých kapitolách bylo pojednáváno o šíření dospělých jedinců hlaváčů prostřednictvím vektorů nebo vlastní pohybové aktivity. I raná vývojová stádia hlaváčovitých ryb přispívají svojí pohybovou aktivitou k procesu kolonizace potažmo invaze. Již dříve zde bylo zmíněno, že raná vývojová stádia hlaváčů ve večerních a nočních hodinách vystupují ke hladině za potravou a při tom mohou být načerpány do balastních nádrží nákladních lodí a převezeny na značné vzdálenosti (Hensler & Jude 2007; Hayden & Miner 2011). I když byl tento druh chování zdokumentován ve stojatých vodách, je nanejvýš pravděpodobné, že v tekoucích vodách se bude vyskytovat podobný druh pohybové aktivity raných vývojových stádií hlaváčovitých ryb. Tímto mechanismem je takzvaný drift, který představuje „pasivní“ poproudý pohyb, objevující se ve specifické fázi ontogenetického vývoje (larvy nebo raná juvenilní stádia) většiny druhů ryb žijících v tekoucích vodách, přičemž navazuje na

třecí protiproudou migraci adultních jedinců. Drift, jako specifický disperzní mechanismus, slouží larválním a juvenilním rybám především k přemístění z třecích míst do habitatu nejvhodnějšího pro jejich růst (Pavlov 1994; Reichard & Jurajda 2007). Celý proces driftu se odehrává téměř výhradně za snížené světelné intenzity s vrcholem v nočních hodinách (Pavlov 1994; Oesmann 2003; Zitek et al. 2004; a mnozí další). Je známo, že raná vývojová stádia hlaváčovitých ryb [u hlaváčů se nesetkáme s pravým larválním stádiem (Jůza et al. 2016)] v původním areálu do driftu vstupují (Pavlov 1994, Vassilev 1994, Zitek et al. 2004), avšak rozsah této specifické pohybové aktivity v nově kolonizovaných areálech je zdokumentován pouze minimálně (Borcherding et al. 2016; Ramler et al. 2016).

2.5.2 Vliv nepůvodních hlaváčů na původní ekosystém

Pohybová aktivita hlaváčovitých ryb velmi úzce souvisí s jejich invazním potenciálem a je proto vhodné alespoň v krátkosti zmínit jak reálná, tak potenciální rizika vyvstávající pro konkrétní ekosystémy z invazí hlaváčů. První a současně nejzávažnější zmínky o ovlivňování ekosystémů hlaváčovitými rybami byly pozorovány nedlouho po invazi hlaváče černoústého do Severní Ameriky. Bezprostředně po úspěšném usazení hlaváče černoústého v oblasti Velkých jezer byl zaznamenán významný pokles v abundanci makrozoobentosu (Kuhns & Berg 1999; Lederer et al. 2008; Kipp & Ricciardi 2012), který se nevyhnul ani populacím měkkýšů (Poos et al. 2010; Kipp et al. 2012). I pokles abundance, zejména malých bentických ryb (Cottus spp., Etheostoma spp.), je dáván do spojitosti s mezidruhovou kompeticí o úkryty a přímou predací ze strany hlaváčovitých ryb (Janssen & Jude 2001; Lauer et al. 2004). Experimentální studie rovněž potvrdily možnost škodlivého působení na některé hospodářsky významné druhy ryb (Micropterus dolomieu; Steinhart et al. 2004). Ve většině případů z Evropy je zmiňován pouze potenciální negativní vliv hlaváčovitých ryb na ichthyofaunu prostřednictvím kompetice o potravu či predace (Jurajda et al. 2005; Karlson et al. 2007; Copp et al. 2008). Pouze v případě vymizení ježdíka obecného (Gymnocephalus cernua) z některých holandských jezer můžeme mluvit o jasně prokazatelném negativním vlivu invaze hlaváčů v Evropě (Jůza et al. 2018).

Hlaváč černoústý stojí také za vznikem nových energetických toků v ekosystému Velkých jezer, kdy zpřístupnil energii vázanou v dalším významném invazním druhu slávičce mnohotvárné (Dreissena polymorpha) do vyšších trofických stupňů (Johnson et al. 2005). Současně ovšem také uvolnil do oběhu škodlivé látky vázané ve slávičkách (Hogan et al. 2007). U zbylých druhů invazních hlaváčovitých ryb (Pontikola kessleri a Babka gymnotrachelus) vyskytujících se v Evropě, je potenciální vliv na původní druhy zdokumentován zejména v laboratorních podmínkách (van Kessel et al. 2011; Kakareko et al. 2013; Grabowska et al. 2016; Błońska et al. 2017), avšak údaje o vlivu na původní společenstva z přirozeného prostředí jsou stále omezené (van Kessel et al. 2016). Ačkoli je parazitofauna nepůvodních hlaváčovitých ryb velmi bohatá, nebyl prokázán významnější přenos parazitů a onemocnění do nově kolonizovaných oblastí (Ondračková et al. 2005; Kvach & Stepien 2008). Naopak v invazních severoamerických a evropských populacích slouží hlaváčovití jako hostitelé lokálních parazitů (Kvach & Stepien 2008; Francová et al. 2011). Z těchto nových hostitelsko- parazitických vztahů však mohou za jistých okolností vzniknout nebezpečné situace pro původní hostitele i parazity. „Parasite spillback“ je stav, kdy se původní druh parazita úspěšně množí na nepůvodním hostiteli, čímž zvyšuje riziko infekce pro původní druhy (Kelly et al. 2009a). Na druhé straně může nastat tzv. „dilution effect“, při kterém dochází k poklesu abundance původních parazitů, kteří nejsou schopni úspěšně dokončit vývoj na nepůvodním hostiteli (Kelly et al. 2009b). Oba tyto jevy mohou mít nepředvídatelné následky pro celý hostitelsko-parazitický systém. Invaze hlaváče nemusí mít pouze negativní dopady. Hlaváč představuje významný komponent v potravě původních severoamerických i evropských predátorů (Sommers et al. 2003; Corkum et al. 2004; Reyjol et al. 2010; Madenjian et al. 2011; Płąchocki et al. 2012). Nicméně, ani tato dílčí pozitiva nezlepší náhled na hlaváče černoústého v Severní Americe, kde platí za jeden z nejhorších sladkovodních invazních druhů. V Evropě rovněž panují obavy z invaze hlaváčovitých ryb a zejména pak hlaváče černoústého, který byl dokonce zařazen mezi 100 nejhorších invazních druhů Evropy (Hirsch et al. 2016b). Přesto se situace v evropských tocích z pohledu škodlivosti hlaváčovitých nejeví natolik vážná jako v Severní Americe, což může být přisouzeno geografické blízkosti původního areálu výskytu hlaváčovitých ryb a značně

pozměněným lokálním společenstvům, která jsou často tvořena směsicí původních i nepůvodních druhů živočichů a rostlin již adaptovaných na silně antropogenně ovlivněné prostředí (Ricciardi 2013). Jako příklad lze uvést vliv hlaváčovitých ryb na zástupce čeledě vrankovitých (Cottidae) v Evropě. Zatímco populace vranky britské (Cottus perifretum) v řece Máze (Belgie) značně poklesla po introdukci hlaváčovitých, především hlaváče černoústého (van Kessel et al. 2016), v rakouském úseku Dunaje je populace blízce příbuzné vranky obecné (Cottus gobio) stále stejně početná i po invazi hlaváčovitých (Janáč et al. 2018). Geografická blízkost původního areálu hlaváčovitých ryb (dolní Dunaj) i historický výskyt hlavačky mramorované na území Rakouska je jednou z možných příčin větší odolnosti lokálních populací vranek vůči invazi hlaváčů.

2.6 Invaze hlaváčů do ČR

Rychlost posunu invazní fronty je výsledkem součinnosti různých faktorů jako jsou populační hustota, přítomnost vhodného habitatu, charakter toku, teplota vody, přítomnost migračních bariér a řady dalších okolností, které v různé míře ovlivňují disperzní schopnosti hlaváčovitých ryb. Z tohoto důvodu není reálné určit přesný vzor v šíření invazního druhu jako takového (obecně platný vzor pro celý druh), ale pouze pro jednotlivé invazní populace v konkrétních podmínkách, podle kterých je následně možné předvídat i dopad na lokální společenstva. Přesné určení doby proniknutí hlaváčovitých ryb do vod České republiky nelze s naprostou jistotou určit. Dané druhy mohly po relativně dlouhou dobu v nízkých populačních hustotách obývat vhodné habitaty, aniž byly zaznamenány nebo mohlo dojít i k jejich chybné determinaci, obzvláště při zachycení sportovními rybáři. Jako počátek invaze bude v dalším průběhu stanoven první oficiálně potvrzený záznam výskytu konkrétního druhu.

2.6.1 Hlavačka poloměsíčitá

První ověřený záznam o výskytu nepůvodní hlaváčovité ryby na území ČR pochází z roku 1994, kdy Lusk a Halačka (1995) zaznamenali 3 dospělé jedince hlavačky

mramorované (obr. 2a) v Novomlýnských nádržích na řece Dyji (horní Mušovská nádrž). Pravděpodobný původ těchto jedinců můžeme hledat v introdukci sportovními rybáři z blízkých původních populací v Rakousku a na Slovensku, odkud byly hlavačky přivezeny jako nástražní ryby a následně vypuštěny do našich vod. V následujících letech hlavačka rychle kolonizovala celý úsek toku Dyje od Novomlýnských nádrží po soutok s řekou Moravou (Prášek & Jurajda 2005). Významnou roli v tomto procesu hrál drift raných vývojových stádií z Novomlýnských nádrží, kde hlavačka poloměsíčitá dosáhla během relativně krátké doby značných populačních hustot (Janáč et al. 2012; Janáč et al. 2013). Následně se v roce 1998 hlavačka poloměsíčitá objevila v řece Moravě nad soutokem s Dyjí (Lusk et al. 2000) a také v malé izolované populaci v Podhradí nad Dyjí (Švátora et al. 2000). Expanze areálu pokračovala proti proudu Dyje a jejich přítoků (Jihlava, Jevišovka, Svratka, Kyjovka) i proti proudu Moravy. Současně byl potvrzen výskyt hlavačky mramorované v některých zemnících a mrtvých ramenech v oblasti soutoku Moravy a Dyje (obr. 3). Přítomnost hlavačky v obhospodařovaných rybnících Rybníkářství Pohořelice představuje další potenciální možnost rozšiřování stávajícího areálu. Hlavačky mohou být neúmyslně převezeny společně s násadou hospodářsky významných druhů ryb do celé řady hospodářsky využívaných vodních těles (Kopeček 2013). Přesnou velikost areálu nepůvodní hlavačky mramorované na území České republiky není možné určit, nicméně lze očekávat postupný posun hranice rozšíření od stavu zdokumentovaného v roce 2012 (Kopeček 2013). Potravní analýzy (Adámek et al. 2010; Všetičková et al. 2014) ani parazitické vyšetření hlavaček (Koubková & Baruš 2010) neprokázaly významný negativní vliv na původní ichtyofaunu. Rovněž habitatová preference je natolik specifická, že nenabízí prostor pro případnou kompetici o úkryty s původními rybami. Jediným možným negativním dopadem tak může pravděpodobně být konkurence o potravní zdroje, zejména s plůdkem původních druhů ryb.

Obrázek 2. Nepůvodní hlaváčovité ryby v České republice; a) hlavačka poloměsíčitá, b) hlaváč černoústý.

2.6.2 Hlaváč černoústý

Proniknutí hlaváče černoústého (obr. 2b) do vod České republiky je poměrně recentní událostí. První potvrzený záznam o výskytu tohoto druhu na území ČR pochází z roku 2008. Lusk et al. (2008) popisují zachycení tří jedinců v řece Moravě v blízkosti soutoku s řekou Dyjí a dvou jedinců v řece Dyji v poměrně velké vzdálenosti proti proudu od soutoku s Moravou (říční kilometr 26,7; jez Břeclav). S největší pravděpodobností mají tito jedinci původ ve Slovenské části Moravy, odkud za vhodných podmínek mohli vlastní pohybovou aktivitou proniknout až do sledovaného území (Lusk et al. 2008). V následujících letech probíhalo postupné zvyšování populační hustoty na lokalitách s dříve potvrzeným výskytem a postupné šíření proti proudu obou řek (Kopeček 2013; Jurajda et al. 2015). V roce 2015 byl hlaváč zaznamenán i v dolním toku českého Labe (Svádov), kam pronikl pravděpodobně prostřednictvím lodní dopravy (Roche et al. 2015). Ačkoli v oblasti kolonizované hlaváčem ústí do Labe několik jeho přítoků (Bílina, Ploučnice, Kamenice), průnik hlaváče do těchto toků nebyl prozatím zjištěn. Aktuální areál rozšíření hlaváče černoústého v ČR tak zahrnuje dolní části Dyje, Moravy, Kyjovky a úsek Labe od státní hranice s Německem až po Střekovský jez (obr. 3). Pronikání hlaváče do izolovaných malých vodních ploch a slepých říčních ramen zmíněných toků je pouze sporadické. Podobně jako v případě hlavačky mramorované ani u hlaváče černoústého nebylo prozatím prokázáno přímé škodlivé působení na naši původní ichtyofaunu. Predátorem našich původních druhů ryb se hlaváč černoústý nestal (Vašek et al. 2014) a ani jako vektor nových parazitů či onemocnění nebyl potvrzen, ačkoli je třeba zmínit možný vliv na dosavadní hostitelsko-parazitické vztahy v nově obsazeném areálu (Ondračková et al. 2015). Potenciální hrozbou zůstává hlaváč pro společenstva makrozoobentosu a některé druhy mlžů (Jurajda et al. 2015; Mikl et al. 2017a). Bohaté společenstvo makrozoobentosu s vysokou populační hustotou na dolní Dyji společně s habitatovou preferencí hlaváčovitých (kamenný zához) pravděpodobně omezilo dopad těchto ryb na původní ichtyofaunu (Mikl et al. 2017a), nicméně pokud by došlo k invazi hlaváče do méně úživného prostředí nebo ke změně aktuálního stavu na stávajícím kolonizovaném území, nelze vyloučit negativní působení hlaváče černoústého prostřednictvím potravní kompetice o omezené zdroje.

Na druhé straně se hlaváč černoústý stává kořistí lokálních predátorů a i v našich vodách představuje významný zdroj potravy původních dravých ryb (Mikl et al. 2017b).

hlaváče ČR. v černoústého a poloměsíčité rozšíření Mapa 3. areálu hlavačky Obrázek

3. Cíle práce

Při studiu menších a středních vodních toků kolonizovaných hlaváčem černoústým se pozornost koncentruje mnohem více na interakce s lokální, často unikátní faunou než na rozsah jeho pohybové aktivity a disperze (Phillips et al. 2003; Poos et al. 2010; Kornis et al. 2013). Rychlost šíření hlaváčů v takovýchto typech toků je tak opomíjena, ačkoli je zdrojem cenných informací. Znalost disperzních schopností hlaváčovitých ryb a intenzity jejich pohybové aktivity by nám umožnila predikci (i) populační dynamiky a s ní spojené předpovídání potenciálního ohrožení ekosystémů v již invadovaných tocích nebo (ii) průběhu (rychlosti) invaze v nově obsazených ekosystémech. Využití nalezne i při prevenci a managementu invazních hlaváčovitých ryb. Cílem této disertační práce je přinést detailní informace o rozsahu pohybové aktivity nepůvodních hlaváčovitých ryb a rovněž podrobně popsat mechanismy invazního procesu v rámci území České republiky i mimo něj. Předložená disertační práce se prostřednictvím jednotlivých publikací věnuje těmto dílčím cílům:

1. Pochopení mechanismů šíření nepůvodních hlaváčovitých ryb (článek A,B, C, D, E)

2. Zjištění rozsahu pohybové aktivity nepůvodních hlaváčovitých ryb pomocí značení (článek A)

3. Zjištění pohybové aktivity juvenilních jedinců pomocí driftových sítí (článek D, E)

4. Případné navržení mechanismů vhodných pro zastavení šíření těchto druhů

4. Shrnutí jednotlivých publikací

4.1 Publikace (Rukopis) A

Šlapanský L., Janáč M., Roche K., Jurajda P. (2019). Round goby movement patterns in a non-navigable river. Odesláno do Canadian Journal of Fisheries and Aquatic Research 11. 12. 2018.

V rámci naší studie jsme se provedením série terénních experimentů pokusili stanovit rozsah pohybové aktivity hlaváče černoústého, jakožto našeho modelového druhu a doplnit tak znalosti o pohybové aktivitě tohoto druhu v invadovaném areálu. Pozornost byla věnována zejména pohybu na individuální úrovni (pohlaví, velikost) a sezónním změnám v rozsahu pohybové aktivity. Pro získání dat o pohybové aktivitě hlaváče černoústého byly použity tři terénní experimenty. Při každém z nich byl jako odlovný prostředek použit elektrický agregát, jakožto nejvhodnější metoda pro odlov hlaváčovitých ryb v podmínkách dolního toku Dyje. V prvním experimentu byly prostřednictvím individuálního značení za použití značek opatřených číselným kódem (Visible Implant Alpha tag; Northwest Marine Technology Inc.) získávány detailní informace o pohybu jedinců v úspěšně usazené populaci během sezóny a potenciálních vlastnostech pionýrských jedinců. Ve druhém experimentu byla značením velkého množství jedinců pomocí barevného viditelného implantovaného elastomeru (Visible Implant elastomer; Northwest Marine Technology Inc.) a jejich následným hromadným vypuštěním simulována introdukční událost, při které byl monitorován následný rozptyl označených jedinců. V posledním, rekolonizačním experimentu, byla sledována rychlost obsazování habitatu uvolněného přechozím vylovením, což nám umožnilo determinovat vlastnosti ryb tvořících invazní frontu. Výsledná data záskaná individuálním značením prokázala, že jedinci v úspěšně zavedené populaci jsou z větší části (58.9%) věrni konkrétnímu místu (extrémním případem jsou jedinci nalezení na stejném místě po 265 dnech), přičemž zde nehrálo roli pohlaví ani velikost ryb. Na druhé straně malý počet jedinců ovšem dokázal překonat poměrně velkou vzdálenost (téměř 30 metrů za den), navzdory obecně 33

zažitému paradigmatu o omezéné pohyblivosti, což nasvědčuje, že hlaváč černoústý může být překvapivě efektivní v rozšiřování svého areálu i prostřednictvím vlastní pohybové aktivity. U pohyblivých jedinců převládal protiproudný pohyb s největší intenzitou během reprodukčního období (64.7% označených jedinců odlovených v reprodukčním období bylo zaznamenáno mimo původní úsek). Tento trend potvrdil i druhý (VIE) experiment. Pokud dojde k vypuštění většího množství jedinců na jedné lokalitě (tak jako se děje například při vypuštění balastní vody), větší část nově vzniklé populace zůstane na místě. Zbylí jedinci však urazí relativně velkou vzdálenosti od místa vypuštění (tato vzdálenost je několikanásobně větší v porovnání s běžným pohybem v úspěšně zavedené populaci). V obou případech převládal protiproudý směr pohybu. U pohlaví nebyl prokázán jednoznačně převládající trend v intenzitě pohybové aktivity ve prospěch ani jednoho pohlaví. Pouze malí samci vykazovali vyšší míru aktivity v porovnání s velkými samci. Rekolonizační experiment pak ukázal jako pohyblivější především menší jedince, což bylo pravděpodobně způsobeno vnitrodruhovou kompeticí. Výsledky našich experimentů prokázaly, že většina populace je tvořena méně pohyblivými jedinci, kteří jsou věrní svému domovskému okrsku. Naproti tomu málá část populace tvořená převážně menšími jedinci, zejména samci, vykazuje vysokou míru exploračního chování a dokáže rozšiřovat areál výskytu na poměrně velké vzdálenosti. Prokázali jsme, že malá bentická ryba, jakou je hlaváč černoústý, je schopna úspěšně kolonizovat dlouhé úseky toků pouze pomocí své vlastní pohybové aktivity.

4.2 Publikace B

Šlapanský L., Janáč M., Roche K., Mikl L., Jurajda P. (2017). Expansion of round gobies in a non-navigable river system. Limnologica, 67, 27-36.

V naší studii jsme se zaměřili na zjištění rychlosti šíření hlaváče černoústého pomocí sledování posunu invazní fronty v nesplavných nížinných tocích bez lodní dopravy, konkrétně v řekách Moravě a Dyji. V návaznosti na rozšiřování tohoto nepůvodního druhu jsme se rovněž zaměřili na vývoj jeho invazní populace a možný dopad na společenstvo původních druhů ryb v nově kolonizovaném kamenném záhozu. Materiál byl získáván pomocí elektrolovu v příbřežním kamenném záhozu na osmi lokalitách po dobu šesti let. Lokality byly rozmístěny v blízkosti migračních bariér a na úsecích toků s vhodným substrátem (výskyt hlaváče černoústého je vázán na kamenný zához) tak, aby byla maximalizována pravděpodobnost detekce pionýrských jedinců. Vzdálenosti mezi lokalitami současně sloužily k odhadnutí rychlosti šíření hlaváče černoústého. Rychlost šíření hlaváče, respektive rychlost posunu jeho invazní fronty, byla vyšší v Dyji (3.2 km/rok) než v Moravě (1.2 km/rok), což bylo pravděpodobně zapříčiněno vyšším výskytem „neprostupných“ migračních bariér v řece Moravě. Invazní fronta je podle našich zjištění tvořena jen malým počtem pionýrských jedinců s tím, že v prvních letech invaze byli mezi pionýry hlavně dospělí jedinci větších velikostí. S dalším postupem fronty proti proudu došlo ke změně ve velikosti pionýrů, kteří byli nově reprezentováni malými dospělými jedinci a dokonce i juvenily. Poměr pohlaví na jednotlivých lokalitách byl poměrně variabilní s častějšími lokálními výchylkami ve prospěch samic, které však nebyly statisticky významné. Závazné určení mobilnějšího pohlaví s významnější rolí v invazním procesu nebylo možné s jistotou určit. Negativní vliv na společenstvo původních druhů ryb nebyl prozatím pozorován. Pravděpodobně jediným ovlivněným druhem byla nepůvodní hlavačka poloměsíčitá, u které došlo po objevení se hlaváče k poklesu populační hustoty na některých lokalitách. Šíření nepůvodních hlaváčovitých ryb vlastní pohybovou aktivitou představuje další fázi invazního procesu, který už řadu let v Evropě i Severní Americe probíhá. Charakteristika invazních populací je však značně variabilní a je obtížné definovat

konkrétní velikost, pohlaví nebo stáří ryb odpovědných za rozšiřování areálu nepůvodního druhu. Stávající situace jen potvrzuje značnou diverzitu panující mezi invazními populacemi hlaváčovitých ryb, čímž přikládá větší význam lokálním studiím při predikci šíření invazních populací a jejich možného vlivu na konkrétní ekosystém.

4.3 Publikace C

Roche K., Janáč M., Šlapanský L., Mikl L., Kopeček L., Jurajda P. (2015). A newly established round goby (Neogobius melanostomus) population in the upper stretch of the river Elbe. Knowledge and Management of Aquatic Ecosystems, 416, 33.

Cílem studie bylo zmapovat aktuální rozšíření hlaváče černoústého v recentně osídleném českém úseku řeky Labe a současně provést charakteristiku invazní populace. Doplňkové získání dat o stavu společenstva původních druhů ryb by mělo v budoucnu sloužit k posouzení vlivu hlaváče na původní ichtyofaunu. Materiál byl sbírán pomocí elektrolovu na čtyřech profilech v úseku Labe od Dolního Žlebu (poblíž německé hranice) až po střekovský jez v Ústí nad Labem. Všechny profily byly umístěny v úsecích upravených kamenným záhozem, jenž představuje preferovaný habitat hlaváče černoústého. Ulovení jedinci hlaváče černoústého byli fixováni a v laboratoři byla provedena jejich podrobná morfometrická charakteristika. Populace hlaváče černoústého objevená v Labi u Svádova (Ústí nad Labem) a v Děčíně v roce 2015 má svůj původ s největší pravděpodobností v lodní dopravě, kdy jsou jedinci nebo jejich jikry „rozváženy“ po Evropských přístavech. Zmíněná teorie nalézá oporu v dalším nejbližším výskytu hlaváčů v Labi, který je lokalizován do okolí Hamburku vzdáleného 603 říčních kilometrů. Během tří let by nebyli hlaváči schopni urazit takovou vzdálenost, aniž by byl zaznamenán jejich výskyt v celém úseku Labe mezi Hamburkem a Svádovem. Hlaváči černoústí ulovení ve Svádově (13 jedinců) byli až na jednu výjimku dospělé ryby, zatímco všichni jedinci z lokality Děčín byli určeni jako juvenilové. Toto rozložení jedinců v podélném profilu toku indikuje poproudné šíření v profilu Labe pomocí driftu raných vývojových stadií. Ryby ze Svádova mají shodné meristické znaky s populací hlaváče z Hamburku a odlišné v porovnání s rybami z dolního toku Dyje a Moravy, které představovaly další možnou zdrojovou populaci. I když přenos přes souš prostřednictvím rybářů (nástražní ryby) je poměrně častý, v tomto případě jsme ho i na základě meristických a genetických dat vyloučili. Nově objevená populace jasně dokazuje důležitost lodní dopravy jako vektoru při šíření hlaváčovitých ryb. Pokud k transferu mezi přístavy připojíme schopnost rychlého

šíření po proudu pomocí tzv. driftu a vlastní pohybovou aktivitu proti proudu, dojdeme k závěru, že hlaváč černoústý je skvěle adaptován k rychlé kolonizaci velkých evropských řek. Včasné objevení populace hlaváče nám současně poskytne příležitost pro sledování rychlosti kolonizace v nově obsazených areálech.

4.4 Publikace D

Janáč M., Šlapanský L., Valová Z., Jurajda P. (2013). Downstream drift of round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their non- native area. Ecology of freshwater Fish, 22, 430-438.

Naším cílem v této studii bylo zjistit, zda a do jaké míry nepůvodní hlaváčovité ryby, konkrétně hlaváč černoústý (Neogbius melanostomus) a hlavačka poloměsíčitá (Proterorhinus semuilunaris), využívají pro šíření v nově obsazeném areálu na dolním toku řeky Dyje pasivní po proudý pohyb, tzv. drift. Rovněž jsme se snažili zjistit v jaké velikosti (stáří) raná vývojová stádia zájmových druhů driftují. Dále bylo naším cílem určení denní doby s nejvyšší intenzitou driftu a odhalení sezónního vrcholu driftové aktivity. Za tímto účelem byly v dolním toku Dyje (Břeclav), na lokalitě s dostatečným prouděním, instalovány v týdenních intervalech od května do září 4 driftové sítě, které sloužily k pravidelnému sledování driftujících ryb a bezobratlých organismů. Ve vzorcích patřil hlaváč černoústý k nejpočetnějším a nejčastěji zastoupeným druhům (44% úlovku). Rovnoměrně rozložená přítomnost driftujících hlaváčů v rámci celé odběrové sezóny byla důsledkem rozmnožování rozděleného do několika dávek. Hlavačka poloměsíčitá se naopak vyskytovala především na začátku sezóny a její strategie byla zaměřená pouze na jeden vrchol rozmnožovací aktivity. Drift byl striktně nočním jevem, který u hlaváčovitých ryb začínal hodinu po soumraku a končil hodinu před úsvitem. Většina driftujících ryb byla velmi malého velikostního rozpětí (5-8 milimetrů) a vše nasvědčuje tomu, že drift je záležitostí ryb ve stáří maximálně několika dní a u starších jedinců rychle vymizí. Naše studie potvrdila, že drift je u raných vývojových stádií nepůvodních hlaváčovitých ryb v nedávno obsazeném dolním toku Dyje běžným jevem. Je pravděpodobné, že tímto způsobem raná vývojová stádia přispívají k rychlé kolonizaci řek v po proudém směru (viz publikace C), kdy posouvají areál rozšíření dále po proudu nebo driftem vyplňují mezery mezi pionýrskými jedinci a jádrovou populací v nově obsazených areálech. Náležitou pozornost je proto třeba věnovat všem vývojovým stádiím invazních druhů.

4.5 Publikace E

Šlapanský L., Jurajda P., Janáč M. (2016). Early life stages of exotic gobiids as new host for unionid glochidia. Freshwater Biology, 61, 979-990.

V této studii jsme se zaměřili především na otázku, zda jsou raná vývojová stádia hlaváčovitých ryb vhodnými novými hostiteli pro parazitická glochidia původních i nepůvodních druhů unioidních mlžů. Současně jsme se pokusili zmapovat potenciální dopad nově vznikajících interakcí na populace původních i nepůvodních druhů ryb a unioidních mlžů. Pro účely studie byl zrevidován materiál z publikace D s důrazem na přítomnost glochidií. Ve výsledku se nám podařilo prokázat, že raná vývojová stádia hlaváčovitých ryb představují nového atraktivního hostitele pro glochidia unioidních mlžů (velevrub nadmutý Unio tumidus, škeblice asijská Sinanodonta woodiana). Glochidia nepůvodní škeblice asijské vykazovala větší intenzitu infekce a prevalenci u původních druhů ryb než glochidia původních druhů unioidních mlžů. Nově vzniklé interakce mají několik potenciálních pozitivních i negativních dopadů na všechny účastníky hostitelsko- parazitických vztahů v dolním toku Dyje. Vysoká intenzita infekce může omezovat pohyblivost larválních hlaváčů a jejich příjem potravy, což může vést až k úhynu hostitele. Z tohoto pohledu larvy hlaváčů představují ekologickou past pro původní druhy škeblí za současného snižování početnosti nepůvodních hlaváčů. Na druhé straně vysoká početnost driftujících hlaváčů (s nízkou intenzitou infekce) představuje potenciální bohatý zdroj naivních hostitelů vhodných pro dokončení vývoje glochidií a může vést k postupnému nárůstu populace unioidních mlžů. Pohybová aktivita larválních hlaváčovitých ryb teoreticky může vést k oslabení populací unioidních mlžů v populacích nacházejících se výše proti proudu, jelikož velké množství glochidií by bylo unášeno s driftujícími rybami po proudu pryč z vhodných lokalit. Drift larválních hlaváčovitých ryb také pravděpodobně usnadnil rozšíření nepůvodní škeblice asijské v dolním toku Dyje. Toto zjištění je ve shodě s jevem, při němž vzájemné interakce nepůvodních druhů vedou k usnadnění a urychlení invazních procesů, tzv. „invasion meltdown“.

Naše studie popsala dříve přehlížený aspekt hostitelsko-parazitických vztahů a zdůraznila fakt, že raná vývojová stádia nepůvodních hlaváčovitých ryb a unioidních mlžů hrají významnou roli ve vývoji společenstev zmíněných živočichů v dolním toku Dyje, respektive v dalších říčních ekosystémech.

5. Závěr

V publikacích, které jsou součástí této disertační práce, jsme se zabývali pohybovou aktivitou nepůvodních hlaváčovitých ryb od raných vývojových stádií až po dospělé jedince. Obzvláště jsme se zaměřili na přirozenou složku pohybu (bez zapojení vektorů), která byla doposud překvapivě málo zdokumentována a dlouho stála na pokraji odborného zájmu (Landsman et al. 2011). Dosavadní znalosti o pohybu hlaváčů byly reprezentovány modely a predikcemi šíření, které často vycházely z dat získaných ve splavných tocích (Veléz-Espino et al. 2010; Bronnenhuber et al. 2011; Brownscombe et al. 2012). Laboratorní studie (Tierney et al. 2011; Marentette et al. 2011) nám v tomto ohledu rovněž neposkytnou tak hodnotná data o pohybu jako výzkum a experimenty in situ. Z nevelkého počtu studií zabývajících se rozsahem pohybové aktivity invazních hlaváčovitých ryb v přirozených podmínkách se část zaměřila pouze na určení velikosti domovského okrsku (Ray & Corkum 2001; Cookingham & Reutz 2008) a jen malé procento publikací pojednává výhradně o disperzi invazních hlaváčovitých ryb ve větším rozsahu (Lynch & Mansinger 2012). Přínos informací získaných v rámci disertační práce spočívá v zaplnění prázdných míst v oblasti přirozené pohybové aktivity jakožto součásti invazního potenciálu hlaváčů, zejména na území České republiky (řeky Morava, Dyje a Labe) s tím, že mohou být aplikovány i na jiné případy invazí hlaváčovitých ryb. Nicméně, je třeba mít neustále na paměti rozdíly panující mezi jednotlivými invazními populacemi (genetická a fenotypová plasticita) a rozdílný charakter a vlastnosti nově obsazeného ekosystému. Prokázali jsme, že ve studovaných invazních populacích hlaváče černoústého se vyskytuje určitý malý podíl disperzně zdatných jedinců, schopných urazit i 30 m denně. Takovíto jedinci jsou pravděpodobně zodpovědní za poměrně rychlé šíření invazní fronty v řece Moravě (1.2 km/rok) a Dyji (3.2 km/rok). Charakter pionýrských jedinců (pohlaví, velikost) tvořících invazní frontu se ukázal být značně variabilní na jednotlivých lokalitách i mezi sezónami, nicméně jako převládající složku lze označit malé jedince. V jádrové populaci byl trend ve velikosti mobilních jedinců podobný, avšak s poměrem pohlaví vychýleným směrem k samcům. 42

Některé tyto charakteristiky jsme pozorovali i v nově vznikající populaci na dolním toku Labe. Nicméně, hlavním cílem v této studii bylo poukázat na lodní dopravu jako hlavní vektor introdukcí invazních druhů do oblastí značně vzdálených od areálu jejich nejbližšího výskytu. Vznik a růst této nové invazní populace dokumentuje efektivitu šíření hlaváče černoústého za využití transportního vektoru a vlastní pohybové aktivity. Za rychlým usazením a šířením hlaváče v dolním toku Labe stojí s největší pravděpodobností druh pohybové aktivity specifický pro určitou část ontogeneze jedince. Drift raných vývojových stadií hlaváčovitých ryb byl po dlouhou dobu přehlížen a jeho podíl na invazním procesu nebyl příslušně zdokumentován. V našich studiích jsme prokázali, že noční drift raných vývojových stádií (délka těla 6-8 mm; stáří cca 3-7 dní) hraje podstatnou roli jak v invazním procesu, tak i v mechanismech stabilizujících populaci hlaváčů v nově obsazeném prostředí. Současně jsme zdokumentovali nové hostitelsko-parazitické vztahy mezi ranými vývojovými stádii hlaváčovitých ryb a glochidii původních i nepůvodních druhů mlžů. Pohybová aktivita invazních hlaváčovitých ryb, tak může mít podstatný vliv na celý tento komplex vzájemných interakcí a v konečném důsledku může vyplynout v celou řadu důsledků s dopadem pro celý lokální ekosystém.

Potencionální i reálné nebezpečí související s invazemi hlaváčovitých ryb vedlo k navržení celé řady opatření zabraňujících pokračovaní tohoto procesu. Ačkoli se jako nejúčinnější opatření proti invazím jeví zabránění pronikání jedinců nepůvodního druhu do nového prostředí omezováním již probíhající invaze (Simberloff 2009), je tento postup jen obtížně realizovatelný. Vzájemné propojení jednotlivých ekosystémů množstvím rozličných transportních vektorů a migračních cest téměř znemožňuje zabránit přenosu některých invazních druhů. Díky malému počtu jedinců nepůvodních (invazních) druhů v jednotlivých introdukčních událostech je navíc téměř nemožné včas odhalit potenciální nebezpečí a zakročit v rané fázi invaze, kdy je možné ji zcela eliminovat. Jakmile dojde k naturalizaci a ustálení životaschopné populace, je prakticky nemožné invazní druh z ekosystému odstranit. Například N'Guyen et al. (2016) vytvořili model, podle kterého by bylo třeba pravidelného konstantního úsilí vyvíjeného po dobu dvaceti let, aby byl hlaváč černoústý úspěšně eradikován z obsazeného areálu na horním toku Rýna.

Největší obavy z již probíhající invaze hlaváčovitých ryb panují v oblasti Velkých Severoamerických jezer. Negativní působení hlaváčovitých ryb na lokální ekosystém vedlo k navrhování různých typů opatření, jež by zabránila dalšímu šíření hlaváčů do toků s často unikátními společenstvy ryb a bezobratlých (Poos et al. 2010). Mezi nejběžnější preventivní opatření patří používání pastí s různými typy vnadění (feromony, zvukové nahrávky, potrava) a instalace elektrických bariér, bublinových stěn či zvyšování rychlosti proudění ve vhodných místech (Savino et al. 2001; Noatch & Suski 2012; Isabella-Valenzi & Higgs 2016). Pro eliminaci invazních hlaváčů jsou navrhovány i chemické prostředky (Cupp et al. 2017) a vhodnou alternativou se může stát kontrola pomocí původních predátorů (N'Guyen et al. 2016). Všechna tato opatření však mohou omezit nebo zabránit šíření invazních druhů hlaváčovitých ryb, jen pokud tyto pronikají do cílové oblasti přirozenou cestou. Introdukce nepůvodních druhů ryb prostřednictvím sportovních rybářů či akvaristů představuje přetrvávající problém a i v případě hlaváčů dochází k introdukcím touto cestou (Bronnenhuber et al. 2011). Bez opatření působících na veřejnost a odpovědné osoby nelze efektivně proti invazím bojovat. Zásahy proti šíření hlaváčovitých ryb prostřednictvím dříve zmíněných metod nejsou pro situaci, panující v České republice, v současnosti adekvátní. I když se invazní populace rozšiřuje, děje se tak hlavně v tocích silně ovlivněných člověkem, kde je společenstvo často tvořeno již celou řadou jiných nepůvodních druhů. Přítoky a části sledovaných toků výše proti proudu, obsahující často cenná původní společenstva, nemusí být invazí vůbec zasaženy ani v budoucnu. Průběžné sledování invazní populace a kontrola těchto přilehlých areálů, doplněná o kooperaci s odpovědnými orgány, na něž navazuje dostatečná informovanost veřejnosti (zejména rybáři zapříčiňují záměrné i náhodné introdukce), by měly být dostačující pro zajištění efektivního kontrolního systému, který by reagoval odpovídajícím způsobem na vývoj „invazní“ populace hlaváčovitých ryb v našich vodách. Nicméně, není na místě polevit v úsilí vynaloženém na sledování hlaváčovitých ryb, jelikož se negativní vliv nebo interakce může projevit s časovým zpožděním v rozmanitých složkách ekosystému. Například v transportu škodlivých látek do vyššího stupně potravního řetězce (Kwon et al. 2006; Hogan et al. 2007) nebo změnou hostitelsko-parazitických stavů (viz glochidie).

V současnosti však můžeme říci, že hlaváč černoústý a hlavačka poloměsíčitá obsadili volnou niku v prostředí kamenného záhozu a začlenili se do ichtyofauny ČR bez působení významnějších škod na původních společenstvech ryb a bezobratlých. S množstvím nově získaných informací vyvstalo i množství nových otázek, které je třeba zodpovědět. Navíc, objevení nové populace na našem území nám dává jedinečnou příležitost k pozorování invazního procesu v odlišných ekosystémech. Další výzkum nám pomůže zkompletovat mozaiku znalostí o invazi nepůvodních hlaváčovitých ryb, která může být využita při dalším průběhu invazí těchto, případně i jiných invazních druhů.

6. Literatura

Adámek, Z., Jurajda, P., Prášek, V. & Sukop, I. (2010). Seasonal diet pattern of non- native tubenose goby (Proterorhinus semilunaris) in a lowland reservoir (Mušov, Czech Republic). Knowledge and Management of Aquatic Ecosystems, 397, 02.

Beck, K. G., Zimmerman, K., Schardt, J. D., Stone, J., Lukens, R. R., Reichard, S., Randall, J., Cangelosi, A. A., Cooper, D. & Johnson, J. P. (2008). Invasive species defined in a policy context: Recommendations from the federal invasive species advisory committee. Invasive Plant Science and Management, 1, 414-421.

Begon, M., Colin, R. T. & Harper, J. L. (2006). Ecology: from Individuals to Populations, Fourth Edition. Blackwell Publishing, Malden.

Bergstrom, M. A., Evrard, L. M. & Mensinger, A. F. (2008). Distribution, abundance, and range of the round goby, Apollonia melanostoma, in the Duluth-Superior Harbor and St. Louis River Estuary, 1998-2004. Journal of Great Lakes Research, 34, 535– 543.

Blackburn, T. M., Pyšek, P., Bacher, S., Carlton, J. T., Duncan, R.P., Jarošík, V., Wilson J. R. U. & Richardson, D.M. (2011). A proposed unified framework for biological invasions. Trends in Ecology and Evolution, 26, 333-339.

Błońska, D., Kobak, J. & Grabowska, J. (2017). Shelter competition between the invasive western tubenose goby and the native stone loach is mediated by sex. Journal of Limnology, 76, 221-229.

Bobeldyk, A. M., Rüegg, J. & Lamberti, G.A. (2015). Freshwater hotspots of biological invasions are a function of species-pathway interactions. Hydrobiologia, 764, 363- 373.

Borcherding, J., Arndt, H., Breiden, S., Brenner, K., Heermann, L., Hoefer, S., Leistenschneider, C., Lindner, J., Staas, S. & Gertzen, S. (2016). Drift of fish larvae and juveniles in the Lower Rhine before and after the goby invasion. Limnologica, 59, 53-62.

Brandner, J., Cerwenka, A. F., Schliewen, U. K. & Geist, J. (2013). Bigger is better: characteristics of round gobies forming an invasion front in the Danube River. PLoS ONE, 8, e73036.

Bronnenhuber, J. E., Dufour, B. A., Higgs, D. M. & Heath, D. M. (2011). Dispersal strategies, secondary range expansion and invasion genetics of the nonindigenous round goby, Neogobius melanostomus, in Great Lakes tributaries. Molecular Ecology, 20, 1845-1859.

Brown, J. E. & Stepien, C. A. (2009). Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns. Molecular Ecology, 18, 64-79.

Brownscombe, J. W. & Fox, M. G. (2012). Range expansion dynamics of the invasive round goby (Neogobius melanostomus) in a river system. Aquatic Ecology, 46, 175- 189.

Brownscombe, J. W., Masson, L., Beresford, D. V. & Fox, M. G. (2012). Modelling round goby Neogobius melanostomus range expansion in a Canadian river system. Aquatic Invasions, 7, 537–545.

Bullock, J. M., Moy, I., Pywell, R. F., Coulson, S. J., Nolan, A. M. & Caswell, A. (2002). Plant dispersal and colonization process at local and landscapes scale. In: Bullock, J. M., Kenward, R. E. & Hails, R. S. (eds): Dispersal ecology. Blackwell Scientific Publications, Oxford, pp. 279-302.

Clobert, J., Baguette, M., Benton, T. G. & Bullock, J. M. (2012). Dispersal ecology and evolution. Oxford University Press, Oxford.

Colautti, R. I. & MacIsaac, H. J. (2004). A neutral terminology to define 'invasive' species. Diversity and Distributions, 10, 135-141.

Cook, E. J., Ashton, G., Campbell, M., Coutts, A., Gollasch, S., Hewitt, Ch., Liu, H., Minchin, D., Ruiz, G. & Shucksmith, R. (2008). Non-native aquaculture species release: implication for aquatic ecosystems. In: Holmer, M., Black, K., Duarte, C. M., Marbà, N. & Karakassis, I. (eds): Aquaculture in the ecosystems. Springer, Dordrecht, pp. 155-184.

Cookingham, M. N. & Ruetz, C. R. III. (2008). Evaluating passive integrated transponder tags for tracking movements of round gobies. Ecology of Freshwater Fish, 17, 303-311.

Copp, G. H., Bianco, P. G., Bogutskaya, N. G., Erős, T., Falka, I., Ferreira, M. T., Fox, M. G., Freyhof, J., Gozlan, R. E., Grabowska, J., Kováč, V., Moreno-Amich, R., Naseka, A. M., Peňáz, M., Povž, M., Przybylski, M., Robillard, M., Russell, I. C., Stakėnas, S., Šumer, S., Vila-Gispert, A. & Wiesner, C. (2005). Journal of Applied Ichthyology, 21, 242-262.

Copp, G. H., Kováč, V., Zweimüller, I., Dias, A., Nascimento, M. & Balážová, M. (2008). Preliminary study of dietary interactions between invading Ponto-Caspian gobies and some native fish species in the River Danube near Bratislava (Slovakia). Aquatic Invasions, 3, 193-200.

Corkum, L. D., Sapota, M. R. & Skóra, K. E. (2004). The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biological Invasions, 6, 173-181.

Crooks, J. A. & Soulé, M. E. (1999). Lag times in population explosions of invasive species: Causes and implications. In: Sandlund, O. T., Shei, P. J. & Viken, Å. (eds): Invasive Species and Biodiversity Management. Kluwer Academic Publishers, Dordrecht, pp. 103-126.

Crooks, J. A. (2005). Lag times and exotic species: The ecology and management of biological invasions in slow-motion. Ecoscience, 12, 316-329.

Crowl, T. A., Crist, T. O., Parmenter, R. R., Belovsky, G. & Lugo, A. E. (2008). The spread of invasive species and infectious disease as driver of ecosystem change. Frontiers in Ecology and the Environment, 6, 238-246.

Cucherousset, J. & Olden, J. D. (2011). Ecological impacts of nonnative freshwater fishes. Fisheries, 36, 215-230.

Cupp, A. R., Tix, J., Smerud, J. R., Erickson, R. A., Fredricks, K. T., Amberg, J., Suski, C. D. & Wakeman, R., (2017). Using dissolved carbon dioxide to alter the behavior of invasive round goby. Management of Biological Invasions, 8, 567-574.

Dillon, A. K. & Stepien, C. A. (2001). Genetic and biogeographic Relationships of the invasive round (Neogobius melanostomus) and tubenose (Proterorhinus marmoratus) gobies in the Great Lakes versus Eurasian populations. Journal of Great Lakes Research, 27, 267-280.

Dingle, H. (1996). Migration. Oxford University Press, New York.

Dingle, H. & Drake, V. A. (2007). What is migration? BioScience, 57, 113-121.

Drake, J. M. & Lodge, D. M. (2004). Global hot spots of biological invasions: evaluating options for ballast-water management. Proceedings of the Royal Society of London Series B, Biological Sciences, 271, 575-580.

Drake, J. M. & Lodge, D. M. (2007). Hull fouling is a risk factor for intercontinental species exchange in aquatic ecosystems. Aquatic Invasions, 2, 121-131.

Dudgeon, D., Arthington, A. H., Gessner, M. O., Kawabata, Z.-I., Knowler, D. J., Lévêque, Ch., Naiman, R. J., Prieur–Richard, A.-H., Soto, D., Stiassny, M. L. J. & Sullivan, C. A. (2006). Freshwater biodiversity: importance, threats, status and conservation challenges. Biological reviews, 81, 163-182.

Francová, K., Ondračková, M., Polačik, M. & Jurajda, P. (2011). Parasite fauna of native and non-native populations of Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the longitudinal profile of the Danube river. Journal of Applied Ichthyology, 27, 879-886.

Freeland, W. J. (1986). Population of cane toad, Bufo marinus, in relation to time since colonization. Australian Wildlife Research, 13, 321-329.

Gallardo, B., Clavero, M., Sánchez, M. I. & Vilà, M. (2016). Global ecological impacts of invasive species in aquatic ecosystems. Global Change Biology, 22, 151-163.

Gollasch, S. (2006). Overview on introduced aquatic species in Europe navigational and adjacent waters. Helgoland Marine Research, 60, 84-89.

Gozlan, R. E. (2008). Introduction of non-native freshwater fish: it is all bad? Fish and Fisheries, 9, 106-115.

Gozlan, R. E., Britton, J. R., Cowx, I. & Copp, G. H. (2010). Current knowledge on no- native freshwater fish introduction. Journal of Fish Biology, 76, 751-786.

Gozlan, R. E. (2017). Interference of non-native species with fisheries and aquaculture. In: Vilà, M. & Hulme, P. E. (eds): Impact of Biological Invasions on Ecosystem Service. Invading Nature-Springer Series in Invasion Ecology, volume 12. Springer, Cham, pp. 119-137.

Grabowska, J., Kakareko, T., Błońska, D., Przybylski, M., Kobak, J., Jermacz, Ł. & Copp, G. H. (2016). Interspecific competition for a shelter between non-native racer goby and native European bullhead under experimental conditions – Effects of season, fish size and light conditions. Limnologica, 56, 30-38.

Gros, A., Poethke, H. J. & Hovestadt, T. (2009). Sex-specific spatiotemporal variability in reproductive success promotes the evolution of sex-biased dispersal. Theoretical Population Biology, 76, 13–18.

Gutowsky, L. F. G. & Fox, M. G. (2011). Occupation, body size and sex ration of round goby (Neogobius melanostomus) in established and newly invaded areas of an Ontario river. Hydrobiologia, 671, 27–37.

Hayden, T. A. & Miner, J. G. (2009). Rapid dispersal and establishment of a benthic Ponto-Caspian goby in Lake Erie: diel vertical migration of early juvenile round goby. Biological Invasions, 11, 1767–1776.

Havel, J. E., Kovalenko, K. E., Thomaz, S. M., Amalfitano, S. & Kats, L. B. (2015). Aquatic invasive species: challenge for the future. Hydrobiologia, 750, 147-170.

Hensler, S. R. & Jude, D. J. (2007). Diel vertical migration of round goby larvae in the Great Lakes. Journal of Great Lakes Research, 33, 295–302.

Hirsch, P. E., Adrian-Kalchhauser, I., Flämig, S., NʼGuyen, A., Defila, R., Di Giulio, A. & Burkhardt-Holm, P. (2016a). A tough egg to crack: recreational boats as vectors for invasive goby eggs and transdisciplinary management approaches. Ecology and Evolution, 6, 707-715.

Hirsch, P. E., NʼGuyen, A., Adrian-Kalchhauser, I. & Burkhardt-Holm, P. (2016b). What do we really know about the impacts of one of the 100 worst invaders in Europe? A reality check. Ambio, 45, 267-279.

Hogan, L. S., Marschall, E., Folt, C. & Stein, R. A. (2007). How non-native species in Lake Erie influence trophic transfer of mercury and lead to top predators. Journal of Great Lakes Research, 33, 46-61.

Hulme, P. E. (2009). Trade, transport and trouble: managing invasive species pathways in an era of globalization. Journal of Applied Ecology, 46, 10-18.

Hutchings, J. A. & Gerber, L. (2002). Sex-biased dispersal in salmonid fish. Proceedings of the Royal Society of London B: Biological Sciences, 269, 2487-2493.

Huxel, G. R. (1999). Rapid displacement of native species by invasive species: effects of hybridization. Biological Conservation, 89, 143-152.

Charlebois, P. M., Marsden, J. E., Goettel, R. G., Wolfe, R. K., Jude, D. J. & Rudnicka, S. (1997). The round goby, Neogobius melanostomus (Pallas), a review of European and North American literature. Illinois-Indiana Sea Grant Program and Illinois Natural History Survey. INHS Special Publication No. 20, 76 pp.

Chuang, A. & Peterson, Ch. R. (2016). Expanding population edges: theories, traits, and trade-offs. Global Change Biology, 22, 494-512.

Isabella-Valenzi, L. & Higgs, D. M. (2016). Development of an acoustic trap for potential round goby (Neogobius melanostomus) management. Journal of Great Lakes Research, 42, 904-909.

Janáč, M., Jurajda, P., Kružíková, L., Roche, K. & Prášek, V. (2012). Reservoir to river passage of age‐0+ year fishes, indication of a dispersion pathway for a non‐native species. Journal of Fish Biology, 82, 994-1010.

Janáč, M., Valová, Z. & Jurajda, P. (2013). Range expansion and habitat preferences of non-native 0+ tubenose goby (Proterorhinus semilunaris) in two lowland rivers in the Danube basin. Fundamental and Applied Limnology, 181, 73-85.

Janáč, M., Roche, K., Šlapanský, L. & Jurajda, P. (2018). Long-term monitoring of native bullhead and invasive gobiids in the Danubian rip-rap zone. Hydrobiologia, 807, 263-275.

Janssen, J. & Jude, D. J. (2001). Recruitment failure of mottled sculpin Cottus bairdi in Calumet Harbor, southern Lake Michigan, induced by the newly introduced round goby Neogobius melanostomus. Journal of Great Lakes Research, 27, 319–328.

Johnson, T. B., Bunnell, D. B. & Knight, C. T. (2005a). A potential new energy pathway in Central Lake Erie: the round goby connection. Journal of Great Lakes Research, 31 (Suppl. 2), 238–225.

Jude, D. J., Reider, R. H. & Smith, G. R. (1992) Establishment of Gobiidae in the Great Lakes basin. Canadian Journal of Fisheries and Aquatic Sciences, 49, 416–421.

Jurajda, P., Černý, J., Polačik, M., Valová, Z., Janáč, M., Blažek, R. & Ondračková, M. (2005). The recent distribution and abundance of non-native Neogobius fishes in the Slovak section of the River Danube. Journal of Applied Ichthyology, 21, 319–323.

Jurajda, P., Adámek, Z., Janáč, M., Mrkvová, M., Ondračková, M., Polačik, M., Roche, K., Vašek, M. & Všetičková, L. (2015). Hlaváči v našich vodách. Ústav biologie obratlovců AV ČR, v.v.i., Brno.

Jůza, T., Zemanová, J., Tušer, M., Sajdlová, Z., Baran, R., Vašek, M., Ricard, D., Blabolil, P., Wagenvoort, A. J., Ketelaars, H. A. M. & Kubečka, J. (2016). Pelagic occurrence and diet of invasive round goby Neogobius melanostomus (Actinopterygii, Gobiidae) juveniles in deep well-mixed European reservoirs. Hydrobiologia, 768, 197-209.

Jůza, T., Blabolil, P., Baran, R., Bartoň, D., Čech, M., Draštík, V., Frouzová, J., Holubová, M., Ketelaars, H. A. M., Kočvara, L., Kubečka, J., Muška, M., Prchalová, M., Říha, M., Sajdlová, Z., Šmejkal, M., Tušer, M., Vašek, M., Vejřík, L., Vejříková, I., Wagenwoort, A. J., Žák, J. & Peterka, J. (2018). Collapse of the native ruffe (Gymnocephalus cernua) population in the Biesbosch lakes (the Netherlands) owing to round goby (Neogobius melanostomus) invasion. Biological Invasions, 20, 1523- 1535.

Kakareko, T., Kobak, J., Grabowska, J., Jermacz, Ł., Przybylski, M., Poznańska, M., Pietraszewski, D. & Copp, G. H. (2013). Competitive interactions for food resources between invasive racer goby Babka gymnotrachelus and native European bullhead Cottus gobio. Biological Invasions, 15, 2519-2530.

Karlson, A. M. L., Almqvist, G., Skóra, K. E. & Appelberg, M. (2007). Indications of competition between non indigenous round goby and native flounder in the Baltic Sea. ICES Journal of Marine Science, 64, 479–486.

Keller, S. R. & Taylor, D. R. (2010). Genomic admixture increases fitness during a biological invasions. Journal of Evolutionary Biology, 23, 1720-1731.

Keller, R. P., Geist, J., Jeschke, J. M. & Kühn, I. (2011). Invasive species in Europe: Ecology status and policy. Environmental Sciences Europe, 23, 1-17.

Kelly, D. W., Paterson, C. R., Townsend, C. R., Poulin, R. & Thompkins, D. M. (2009a). Parasite spillback: A neglected concept in invasion ecology? Ecology, 90, 2047-2056.

Kelly, D. W., Paterson, C. R., Townsend, C. R., Poulin, R. & Thompkins, D. M (2009b). Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology, 54, 1805-1818.

Kipp, R., Hébert, I., Lacharité, M. & Ricciardi, A. (2012). Impacts of predation by the Eurasian round goby (Neogobius melanostomus) on molluscs in the upper St. Lawrence River. Journal of Great Lakes Research, 38, 78-89.

Kipp, R. & Ricciardi, A. (2012). Impacts of the Eurasian round goby (Neogobius melanostomus) on benthic communities in the upper St. Lawrence River. Canadian Journal of Fisheries and Aquatic Research, 69, 469-486.

Kopeček, L. (2013). Aktuální rozšíření hlaváčovitých ryb v ČR. Bakalářská práce, Masarykova univerzita, Brno.

Kornis, M. S., Mercado-Silva, N. & Vander Zanden, M. J. (2012). Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. Journal of Fish Biology, 80, 235-285.

Kornis, M. S., Sharma, S. & Vander Zanden, M. J. (2013). Invasion success and impact of an invasive fish, round goby, in Great Lakes tributaries. Biodiversity and Distributions, 19,184-198.

Kornis, M. S., Weidel, B. C. & Vander Zanden, M. J. (2017). Divergent life histories of invasive round gobies (Neogobius melanostomus) in Lake Michigan and its tributaries. Ecology of Freshwater Fish, 26, 563-574.

Koubková, B. & Baruš, V. (2010). Metazoan parasites of the recently established tubenose goby (Proterorhinus marmoratus: Gobiidae) population from the South Moravian reservoir, Czech Republic. Helmintologica, 37, 89-95.

Kovach, R. P., Muhlfeld, C. C., Boyer, M. C., Lowe, W. H., Allendorf, F. W. & Luikart, D. (2015). Dispersal and selection mediate hybridization between a native and invasive species. Proceedings of the Royal Society of London B: Biological Sciences, 282, 20142454.

Kuhns, L. A. & Berg, M. B. (1999). Benthic invertebrate community responses to round goby (Neogobius melanostomus) and zebra mussel (Dreissena polymorpha) invasion in southern Lake Michigan. Journal of Great Lakes Research, 25, 910–917.

Kvach, Y. & Stepien, C. A. (2008). Metazoan Parasites of Introduced Round and Tubenose Gobies in the Great Lakes: Support for the “Enemy Release Hypothesis”. Journal of Great Lakes Research, 34, 23-35.

Kwon, T. D., Fisher, S. W., Kim, G. W., Hwang, H. & Kim, J. E. (2006). Trophic transfer and biotransformation of polychlorinated biphenyls in zebra mussel, round goby, and smallmouth bass in Lake Erie, USA. Environmental Toxicology and Chemistry, 25, 1068–1078.

Landsman, S. J., Nguyen, V. M., Gutowsky, L. F. G., Gobin, J., Cook, K. V., Binder, T. R., Lower, N., McLaughlin, R. L. & Cooke, S. J. (2011). Fish movement and migration studies in the Laurentian Great Lakes: research trends and knowledge gaps. Journal of Great Lakes Research, 37, 365-379.

Lauer, T. E., Allen, P. H. & McComish, T. S. (2004). Changes in mottled sculpin and Johnny darter trawl catches after the appearance of round gobies in the Indiana water of Lake Michigan. Transactions of the American Fisheries Society, 133, 185–189.

Lederer, A. M., Janssen, J., Reed, T. & Wolf, A. (2008). Impacts of the introduced round goby (Apollonia melanostoma) on Dreissenids (Dreissena polymorpha and bugensis) and on macroinvertebrate community between 2003 and 2006 in the littoral zone of Green Bay, Lake Michigan. Journal of Great Lakes Research, 34, 690–697.

Lockwood, J. L. Hoopes, M. F. & Marchetti, M. P. (2007). Invasion ecology. Blackwell Publishing, Oxford.

Lodge, D. M. & Shrader-Frechette, K. (2003). Nonindigenous species: Ecological explanation, environmental ethics, and public policy. Conservation Biology, 17, 31- 37.

Lucas, M. C. & Baras, E. (2001). Migration of Freshwater Fishes. Blackwell Science, Oxford.

Lusk, S. & Halačka, K. (1995). The first finding of the tubenose goby Proterorhinus semilunaris, in Czcech Republic. Folia Zoologica, 44, 90-92.

Lusk, S., Lusková, V., Halačka, J. & Lojkásek, B. (2000). Změny v druhové skladbě ichtyofauny na zemí České republiky po roce 1990 [Changes in the species composition of the ichtyofauna in the territory of the Czech republic after 1990]. Biodiverzita ichtyofauny ČR, 3, 29-36.

Lusk, S., Vetešník, L., Halačka, K., Lusková, V., Pekárik, L. & Tomeček, J. (2008). První záznam o průniku hlaváče černoústého Neogobius (Apollonia) melanostomus do oblasti soutoku Moravy a Dyje (Česká Republika). Biodiverzita Ichtyofauny České Republiky, 7, 114-118.

Lynch, M. P. & Mensinger, A. F. (2012). Seasonal abundance and movement of the invasive round goby (Neogobius melanostomus) on rocky substrate in the Duluth– Superior Harbor of Lake Superior. Ecology of Freshwater Fish, 21, 64–74.

MacIsaac, H. J. (1996). Potential abiotic and biotic impacts of zebra mussel on the inland water of North America. American Zoologist, 36, 297-299.

Madenjian, C. P., Tapanian, M. A., Witzel, L. D., Einhouse, D. W., Pothoven, S. A. & Whitford, H. L. (2011). Evidence for predatory control of the invasive round goby. Biological Invasions, 13, 987–1002.

Marchetti, M. P., Moyle, P. B. & Levine, R. (2004). Invasive species profiling? Exploring the characteristics of non-native fishes across invasion stages in California. Freshwater Biology, 49, 646-661.

Marentette, J. R., Fitzpatrick, J. L., Berger, R. G. & Balshine, S. (2009). Multiple male reproductive morphs in the invasive round goby (Apollonia melanostoma). Journal of Great Lakes Research, 35, 302–308.

Marentette, J. R., Wang, G., Tong, S., Sopinka, N. M., Taves, M. D., Koops, M. A. & Balshine, S. (2011). Laboratory and field evidence of sex-biased movement in the invasive round goby. Behavioral Ecology and Sociobiology, 65, 2239-2249.

Masson, L., Brownscombe, J. W. & Fox, M. J. (2016). Fine scale spatio-temporal life history shifts in an invasive species at its expansion front. Biological Invasions, 18, 775-792.

Mikl, L., Adámek, Z., Všetičková, L., Janáč, M., Roche, K., Šlapanský, L. & Jurajda, P. (2017a). Response of benthic macroinvertebrate assemblages to round (Neogobius melanostomus, Pallas 1814) and tubenose (Proterorhinus semilunaris, Heckel 1837) goby predation pressure. Hydrobiologia, 785, 219-232.

Mikl, L., Adámek, Z., Roche, K., Všetičková, L., Šlapanský, L. & Jurajda, P. (2017b). Invasive Ponto-Caspian gobies in the diet of piscivorous fish in a European lowland river. Fundamental and Applied Limnology, 192, 157 – 171.

Miller, P.J. (1986). Gobiidae. In: Whitehead, P. J. P., Bauchot, M.-L., Hureau, J.-C., Nielsen, J. & Tortonese, E. (eds): Fishes of the North-Eastern Atlantic and the Mediterranean. UNESCO, Paris. pp. 1019-1085.

Milner-Gulland, E. J., Fryxell, J. M. & Sinclair, A. R. E. (2011). Animal Migration: A Synthesis. Oxford University Press, Oxford.

Mollot, G., Pantel, J. H. & Romanuk, T. N. (2017). The effect of invasive species on the decline in species richness: A global meta-analysis. Advances in Ecological Research, 56, 61-83.

Nathan, R. (2001). The challenges of studying dispersal. Trends in Ecology and Evolution, 16, 481-483.

Nathan, R., Getz, W. M., Revilla, E., Holyoak, M., Kadmon, R., Saltz, D. & Smouse, P. E. (2008). A movement ecology paradigm for unifying organismal movement research. Proceedings of the National Academy of Sciences of the United States of America, 105, 19052-19059.

Nelson, J. S. (1994). Fishes of the World, Third Edition. John Wiley & Sons, New York.

NʼGuyen, A., Hirsch, P. E., Adrian-Kalchhauser, I. & Burkhardt-Holm, P. (2016). Improving invasive species management by integrating priorities and contributions of scientists and decision makers. Ambio, 45, 280-289.

Noatch, M. & R. Suski, C. D. (2012). Non-physical barriers to deter fish movements. Environmental Reviews, 20, 71–82.

Oesmann, S. (2003). Vertical, lateral and diurnal drift patterns of fish larvae in a large lowland river, the Elbe. Journal of Applied Ichthyology, 19, 284-293.

Ondračková, M., Dávidová, M., Pečínková, M., Blažek, R., Gelnar, M., Valová, Z., Černý, J. & Jurajda, P. (2005). Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube. Journal of Applied Ichthyology, 21, 345-349.

Ondračková, M., Hudcová, I., Dávidová, M., Adámek, Z., Kašný, M. & Jurajda, P. (2015). Non-native gobies facilitate transmission of Bucephalus polymorphus (Trematoda). Parasites and Vectors, 8, 382.

Padilla, D. K. & Williams, S. L. (2004). Beyond ballast water: Aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environment, 2, 131-138.

Panov, V., Dgebuadze, Y., Shiganova, T., Filippov, A. & Minchin, D. 2007. A risk assessment of biological invasions: Inland waterways of Europe - The northern invasion corridor case study. In: Gherardi, F. (eds): Biological invaders in inland waters: Profiles, distribution and threats. Invading nature - Springer Series in Invasion Ecology, Volume 2. Springer, Heidelberg, pp 639–656.

Panov, V. E., Alexandrov, B., Arbačiauskas, K., Binimelis, R., Copp, G. H., Grabowski, M., Lucy, F., Leuven, R. S. E. W., Nehring, S., Paunović, M., Semenchenko, V. & Son, M. O. (2009). Assessing the risk of aquatic species invasion via European waterways: From concepts to environmental indicators. Integrated Environmental Assessment and Management, 5, 110-126.

Pavlov, D. S. (1994). The downstream migration of young fishes in rivers: mechanisms and distribution. Folia Zoologica, 43, 193-208.

Phillips, E. C., Washek, M. E., Hertel, A. W. & Niebel, B. M. (2003). The round goby (Neogobius melanostomus) in Pennsylvania tributary streams of Lake Erie. Journal of Great Lakes Research, 29, 34–40.

Płąchocki, D., Kobak, J., Kakareko, T., 2012: First report on the importance of alien gobiids in the diet of native piscivorous fishes in the lower Vistula River (Poland). International Journal of Oceanography and Hydrobiology, 4, 83 – 89.

Poos, M., Dextrase, A. J., Schwalb, A. N. & Ackerman, J. D. (2010). Secondary invasion of the round goby into high diversity Great Lakes tributaries and species at risk hotspots: potential new concerns for endangered freshwater species. Biological Invasions, 12, 1269–1284.

Powell, R. A. (2000). Animal home ranges and territories and home range estimators. In: Boitani, L. & Fuller, T. K. (eds): Research Techniques in Animal Ecology Controversies and Consequences. Columbia University Press, New York, pp. 65– 110.

Prášek, V. & Jurajda, P. (2005). Expansion of Proterorhinus marmoratus in the Morava River basin (Czech Republic, Danube R. watershed). Folia Zoologica, 54, 189-192.

Prenter, J., MacNeil, C., Dick, J. T. A. & Dunn, A. M. (2004). Roles of Parasites in animal invasions. Trends in Ecology and Evolution, 19, 385-390.

Pyšek, P., Richardson, D. M., Rejmánek, M., Webster, G. L., Williamson, M. & Kirschner, J. (2004). Alien plants in checklists and floras: towards better communication between taxonomists and ecologists. Taxon, 53, 131-143.

Rahel, F. J. (2002). Homogenization of freshwaters faunas. Annual Review of Ecology and Systematics, 33, 291-315.

Rahel, F. J. & Olden, J. D. (2008). Assessing the effects of climate change on aquatic invasive species. Conservation Biology, 22, 521-533.

Rakauskas, V., Stakėnas, S., Virbickas, T. & Bukelskis, E. (2016). Non-indigenous in the northern branch of the central European invasion corridor. Reviews in Fish Biology and Fisheries, 26, 491-508.

Ramler, D., Anhelt, A., Nemechkal, H. L. & Keckeis, H. (2016). The drift of early life stages of Percidae and Gobiidae (Pisces: Teleostei) in a free-flowing section of the Austrian Danube. Hydrobiologia, 781, 199-216.

Ray, W. J. & Corkum, L. D. (2001). Habitat and site affinity of the round goby. Journal of Great Lakes Research, 27, 329–334.

Reichard, M. & Jurajda, P. (2007). Seasonal dynamics and age structure of drifting cyprinid fishes: an interspecific comparison. Ecology of Freshwater Fish, 16, 482– 492.

Reyjol, Y., Brodeur, P., Mailhot, Y., Mingelbier, M. & Dumont, P. (2010). Do native predators feed on non-native prey? The case of round goby in a fluvial piscivorous fish assemblage. Journal of Great Lakes Research, 36, 618–624.

Ricciardi, A. & MacIsaac, H. J. (2000). Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology and Evolution, 15, 62-65.

Ricciardi, A. (2001): Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences, 58, 2513-2525.

Ricciardi, A. & Kipp, R. (2008). Predicting the number of ecologically harmful exotic species in an aquatic ecosystem. Diversity and Distributions, 14, 374-380.

Ricciardi, A. & MacIsaac, H. J. (2011). Impact of biological invasions on freshwater ecosystems. In: Richardson, D. M. (eds): Fifty Years of Invasion Ecology: The Legacy of Charles Elton. Wiley-Blackwell, Oxford, pp. 211-224.

Ricciardi, A., Hoopes, M. F., Marchetti, M. P. & Lockwood, J. L. (2013). Progress toward understanding the ecological impacts of non-native species. Ecological Monographs, 83, 263-282.

Richardson, D. M., Pyšek, P., Rejmánek, M., Barbour, M. G., Panetta, F. D. & West, C. J. (2000). Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions, 6, 93-107.

Richardson, D. M. & Pyšek, P. (2006). Plant invasions: merging the concepts of species invasiveness and community invasibility. Progress in Physical Geography, 30, 409- 431.

Rodriguez, L. F. (2006). Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biological Invasions, 8, 927-939.

Roche, K. F., Janáč, M. & Jurajda, P. (2013). A review of Gobiid expansion along the Danube-Rhine corridor – geopolitical change as a driver for invasion. Knowledge and Management of Aquatic Ecosystems, 411: 01.

Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., Oʼneil, P., Parker, I. M., Thompson, J. M. & Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305-332.

Sapota, M. R. & Skóra, K. E. (2005). Spread of alien (Non-indigenous) fish species Neogobius melanostomus in the Gulf of Gdańsk (south Baltic). Biological Invasions, 7, 157-164.

Savino, J. F., Jude, D. J. & Kostich, M. J. (2001). Use of electrical barriers to deter movement of round goby. American Fisheries Society Symposium, 26, 171–182.

Simberloff, D. & von Holle, B. (1999). Positive interaction of nonindigenous species: invasional meltdown? Biological Invasions, 1, 21-32.

Simberloff, D. & Gibbons, L. (2004). Now you see them, now you don’t! – population crashes of established introduced species. Biological Invasions, 6, 161-172.

Simberloff, D. (2009). The role of propagule pressure in biological invasions. Annual Review of Ecology, Evolution, and Systematics, 40, 81-102.

Simberloff, D. (2011). How common are invasion-induced ecosystem impact? Biological Invasion, 13, 1255-1268.

Skóra, K. E. & Stolarski, J. (1993). New fish species in the Gulf of Gdansk. Bulletin of the Sea Fisheries Institute, 1, 83.

Sommers, Ch. M., Lozer, M. N., Kjoss, V. A. & Quinn, J. S. (2003). The invasive round goby (Neogobius melanostomus) in the diet of nestling double-crested cormorants (Phalacrocorax auritus) in Hamilton Harbour, Lake Ontario. Journal of Great Lakes Research, 29, 392-399.

Švátora, M., Křížek, J. & Reiter, A. (2000). Ichtyofauna horní Dyje - Bílý Kříž. Biodiverzita ichtyofauny ČR, 3, 161 – 164.

Steinhart, G. B., Marschall, E. A. & Stein, R. A. (2004). Round goby predation on smallmouth bass offspring in nests during simulated catch-and-release angling. Transactions of the American Fisheries Society, 133, 121–131.

Strayer, D. L. (2010). Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology, 55, 152-174.

Thompson, H. A. & Simon, T. P. (2015). Age and growth of round goby Neogobius melanostomus associated with depth and habitat in the western basin of Lake Erie. Journal of Fish Biology, 86, 558-574.

Toussaint, A., Charpin, N., Beauchard, O., Grenouillet, G., Oberdorff, T., Tedesco, P. A., Brosse, S. & Villéger, S. (2018). Non-native species led to marked shifts in functional diversity of the world freshwater fish faunas. Ecology Letters, 21, 1649- 1659.

Trexler, J. C., Loftus, W. F., Jordan, F., Lorenz, J., Chick, J. & Kobza, R. M. (2000). Empirical assessment of fish introductions in a subtropical wetland: an evaluation of contrasting views. Biological Invasions, 2, 265-277.

Tierney, K. B., Kasurak, A. V., Zielinski, B. S. & Higgs, D. M. (2011). Swimming performance and invasion potential of the round goby. Environmental Biology of Fishes, 92, 941-502.

Valéry, L., Fritz, H., Lefeuvre, J.-C. & Simberloff, D. (2009). Invasive species can also be native….Trends in Ecology and Evolution, 24, 585.

Vander Zanden, M. J., Lapointe, N. W. R. & Marchetti, M. P. (2016). Non-indigenous fishes and their role in freshwater fish imperilment. In: Closs, G. P., Krkosek, M. & Olden J. D. (eds): Conservation of Freshwater Fishes. Cambridge University Press, Cambridge. van Kessel, N., Dorenbosch, M., de Boer, M. R. M., Leuven, R. S. E. W. & Van der Velde, G. (2011) Competition for shelter between four invasive gobiids and two native benthic fish species. Current Zoology, 57, 844–851. van Kessel, N., Dorenbosch, M., Kranenbarg, J., van der Velde, G. & Leuven, R. S. E. W. (2016). Invasive Ponto-Caspian gobies rapidly reduce the abundance of protected native bullhead. Aquatic Invasions, 11, 179-188.

Vassilev, M. 1994. On the downstream migration of ichthyoplankton along the Bulgarian shore of the Danube river. Vie Et Milieu, 44, 273–280.

Vašek, M., Všetičková, L., Roche, K. & Jurajda, P. (2014). Diet of two invading gobiid species (Proterorhinus semilunaris and Neogobius melanostomus) during the breeding and hatching season: No field evidence of extensive predation on fish eggs and fry. Limnologica, 46, 31-36.

Veléz-Espino, L. A., Koops, M. A. & Balshine, S. (2010). Invasion dynamics of round goby (Neogobius melanostomus) in Hamilton Harbour, Lake Ontario. Biological Invasions, 12, 3861-3875.

Vilà, M., Espinar, J. L., Hejda, M., Hulme, P. E., Jarošik, V., Maron, J. L., Pergl, J., Schaffner, U., Yan, S. & Pyšek, P. 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effect on species, communities and ecosystems. Ecology Letters, 14, 702-708.

Vörösmarty, C. J., McIntyre, P. B., Gessner, M. O., Dudgeon, D., Prusevich, A., Green, P., Glidden, S., Bunn, S. E., Sullivan, C. A., Reidy Liermann, C. & Davies, P. M. (2010). Global threats to human water security and river biodiversity. Nature, 467, 555-561.

Všetičková, L., Janáč, M., Vašek, M., Roche, K. & Jurajda, P. (2014). Non-native western tubenose gobies Proterorhinus semilunaris show distinct site, sex and age- related differences in diet. Knowledge and Management of Aquatic Ecosystems, 414, 10.

Wiesner, C. (2005). New records of non-indigenous gobies (Neogobius sp.) in the Austrian Danube. Journal of Applied Ichthyology, 21, 324–327.

Williamson, M. H. & Fitter, A. (1996). The varying success of invaders. Ecology, 77, 1661-1666.

Witte, F., Goldschmidt, T., Wanink, J., van Oijen, M., Goudswaard, K., Witte-Maas, E. & Bouton, N. (1992). The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environmental Biology of Fishes, 34, 1-28.

Wolter, Ch. (2001). Rapid change of fish assemblages in artificial lowland waterways. Limnologica, 31, 27-35.

Wolter, Ch. & Arlinghaus, R. (2003). Navigation impact on freshwater fish assemblages: the ecological relevance of swimming performance. Reviews in Fish Biology and Fisheries, 13, 63-89.

Wonham, M. J., Carlton, J. T., Ruiz, G. M. & Smith, L. D. (2000). Fish and ships: relating dispersal frequency to success in biological invasions. Marine Biology, 136, 1111-1121.

Young, J. A. M., Marentette, J. R., Gross, C., McDonald, J. I., Verma, A., Marsh-Rollo, S. E., Macdonald, P. D. M., Earn, D. J. D. & Balshine, S. (2010). Demography and substrate affinity of the round goby (Neogobius melanostomus) in Hamilton Harbour. Journal of Great Lakes Research, 26, 115–122.

Zitek, A., Schmutz, S. & Ploner, A. (2004). Fish drift in a Danube sidearm-system: II. Seasonal and diurnal patterns. Journal of Fish Biology, 65, 1339-1357.

7. Přílohy

7.1 Publikace a rukopisy vztahující se k tématu disertační práce 7.2 Podíl studenta na jednotlivých rukopisech 7.3 Seznam impaktovaných publikací 7.4 Příspevky na konferencích 7.5 Ostatní výzkumná činnost

7.1 Publikace a rukopisy vztahující se k tématu disertační práce

Publikace A

Šlapanský, L., Janáč, M., Roche, K., & Jurajda, P. (2019). Round goby movement patterns in a non-navigable river. Odesláno do Canadian Journal of Fisheries and Aquatic Research 11. 12. 2018.

Publikace B

Šlapanský, L., Janáč, M., Roche, K., Mikl, L. & Jurajda, P. (2017). Expansion of round gobies in a non-navigable river system. Limnologica, 67, 27-36.

Publikace C

Roche, K., Janáč, M., Šlapanský, L., Mikl, L., Kopeček, L., & Jurajda, P. (2015). A newly established round goby (Neogobius melanostomus) population in the upper stretch of the river Elbe. Knowledge and Management of Aquatic Ecosystems, 416, 33.

Publikace D

Janáč, M., Šlapanský, L., Valová, Z. & Jurajda, P. (2013). Downstream drift of round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their non-native area. Ecology of Freshwater Fish, 22 (3), 430-438.

Publikace E

Šlapanský, L., Jurajda, P. & Janáč, M. (2016). Early life stages of exotic gobiids as new host for unionid glochidia. Freshwater Biology, 61, 679-690.

Publikace A

Round goby movement patterns in a non-navigable river

Šlapanský, L., Janáč, M., Roche, K., & Jurajda, P. (2019)

Odesláno do Canadian Journal of Fisheries and Aquatic Research 11. 12. 2018

Canadian Journal of Fisheries and Aquatic Sciences

Round goby movement patterns in a non-navigable river

Journal: Canadian Journal of Fisheries and Aquatic Sciences

Manuscript ID Draft

Manuscript Type: Article

Date Submitted by the n/a Author:

Complete List of Authors: Šlapanský, Luděk; The Czech Academy of scinces , Institute of the Vertebrate Biology; Masarykova univerzita Prirodovedecka Fakulta, Institute of Botany and Zoology Janac, Michal; Academy of Sciences of the Czech Republic Roche, Kevin; The Czech Academy of Sciences, Institute of the VertebrateDraft Biology Jurajda, Pavel; The Czech Academy of Sciences, Institute of the Vertebrate Biology

DISPERSAL < General, aquatic biological invasions, invasion front, Keyword: TAGGING < General, Ponto-Caspian gobiids

Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? :

https://mc06.manuscriptcentral.com/cjfas-pubs Page 1 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Round goby movement patterns in a non-navigable river

Luděk Šlapanský, Michal Janáč, Kevin Roche, Pavel Jurajda

Luděk Šlapanský 1,2

E-mail address: [email protected]

Michal Janáč 1

E-mail address: [email protected]

Kevin Roche 1

E-mail address: [email protected]

Pavel Jurajda 1 E-mail address: [email protected] Draft

1The Czech Academy of Sciences, Institute of the Vertebrate Biology, Květná 8, 603 65 Brno,

Czech Republic.

2Institute of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 246/2,

611 37, Brno, Czech Republic

Corresponding author:

Luděk Šlapanský

Address: The Czech Academy of Sciences, Institute of the Vertebrate Biology, Květná 8, 603

65 Brno, Czech Republic.

E-mail: [email protected]

Phone number: +420 723 059 612

Fax number: 543 211 346

1 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 2 of 42

ABSTRACT

Understanding non-native species dispersal is vital for their future management. The round goby (Neogobius melanostomus ) has greatly extended its range since 1990s, with commercial shipping being the main vector. However, our knowledge regarding their secondary dispersal from points of introduction is surprisingly limited. In this study, a series of field experiments were undertaken on a mid-sized river to assess goby dispersal patterns within an established population, following a simulated release of a large number of propagules, or at a simulated invasion front. Most of the established population remained stationary and just a few individuals undertook long-distance dispersal (principally upstream). Mean distance travelled was 1.1 m.day -1 (max. 29.6 m.day -1 ). DraftWhile the site fidelity appeared to last for most of the year (including winter), it was surprisingly relaxed during the spawning season. Concentrated release of a large number of propagules resulted in appreciably greater movement rates than in the established population, with upstream movement again dominating. In general, smaller, mostly male fish tended to move further and appeared as first colonisers in uninvaded areas.

2 https://mc06.manuscriptcentral.com/cjfas-pubs Page 3 of 42 Canadian Journal of Fisheries and Aquatic Sciences

1 Introduction

Quantifying the extent of movement activity (dispersal) in non-native fish is one of the

key factors in predicting invasion potential and speed of colonisation in a new area (Radinger

and Wolter 2014). Fish introductions outside of their native range have been relatively well

studied, with most cases attributable to shipping (Ricciardi and MacIsaac 2000; Wonham et

al. 2000; Gozlan et al. 2010), imports of ornamental fish (Padilla and Williams 2004; Keller

and Lodge 2007), escapes from aquaculture (Cook et al. 2008; Gozlan et al. 2010) or

intentional introductions for sport fishing (Gozlan 2008; Rahel and Smith 2018). However,

relatively little is known about non-native fish movements after the initial introduction. Yet

such knowledge could yield valuable information on the species’ biology and inform

management and control efforts (Skalski and Gilliam 2000; Landsman et al. 2011, Coulter et

al. 2016). In other words, while we knowDraft much about how fish can be transported over long

distances (e.g. via shipping), we know very little about what happens after they are released.

The round goby ( Neogobius melanostomus ), a small benthic fish originating in the

Ponto-Caspian region, has greatly increased its range since the 1990s (see Roche et al. 2013

for a review). Round gobies usually become established relatively quickly in newly colonised

areas due to a number of traits typical of invasive species, e.g. rapid range expansion, super-

dominant population growth, rapid genomic adaptation and life history trait plasticity

(Brandner et al. 2015) . Nevertheless, aspects of movement activity and the scale of movement

have received relatively little scientific attention. For example, while numerous otherwise-

oriented studies have taken place in the Laurentian Great Lakes region following round goby

introduction in the 1990s, just 2.7% (3 of 112) of all fish movement studies dealt with aspects

of round goby movement in 2010, despite the species’ potential for altering and disrupting

native fish communities (Landsman 2011).

3 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 4 of 42

While the number of studies on round goby range expansion has increased in recent years, most such studies describe expansion along navigable rivers and canals, based on the assumption that transport via shipping has been the main vector facilitating long-range ‘leap- frog’ dispersal (e.g. see Ahnelt et al. 1998; Wiesner 2005; Gutowsky and Fox 2011;

Cammaerts et al. 2012; Roche et al. 2013). ‘Natural’ expansion (i.e. continuous range expansion by swimming alone) into and along invaded non-navigable rivers has been examined much less intensively, with most studies restricted to reporting the pace of invasion front shifts (Bronnenhuber et al. 2011; Brownscombe and Fox 2012; Šlapanský et al. 2017) or describing which fish occur first in newly colonised areas (Phillips et al. 2003; Brandner et al.

2013b). Little is known about the mobility of invasive gobies at small spatial scales (Brandner et al. 2015), even though small-scale post-introduction movements are crucial to our understanding of subsequent dispersalDraft and for predicting the extent and speed of range expansion (LaRue et al. 2011). Papers that have dealt with small-scale round goby dispersal to date have tended to do so only marginally (e.g. Wolfe and Marsden 1998; Cookingham and

Reutz 2008; Brandner et al. 2015). To the best of our knowledge, only the study of Lynch and

Mensinger (2012) has provided a more in-depth view by quantifying movement patterns of individually tagged round gobies in Lake Superior. In addition, it is hard to generalise the information gained as it is restricted by regional and ecotype coverage (most information originating exclusively from slow flowing or standing waters, with Europe largely understudied) and contrasting results.

In early studies, it was reported that round gobies display poor natural dispersal ability, especially when travelling upstream (Bronnenhuber et al. 2011, Brownscombe and

Fox 2012), due to their morphology (typical of small benthic fishes) and small home ranges

(based on the studies of Wolfe and Marsden (1998) and Ray and Corkum (2001)). However, subsequent studies have reported both larger home ranges (Cookingham and Reutz 2008),

4 https://mc06.manuscriptcentral.com/cjfas-pubs Page 5 of 42 Canadian Journal of Fisheries and Aquatic Sciences

long-distance natural dispersal (Šlapanský et al. 2017) and a relatively fast rate of spread into

non-navigable rivers (Kornis and Vander-Zanden 2010; Bronnenhuber et al. 2011;

Brownscombe and Fox 2012; Brandner et al. 2013b). Furthermore, it remains unclear as to

which individuals (in terms of sex and size) are most involved in the process of invasion, i.e.

as first colonisers or pioneers (Gutowsky and Fox 2011; Brandner 2013b; Brownscombe and

Fox 2012; Masson et al. 2016).

The main goal of this study was to evaluate both the extent of round goby movement

in a European mid-sized lowland river and any sex- or size-specific or seasonal patterns. To

this end, we conducted a series of field experiments designed to ensure that the dispersal

observed was free of any possible human involvement. The first of these experiments

describes dispersal patterns in an established round goby population, allowing us to determine

common movement rates, identify the Draftmost probable migrants (pioneers) and the time of year

when migration is most likely. The second describes dispersion patterns following a simulated

mass release of propagules (i.e. introduction), while the third describes dispersion patterns in

a simulated invasion front by monitoring recolonisation of areas cleared of gobies.

2 Material and methods

2.1 Study area

The study took place on a 23 km stretch (river km 17 to river km 40) of the River Dyje

(Danube basin, Czech Republic; Fig. 1). Between 1968 and 1982, the Dyje was channelised

and its riverbanks stabilised with rocky rip-rap (15–25 cm diameter; though stones of 40-60

cm also occur at some locations). The river has a channel width of 30–50 m, a depth of 0.5–

1.0 m. and an annual mean discharge rate over the study stretch of 41.7 m 3.s -1 (Czech

Hydrometeorological institute; http://portal.chmi.cz). Current velocity along the banks rarely

5 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 6 of 42

exceeds 0.4 m.s -1 . The bottom substrate comprises sand, gravel and pebbles with patches of silt and aquatic vegetation, woody debris, pools and riffles occur only rarely. The Dyje is non- navigable throughout the study stretch, ensuring that the dispersal observed was through natural means alone.

The Dyje has a relatively diverse fish assemblage, originally dominated by native cyprinid species such as roach Rutilus rutilus , chub Leuciscus cephalus, common bream

Abramis brama , barbel Barbus barbus , bleak Alburnus alburnus , European bitterling Rhodeus amarus and white-finned gudgeon Romanogobio vladykovi (Jurajda and Peňáz 1994; Valová et al. 2006). In recent years, the assemblage has come to include stable populations of non- native tubenose goby ( Proterorhinus semilunaris ), which was introduced in the 1990s, and round goby, introduced in 2008. Both gobiid species soon became established following introduction ( Janáč et al. 2012; Janáč Draft et al. 2016) and have come to dominate the Dyje fish assemblage (Valová et al. 2015; Šlapanský et al. 2017).

2.2 Data collection

For all three field experiments, fish were sampled by electrofishing, using a portable backpack unit (SEN, f. Bednář, Czech Republic; frequency 75-85 Hz; maximum output

225/300 V) fitted with a small elliptical stainless-steel anode (25 x 15 cm) with 4 mm mesh netting (see Janáč et al. 2016 for further details). Sampling always took place during the day between 9:00 and 17:00.

Based on our own long-term experience, electrofishing by slow wading upstream along the bank has proved to be the most effective method for catching all age-classes of fish inhabiting the littoral rip-rap. Other methods were not used due to inappropriate conditions

(beach seining) or low efficiency (traps) in this part of the Dyje. Electrofishing of the nearshore zone is a reliable and commonly used method for sampling not only round goby

6 https://mc06.manuscriptcentral.com/cjfas-pubs Page 7 of 42 Canadian Journal of Fisheries and Aquatic Sciences

assemblages (Brander et al. 2013a) but also for describing riverine fish communities in

general (FAME Consortium 2004). As the river is relatively shallow, we were able to sample

the whole nearshore water column up to a distance of 2–4 m from the bank (depending on

slope), thus covering the whole rip-rap zone in this stretch of the river. Earlier observations

(using angling, traps and electrofishing) showed no presence of round gobies on the sandy

bottom in the middle of the river.

All fish captured were identified to species and measured to the nearest millimetre

(standard length, SL) on the bankside. Non-gobiid species were released to the water after

noting the numbers caught. Goby sex was determined through examination of the urogenital

papillae. Fish with a SL < 40 mm, or those with a SL of 40-55 mm whose sex could otherwise

not be determined, were recorded as juveniles. Draft

2.3 Field experiments

Three field experiments were conducted in order to: (i) reveal common movement rates of

gobies in an established population and seasonal aspects of any movement patterns (herein

Movement ); (ii) reveal how far gobies spread following simulated colonisation events from

single release points (herein Release ); and (iii) reveal which gobies first colonise a stretch

where gobies have previously been eradicated (herein Colonisation ).

2.3.1 Movement experiment

In this experiment, we divided an approximately 2 km long river stretch into 10 m sections,

the GPS coordinates at the start and end of each stretch being recorded to ensure localisation

during recapture events. We continuously surveyed sections in the middle of the stretch

(approx. 300-500 m from each end) by electrofishing. Each round goby caught was measured

and sexed and, with the exception of fish in poor condition and small fish (SL < 50 mm), 7 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 8 of 42

tagged with an VI Alpha tag (Visible Implant Alpha Tag; Northwest Marine Technology Inc.) inserted subcutaneously to the ventral part of body with a VI Alpha injector needle (Standard

1.2 mm x 2.7 mm needle V; Northwest Marine Technology Inc.). Each tag carried a unique alphanumerical code allowing identification of each individual. After tagging, the fish were placed into buckets containing clean river water and allowed to recover for 15 minutes. Each tagged fish was then released in the same 10 m section from which it was captured.

Three short-term capture-mark-recapture campaigns were undertaken to assess movement during the pre-spawning (691 fish tagged, capture 22.4.15, recapture 18.5.15, 26 days), spawning (635 fish tagged, capture 13.5.14, recapture 17.6.14, 35 days) and post-spawning

(390 fish tagged, capture 14.8.13, recapture 16.9.13, 33 days) periods. Seventeen tagged fish were recaptured after more than 200 days (i.e. outside of the planned recapture date), all fish being recaptured after winter. These fishDraft were not included into the analysis but are reported in the text as overwintering individuals. Recapture surveys started at the same site where the fish were tagged and extended 300–600 m upstream and downstream. When an individual was captured at the edge of the defined area, electrofishing was extended by a minimum of

200 m upstream or downstream. Several control sites were also sampled at greater distances in order to ensure capture of potential remote migrants. During the recapture campaigns, all round gobies caught were measured, sexed, checked for tags and the section in which they were captured recorded. Each tagged fish was humanely dispatched with an overdose of clove oil and frozen for later laboratory analysis. Round goby movement was quantified by recording the displacement distance between capture and recapture.

2.3.2 Release experiment

In this experiment, we simulated the release of a large number of individuals (propagules) at a single release point in order to monitor movement activity of fish originating from a single strong introduction event (e.g. by release of large numbers of fish from ship ballast water).

8 https://mc06.manuscriptcentral.com/cjfas-pubs Page 9 of 42 Canadian Journal of Fisheries and Aquatic Sciences

First, we partially depleted both banks (right bank = 900 m, left bank = 600 m) of a selected

river stretch by electrofishing over 16-17 July 2013. All fish captured in each section were

measured and sexed and then tagged with VIE tags (Visible Implant Elastomer, Northwest

Marine Technology, Inc.) using a 1 mm single-use syringe (0.30 mm diameter needle). Each

tag was inserted subcutaneously to the ventral part of the body along the anal fin on the right

or left side at the place of capture (left or right bank). In total, 1912 round gobies were tagged;

984 on the right bank and 928 on the left bank. After tagging, all fish were held in a large wire

cage in the river for one hour to recover. After convalescence, the gobies were released at a

single release point located in the middle of the respective stretch.

After 30 days, we continuously sampled 1400 m of the right bank and 1200 m of the left bank

immediately adjacent to the release points. In addition, several 200 m control stretches were

sampled at greater distances from the centralDraft release point in order to check for possible strays

with exceedingly high levels of movement activity. The control stretches comprised sections

of rip-rap (chosen as the most appropriate habitats for round gobies) located 1.6 and 16.1 km

upstream and 6.3 km downstream from the release point (Fig. 1). Within the main control

stretch, the length sampled was determined by the distance to which tagged fish were

observed, the minimum being 200 m from the last point where a tagged goby was captured.

For the recapture campaigns, the river stretch divided into 10 m sections and movement was

quantified by recording the distance between the release point and the 10 m recapture section

(i.e. based on a 10 m scale).

Fish tagging appeared to have no negative effect on specific groups of fish as the sex and size

of recaptured fish did not differ from a random subsample of tagged fish from the Release

experiment and the three mark-recapture campaigns in the Movement experiment

(Supplementary information, Table S1, Figs. S1-S4).

9 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 10 of 42

2.3.3 Colonisation experiment

This experiment took place in September 2012 over a 1 km rip-rap stretch of the Dyje, within ten 20 m sections randomly chosen for sampling. Each section was then electrofished (three pass depletion) and all fish caught (894 round gobies, 952 other fish species) were removed from the section. The round gobies were then overdosed with clove oil and frozen for later dietary analysis in the laboratory and all other fish were released back to the river. Four days after depletion, a resampling campaign took place in the same 20 sections, again using three pass electrofishing. For each round goby captured colonising the emptied section, we measured the distance from the edge of the section (0.1 m precision) and recorded the sex and size. Draft 2.4 Data analysis

2.4.1 Movement experiment

The distances recorded in the Movement experiment included a large proportion of zeros (see

Results); hence, we analysed movement patterns using three independent tests. First, using generalised linear models (GLM) we assessed which factors affected whether a fish had moved or not from the original 10 m capture section (response variable Bernoulli distributed; binomial part of the zero-altered model, according to Zuur et al. 2009), with sex, size, season and their interaction used as predictors. Second, using GLM, we assessed which factors affected the distance reached by those fish that had moved from the capture (release) section

(response variable negative binomial distributed; count part of the zero-altered model), with sex, size and season used as predictors (interactions excluded due to small dataset size).

10 https://mc06.manuscriptcentral.com/cjfas-pubs Page 11 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Finally, we assessed whether the fish that had moved had gone upstream or downstream, by

testing the significance of the intercept in GLM predicting direction (0 = downstream, 1 =

upstream; Bernoulli distributed).

2.4.2 Release experiment

For each fish, the distance reached from the release point was expressed as the number of 10

m sections travelled (independent of whether movement was upstream or downstream). The

effect of dispersal direction (upstream, downstream), sex, size and their interaction on

distance reached was tested using GLM (response variable negative binomial distributed). In order to test whether recaptured fish movedDraft preferentially upstream or downstream from the release point, we tested the significance of the intercept in GLM predicting direction (0 =

downstream, 1 = upstream; Bernoulli distributed).

2.4.3 Colonisation experiment

In order to show which fish were the most ‘active’ colonisers, we tested for the possible effect

of size, direction of colonisation (upstream, downstream) and their interaction on distance

from the 20m section border using generalised linear mixed models (GLMM; response

variable distance binomially distributed [ranging from 0 to 100 dm sections of the 100

possible]), with section as the random factor. The analysis was repeated on a reduced dataset

containing only adult fish in order to reveal any effect of sex, colonisation direction and their

interaction. As overdispersion was detected in both original GLMMs, individual-level random

effects (Elston et al 2001) were included into the binomial GLMMs.

11 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 12 of 42

2.4.4 Model selection and validation

In all analyses, non-significant terms were removed from the model based on a comparison of

Akaike information criteria (AIC) for models with and without the particular term (choosing models with a lower number of parameters with ΔAICc < 2). This rule was relaxed for the

GLMM, which provides only rough AIC estimates. In this case, the degree of

(non)significance in the removed term was used as a supporting criterion for removing a term from the model. Where the removal of a term was uncertain (ΔAICc was close to 2 after removing the term), we present both possible final models. The models were validated through visual inspection of residual patterns, with an alpha level of 0.05 set for all analyses.

All data were analysed using R statistical software v 3.5.0 (R Core Team 2018), using the base (R Core Team 2018), MASS (VenabelsDraft and Ripley 2002), VGAM (Yee 2015), lme4

(Bates et al. 2015), MuMIn (Bartoń 2018) and pscl packages (Zeileis et al. 2008).

3 Results

3.1 Movement experiment

Fish in the established population were predominantly stationary, with more than half (56 of

95, 58.9%) being recaptured within the same 10 m section in which they were released. While sex and size did not affect whether fish moved from the release section (all interactions containing these terms, as well as the terms themselves, were removed from the model; Table

S2), there was a significant difference between seasons (GLM, df = 2, 92, P = 0.002).

Sampling in both the pre-spawning and post-spawning periods produced a higher proportion of 'no-moves' (i.e. fish recaptured in the same section in which they were released) than in the spawning period (pre-spawn: 30 of 41 fish, 73.2 %; spawn: 12 of 34, 35.3%; post-spawn: 14

12 https://mc06.manuscriptcentral.com/cjfas-pubs Page 13 of 42 Canadian Journal of Fisheries and Aquatic Sciences

of 20, 70%; GLM, df = 1,73, P < 0.001, df = 1,52, P = 0.012, both significant after

Bonferroni correction for multiple testing).

Two thirds of fish that moved beyond the area of release moved upstream (26 fish upstream,

13 downstream, the difference being significant: GLM, df=37, P = 0.041). On average, fish

moving beyond the release section travelled 79 m, compared to an average of 33.3 m for all

recaptures. This figure was significantly affected by three long-distance migrants that

travelled 420, 560 and 770 m (Fig. 2). Distance reached was unaffected by movement

direction, season, size or sex (all terms removed from the model; Table S2). Note, however,

that both size and sex were close to significance (Table S2; GLM, both df = 1, 37, P = 0.072

for size and 0.051 for sex) and, if kept in the final model, this would suggest that smaller fish

and males travelled longer distances (Fig. 2).

Distances reached by overwintering fishDraft (i.e. fish from long-term recaptures that stayed over

winter) were similar to those of short-term recaptures. Of the 17 fish caught, eleven were

recaptured within 40 m of the release section (64.7%, six males, five females; Fig. 3), seven

(41.3 %) within 10 m and four (23.5%, two males, two females) within the same section

where they were released. Five fish were recaptured downstream of the original section and

eight upstream (Fig. 3).

3.2 Release experiment

Of the 107 gobies (68 females, 39 males) recaptured 30 days after release, six (5.6 %; three

males, three females) moved less than 10m, 20 (18.7 %; nine females, eleven males) moved

downstream and 81 (75.7 %; 56 females, 25 males) upstream (Figs. 4 and 5), the difference

between upstream and downstream movement being significant (GLM, df = 100, P < 0.001).

Recaptured fish accounted for 5.7 % of the 1867 tagged fish released.

13 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 14 of 42

Two final models were chosen when predicting distance reached, the first including the term direction only (lowest AICc; Table S3) and the second including the terms direction, sex, size and sex:size interaction (ΔAICc after removing interaction term = 1.8; Table S3). The first model indicated that fish moved a significantly longer distance upstream (mean upstream distance reached = 199.17 m, mean downstream distance = 65.65 m; Fig. 5). In the second model, only the terms direction and sex:size interaction were significant (all df = 1,105, P <

0.001 for direction, P = 0.603 for sex, P = 0.605 for size and P = 0.045 for sex:size). Partial tests showed that, while distance was independent of size in females (GLM, df= 1,66, P =

0.193), smaller males moved significantly more than larger males (GLM, df =1, 37, P =

0.038; Fig. 6). Eight fish were also recorded crossing to the other riverbank (7.5 % of recaptured fish) where they moved 200 to 670 upstream, thereby exceeding the overall mean distance reached. Draft

3.3 Colonisation experiment

While distance reached from the section border was independent of sex and colonisation direction (the terms sex, direction, sex:direction and size:direction removed from the final model; Table S4), it decreased significantly with fish size (GLMM, df =1,361, P =0.009; Fig.

7).

4 Discussion

Movement of the established round goby population ( Movement experiment) corresponded well with a leptokurtic dispersal kernel (Fraser et al. 2001; Radinger and Wolter

2014), i.e. a large number of no- or small movements with few individuals exhibiting large- scale movement activity. The majority of fish, therefore, exhibited high site fidelity, with

14 https://mc06.manuscriptcentral.com/cjfas-pubs Page 15 of 42 Canadian Journal of Fisheries and Aquatic Sciences

almost 60 % being recaptured within the same 10 m section they were released in. Such high

site fidelity has been reported previously (Wolfe and Marsden 1998; Ray and Corkum 2001;

Lynch and Mensinger 2012), with some reports of over 90 % fidelity. One possible reason for

the relatively low fidelity (compared with the studies above) recorded in our study may be our

use of unbaited sampling. Previous studies used either baited traps or rod and line fishing,

thereby introducing possible bias from over-estimating stationarity in fish that are attracted to

the bait. Furthermore, we studied relatively small-scale fish movements (over 10m sections)

and/or used relatively long recapture times (approx. 30 days). Nevertheless, our rate of

fidelity was still high and provides strong evidence that the majority of the established goby

population consisted of highly stationary individuals. A similar pattern has also been reported

for other small benthic fishes, including darters (Hicks and Servos 2017), balitorids (Mitsuo et

al. 2013) and, especially, cottids (HudyDraft and Shiflet 2009).

During the spawning period, site fidelity in the established population appears to have

relaxed, with 35.3 % of fish remaining stationary compared with 73.2% during pre-spawning

and 70% post-spawning. Such a difference was not expected, however, as fish are likely to be

more active in the pre-spawning season as they return from their overwintering refuges,

increase feeding and seek spawning sites. Our finding of increased movement during the

spawning season was somewhat surprising as it is presumed that large territorial males remain

stationary at this time while they guard egg clutches (Corkum et al. 1998; Meunier et al. 2009;

but see Všetičková et al. 2015). A possible explanation could be that while larger territorial

males remain stationary, the activity of both smaller males (supposed sneakers; Bleeker et al.

2017) and females increases as they search for suitable nests. Interestingly, while a similar

seasonal activity pattern (increased activity in the spawning season) is occasionally

documented in cottids (Knaepkens et al. 2004) and other, non-benthic fishes (Freeman 1995;

Ovidio et al. 2002), it is not a general pattern among fish (Lucas and Baras 2008).

15 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 16 of 42

Site fidelity appears to be typical for gobies as long-term fidelity was also apparent in overwintering fish, most of which were recaptured within 40 m of the original capture site after more than 200 days. Though surprising, such long-term fidelity has been reported in previous studies. Lynch and Mensinger (2012), for example, noted similar fidelity in overwintering round gobies from Lake Superior, while Breen et al. (2009) and Huddy and

Shiflet (2009) have reported long-term site affinity in cottids. One interpretation for our own observations is that round gobies overwinter at the same site where they stay the remainder of the year (with the exception of spawning). However, this would contradict previous studies that interpret decreases in winter round goby abundance as evidence of winter migrations to deeper areas (Sapota and Skóra 2005; Pennuto et al. 2010). While a similar decrease in winter nearshore abundance has been documented from our study site (Jurajda, unpublished data), the fidelity of overwintering fish suggestsDraft that the decrease may be attributable to reduced catchability, e.g. through temperature-related activity suppression. On the other hand, our data do not disprove the occurrence of winter migrations as our results could also be showing that gobies migrated to an (unknown) winter refuge, from where they were able to return to the same spot they left. Though there have been previous suggestions of such behaviour in round goby (e.g. see Marentette et al. 2011; Lynch and Mensinger 2012), it has yet to be confirmed; hence, this question remains open and calls for further research.

Round gobies in the established population moved 1.97 m per day on average and a maximum of 16 m per day upstream, distances similar to those reported from Lake Superior by Lynch and Mensinger (2012), i.e. 0.79 m per day on average and a maximum of 7-15 m per day during long-term dispersal (more than two weeks). While recording upstream movement of the round goby invasion front on the River Dyje, Šlapanský et al. (2017) recorded movements of 3.2 km per year, equivalent to 8.77 m per day. A more conservative estimate by Bergstrom et al. (2008) suggested natural invasion front movements of 1 km per

16 https://mc06.manuscriptcentral.com/cjfas-pubs Page 17 of 42 Canadian Journal of Fisheries and Aquatic Sciences

year, i.e. 2.74 m per day, in Lake Superior. The average movement rates of fish in established

populations clearly do not match the speeds achieved in invasive front shifts. However, such a

speed could theoretically be achieved if one considers the maximum distances recorded in

established populations, which can be even higher for short-term observations, with

individuals even achieving 40 to 50 m per day (Lynch and Mensinger 2012; Brandner et al.

2015). Potentially, high rates of invasion front shift thus could be maintained by a series of

short-term intensive jumps. Thus far, however, it is uncertain whether long-distance

dispersers can maintain such high movement rates over long periods (i.e. longer than a

month), with the evidence generally suggesting otherwise (Lynch and Mensinger et al. 2012).

On the other hand, fish in the invasion front encounter significantly lower intraspecific

density than those in the established population (Azour et al. 2015; Šlapanský et al. 2017).

Further, a number of studies have documentedDraft increased boldness and greater phenotypic

plasticity in fish at the invasive front (Brandner et al. 2013b; Myles-Gonzales et al. 2015;

Thorlacius et al. 2015), which may even result in the ‘Olympic village effect’ (Phillips et al.

2008). Such factors can result in fish at the invasion front moving at greater rates than those in

the established population (Phillips et al. 2008; Chuang and Peterson 2016).

Fish in the Release experiment (simulating the release of large numbers at a single

spot) moved approximately three times further than those in the established population,

reaching up to 670 m over 30 days (average 199.17 m), or 22.33 m per day (av. 6.64 m). This

relatively high movement rate most likely reflects increased intraspecific competition due to

high propagule pressure, though several other factors may also have contributed. The optimal

rip-rap habitat is limited to a narrow strip along the Dyje; hence, limited access to usable

shelters could also increase intraspecific competition, and thus movement activity. Those

gobies ‘forced’ out of the narrow rip-rap zone may be forced to enter the faster-flowing gravel

section in the middle of the stream, which could further facilitate dispersal by increasing the

17 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 18 of 42

intensity of movement to avoid unfavourable conditions (Ray and Corkum 2001; Brandner et al. 2015).

It is likely that the sub-optimal conditions in the middle of the stream contributed to the low proportion of fish crossing to the other bank (eight individuals, 7.5 %). Support for this is provided by Brandner et al. (2015), who noted that gobies in the Danube never crossed the river and that spreading took place solely along near-bank rip-rap structures. The fact that some gobies did cross the Dyje may be explained by two factors. First, the Dyje is much narrower than the Danube, making the crossing easier; second, high competition pressure generated at the release point forced large numbers of gobies to move out of the rip-rap, thereby generating short-term competitive pressure outside of the rip-rap zone itself. This may have resulted in some individuals breaking away from the population and moving to the other bank, a hypothesis supported by the Draft above-average distances reached by the river-crossers

(200–670 m). In fact, high propagule pressure at the release site (as has been suggested by genetic studies; Janáč et al. 2017) may be one cause of round gobies colonising both banks of large rivers, without the need for independent introductions to both banks and despite a general unwillingness to cross under normal conditions (Brandner et al. 2015).

Both the Movement and Release experiments provided evidence of directional movement, with a clear preference for moving upstream. This corresponds with previous observations of relatively rapid upstream spread of round goby populations (Phillips et al.

2003; Poos et al. 2010; Šlapanský et al. 2017), with less intense downstream dispersal

(Brownscombe and Fox 2012), though the latter has received relatively little study. On the other hand, passive downstream dispersal of gobiid early life stages could serve as a counterbalance for the predominant upstream movement of adults (Janáč et al. 2013a, 2013b), i.e. different age groups are responsible for the invasion process, with upstream dispersal

18 https://mc06.manuscriptcentral.com/cjfas-pubs Page 19 of 42 Canadian Journal of Fisheries and Aquatic Sciences

predominantly undertaken by adults while early life stages contribute to rapid downstream

dispersal (Janáč et al. 2012; Roche et al. 2015).

In each of the three experiments, there were signs of size-related movement patterns,

though with some differences in each case. In the Movement experiment, for example, smaller

fish tended to travel greater distances, though the effect of size was only close to significance,

suggesting smaller fish in established populations travel further. In the Release experiment,

smaller males moved further from the common release point than larger males, but not

females. Finally, in the Colonisation experiment, smaller fish were found further from the

edges of the re-colonised sections, again suggesting that smaller fish are the first colonisers of

‘goby-free’ stretches.

Greater movement by smaller fish could be explained by interspecific competition

(especially in the Release experiment),Draft with smaller fish presumably having inferior

competitive ability. Ray and Corkum (2001), for example, suggested that larger gobies

outcompete smaller gobies, forcing them out of the preferred rip-rap areas and onto beaches

(see also Johnson et al. 2005; Bergstrom et al. 2008; Brownscombe and Fox 2012). Likewise,

Groen et al. (2012) showed that, if an opponent was only slightly larger, then the smaller

round goby did not interact aggressively but rather moved to another site. This would suggest

that, as the population density in the core area grows and the number of larger individuals

increases, then smaller individuals are pushed to the edge of the core area and there create the

invasion front (Ray and Corkum 2001, Thorlacius et al. 2015).

Our results for size-biased movement in the Colonisation experiment may provide the most

significant contribution in the ongoing debate as to whether smaller or larger gobies are the

‘pioneers’ leading the invasion front into unsettled areas (Šlapanský et al. 2017). While the

experiment was not an ideal model of an invasion front (as goby density in adjacent stretches

was still high, corresponding to an established population), it demonstrated that smaller

19 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 20 of 42

gobies were the first to move into ‘goby-free’ stretches. However, previous studies show wide variation in invasion front size composition, with fish ‘pioneers’ ranging from small (Johnson et al. 2005; Bergstrom et al. 2008; Brownscombe and Fox 2012), through medium (Azour et al. 2015) and large (Gutowsky and Fox 2011; Brandner et al. 2013), and even with differences occurring in the same river (Šlapanský et al. 2017). There are several possible explanations for this variation. First, pioneers may represent a combination of outcompeted smaller fish and larger bolder individuals that are predisposed to move further and explore areas outside the core population (e.g. see Brownscombe and Fox 2012). Indeed, many invasion front and edge populations have been shown to contain a large proportion of bolder individuals (Groen et al. 2012; Myles-Gonzales et al. 2015; Hirsch et al. 2017), though it has yet to be proved whether these fish are bold because they live in an area of low goby density or because their boldness caused them to move away fromDraft the core population. Secondly, it may take a relatively long time for gobies to disperse to the invasion edge from the core population.

Hence, while the pioneer fish starts small, it may increase in weight and length relatively rapidly in new habitats with an abundant (competition free) food source. The size of fish caught at the invasion front, therefore, would depend on any temporal lag (detection lag phase) and regional conditions (Sakai et al. 2001).

To conclude, round goby movement activity within an established population displayed a typical leptokurtic movement pattern, with the vast majority of the population remaining stationary and just a few small long-range dispersers. These results also suggest that smaller individuals most likely contribute to ‘natural’ range expansion, with intraspecific competition the likely driver. These patterns appear to be accentuated in the lower Dyje, where optimal habitat is limited to a narrow strip of bankside rip-rap and upstream expansion is the only option for competitively weak smaller individuals, and especially males. Local

20 https://mc06.manuscriptcentral.com/cjfas-pubs Page 21 of 42 Canadian Journal of Fisheries and Aquatic Sciences

conditions, whether biotic or abiotic, also play a substantial role in round goby movement

patterns.

Acknowledgements

This study was supported through Czech Science Foundation (GA CR) Grant No.

505/12/G112: ECIP. We thank L. Mikl, L. Všetičková, Z. Jurajdová and M. Koníčková for

their help with the fieldwork. We are much indebted to the representatives of the Moravian

Angling Union (V. Habán) for allowing us to undertake this study in their waters.

Literature Draft

Ahnelt, H., Bănărescu, P., Spolwind, R., Harka, A., and Waidbacher, H. 1998. Occurrence

and distribution of three gobiid species (Pisces: Gobiidae) in the middle and upper Danube

region – example of different dispersal patterns? Biológia, Bratislava, 53 : 661-674.

Azour, F., van Deurs, M., Behrens, J., Carl, H., Hüssy, K., Greisen, K., Ebert, R., and Møller,

P.R. 2015. Invasion rate and population characteristics of the round goby Neogobius

melanostomus : effects of density and invasion history. Aquat. Biol. 24 (1): 41-52.

doi:10.3354/ab00634.

Bartoń, K. 2015. MuMIn: Multi-Model Inference. R package version 1.15.1. Available from

http://CRAN.R-project.org/package=MuMIn.

21 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 22 of 42

Bates, D., Maechler, M., Bolker, B., and Walker, S. 2015. Fitting Linear Mixed-Effects

Models Using lme4. J. Stat. Soft. 67 (1): 1-48. doi:10.18637/jss.v067.i01.

Bergstrom, M.A., Evrard, L.M., and Mensinger, A.F. 2008. Distribution, abundance, and range of the round goby, Apollina melanostoma , in the Duluth-Superior harbour and St. Louis river estuary, 1998-2004. J. Great Lakes Res. 34 (3): 535-543. doi.org/10.3394/0380-

1330(2008)34[535:DAAROT]2.0.CO;2.

Bleeker, K., de Jong, K., van Kessel, N., Hinde, C.A., and Nagelkerke, L.A.J. 2017. Evidence for ontogenetically morphologically distinct alternative reproductive tactics in the invasive round goby Neogobius melanostomus . PLoS ONE. 12 (4): e0174828. doi.org/10.1371/journal. pone.0174828. Draft

Brandner, J., Pander, J., Mueller, M., Cerwenka, A.F., and Geist, J. 2013a. Effect of sampling techniques on population assessment of invasive round goby Neogobius melanostomus . J.

Fish Biol. 82 (6): 2063-2079. doi:10.1111/jfb.12137.

Brandner, J., Cerwenka, A.F., Schliewen, U.K., and Geist, J. 2013b. Bigger is Better: characteristics of round gobies forming an invasion front in the Danube river. PLoS One 8(9). e73036. doi:10.1371/journal.pone.0073036.

Brandner, J., Auerswald, K., Schäufele, R., Cerwenka, A.F., and Geist, J. 2015. Isotope evidence for preferential dispersal of fast-spreading invasive gobies along man-made river bank structures. Isot. Environ. Healt. S. 51 (1): 80-92. doi:10.1080/10256016.2014.993978.

22 https://mc06.manuscriptcentral.com/cjfas-pubs Page 23 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Breen, M.J., Reutz, C.R.III., Thompson, K.J., and Kohler, S.L. 2009. Movements of mottled

sculpins ( Cottus bairdii ) in a Michigan stream: how restricted are they? Can. J. Fish. Aquat.

Sci. 66 (1): 31-41. doi:10.1139/F08-189.

Bronnenhuber, J.E., Dufour, B.A., Higgs, D. M., and Heath, D.D. 2011. Dispersal strategies,

secondary range expansion and invasion genetics of the nonindigenous round goby,

Neogobius melanostomus , in Great Lakes tributaries. Mol. Ecol. 20 (9): 1845-1859.

doi:10.1111/j.1365-294X.2011.05030.x.

Brownscombe, J.W., and Fox, M.J. 2012. Range expansion dynamics of the invasive round

goby (Neogobius melanostomus ) in a river system. Aquat. Ecol. 46 (2): 175-189.

doi:10.1007/s10452-012-9390-3. Draft

Cammaerts, R., Spikmans, F., van Kessel, N., Verreycken, H., Chérot, F., Demol, T., and

Richez, S. 2012. Colonization of the Border Meuse area (The Netherlands and Belgium) by

the non-native western tubenose goby Proterorhinus semilunaris (Heckel, 1837) (Teleostei,

Gobiidae). Aquat. Invasions. 7(2): 251–258. doi:10.3391/ai.2012.7.2.011.

Cook, E.J., Ashton, G., Campbell, M., Coutts, A., Gollasch, S., Hewitt, CH., Liu H., Minchin,

D., Ruiz, G., and Shucksmith, R. 2008. Non-native aquaculture species release: Implications

for aquatic ecosystems. In: Aquaculture in the Ecosystem. Edited by M. Holmer, K. Black,

C.M. Duarte, N. Marbà and I. Karakassis). Springer, London, UK. pp. 155-184.

23 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 24 of 42

Cookingham, M.N., and Reutz, C.R., III. 2008. Evaluating passive integrated transponder tags for tracking movements of round gobies. Ecol. Fresh. Fish. 17 (2): 303-311. doi:10.1111/j.1600-0633.2007.00282.x.

Corkum, L.D., MacInnis, A.J., and Wickett, R.G. 1998. Reproductive habits of round gobies.

Great Lakes Res. Rev. 3: 13-20.

Coulter, A.A., Bailey, E.J., Keller, D., and Goforth, R.R. 2016. Invasive Silver Carp movement patterns in the predominantly free-flowing Wabash River (Indiana, USA). Biol.

Invasions. 18 (2): 471-785. doi:10.1007/s10530-015-1020-2.

Elston, D.A., Moss, R., Boulinier, T.,Draft Arrowsmith, C., and Lambin, X. 2001. Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology. 122(5):

563-569. doi:10.1017/S0031182001007740.

FAME Consortium. 2004. Manual for the application of the European Fish Index - EFI. A fish-based method to assess the ecological status of European rivers in support of the Water

Framework Directive. Version 1.1, January 2005. Available from http://fame.boku.ac.at/downloads/manual_Version_Februar 2005.pdf.

Fraser, D.F., Gilliam, G.F., Daley, M.J., Le, A.N., and Skalski, G.T. 2001. Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration.

Am. Nat. 158 (2): 124-135. doi:10.1086/321307.

24 https://mc06.manuscriptcentral.com/cjfas-pubs Page 25 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Freeman, M.C. 1995. Movements by two small fishes in a large stream. Copeia. 1995(2): 361-

367. doi:10.2307/1446899.

Gozlan, R.E. 2008. Introduction of non-native freshwater fish: is it all bad? Fish Fish. 9(1):

106-115. doi:10.1111/j.1467-2979.2007.00267.x.

Gozlan, R.E., Britton, J.R., Cowx, I., and Copp, G.H. 2010. Current knowledge on non-native

freshwater fish introductions. J. Fish Biol. 76 (4): 751-786. doi:10.1111/j.1095-

8649.2010.02566.x.

Groen, M., Sopinka, N.M., Marentette, J.R., Reddon, A.R., Brownscombe, J.W., Fox, M.G., Marsh-

Rollo, S.E., and Balshine, S. 2012. Is Draft there role of aggression in round goby invasion fronts?

Behaviour. 149: 685-703. doi:10.1163/1568539X-00002998.

Gutowsky, L.F.G., and Fox, M.J. 2011. Occupation, body size and sex ratio of round goby

(Neogobius melanostomus ) in established and newly invaded areas of an Ontario river.

Hydrobiologia. 671(1): 27-37. doi: 10.1007/s10750-011-0701-9.

Hicks, K.A., and Servos, M.R. 2017. Site fidelity and movement of a small-bodied fish

species, the rainbow darter ( Etheostoma caeruleum ): Implications for environmental effects

assessment. River Res. Applic. 33 (7): 1016-1025. doi:10.1002/rra.3161.

Hirsch, P.E., Thorlacius, M., Brodin, T., and Burkhardt-Holm, P. 2017. An approach to

incorporate individual personality in modelling fish dispersal across in-stream barriers. Ecol.

Evol. 7(2): 720-732. doi:10.1002/ece3.2629.

25 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 26 of 42

Hudy, M., and Shiflet, J. 2009. Movement and recolonization of Potomac sclupin in a

Virginia stream. N. Am. J. Fish. Manage. 29 (1): 196-204. doi:10.1577/M07-101.1.

Chaung, A., and Peterson, CH.R. 2016. Expanding population edges: theories, traits, and trade-offs. Global Change Biol. 22 (2): 494-512. doi:10.1111/gcb.13107.

Janáč, M., Valová, Z., and Jurajda, P. 2012. Range expansion and habitat preferences of non- native 0+ tubenose goby ( Proterorhinus semilunaris ) in two lowland rivers in the Danube basin. Fund. Appl. Limnol. 181(1): 73-85. doi: 10.1127/1863-9135/2012/0321.

Janáč, M., Jurajda, P., Kružíková, L., Roche, K., and Prášek, V. 2013a. Reservoir to river passage of age-0+ year fishes, indicationDraft of a dispersion pathway for a non-native species, J. Fish Biol. 82 (3): 994-1010. doi:10.1111/jfb.12037.

Janáč, M., Šlapanský, L., Valová, Z., and Jurajda, P. 2013b. Downstream drift of round goby

(Neogobius melanostomus ) and tubenose goby ( Proterorhinus semilunaris ) in their non- native area. Ecol. Freshwat. Fish. 22 (3): 430-438. doi: 10.1111/eff.12037.

Janáč, M., Valová, Z., Roche, K., and Jurajda, P. 2016. No effect of round goby Neogobius melanostomus colonization on young-of-the-year fish density or microhabitat use. Biol.

Invasions. 18 (8): 2333-2347. doi:10/1007/s10530-016-1165-7.

Janáč, M., Bryja, J., Ondračková, M., Mendel, J., and Jurajda, P. 2017. Genetic structure of three invasive gobiid species along the Danube-Rhine invasion corridor, similar distributions, different histories. Aquat. Invasions. 12 (4): 551-564. doi:10.3391/ai.2017.12.4.11.

26 https://mc06.manuscriptcentral.com/cjfas-pubs Page 27 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Johnson, T.B., Allen, M., Corkum, L.D., and Lee, V.A. 2005. Comparison of methods needed

to estimate population size of round gobies ( Neogobius melanostomus ) in western Lake Erie.

J. Great Lakes Res. 31(1): 78-86. doi:10.1016/S0380-1330(05)70239-2.

Jurajda, P., and Peňáz, M. 1994. Fish community of the lower regulated stretch of the river

Morava, Czech Republic. Fol. Zool. 43 (1): 57-64.

Kelle,r R.P., and Lodge, D.M. 2007. Species invasions from commerce in live aquatic

organisms: problems and possible solutions. BioScience 57 (5): doi:428-436.

10.1641/B570509.

Knaepkens, G., Bruyndoncx, L., and Eens,Draft M. 2004. Assessment of residency and movement

of the endangered bullhead ( Cottus gobio ) in two Flemish rivers. Ecol. Freshwat. Fish. 13 (4):

317-322. 10.1111/j.1600-0633.2004.00065.x.

Kornis, M.S., and Vander Zanden, M.J. 2010. Forecasting the distribution of the invasive

round goby (Neogobius melanostomus ) in Wisconsin tributaries to lake Michigan. Can. J.

Fish. Aquat. Sci. 67 (3): 553-562. doi:10.1139/F10-002.

Kornis, M.S., Mercado-Silva, N., and Vander Zanden, M.J., 2012. Twenty years of invasion:

a review of round goby Neogobius melanostomus biology, spread and ecological implications.

J. Fish Biol. 80 (2): 235-285. doi:10.1111/j.1095-8649.2011.03157.x.

Landsman, S.J., Nguyen, V.M., Gutowsky, L.F.G., Gobin, J., Cook, K.V., Binder, T.R.,

Lower, N., McLaughlin, R.L., and Cooke, S.J. 2011 . Fish movement and migration studies in

27 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 28 of 42

the Laurentian Great Lakes: Research trends and knowledge gaps. J. Great Lakes Res. 37 (2):

365-379. doi:10.1016/j.jglr.2011.03.003.

LaRue, E.A., Reutz, C.R.III., Stacey, M.B., and Thum, R.A. 2011. Population genetic structure of the round goby in Lake Michigan: implications for dispersal of invasive species.

Hydrobiologia 663(1): 71-82. doi:10.1007/s10750-010-0555-6.

Lucas, M.C., and Baras, E. (2001). Migration of freshwater fish. Blackwell Science Ltd.,

Oxford, UK.

Lynch, M.P., and Mensinger, A.F. 2012. Seasonal abundance and movement of the invasive round goby (Neogobius melanostomus Draft) on rocky substrate in the Duluth – Superior harbour of lake Superior. Ecol. Freshwat. Fish. 21 (1): 64-74. doi:10.1111/j.1600-0633.2011.00524.x.

Marentette ,J.R., Wang, G., Tong, S., Sopinka, N.M., Taves, M.D., Koops, M.A., and

Balshine, S. 2011. Laboratory and field evidence of sex-biased movement in the invasive round goby. Behav. Ecol. Sociobiol. 65 (12): 2239-2249. doi:10.1007/s00265-011-1233-z.

Masson, L., Brownscombe, J.W., and Fox, M.G. 2016. Fine scale spatio-temporal life history shifts in an invasive species at its expansion front. Biol. Invasions. 18 (3): 775-792. doi:10.1007/s10530-015-1047-4.

Meunier, B., Yavno, S., Ahmed, S., and Corkum, L.D. 2009. First documentation of spawning and nest guarding in the laboratory by the invasive fish, the round goby ( Neogobius melanostmus ). J. Great Lakes Res. 35 (4): 608-612. doi:10.1016/j.jglr.2009.08.012.

28 https://mc06.manuscriptcentral.com/cjfas-pubs Page 29 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Mitsuo, Y., Ohira, M., Tsunoda, H., and Yuma, M. 2013. Movement patterns of small benthic

fish in lowland headwater streams. Freshwater Biol. 58 (11): 2345-2354.

doi:10.1111/fwb.12214.

Myles-Gonzales, E., Burness, G., Yavno, S., Rooke, A., and Fox, M.G. 2015. To boldly go

where no goby has gone before: boldness, dispersal tendency, and metabolism at the invasion

front. Behav. Ecol. 26 (4): 1083-1090. doi:10.1093/beheco/arv050.

Ovidio, M., Baras, E., Goffaux, D., Giroux, F., and Philippart, J.C. 2002. Seasonal variations

of activity pattern of brown trout ( Salmo trutta ) in a small stream, as determined by radio-

telemetry. Hydrobiologia. 470(1-3): 195-202.Draft doi:10.1023/A:1015625500918.

Padilla, D.K., and Williams, S.L. 2004. Beyond ballast water: aquarium and ornamental

trades as resource of invasive species in aquatic ecosystems. Front. Ecol. Environ. 2(3): 131-

138. doi:10.1890/1540-9295(2004)002[0131:BBWAAO]2.0.CO;2.

Penuto, C.M., Krakowiak, P.J., and Janik, C.E. 2010. Seasonal abundance, diet, and energy

consumption of round gobies ( Neogobius melanostomus ) in Lake Erie tributary streams. Ecol.

Freshwat. Fish. 19(2): 206-215. doi:10.1111/j.1600-0633.2010.00405.x.

Phillips, B.L., Brown, G.P., Travis, J.M.J., and Shine, R. 2008. Reid´s paradox revisited: The

evolution of dispersal kernels during range expansion. Am. Nat. 172(1): 34-48.

doi:10.1086/588255.

29 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 30 of 42

Phillips, E.C., Washek, M. E., Hertel, A.W., Niebel, B.M., 2003. The round goby ( Neogobius melanostomus ) in Pennsylvania tributary streams of Lake Erie. J. Great Lakes Res. 29 (1): 34-

40. doi:10.1016/S0380-1330(03)70413-4.

Poos, M., Dextrase, A.J., Schwalb, A.N., and Ackerman, J.D. 2010. Secondary invasion of the round goby into high diversity Great Lakes tributaries and species at risk hotspots: potential new concerns for endangered freshwater species. Biol. Invasions. 12 (5): 1269-1284. doi:10.1007/ s10530-009-9545-x.

Radinger, J., and Wolter, Ch. 2014. Patterns and predictors of fish dispersal in rivers. Fish

Fish. 15 (3): 456-473. doi:10.1111/faf.12028. Draft

Rahel, F.J., and Smith, M.A. 2018. Pathways of unauthorized fish introductions and types of management responses. Hydrobiologia. 817(1), 41-56. doi:10.1007/s10750-018-3596-x.

Ray, W.J., and Corkum, L.D. 2001. Habitat and site affinity of the round goby. J. Great Lakes

Res. 27 (3): 329-334. doi:10.1016/S0380-1330(01)70648-X.

R Core Team 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org/.

Ricciardi, A., and McIsaac, H.J. 2000. Recent mass invasion of the North American Great

Lakes by Ponto-Caspian species. Trends Ecol. Evol. 15 (2): 62-65. doi:10.1016/S0169-

5347(99)01745-0.

30 https://mc06.manuscriptcentral.com/cjfas-pubs Page 31 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Roche, K.F., Janač, M., and Jurajda, P. 2013. A review of Gobiid expansion along the

Danube-Rhine corridor – Geopolitical change as a driver for invasion. Knowl. Manage.

Aquat. Ecosyst., 411(01): pp. 1-23. doi:10.1051/kmae/2013066.

Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman,

S., Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O'neil, P., Parker, I.M.,

Thompson, J.N., and Weller, S.G. 2001. The population biology of invasive species. Annu.

Rev. Ecol. Syst. 32: 305-332. doi:10.1146/annurev.ecolsys.32.081501.114037.

Sapota, M.R., and Skóra, K.E. 2005. Spread of alien (non-indigenous) fish species Neogobius

melanostomus in the Gulf of Gdansk (south Baltic). Biol. Invasions. 7(2): 157-164.

doi:10.1007/s10530-004-9035-0. Draft

Skalski, T.S., and Gilliam, J.F. 2000. Modelling diffusive spread in a heterogeneous

population: a movement study with stream fish. Ecology 81(6): 1685-1700.

doi:10.1890/0012-9658(2000)081[1685:MDSIAH]2.0.CO;2.

Šlapanský, L., Janáč, M., Roche, K., Mikl, L., and Jurajda, P. 2017. Expansion of round

gobies in a non-navigable river system. Limnologica. 67: 27-36. doi:10.1016/j.limno.

2017.09.001.

Thorlacius, M., Hellström, G., and Brodin, T. 2015. Behavioral dependent dispersal in the

invasive round goby Neogobius melanostomus depends on population age. Curr. zool. 61 (3):

529-542. doi:10.1093/czoolo/61.3.529.

31 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 32 of 42

Valová, Z., Jurajda, P., and Janáč, M. 2006. Spatial distribution of 0+ juvenile fish in differently modified lowland rivers. Folia zool. 55 (3): 293-308.

Valová, Z., Konečná, M., Janáč, M., and Jurajda, P. 2015. Population and reproductive characteristics of a non-native western tubenose goby ( Proterorhinus semilunaris ) population unaffected by gobiid competitors. Aquat. Invasions. 10 (1): 57-68. doi:10.3391/ai.2015.10.1.06.

Venables, W.N., & Ripley, B.D. 2002. Modern Applied Statistics with S. Fourth Edition.

Springer, New York, NY.

Všetičková, L., Janáč, M., Roche, K.,Draft and Jurajda, P. 2015. Assessment of posible diel and sex-related differencies in round goby ( Neogobius melanostomus ) diet. Folia Zool. 64 (2):

104-111. doi:10.25225/fozo.v64.i2.a3.2015.

Wiesner, C. 2005. New records of non-indigenous gobies ( Neogobius sp .) in the Austrian

Danube. J. Applied Ichthyol., 21 (4): 324-327. doi:10.1111/j.1439-0426.2005.00681.x.

Wonham, M.J., Carlton, J.T., Ruiz, G.M., and Smith, L.D. 2000. Fish and ships: relating dispersal frequency to success in biological invasions. Mar. Biol. 136(6): 1111-1121. doi:10.1007/s002270000303.

Wolfe, K.R., and Marsden, E.J. 1998. Tagging methods for the round goby ( Neogobius melanostomus ). J. Great Lakes Res. 24(3): 731-735. doi:10.1016/S0380-1330(98)70857-3.

32 https://mc06.manuscriptcentral.com/cjfas-pubs Page 33 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Yee, T. W. 2015. Vector Generalized Linear and Additive Models: With an Implementation

in R. Springer, New York, NY.

Zeileis, A., Kleiber, CH., and Jackman, S. 2008. Regression Models for Count Data in R. J.

Stat. Soft. 27 (8): pp. 1-25. doi:10.18637/jss.v027.i08.

Zuur, A.F., Ieno, E.F., Walker, N.J., Saveliev, A.A., and Smith, G.M. 2009. Zero-truncated

and zero-inflated models for count data. In: Mixed effects models and extensions in ecology

with R. Edited by A.F. Zuur, E.L. Ieno, N.J. Walker, A.A. Saveliev and G.M. Smith.

Springer, New York, NY. pp. 261-293. Draft

33 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 34 of 42

Figure captions:

Fig 1. Map of the area studied. (a ) Section of the Dyje River that was searched for tagged round gobies ( Neogobius melanostomus ). Empty circles indicate control points (200m long) checked for the presence of potential long-distance dispersers. ( b) Enlargement showing ‘core’ study section, where all fish were initially tagged and released. Black points indicate release points for Release experiment, grey points indicate upper and lower borders of the shoreline searched in recapture campaign. Tagging section (TS) for the Movement experiment is indicated by the dark grey area. Light grey area shows upstream and downstream buffer zones (BZ), at least 200 meters long, which were searched to capture fish that potentially moved out of the TS. The Colonisation experiment sites were randomly situated within the TS. ( c) Localisation of the site (empty square) within the European continent. The Danube River and the Czech Republic are highlighted.

Fig. 2. Distance reached between captureDraft and recapture by round goby males (points) and females (triangles) during the pre-spawning (green), spawning (red) and post-spawning (blue) seasons ( Movement experiment). Positive values show upstream movement, negative downstream. Only fish that moved beyond the original 10-m stretch (non-null movement) are shown. Fish size values in the figure were slightly adjusted by adding a random small number in order to prevent overlap of two or more points. Please note that x-axis scale interruptions were needed to show long-distance movements.

Fig. 3. Distance reached by round goby males (points) and females (triangles) between capture and recapture over periods > 200 days (includes winter months; Movement experiment). Positive values show upstream movement, negative downstream. Fig. 4. Distance reached from release point by round goby males (full points) and females (empty squares) within 30 days and its relationship to fish size ( Release experiment). Positive values show upstream movement, negative downstream.

Fig. 5. Cumulative proportion of round gobies dispersing up-(red area) and downstream (blue area) of the release point (0) within 30 days ( Release experiment). Dashed and dotted white lines determine how far 50 % and 75 % of fish dispersed, respectively (calculated separately for up- and downstream dispersers). Points determine the mean distance reached.

34 https://mc06.manuscriptcentral.com/cjfas-pubs Page 35 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Fig. 6. Distance reached from the introduction point as a function of fish size in male (upper panel) and female (lower panel) round gobies ( Release experiment). Full points = upstream dispersal, empty squares = downstream dispersal. In males, the curve predicted by GLM is shown as a solid line and 95% confidence intervals as dashed lines. No such curve is shown for females as the relationship was not significant.

Fig. 7. Distance from the 20m section border in relation to fish size ( Colonisation experiment). The curve predicted by GLMM is depicted by a solid line and 95% confidence intervals as dashed lines.

Draft

35 https://mc06.manuscriptcentral.com/cjfas-pubs " Page 36 of 42 !

Draft https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences

฀฀ Draft https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences

฀฀ Page 37 of 42 Canadian Journal of Fisheries and Aquatic Sciences Page 38 of 42

Draft

https://mc06.manuscriptcentral.com/cjfas-pubs Page 39 of 42 Canadian Journal of Fisheries and Aquatic Sciences

Draft

https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 40 of 42

฀฀ Draft

฀฀

https://mc06.manuscriptcentral.com/cjfas-pubs Page 41 of 42 Canadian Journal of Fisheries and Aquatic Sciences

฀฀ Draft

฀฀

https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 42 of 42

Draft

https://mc06.manuscriptcentral.com/cjfas-pubs Publikace B

Expansion of round gobies in a non-navigable river system

Šlapanský, L., Janáč, M., Roche, K., Mikl, L. & Jurajda, P. (2017)

Limnologica, 67, 27-36

Limnologica 67 (2017) 27–36

Contents lists available at ScienceDirect

Limnologica

journal homepage: www.elsevier.com/locate/limno

Expansion of round gobies in a non-navigable river system MARK ⁎ Luděk Šlapanskýa,b, , Michal Janáča, Roche Kevina, Mikl Libora,b, Jurajda Pavela a Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, Brno 603 65, Czech Republic b Institute of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 246/2, 611 37, Brno, Czech Republic

ARTICLE INFO ABSTRACT

Keywords: A number of Ponto-Caspian Gobiid species have greatly increased their geographical ranges over recent decades. Impact Most expansion studies to date, however, have focused on navigable waterways. In this study, we present a Invasive species summary of six-years (2008–2013) monitoring of round goby Neogobius melanostomus expansion along two Neogobius melanostomus connected non-navigable rivers. Contiguous range expansion was observed in both rivers, with dispersal rate Pioneer fish ranging from 1.2 to 3.2 km/year. Gobies at newly invaded sites ranged from 20 to 117 mm, with both juveniles Population characteristics and adult fish observed. Though the data did not allow us to see any consistent pattern in the first years after Proterorhinus semilunaris detection, there was some evidence for a shift to a female-biased, juvenile-dominated population over time. While the abundance of non-native tubenose goby Proterorhinus semilunaris appeared to be negatively influenced by round goby establishment, diversity of nearshore native fish showed no evidence of dramatic decline attributable to round goby.

1. Introduction gobies in an area immediately adjacent to (and partially overlapping with) the navigated section of the upper Danube, and Zarev et al. Several Ponto-Caspian gobiid species have greatly increased their (2013), who documented round gobies 100 km upstream along non- ranges over recent decades (see Roche et al., 2013 for a review). Of navigable tributaries of the Danube in the species’ native range (Bul- these, the most successful has been the round goby Neogobius mela- garia), though the authors provided no information on the rate of nostomus, which has now spread throughout several major European movement. river basins, including the Rhine (Borcherding et al., 2011) and Danube Those studies that have examined expansion along non-navigable (spreading beyond their original range; Jurajda et al., 2005; Wiesner, tributaries (USA or Europe) have noted considerable variation in the 2005; Paintner and Seifert, 2006). In addition, round gobies have been results. Speed of expansion, for example, was recorded at 0.5 km per introduced into the Laurentian Great Lakes Basin of North America and year by Bronnenhuber et al. (2011) but at 17 km per year by Brandner have gone on to colonise a number of major rivers and streams et al. (2013b). There is also disagreement over the character of ‘pioneer’ (Marsden and Jude, 1995). fish found at the invasion front, with some studies reporting larger While this range expansion has been the subject of numerous studies individuals (Gutowsky and Fox, 2011; Brandner et al., 2013b) and in recent years, most have described expansion along navigable rivers others suggesting that the driving force behind the invasion process are and canals, presumably as transport in and on shipping is considered smaller (mainly male) fish that are forced into new areas through the main vector for long-range, ‘leap-frog’ dispersal (e.g. see Ahnelt competition with larger individuals (Ray and Corkum, 2001; et al., 1998; Wiesner, 2005; Gutowsky and Fox, 2011; Cammaerts et al., Brownscombe and Fox, 2012; Masson et al., 2016). 2012; Roche et al., 2013). To date, relatively little has been written on On top of this, relatively little is known about how non-native go- ‘natural’ expansion (i.e. continuous range expansion by swimming bies affect fish assemblages in rivers, despite this being one of the major alone) into and along non-navigable rivers and streams. Furthermore, concerns of gobiid invasion (Janssen and Jude, 2001; French and Jude, most existing studies have concentrated on round goby occurrence in 2001; Balshine et al., 2005). Experimental studies suggest that round tributaries of the Great Lakes (Phillips et al., 2003; Krakowiak and goby should have a negative impact on native fish assemblages via Pennuto, 2008; Bronnenhuber et al., 2011; Brownscombe and Fox, competition for shelter and food, spawning interference and predation 2012). To the best of our knowledge, just two studies have examined on eggs and juveniles (e.g. Steinhart et al., 2004; Balshine et al., 2005; natural dispersal of round goby in non-navigable European tributaries, Bergstrom and Mensinger, 2009), with benthic species utilising similar that of Brandner et al. (2013b), who reported rapid spread of round niches considered the most vulnerable (Van Kessel et al., 2011). This

⁎ Corresponding author at: Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, Brno 603 65, Czech Republic. E-mail address: [email protected] (L. Šlapanský). http://dx.doi.org/10.1016/j.limno.2017.09.001 Received 21 March 2017; Received in revised form 1 August 2017; Accepted 5 September 2017 Available online 14 October 2017 0075-9511/ © 2017 Elsevier GmbH. All rights reserved. Š L. lapanský et al. Limnologica 67 (2017) 27–36 includes not only native cottids (Verreycken, 2015) but also other non- Republic (Fig. 1). Both the Morava, a main tributary of the Danube, and native gobiids. Valová et al. (2015), for example, suggested that tube- the Dyje, the Morava’s most important tributary, are non-navigable nose goby Proterorhinus semilunaris, another, smaller Ponto-Caspian throughout (with the exception of occasional recreational canoes). The invader with a similar distribution to round goby, should prove an in- study covers a 44 km stretch of the Morava starting from the Czech ferior competitor. Studies that have actually set out to determine im- border (70 km from its confluence with the Danube) and a 42 km pact at the population/assemblage level in the field are even rarer, with stretch of the Dyje, starting from its confluence with the Morava only three assessing round goby impact in rivers (Kornis et al., 2013; (Fig. 1). Janáč et al., 2016; Van Kessel et al., 2016). While studies from the Great Between 1968 and 1982, both rivers were channelised and their Lakes have tended to document immediate and profound impacts on riverbanks stabilised with rip-rap, that on the Morava generally larger demersal fish communities following introduction of round goby (e.g. (30–80 cm max. diameter) than on the Dyje (15–25 cm; though stones Janssen and Jude, 2001; Lauer et al., 2004), such an impact has only of 40–60 cm are found at some locations). Channel width on the been observed in one (Van Kessel et al., 2016) of the three riverine Morava varies between 40 and 60 m and depth ranges between 0.8 and studies thus far undertaken. 1.0 m. The Dyje is slightly narrower at 30–50 m, with depth similar at Clearly, more studies are needed before population patterns pre- between 0.5 and 1.0 m. Annual mean discharge near the confluence is − − valent at the goby invasion front can be generalised and actual impacts 61.1 m3 s 1 for the Morava and 41.7 m3 s 1 for the Dyje (Czech on native fish communities identified, both essential for the future Hydrometeorological institute; http://portal.chmi.cz). Current speed − − management of this invasive species. In this paper, we present long- along the banks rarely reaches 0.2 m s 1 on the Morava and 0.4 m s 1 term data on the expansion of round goby along two connected non- on the Dyje. The bottom substrate of both rivers comprises sand, gravel navigable European rivers. In doing so, we a) estimate speed of colo- and pebbles with patches of silt. Aquatic vegetation, woody debris, nisation, b) describe population structure characteristics (body size, pools and riffles occur rarely. sex-ratio, proportion of juveniles) at first occurrence (along with any Prior to round goby invasion, both rivers supported a relatively changes over the years following first occurrence), and c) assess pos- diverse fish assemblage (Valová et al., 2006) dominated by native cy- sible impacts on the assemblage of fish captured in the nearshore rip- prinid species (e.g. roach Rutilus rutilus; chub Leuciscus cephalus; rap zone over time. common bream Abramis brama; barbel Barbus barbus; bleak Alburnus alburnus; European bitterling Rhodeus amarus and white-finned gud- ň 2. Material and methods geon Romanogobio albipinatus (Jurajda and Pe áz, 1994), along with a stable population of non-native tubenose goby Proterorhinus semilunaris, 2.1. Study area which quickly became established after its introduction in the 1990s (Janáč et al., 2012). This study took place on the Rivers Morava and Dyje in the Czech Round goby have been recorded in the middle Danube since 2000

Fig. 1. The Rivers Morava and Dyje, with the study sites indicated. In the brackets are listed ﬁrst records of the round goby. Please check Table 1 for precise location of the sites.

28 Š L. lapanský et al. Limnologica 67 (2017) 27–36

Table 1 River kilometre and GPS coordinates for sampling sites on the Rivers Dyje and Morava. Dyje: DD = distance from Danube; Morava: River km = distance from Danube. Aﬃliation to primary (P, colonized in 2008), secondary (S, colonized later) or unanalysed (N; without round goby) sites provided for each site.

Dyje GPS Morava GPS

Locality River km DD N E Locality River km N E

D1 (P) 4.9 74.9 48.6412869 16.9268337 M1 (P) 73 48.6355256 16.9626603 D2 (P) 11.7 81.7 48.6914906 16.9170981 M2 (S) 74.3 48.6477614 16.9694194 D3 (P) 19 89 48.7340610 16.8849114 M3 (S) 78.7 48.6807642 16.9786092 D4 (S) 28 98 48.8277258 16.8594947 M4 (N) 85.7 48.7335697 17.0192761 D5 (S) 36 106 48.8277258 16.7731198 M5 (N) 93 48.7813386 17.0753558 D6 (N) 42.1 116 48.8572831 16.7245047

(see Roche et al., 2013). The first individuals caught in the Morava shoreline (typically 200 m). The sampling effort in this study corre- (Slovakia-Austria stretch; see Fig. 1) were found at several localities up sponds roughly with that of previous studies on gobiid impact on riv- to 19 km upstream of the confluence in 2006 (Lusk et al., 2008), with erine fish communities (Kornis et al., 2013; Van Kessel et al., 2016). As the first specimens in the Czech stretch being caught in 2008 below a sampling did not cover the whole width of the river, we only consider weir at rkm 74.3 (Lusk et al., 2008; Fig. 1). In the same year, examples the fish assemblage captured along the rip-rap in our analysis of pos- were also recorded at rkm 13.8 on the Dyje and below a weir near the sible gobiid impact. town of Břeclav at rkm 22.3 (Lusk et al., 2008; Fig. 1). All fish captured were identified to species and measured to the nearest millimetre (standard length, SL) on the bankside. Non-gobiid species were released to the water after noting the numbers caught. 2.2. Data collection Goby sex was determined through examination of the urogenital papillae (Kornis et al., 2012). Fish with a SL < 40 mm, or those with a SL The Institute of Vertebrate Biology, Czech Academy of Sciences, has of 40–55 mm whose sex could otherwise not be determined, were re- fi monitored the progress of this round goby invasion since the rst record corded as juveniles. All gobiid fish were then overdosed with clove oil in 2008. Sampling takes place each autumn when water discharge is and fixed in 4% formaldehyde for later analysis in the laboratory. Fish fi more stable, sh are easily sampled and are old enough to be easily abundance was estimated using catch per unit effort (CPUE), measured fi identi ed. as individuals captured per metre of shoreline (per 100 m in Tables 2 fl Five sampling sites were initially established near the con uence of and 3). the Dyje (D1, D2, D3) and Morava (M1, M2) in 2008 (Table 1, Fig. 1), with sites D1, D2 and M1 below the round goby invasion front and sites D3 and M2 approximately at the invasion front itself (note that, while 2.3. Statistical analysis round gobies had been caught at M2 in early 2008, no further gobies were caught there until 2011. For this reason, only D1, D2, D3 and M1 As gobies were already present at the four initial sites (D1, D2, D3, are treated as ‘initial’ monitoring sites in the analysis). From 2009, M1) in 2008, and as irregular sampling at these sites before 2008 failed sampling was extended with three further ‘secondary’ sites along the to detect round goby, all sites were probably settled in the same year, Dyje (D3-D6; Fig. 1) in order to allow repeated sampling of the fish i.e. 2008; hence, data from these four sites were pooled in order to community at sites at and above the invasion front. Following the re- better describe body size, sex-ratio and proportion of juveniles for each appearance of gobies at site M2 in 2011, three secondary upstream sites year after goby detection. were also added to allow repeat sampling of the fish assemblage (M3- The G-test was used to test for deviation of sex-ratio from parity in M5; Fig. 1). each year (exact binomial tests were used when expected frequencies Sampling always took place during the day (10:00-16:00) in autumn were lower than five). Sex-ratio was expressed as number of females per (from 20 October to 24 November). Conditions at the sampling sites male. Although our original aim was to statistically test for differences remained relatively stable at each site between years, i.e. river dis- in fish-size, proportion of juveniles and proportion of females between − charge (maximum inter-annual divergence 11 m3 s 1) and mesohabitat years, we restricted ourselves to a simple description of any observable (substrate, vegetation cover) changed little, leaving little room for patterns as the sample sizes in the first years of invasion were too small inter-annual changes in fish assemblage attributable to habitat change. (even when pooled across the initial sites) to provide more than in- Fish were sampled by electrofishing using a portable backpack unit dications. Due to the relatively low abundance and high turnover of (SEN f. Bednář, Czech Republic; maximum output 225/300 V, fre- native species (see Results), we restricted our analysis of impact on the quency 75–85 Hz) fitted with an small elliptical stainless-steel anode fish assemblage to a) abundance (log-transformed) of tubenose goby (25 × 15 cm) with 4 mm mesh netting (Janáč et al., 2016). Based on (the only species showing a suitably high abundance) and the native our own long-term experience, electrofishing by slow wading upstream fish pool, and b) native fish diversity indices (species richness, Shannon along the bank has proved to be the most effective method for catching index, Simpson index, evenness). Effects on these response variables all age-classes of all fish inhabiting the littoral rip-rap. Electrofishing of were tested using linear mixed models (LMM), with site as a random the nearshore zone is a reliable and commonly used method for sam- effect and measurements of round goby population status as fixed pling not only round goby assemblages (Brandner et al., 2013a) but also predictors. Three possible measurements of round goby population for describing riverine fish communities in general (Fame Consortium, status were considered: a) simple abundance, b) abundance in the 2004). Indeed, electrofishing was the method used in all three studies previous year (controlling for a possible time-lag in round goby effect) thus far published documenting round goby impact on native fish in and c) phase of round goby establishment (categorical predictor with rivers (i.e. Kornis et al., 2013; Van Kessel et al., 2016; Janáč et al., two levels: ‘non-established’, which merged years with no round goby 2016). and the first years after occurrence with few size classes present and − As the rivers are relatively shallow, we were able to sample the relatively low goby density [ < 6 inds.100 m 1]; and ‘established’, whole nearshore water column up to a distance of 2–4 m from the bank, which included years with many size-classes present and a relatively − depending on slope, thus covering almost the whole rip-rap zone in this high goby density [ > 25 inds. 100 m 1]). As fish assemblage structure stretch of river. Each sample site consisted of 100–400 m of rip-rap could also have been affected by environmental conditions in previous

29 Š L. lapanský et al. Limnologica 67 (2017) 27–36 years (e.g. strong cohorts may arise from years with suitable environ- 3.4. Body size mental conditions), we controlled for the possible effect of calendar year by including calendar year as a fixed covariate (treated as a ca- Round gobies captured at the initial sites in 2008 were generally tegorical factor). larger than those captured in subsequent years (Fig. 2A; note, however, the low sample size), with some fish being amongst the largest gobies 3. Results ever captured at some sites (M1, D1, D2; Fig. 3). This held true (though less strongly) even after juvenile fish had been discounted (Fig. 2B). 3.1. Assemblage of fish captured along the rip-rap Length-frequency distribution at the initial sites appeared to stabilise, with clearly separated size categories apparent from 2010 on (Fig. 3). In fi fi We caught 12 140 fish during the study (6 342 tubenose goby; 1 719 contrast to the initial sites, the rst sh colonising secondary sites were round goby and 4 079 other), comprising 31 species (29 on the Dyje, 27 mostly smaller individuals, including juveniles (Fig. 4). on the Morava; Supplementary Tables S1 and S2). The fish assemblage along the rip-rap zone of both rivers was relatively similar 3.5. Sex ratio (Supplementary Tables S1 and S2). Tubenose goby was the most fi common species on both the Morava and Dyje, representing between 10 During the early phase of invasion, the low numbers of sh caught ffi and 94% of all fish caught each year (Supplementary Tables S1 and S2). were insu cient to state whether there was a clear trend in sex ratio at fi Perch (Perca fluviatilis), burbot (Lota lota), roach and chub were the the initial sites, despite a signi cant female-dominated ratio in 2010 most common native species in the Dyje, and European bitterling, (1:8; G-test, P < 0.05; Table 2). While the sex ratio remained close to white-fine gudgeon, barbel, chub and perch in the Morava parity in 2011, there was an increasing trend towards female dom- fi (Supplementary Tables S1 and S2). Within three years of detection, inance from then on, with a signi cant deviation from parity observed round gobies had become common in both rivers, representing between in 2013 (1:1.6; G-test, P < 0.05; Table 2). At the secondary sites, the 14 and 75% of all fish caught. sex ratio was very close to parity almost every year (G-test, all P > 0.05; Table 2). Only at site D4 in 2013 was the sex ratio distinctly female dominated (1:16; G-test, P < 0.001); though again, numbers 3.2. Round goby dispersal caught were relatively low (Table 2). fi The rst round gobies caught along the Czech stretch of the Morava 3.6. Effect on the nearshore fish assemblage were found just below a weir at rkm 74.3 (site M2) in 2008 (Lusk et al., 2008). Our own sampling in 2008 recorded only two individuals at site Round goby invasion appears to have had no significant effect on M1 (rkm 73, Fig. 1), however, and no round gobies at M2 until 2011, diversity or pooled abundance of the assemblage of native fish captured despite regular sampling. In 2011, the invasion front moved a further along the nearshore rip-rap zone (LMM, all P > 0.05; Table 3). On the 4.4 km upstream to site M3 (Fig. 1) and several specimens were re- other hand, there was a significant decline in tubenose goby abundance corded just under a weir at rkm 79.5 in 2012, approximately 1 km following round goby establishment (LMM, P < 0.05; Table 3), though upstream of site M3 (Jurajda, unpublished data). No further occurrence with no direct correlation between abundance of the two species (LMM, of gobies has been recorded upstream of this apparent migration barrier P > 0.05; Table 3). An apparent decline in tubenose goby abundance fi – since then. During this ve-year period (2008 2013), round gobies following a sudden increase in round goby density is particularly visible colonised 5.8 km of the Morava, representing an average of 1.2 km at sites D1, D2, D3 and D5, with a weaker or no response visible at other upstream expansion per year. In doing so, the gobies overcame two sites (Fig. 5). migration barriers, the first a 1.5 m ogee-type weir (rkm 74.3; site M2) fl and the second an inoperable 0.5 m in atable weir (rkm 77.4), neither 4. Discussion of which had fish ladders. fi The rst round gobies on the Dyje were also recorded in 2008 (Lusk In the Czech Republic, we were lucky enough to identify invasive et al., 2008), at rkm 13.8 close to our locality D2 (rkm 11.7) and near gobies entering the country at a very early stage. This has allowed us to ř the town of B eclav, close to our locality D3 (rkm 19; Fig. 1). Our own accumulate long-term data on the expansion of the round goby popu- fi monitoring con rmed round goby presence at two downstream lo- lation along two connected non-navigable rivers. In doing so, we were calities (D1 [rkm 4.9] and D2) later the same year. In 2010, a single able to estimate speed of colonisation and, to some extent, document a fi specimen was captured 9 km upstream of D3 (site D4, rkm 28) and ve range of population structure characteristics (i.e. body size, sex-ratio, specimens were collected 8 km upstream of site D4 in 2012, below a proportion of juveniles) at first occurrence, along with any changes weir near the village of Bulhary (site D5, rkm 36). Round gobies have several years after first occurrence. Furthermore, multi-year sampling not progressed upstream of this point since 2012. Thus, the round goby along the rip-rap provided data with the potential to reveal large det- invasion front moved 12.9 km over four years on the Dyje, representing rimental changes in the native fish assemblage along the nearshore rip- an average movement of 3.2 km per year. During this time they over- rap zone attributable to round goby. came two migration barriers, a 2 m ogee-type weir at rkm 23.1 and a partly submerged broad-crested bottom-sill at rkm 32, both passable by 4.1. Range expansion boulder-ramp fi sh ladders. Round goby expansion up (and down) navigable rivers has been 3.3. Proportion of juveniles rapid and wide-ranging thanks to long-distance transfer of fish via shipping and boat transport (Borcherding et al., 2011; Kalchhauser At the initial sites, lowest numbers of juveniles were recorded et al., 2013; Mombaerts et al., 2014; Roche et al., 2015), subsequently during 2008 (the year round gobies were first detected), though the followed by natural expansion through swimming and downstream proportion was still relatively high at 40% (Table 2; note the relatively drift of juveniles (Janáč et al., 2013b). While studies on the Rhine have low sample size, though). From 2009 on, the proportion of juveniles shown an average expansion rate of around 67 km/year (Manné et al., never dropped below 60%, peaking in 2010 at 93% (Table 2). At the 2013), expansion rates in open waters or lentic systems tend to be secondary sites, the proportion of juveniles in the first year of occur- lower, reaching around 6–10 km/year in the Baltic Sea (Rakauskas rence varied widely, ranging from almost 100% at D4 to just 20% at D5 et al., 2013) and 14 km/year in Lake Michigan, USA (Bergstrom et al., (Table 2). 2008). The few studies to have monitored natural (i.e. swimming only)

30 Š L. lapanský et al. Limnologica 67 (2017) 27–36

Table 2 Proportion of juveniles and sex-ratio at initial sites (pooled) and secondary sites. Sex-ratio values deviating signiﬁcantly from parity are in bold. Sample sizes are in parentheses.

a) Proportion of juveniles

2008 2009 2010 2011 2012 2013

Initial 40% (10) 79% (19) 93% (125) 77% (319) 60% (236) 66% (280) D4 ––––100% (1) –– 99% (82) 63% (46) D5 ––––– – –– 20% (5) 81% (27) M2 ––––– – 48% (31) 0% (1) 54% (11) M3 ––––– – 26% (35) 74% (54) 78% (49)

b) Sex ratio (number of females per male)

2008 2009 2010 2011 2012 2013

Initial NA (1) 3.0 (4) 8.0 (9) 0.9 (74) 1.3 (94) 1.6 (95) D4 –––––––– NA (1) 16.0 (17) D5 –––––––– 1 (4) 4.0 (5) M2 ––––––1.0 (16) NA (1) 4.0 (5) M3 ––––––1.0 (26) 1.3 (14) 1.2 (11)

ladders to facilitate movement of native fish species (Klíma, 2009). Indeed, the first occurrence of round goby in the Czech Republic was documented from one of these fish ladders (Lusk et al., 2008). In contrast, weirs on the Morava have not been equipped with any form of fish bypass. Despite this, the weirs only appear to have delayed migration (see Bronnenhuber et al., 2011), suggesting that round gobies are capable of bypassing such obstructions under favourable conditions (e.g. increased water level). Tierney et al. (2011) were able to demonstrate that round gobies were surprisingly good swimmers, despite their benthic adaptations, utilising a form of ‘burst-and-hold’ swimming − (startle bursts of up to 163 cm s 1 recorded), which would also help them overcome barriers. In the absence of such barriers, expansion rate is likely to have been much faster. Brandner et al. (2013b), for example, noted a rate of 17 km/year in a stretch without barriers (comparable to rates for lentic, open-water habitats), almost certainly by natural movement alone. Even higher rates can be assumed for movement along the barrier-free stretch between the uppermost known occurrence along the Morava in 2006 (rkm 19) and the Morava-Dyje confluence (rkm 70), which took just two years (a total of 51 km, or 25.5 km per year). The addition of 4 km up the Morava and 20 km up the Dyje (this study; Lusk et al., 2008) results in a rate of 27.5 and 31.5 km/year, respectively. In both cases, gobies upstream dispersal have stopped (for that time) under the first weir. Hence, round gobies certainly have the Fig. 2. Fish size (standard length in mm) at initial sites, calculated (A) for the whole potential for rapid natural upstream migration, with weirs slowing the population and (B) for non-juvenile fish only. Solid bar = median, Box = quartiles, pace of upstream expansion but not necessarily preventing it (see also Whiskers = non-outlier range (1.5 * quartiles), point = outlier. Bronnenhuber et al., 2011). We are convinced, based on our results and experience, that the upstream migration have recorded much lower rates, typically ranging ‘natural’ round goby expansion process is a combination of two com- from 0.5 km to 5 km/year (Bergstrom et al., 2008; Bronnenhuber et al., ponents, i.e. rapid movement by pioneers from the source population 2011; Brownscombe and Fox, 2012). Our results fit into this latter over a relatively long distance, followed by a slow filling of the gap range, with an average progress of 3.2 km/year on the Dyje and between the source and ‘invasion front’ sub-populations. The invasion 1.2 km/year on the Morava. It should be noted, however, that all these front comprises just a small number of pioneers exhibiting high levels of studies, including our own, have estimated upstream dispersion rates movement activity compared to the rest of the population (Lynch and using data based on first recording only, i.e. not through direct ob- Mensinger, 2012; Masson et al., 2016). Indeed, Myles-Gonzales et al. servation of tagged fish movements, for example. As such, none of these (2015) demonstrated that individuals predisposed to behaviours asso- studies can exclude the possibility that the observed dispersion rate was ciated with dispersal, such as high levels of exploration activity, are facilitated, or even ensured, through anthropogenic means, e.g. through more likely to be located along an invasion front. Brownscombe and transfer in angler’s bait buckets. On the other hand, the order in which Fox (2012) suggested that these pioneers tend to disperse into high gobies passed the inter-weir sections in our study (never moving further quality habitats during the initial stages of invasion. This was confirmed than the next upstream section on each occasion) decreases the prob- by our data from locality D5 (unpublished). Here, round gobies were ability of human-mediated transfer, suggesting natural migration as a first recorded over a relatively short stretch of rip-rap comprising rocks more probable option. 40–60 cm in diameter (our past experience suggests that this size tends Differences in the rate of expansion between rivers could be attri- to be preferred by round goby), while an 8 km stretch downstream butable to the type and number of migration barriers along their length. consisting of 10–20 cm rip-rap combined with gravel beaches and In our own case, weirs on the Dyje almost all have baffle or bypass fish eroded banks remained uncolonised (L. Šlapanský, unpublished data).

31 Š L. lapanský et al. Limnologica 67 (2017) 27–36

Fig. 3. Size distribution (frequency of occurrence in 5 mm size classes; standard length) of round goby from the initial sites on the Rivers Dyje (D1–3) and Morava (M1).

Fig. 4. Size distribution (frequency of occurrence in 5 mm size classes; standard length) of round goby from secondary sites on the Rivers Dyje (D4–5) and Morava (M2–3).

32 Š L. lapanský et al. Limnologica 67 (2017) 27–36

Table 3 The gap between pioneers at the invasion front and the source popu- Results for linear mixed models predicting the effect of round goby abundance on the lation is then filled via a) downstream drift of early life stages (Janáč abundance or diversity of native species and non-native tubenose goby. For each model, et al., 2013a,2013) originating from the ‘invasion front’ sub-population, significance of round goby-related predictors (P values) and degrees of freedom are shown. Significant P values (P < 0.05) are in bold. and/or b) slow upstream movement of (presumably) juveniles from the source sub-population. The combination of these phenomena will lead Response variable/ Abundance Abundance Establishment phase to stratified dispersal and an increasing rate of expansion into new areas Predictor previous year (Bronnenhuber et al., 2011). Degrees of freedom 1,26 1,20 1,26

Native species richness 0.613 0.543 0.305 Native species Shannon 0.298 0.591 0.515 4.2. Population characteristics diversity Native species Simpson 0.409 0.496 0.901 In our study, round gobies tended to be either relatively small diversity (< 50 mm, mostly corresponding to 0+ fish) when first detected at a Native species Shannon 0.437 0.549 0.336 site, or relatively large (> 90 mm, mostly corresponding to fish 2+ and evenness Native species pooled 0.415 0.956 0.833 older). Both cases have been documented in the literature. Ray and abundance Corkum (2001), for example, reported a high proportion of small fish in Tubenose goby 0.625 0.208 0.010 the earliest years of colonisation, attributing this to displacement from abundance optimal habitats through competition, smaller individuals tending not to interact aggressively but move to another area when their opponent is slightly larger (Groen et al., 2012). Both Ray and Corkum (2001) and Johnson et al. (2005b) reported juveniles as the most mobile members

Fig. 5. Catch per unit eﬀort for round goby (black bars), tubenose goby (grey bars) and native ﬁsh (white bars) for each site on the Rivers Dyje (D1-D6) and Morava (M1-M5). X = unsampled year.

33 Š L. lapanský et al. Limnologica 67 (2017) 27–36 of round goby populations, with larger individuals (> 50 mm TL) indicated no such dramatic impacts. moving outside of small home ranges only rarely (Lynch and Previous studies along the Morava and Dyje, at sites similar to ours, Mensinger, 2012). Several other studies, however, have recorded large have also demonstrated i) a lack of any round goby impact on native individuals during the initial phase of invasion; hence, their role as fish young-of-the-year abundance or habitat use (Janáč et al., 2016), pioneers cannot be ruled out (Gutowsky and Fox, 2011; Brownscombe and ii) no sign of gobiid predation on native fish eggs or juveniles and Fox, 2012; Brandner et al., 2013b). Myles-Gonzales et al. (2015), (Vašek et al., 2014; Všetičková et al.,2014). This, in combination with for example, noted that a propensity for explorative behaviour in in- our own data, tends to support a growing consensus that the con- vasion-front gobies was independent of body size, sex or age. sequences of invasion in rivers such as the Dyje and Morava differ from Overall, it is almost impossible to demonstrate empirically which those reported for the Great Lakes. In the Great Lakes (but not in their fish are the invasion pioneers as the low numbers of fish at the invasion tributaries, see Kornis et al., 2013), round goby have been shown to front lowers the probability of timely detection (Clapp et al., 2001). It is have a strong negative effect on some native fish species, especially possible, for example, that the invasion pioneers are always large in- benthic fish such as cottids (Janssen and Jude, 2001; Lauer et al., dividuals, but their numbers are too low for early detection (Veléz- 2004). Such species are absent along the lower Morava and Dyje, for Espino et al., 2010), meaning they are missed during early surveys and example, and other native benthic species are relatively rare and tend to first detection follows only after a lag of a year or more. In this case, the be found in different habitats than round goby (Janáč et al., 2016). first individuals caught may be the progeny of the first large pioneers, The only documented impact by round goby in a European riverine juveniles being naturally dominant at the invasion front. system to date was indeed demonstrated on a cottid, Cottus perifretum A number of authors have also found contradictory results for sex from the River Meuse (Van Kessel et al., 2016). In contrast, our own ratio. Studies in the Great Lakes, for example, have recorded male- unpublished data suggests that another common cottid, the European biased populations in both the core (source) area (Corkum et al., 2004; bullhead (Cottus gobio), can form viable populations on the Danube, Young et al., 2010; Thompson and Simon, 2015) and at the invasion even in the presence of invasive gobiids. Notably, Piria et al. (2016) front (Gutowsky and Fox, 2011), which would be consistent with males recorded some correlations between the abundance of round goby and tending to be the more mobile sex (Marentette et al., 2011). On the two native benthic species, zingel (Zingel zingel) and the Balkan spined other hand, other studies (Brownscombe and Fox, 2012; Brandner et al., loach (Sabanejewia balcanica). Clearly, therefore, while the round goby 2013b) have recorded a female-dominated population at the invasion has the potential to affect native benthic fish assemblages (e.g. through front. Our samples showed no sex-bias in invasion front, with relatively competition for diet or shelter; Van Kessel et al., 2011; Piria et al., 2016; large variability among sites. It is possible that the differences in sex- Števove and Kováč, 2016), things are not so straightforward, suggesting ratio are a reflection of the time (season) of sampling, with studies that local conditions may play a stronger role than once thought in undertaken in autumn, when highest movement activity might be ex- determining whether such potential impacts are realised. pected (Thompson and Simon, 2015), for example, showing fewer It is conceivable that our system may have been previously im- males due to increased mortality after spawning, as observed in the pacted by tubenose goby, which colonised our sites ten years before the Black Sea (Miller, 1986). It is also possible that different sampling arrival of round goby. As no such effect has ever been reported else- methods result in a sex bias in the catch (Clapp et al., 2001; Jurajda where (e.g. Van Kessel et al., 2016), however, we consider this highly et al., 2013). Alternatively, differences in sex ratio at the invasion front improbable. Instead, we suggest that round goby in these rivers are not could simply be the result of high levels of variation. We suggest that outcompeting native fish but are, in effect, utilising a “vacant niche” any future studies should concentrate on exactly which factors result in (Janáč et al., 2016). River channelisation along the Morava and Dyje male or female-biased sex ratios at the invasion front. resulted in both rivers being straightened and the banks strengthened with rip-rap. While such a habitat alteration apparently provided a sub- 4.3. Effect on the nearshore fish assemblage optimal habitat for most native species (Wolter, 2001), rip-rap appears to provide optimal habitat conditions for round and tubenose goby (Ray Although round goby have quickly dominated the nearshore fish and Corkum, 2001; Erős et al., 2005; Young et al., 2010). assemblage (Supplementary Table S2), our data suggest no detrimental In contrast to native fish, round gobies do appear to have had an at effect of round goby on native nearshore fish assemblage diversity or least partial effect on tubenose goby abundance. The relatively small pooled abundance. However, this does not necessarily mean that there tubenose goby is an inferior competitor to round goby and is expected was no detrimental effect on the overall fish assemblage. As we sampled to decrease in abundance at sites with other gobiid species (Valová only the rip-rap zone (2–4 m from the bank), fish concentrating in the et al., 2015), as appears to have been the case at some of our sites. main channel (typically bleak, asp Aspius aspius (Linnaeus) and large Round and tubenose goby habitat and dietary requirements overlap to a specimens of barbel, common bream and nase Chondrostoma nasus large extent (Pettit-Wade et al., 2015; Janáč et al., 2016) and it is quite (Linnaeus); Adámek et al., 2013) were not effectively sampled. On the possible that some resources were restricted to the extent that direct other hand, round goby in the Morava and Dyje avoid the clean flat competition occurred between the two species, resulting in tubenose gravel and sandy bottom of the main channel (Jurajda, unpublished goby being outcompeted. Such cases of out-competition between two data). As goby occurrence is restricted almost exclusively to the near- invasive species are only rarely reported (e.g. Braks et al., 2004). shore rip-rap zone, any direct impact is likely to manifest itself on those We should stress here that there was no direct negative correlation species residing mainly along the banks, i.e. those residing the habitat between abundance of round and tubenose goby and that we only ob- we sampled (e.g. tubenose goby, chub, perch or burbot). served differences in tubenose goby abundance between periods prior Given the relatively low density of native fish species along the to and after establishment of round goby (Fig. 5). Furthermore, the nearshore zone, even before round goby invasion (Adámek et al., 2013; impact on tubenose goby appeared to vary between sites, probably as a this study), sampling effort may have been too low to provide data result of site-specific environmental conditions such as resource rich- robust enough for assessing direct effects of invasion. While we are ness or local fish assemblage. Such small-scale differences in the degree aware of such a limitation, we are also convinced that our sampling of impact of an invasive species are rarely considered and we suggest design (multiple years at multiple sites) would have revealed the dra- further studies on ecosystem-specific impacts could prove useful for matic impacts (i.e. complete failure of reproduction or abundance de- improving predictions of invasive species impact generally. crease in orders of magnitude) reported elsewhere (e.g. Janssen and It should also be noted that, while our paper provides a view on Jude, 2001; Lauer et al., 2004; Van Kessel et al., 2016). Though we did direct impact on the nearshore native fish assemblage, round goby also not statistically test for effects on particular species, a simple visual have the potential to affect aquatic ecosystems through other direct or check of nearshore native fish abundance (Supplementary Table S2) indirect routes. These may, for example, include a negative impact on

34 Š L. lapanský et al. Limnologica 67 (2017) 27–36 the invertebrate assemblage (Lederer et al., 2008; Mikl et al., 2017), Neogobius melanostomus, in Great Lakes tributaries. Mol. Ecol. 20 (9), 1845–1859. http://dx.doi.org/10.1111/j.1365-294X.2011.05030.x. altering trophic pathways (Rush et al., 2012), pollution recycling Brownscombe, J.W., Fox, M.J., 2012. Range expansion dynamics of the invasive round (Johnson et al., 2005a; Kornis et al., 2012; Polačik et al., 2015)or goby (Neogobius melanostomus) in a river system. Aquat. Ecol. 46 (2), 175–189. parasite spillback/dilution (Poos et al., 2010; Ondračková et al., 2015; http://dx.doi.org/10.1007/s10452-012-9390-3. Š Cammaerts, R., Spikmans, F., van Kessel, N., Verreycken, H., Chérot, F., Demol, T., lapanský et al., 2016). Richez, S., 2012. Colonization of the Border Meuse area (The Netherlands and The spreading of round goby into non-navigable rivers represents a Belgium) by the non-native western tubenose goby Proterorhinus semilunaris (Heckel, secondary phase in the range expansion that has been ongoing in 1837) (Teleostei, Gobiidae). Aquat. Invasions 7 (2), 251–258. http://dx.doi.org/10. Europe and the US for a number of decades now. To date, population 3391/ai.2012.7.2.011. Clapp, D.F., Schneeberger, P.J., Jude, D.J., Madison, G., Pistis, C., 2001. Monitoring characteristics of invasive populations have shown high variation, round goby (Neogobius melanostomus) population expansion in eastern and northern probably connected with low numbers and specific environmental Lake Michigan. J. Great Lakes Res. 27 (3), 335–341. http://dx.doi.org/10.1016/ conditions found in individual streams and sites within them. As a re- S0380-1330(01)70649-1. ffi fi fi Corkum, L.D., Sapota, M.R., Skora, K.E., 2004. The round goby, Neogobius melanostomus,a sult, it is still proving di cult to clearly de ne any speci c age group, fish invader on both sites of the Atlantic Ocean. Biol. Invasions 6 (2), 173–181. sex or body size of fish in relation to the invasion pioneers. What is http://dx.doi.org/10.1023/B:BINV.0000022136.43502.db. certain, however, is that active movement upstream is neither limited Erős, T., Sevcsik, A., Tóth, B., 2005. Abundance and night-habitat use patterns of Ponto- Caspian gobiid species (Pisces, Gobiidae) in the littoral zone of the River Danube, by an absence of shipping nor necessarily by the presence of migration Hungary. J. Appl. Ichthyol. 21 (4), 350–357. http://dx.doi.org/10.1111/j.1439- obstacles. To date, the consequences of this invasion have only been 0426.2005.00689.x. monitored for a relatively short period and further detailed monitoring FAME CONSORTIUM, 2004. Manual for the application of the European Fish Index − EFI. A fish-based method to assess the ecological status of European rivers in support is still needed in order to determine general population trends and long- of the Water Framework Directive. Version 1.1, January 2005. term impacts on native fish assemblages in non-navigable river systems. French, J.R.P., Jude, D.J., 2001. Diets and diet overlap of nonindigenous gobies and small benthic native fishes co-inhabiting the St. Clair River, Michigan. J . Great Lakes Res. 27 (3), 300–311. http://dx.doi.org/10.1016/S0380-1330(01)70645-4. Acknowledgements Groen, M., Sopinka, N.M., Marentette, J.R., Reddon, A.R., Brownscombe, J.W., Fox, M.G., Marsh-Rollo, S.E., Balshine, S., 2012. Is there a role for aggression in round goby This study was supported by Czech Science Foundation (Grant invasion fronts? Behaviour 149 (7), 685–703. http://dx.doi.org/10.1163/1568539X- Agency of the Czech Republic) Project no. P505/11/1768. We thank Z. 00002998. Gutowsky, L.F.G., Fox, M.J., 2011. Occupation, body size and sex ratio of round goby Jurajdová, G. Konečná, M. Koníčková, M. Mrkvová, M. Pravdová and L. (Neogobius melanostomus) in established and newly invaded areas of an Ontario river. Všetičková for help with fieldwork. We are much indebted to re- Hydrobiologia 671 (1), 27–37. http://dx.doi.org/10.1007/s10750-011-0701-9. č presentatives of the Moravian Angling Union (V. Habán) and the Janá , M., Valová, Z., Jurajda, P., 2012. Range expansion and habitat preferences of non- Ž native 0+ tubenose goby (Proterorhinus semilunaris) in two lowland rivers in the idlochovice Forest Enterprise (J. Netik) for allowing research in their Danube basin. Fund. Appl. Limnol. 181 (1), 73–85. http://dx.doi.org/10.1127/1863- waters and grounds. 9135/2012/0321. Janá č, M., Jurajda, P., Kružíková, L., Roche, K., Prášek, P., 2013a. Reservoir to river passage of age-0+ year fish, indication of the dispersion pathway for a non-native Appendix A. Supplementary data species. J. Fish Biol. 82 (3), 994–1010. http://dx.doi.org/10.1111/jfb.12037. Janáč, M., Šlapanský, L., Valová, Z., Jurajda, P., 2013b. Downstream drift of round goby Supplementary data associated with this article can be found, in the (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their non- native area. Ecol. Freshw. Fish 22 (3), 430–438. http://dx.doi.org/10.1111/eff. online version, at http://dx.doi.org/10.1016/j.limno.2017.09.001. 12037. Janáč, M., Valová, Z., Roche, K., Jurajda, P., 2016. No effect of round goby Neogobius References melanostomus colonisation on young-of-the-year fish density or microhabitat use. Biol. Invasions 18 (8), 2333–2347. http://dx.doi.org/10.1007/s10530-016-1165-7. Janssen, J., Jude, D.J., 2001. Recruitment failure of mottled sculpin Cottus bairdi in Adámek, A., Zahrádková, S., Jurajda, P., Bernardová, I., Jurajdová, Z., Janáč, M., Calumet harbor, southern Lake Michigan, induced by the newly introduced round Němejcová, D., 2013. The response of the benthic macroinvertebrate and fish as- goby Neogobius melanostomus. J. Great Lakes Res. 27 (3), 319–328. http://dx.doi.org/ semblages to human impact along the lower stretch of the rivers Morava and Dyje 10.1016/S0380-1330(01)70647-8. (Danube basin, Czech Republic). Croat. J. Fish. 71, 93–115. http://hrcak.srce.hr/ Johnson, T.B., Bunnell, D.B., Knight, C.T., 2005a. A potential new energy pathway in 108849. central Lake Erie: the round goby connection. J. Great Lakes Res. 31 (2), 238–251. Ahnelt, H., Bănărescu, P., Spolwind, R., Harka, A., Waidbacher, H., 1998. Occurrence and http://dx.doi.org/10.1016/S0380-1330(05)70317-8. distribution of three gobiid species (Pisces: Gobiidae) in the middle and upper Johnson, T.B., Allen, M., Corkum, L.D., Lee, V.A., 2005b. Comparison of methods needed Danube region −example of different dispersal patterns? Biológia (Bratislava) 53 (5), to estimate population size of round gobies (Neogobius melanostomus) in western Lake 661–674. Erie. J. Great Lakes Res. 31 (1), 78–86. http://dx.doi.org/10.1016/S0380-1330(05) Balshine, S., Verma, A., Chant, V., Theysmeyer, T., 2005. Competitive interactions be- 70239-2. tween round gobies and logperch. J. Great Lakes Res. 31 (1), 68–77. http://dx.doi. Jurajda, P., Peňáz, M., 1994. Fish community of the lower regulated stretch of the River org/10.1016/S0380-1330(05)70238-0. Morava, Czech Republic. Folia Zool. 43 (1), 57–64. Bergstrom, M.A., Mensinger, A.F., 2009. Interspecific resource competition between the Jurajda, P., Černý, J., Polačik, M., Valová, Z., Janáč, M., Blažek, R., Ondračková, M., invasive round goby and three native species: logperch, slimy sculpin, and spoonhead 2005. The recent distribution and abundance of non-native Neogobius fishes in the sculpin. Trans. Am. Fish. Soc. 138 (5), 1009–1017. http://dx.doi.org/10.1577/T08- Slovak section of the River Danube. J. Appl. Ichthyol. 21 (4), 319–323. http://dx.doi. 095.1. org/10.1111/j.1439-0426.2005.00688.x. Bergstrom, M.A., Evrard, L.M., Mensinger, A.F., 2008. Distribution, abundance and range Jurajda, P., Všetičková, L., Polačik, M., Vassilev, M., 2013. Can round goby (Neogobius of the round goby, Apollina melanostoma, in the Duluth-Superior Harbor and St. Louis melanostomus) caught by rod and line be used for diet analysis? J. Great Lakes Res. 39 river estuary, 1998–2004. J. Great Lakes Res. 34 (3), 535–543. http://dx.doi.org/10. (1), 182–185. http://dx.doi.org/10.1016/j.jglr.2012.12.002. 3394/0380-1330(2008)34[535:DAAROT]2.0.CO;2. Kalchhauser, I., Mutzner, P., Hirch, P.E., Burkhardt-Holm, P., 2013. Arrival of round goby Borcherding, J., Staas, S., Krüger, S., Ondračková, M., Šlapanský, L., Jurajda, P., 2011. Neogobius melanostomus (Pallas, 1814) and bighead goby Ponticola kessleri (Günther, Non-native Gobiid species in the lower River Rhine (Germany): recent range exten- 1861) in the high Rhine (Switzerland). Bioinvasions Rec. 2 (1), 79–83. http://dx.doi. sions and densities. J. Appl. Ichthyol. 27, 153–155. http://dx.doi.org/10.1111/j. org/10.3391/bir.2013.2.1.14. 1439-0426.2010.01662.x. Klíma, O., 2009. Importance of permeability of migration barriers for fish community in Braks, M.A.H., Honório, N.A., Lounibos, L.P., Lourenço-De-Oliveira, R., Juliano, S.A., the streams. Masaryk University, Faculty of Science, Brno (Bachelor thesis) 48p. 2004. Interspecific competition between two invasive species of container mosqui- Available from https://is.muni.cz/th/222900/prif_b. toes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. Ann. Entomol. Kornis, M.S., Mercado-Silva, N., Vander Zanden, M.J., 2012. Twenty years of invasion: a Soc. Am. 97 (1), 130–139. http://dx.doi.org/10.1603/0013-8746(2004) review of round goby Neogobius melanostomus biology, spread and ecological im- 097[0130:ICBTIS]2.0.CO;2. plications. J. Fish Biol. 80 (2), 235–285. http://dx.doi.org/10.1111/j.1095-8649. Brandner, J., Pander, J., Mueller, M., Cerwenka, A.F., Geist, J., 2013a. Effects of sampling 2011.03157.x. techniques on population assessment of invasive round goby Neogobius melanostomus. Kornis, M.S., Sharma, S., Vander Zanden, M.J., 2013. Invasion success and impact of an J. Fish Biol. 82 (6), 2063–2079. http://dx.doi.org/10.1111/jfb.12137. invasive fish, round goby, in Great Lakes tributaries. Divers. Distrib. 19 (2), 184–198. Brandner, J., Cerwenka, A.F., Schliewen, U.K., Geist, J., 2013b. Bigger is better: char- http://dx.doi.org/10.1111/ddi.12001. acteristics of round gobies forming an invasion front in the Danube River. PLoS One 8 Krakowiak, P.J., Pennuto, C.M., 2008. Fish and macroinvertebrate communities in tri- (9), e73036. http://dx.doi.org/10.1371/journal.pone.0073036. butary streams of eastern Lake Erie with and without round gobies (Neogobius mel- Bronnenhuber, J.E., Dufour, B.A., Higgs, D.M., Heath, D.D., 2011. Dispersal strategies, anostomus, Pallas 1814). J. Great Lakes Res. 34 (4), 675–689. http://dx.doi.org/10. secondary range expansion and invasion genetics of the nonindigenous round goby, 1016/S0380-1330(08)71610-1.

35 Š L. lapanský et al. Limnologica 67 (2017) 27–36

Lauer, T.E., Allen, P.J., McComish, T.S., 2004. Changes in mottled sculpin and Johnny Ray, W.J., Corkum, L.D., 2001. Habitat and site affinity of the round goby. J. Great Lakes Darter trawl catches after the appearance of round gobies in the Indiana Waters of Res. 27 (3), 329–334. http://dx.doi.org/10.1016/S0380-1330(01)70648-X. Lake Michigan. Trans. Am. Fish. Soc. 133 (1), 185–189. http://dx.doi.org/10.1577/ Roche, K.F., Janáč, M., Jurajda, P., 2013. A review of Gobiid expansion along the Danube- T02-123. Rhine corridor −Geopolitical change as a driver for invasion. Knowl. Manage. Aquat. Lederer, A.M., Janssen, J., Reed, T., Wolf, A., 2008. Impacts of the introduced round goby Ecosyst. 411, 01. http://dx.doi.org/10.1051/kmae/2013066. (Apollonia melanostoma) on dreissenids (Dreissena polymorpha and Dreissena bugensis) Roche, K., Janáč, M., Šlapanský, L., Mikl, L., Kopeček, L., Jurajda, P., 2015. A newly and on macroinvertebrate community between 2003 and 2006 in the littoral zone of established round goby (Neogobius melanostomus) population in the upper stretch of Green Bay, Lake Michigan. J. Great Lakes Res. 34 (4), 690–697. http://dx.doi.org/10. the river Elbe. Knowl. Manage. Aquat. Ecosyst. 416, 33. http://dx.doi.org/10.1051/ 1016/s0380-1330(08)71611-3. kmae/2015030. Lusk, S., Vetešník, L., Halačka, K., Lusková, V., Pekárik, V., Tomeček, J., 2008. Round Rush, S.A., Paterson, G., Johnson, T.B., Drouillard, K.G., Haffner, G.D., Hebert, C.E., Arts, goby Neogobius (Apollonia) melanostomus recorded for the first time in the confluence M.T., McGoldrick, D.J., Backus, S.M., Lantry, B.F., Lantry, J.R., Schaner, T., Fisk, area of the Morava and Dyje rivers (Czech Republic). Biodivers. Fish. Czech Republic A.T., 2012. Long-term impacts of invasive species on a native top predator in a large 7, 114–118 (in Czech with English summary). lake system. Freshw. Biol. 57 (11), 2342–2355. http://dx.doi.org/10.1111/fwb. Lynch, M.P., Mensinger, A.F., 2012. Seasonal abundance and movement of the invasive 12014. round goby (Neogobius melanostomus) on rocky substrate in the Duluth-Superior Šlapanský, L., Jurajda, P., Janáč, M., 2016. Early life stages of exotic gobiids as new hosts Harbor of Lake Superior. Ecol. Freshw. Fish 21 (1), 64–74. http://dx.doi.org/10. for unionid glochidia. Freshw. Biol. 61 (6), 979–990. http://dx.doi.org/10.1111/fwb. 1111/j.1600-0633.2011.00524.x. 12761. Manné, S., Poulet, N., Dembski, S., 2013. Colonisation of the Rhine basin by non-native Števove, B., Kováč, V., 2016. Ontogenetic variations in the diet of two invasive gobies, gobiids: an update of the situation in France. Knowl. Manage. Aquat. Ecosyst. 411, Neogobius melanostomus (Pallas, 1814) and Ponticola kessleri (Gunther, 1861), from 02. http://dx.doi.org/10.1051/kmae/2013069. the middle Danube (Slovakia) with notice on their potential impact on benthic in- Marentette, J.R., Wang, G., Tong, S., Sopinka, N.M., Taves, M.D., Koops, M.A., Balshine, vertebrate communities. Sci. Total Environ. 557–558, 510–519. http://dx.doi.org/ S., 2011. Laboratory and field evidence of sex-biased movement in the invasive round 10.1016/j.scitotenv.2016.03.048. goby. Behav. Biol. Sociobiol. 65 (12), 2239–2249. http://dx.doi.org/10.1007/ Steinhart, G.B., Marschall, E.A., Stein, R.A., 2004. Round goby predation on smallmouth s00265-011-1233-z. bass offspring in nest during simulated catch-and-release angling. Trans. Am. Fish. Marsden, J.E., Jude, D.J., 1995. Round Gobies Invade North America. Illinois-Indiana Sea Soc. 133 (1), 121–131. http://dx.doi.org/10.1577/T03-020. Grant College Program Fact Sheet FS-065. Illinois-Indiana Sea Grant College pro- Thompson, H.A., Simon, T.P., 2015. Age and growth of round goby Neogobius melanos- gram, Columbus, OH. tomus associated with depth and habitat in the western basin of Lake Erie. J. Fish Biol. Masson, L., Brownscombe, J.W., Fox, M.G., 2016. Fine scale spatio-temporal life history 86 (2), 558–574. http://dx.doi.org/10.1111/jfb.12576. shifts in an invasive species at its expansion front. Biol. Invasions 18 (3), 775–792. Tierney, K.B., Kasurak, A.V., Ziekinski, B.S., Higgs, D.M., 2011. Swimming performance http://dx.doi.org/10.1007/s10530-015-1047-4. and invasion potential of the round goby. Environ. Biol. Fish. 98, 491–502. http://dx. Mikl, L., Adámek, Z., Všetičková, L., Janáč, M., Roche, K., Šlapanský, L., Jurajda, P., 2017. doi.org/10.1007/s10641-011-9867-2. Response of benthic macroinvertebrate assemblages to round (Neogobius melanos- Všetičková, L., Janáč, M., Vašek, M., Roche, K., Jurajda, P., 2014. Non-native western tomus, Pallas 1814) and tubenose (Proterorhinus semilunaris, Heckel 1837) goby pre- tubenose gobies Proterorhinus semilunaris show distinct site, sex and age-related dation pressure. Hydrobiologia 785 (1), 219–232. http://dx.doi.org/10.1007/ differences in diet. Knowl. Manage. Aquat. Ecosyst. 414, 10. http://dx.doi.org/10. s10750-016-2927-z. 1051/kmae/2014022. Miller, P.J., 1986. Gobiidae. In: Whitehead, P.J.P., Bauchot, M.-L., Hureau, J.-C., Nielsen, Vašek, M., Všetičková, L., Roche, K., Jurajda, P., 2014. Diet of two invading gobiid species J., Tortonese, E. (Eds.), Fishes of the North-eastern Atlantic and the Mediterranean. (Proterorhinus semilunaris and Neogobius melanostomus) during the breeding and UNESCO, Paris, pp. 1019–1085. hatching season: no field evidence of extensive predation on fish eggs and fry. Mombaerts, M., Verreycken, H., Volckaert, F.A.M., Huyse, T., 2014. The invasive round Limnologica 46, 31–36. http://dx.doi.org/10.1016/j.limno.2013.11.003. goby Neogobius melanostomus and tubenose goby Proterorhinus semilunaris: two in- Valová, Z., Jurajda, P., Janáč, M., 2006. Spatial distribution of 0+ juvenile fish in dif- troduction routes into the Belgium. Aquat. Invasions 9 (3), 305–314. ferently modified lowland rivers. Folia Zool. 55 (3), 293–308. Myles-Gonzales, E., Burness, G., Yavno, S., Rooke, A., Fox, M.G., 2015. To boldly go Valová, Z., Konečná, M., Janáč, M., Jurajda, P., 2015. Population and reproductive where no goby has gone before: boldness, dispersal tendency, and metabolism at the characteristics of a non-native western tubenose goby (Proterorhinus semilunaris) invasion front. Behav. Ecol. 26 (4), 1083–1090. http://dx.doi.org/10.1093/beheco/ population unaffected by gobiid competitors. Aquat. Invasions 10 (1), 57–68. http:// arv050. dx.doi.org/10.3391/ai.2015.10.1.06. Ondračková, M., Hudcová, I., Dávidová, M., Adámek, Z., Kašný, M., Jurajda, P., 2015. Van Kessel, N., Dorenboch, M., De Boer, M.R.M., Leuven, R.S.E.W., Van der Velde, G., Non-native gobies facilitate the transmission of Bucephalus polymorphus (Trematoda). 2011. Competition for shelter between four invasive gobiids and two native benthic Parasit. Vectors 8. http://dx.doi.org/10.1186/s13071-015-0999-7. fish species. Curr. Zool. 57 (6), 844–851. http://dx.doi.org/10.1093/czoolo/57.6. Paintner, S., Seifert, K., 2006. First record of the round goby, Neogobius melanostomus 844. (Gobiidae), in the German Danube. Lauterbornia 58, 101–107. Van Kessel, N., Dorenbosch, M., Kranenbarg, J., van der Velde, G., Leuven, R.S.E.W., Pettit-Wade, H., Wellband, K.W., Heath, D.D., Fisk, A.T., 2015. Niche plasticity in in- 2016. Invasive Ponto-Caspian gobies rapidly reduce the abundance of protected na- vasive fishes in the Great Lakes. Biol. Invasions 17, 2565–2580. http://dx.doi.org/10. tive bullhead. Aquat. Invasions 11 (2), 179–188. http://dx.doi.org/10.3391/ai.2016. 1007/s10530-015-0894-3. 11.2.07. Phillips, E.C., Washek, M.E., Hertel, A.W., Niebel, B.M., 2003. The round goby (Neogobius Veléz-Espino, L.A., Koops, M.A., Balshine, S., 2010. Invasion dynamics of round goby melanostomus) in Pennsylvania tributary streams of Lake Erie. J. Great Lakes Res. 29 (Neogobius melanostomus) in Hamilton Harbour, Lake Ontario. Biol. Invasions 12, (1), 34–40. http://dx.doi.org/10.1016/S0380-1330(03)70413-4. 3861–3875. Piria, M., Jakšić, G., Jaklović, I., Treer, T., 2016. Dietary habits of invasive Ponto-Caspian Verreycken, H., 2015. Risk Analysis of the Round Goby, Neogobius Melanostomus, Risk gobies in the Croatian part of the Danube River basin and their potential impact on Analysis Report of Non-native Organisms in Belgium. Rapporten Van Het Instituut benthic fish communities. Sci. Total Environ. 540, 386–395. http://dx.doi.org/10. Voor Natuur- En Bosonderzoek 2013 (INBO.R.2013.42). Instituut voor Natuur- en 1016/j.scitotenv.2015.05.125. Bosonderzoek, Brussels. Polačik, M., Jurajda, P., Blažek, R., Janáč, M., 2015. Carcass feeding as a cryptic foraging Wiesner, C., 2005. New records of non-indigenous gobies (Neogobius sp.) in the Austrian mode in round goby Neogobius mellanostomus. J. Fish Biol. 87 (1), 194–199. http://dx. Danube. J. Appl. Ichthyol. 21 (4), 324–327. http://dx.doi.org/10.1111/j.1439-0426. doi.org/10.1111/jfb.12708. 2005.00681.x. Poos, M., Dextrase, A.J., Schwald, A.N., Ackerman, J.D., 2010. Secondary invasion of the Wolter, C.H., 2001. Conservation of fish species diversity in navigable waterways. Landsc. round goby into high diversity Great Lakes tributaries and species at risk hotspots: Urban Plan. 53, 135–144. http://dx.doi.org/10.1016/S0169-2046(00)00147-X. potential new concerns for endangered freshwater species. Biol. Invasions 12 (5), Young, J.A.M., Marentette, J.R., Gross, C., McDonald, J.I., Verma, A., Marsh-Rollo, S.E., 1268–1284. http://dx.doi.org/10.1007/s10530-009-9545-x. Macdonald, P.D.M., Earn, D.J.D., Balshine, S., 2010. Demography and substrate af- Rakauskas, V., Pūtys Ž, Daynis, J., Lesutienė, J., Ložys, L., Arbač iauskas, K., 2013. finity of the round goby (Neogobius melanostomus) in Hamilton Harbour. J. Great Increasing population of the invader round goby, Neogobius melanostomus Lakes Res. 36 (1), 115–122. http://dx.doi.org/10.1016/j.jglr.2009.11.001. (Actinopterygii: Perciformes: Gobiidae), and its trophic role in the Curonian lagoon, Zarev, V.Y., Apostolou, A.I., Velkov, B.K., Vassilev, M.V., 2013. Review of the distribution se Baltic Sea. Acta ichtyol. Pisc. 43, 95–108. http://dx.doi.org/10.3750/aip2013.43. of the family Gobiidae (Pisces) in the Bulgarian Danube tributaries. Ecol. Balk. 5 (2), 2.02. 81–89.

36 Publikace C

A newly established round goby (Neogobius melanostomus) population in the upper stretch of the river Elbe

Roche, K., Janáč, M., Šlapanský, L., Mikl, L., Kopeček, L., & Jurajda, P. (2015)

Knowledge and Management of Aquatic Ecosystems, 416, 33

Knowledge and Management of Aquatic Ecosystems (2015) 416, 33 Knowledge & c K. Roche et al., published by EDP Sciences , 2015 Management of DOI: 10.1051/kmae/2015030 Aquatic Ecosystems www.kmae-journal.org Journal fully supported by Onema

A newly established round goby ( Neogobius melanostomus ) population in the upper stretch of the river Elbe K. Roche (1), ⋆, M. Janá cˇ (1) , L. Šlapanský (1) , L. Mikl (1) , L. Kope cekˇ (1) , P. Jurajda (1)

Received October 9, 2015 Revised October 22, 2015 Accepted October 26, 2015

ABSTRACT

Key-words: The invasive round goby ( Neogobius melanostomus , Pallas, 1814) has in- Gobiidae, creased its European range dramatically over recent decades, with inter- species national shipping suspected as the main vector. Here, we provide the introduction, ﬁrst population and morphological data for a newly established round non-native goby population in the upper Elbe (Ústí nad Labem, Czech Republic). species, Surveys in 2013 along the same stretch found no evidence of gobies, in- population dicating introduction within the past two years. Analysis of morphological expansion, similarity conﬁrms the most likely source as the recently established pop- ship-mediated ulation in the tidal Elbe near the port of Hamburg. Due to the species’ transport restricted range ( <15 km; with density localised on Ústí nad Labem port), distance from proposed source (600 km; no reports from the interven- ing stretch) and the speed with which this distance was crossed (less than three years), we suggest port-to-port transfer as the most likely vector route. Our data highlight the speed with which this species has been able to colonise most watersheds in Europe via establishment of widely- separated populations through port-to-port transfer and rapid inter-site connection through downstream drift and natural migration.

RÉSUMÉ

La population de gobie à taches noires nouvellement implantée ( Neogobius melanostomus ) dans un bief amont du ﬂeuve Elbe

Mots-clés : Le gobie à taches noires invasif ( Neogobius melanostomus , Pallas, 1814) a aug- Gobiidae, menté son aire de répartition européenne de façon spectaculaire au cours des introduction dernières décennies, le transport maritime international étant soupçonné d’être le d’espèce, principal vecteur. Ici, nous fournissons les premières données populationnelles et espèce morphologiques sur ce gobie à taches noires nouvellement implanté dans l’Elbe non indigène, supérieure (Ústí nad Labem, République tchèque). Des sondages en 2013 le long expansion du même tronçon n’ont trouvé aucune preuve de gobies, impliquant que l’intro- de population, duction date des deux dernières années. L’analyse de similitude morphologique conﬁrme que la source la plus probable de la population récemment établie est dans l’estuaire de l’Elbe près du port de Hambourg. En raison de l’extension

(1) Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Kv etnáˇ 8, 60365, Brno, Czech Republic ⋆ Corresponding author: [email protected]

This is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND ( http://creativecommons.org/licenses/by-nd/4.0/ ),which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modiﬁed material. K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

1 transfert locale restreinte de l’espèce ( <15 km ; avec la densité localisée près du port Ústí par bateau nad Labem), et de la distance de la source proposée (600 km, pas de données sur le tronçon intermédiaire) et la rapidité avec laquelle cette distance a été franchie (moins de trois ans), nous suggérons un transfert de port à port comme vecteur de transport le plus probable. Nos données mettent en évidence la rapidité avec laquelle cette espèce a été capable de coloniser la plupart des bassins hydro- graphiques en Europe par la création de populations largement séparées par le transfert de port à port et la connexion rapide inter-site par la dérive vers l’aval et la migration naturelle.

INTRODUCTION

2 The round goby ( Neogobius melanostomus , Pallas, 1814) is one of a number of Ponto- 3 Caspian Gobiids that have expanded their ranges over recent decades (see review in Roche 4 et al. , 2013 ). A native of the Black, Caspian and Azov Seas and their tributaries (Miller, 2004 ), 5 the species became established in several major European watersheds around the 1990s, 6 including those of the Danube (Jurajda et al. , 2005 ; Painter and Seifert, 2006 ; Wiesner, 2005 ), 7 Rhine (Borcherding et al. , 2011 ; Kalchhauser et al. , 2013 ; Van Beek, 2006 ) and the Vistula and 8 Oder (Grabowska et al. , 2010 ). They have even been introduced into the Laurentian Great 9 Lakes of North America (Jude et al. , 1992 ). It is now generally accepted that initial introduc- 10 tions have been through international shipping at major ports (Wiesner, 2005 ) through acci- 11 dental transport of juveniles/eggs in ballast water or as eggs attached to the ship’s hull (Ahnelt 12 et al. , 1998 ; Hayden and Miner 2009 ), followed by natural spreading from the point(s) of intro- 13 duction (Roche et al. , 2013 ). Movement may also be assisted through introduction by anglers 14 as bait or by transport of eggs/juveniles on equipment (Kornis et al. , 2012 ). In this way, widely 15 separated introduction points have quickly been joined and large stretches of navigable river 16 colonised. This has been supported in many cases by the ubiquitous presence of rip-rap 17 banks, a preferred habitat of this species (Jurajda et al. , 2005 ; Ray and Corkum, 2001 ), along 18 Europe’s navigable rivers. Natural colonisation, e.g. along non-navigable tributaries, tends 19 to be slower (Schomaker and Wolter, 2014 ). The round goby has also been introduced into 20 brackish and marine waters in Europe; indeed, the first reported introduction outside of its 21 native area was into the Gulf of Gdansk (Southern Baltic Sea) in 1990 (Skóra and Stolarski, 22 1993 ). Since then, they have spread along the Baltic Sea coast (Michalek et al. , 2012 ; Sapota 23 and Skóra, 2005 ), with the western dispersal route reaching the coastal waters of the Jutland 24 peninsula. Further expansion of this branch, together with eastward spread through canals 25 connecting North Sea Basin rivers (Brunken et al. , 2012 ; van Beek, 2006 ), was the probable 26 source of round goby colonisation of the lower River Elbe (Hempel and Thiel, 2013 ). 27 Round gobies were first reported on the River Elbe on the tidal stretch at Hamburg (Germany; ◦ ′ ′′ ◦ ′ ′′ 28 53 31 28 N, 9 59 11 E; Figure 1) in 2008, having been caught by a commercial fisherman 29 (Hempel and Thiel, 2013 ). Between 2011 and 2013, the species was being caught relatively 30 frequently by anglers around Hamburg. Despite the presence of a large weir separating the 31 freshwater upstream Elbe and the tidally influenced Elbe “estuary”, one specimen has been ◦ ′ ′′ ◦ ′ ′′ 32 caught further upstream, near the town of Geesthacht (53 43 58 N, 10 37 79 E; r. km 936), 33 34 km southeast of Hamburg in 2012 (Hempel and Thiel, 2013 ). No fish have been reported 34 above this point to date. 35 On the 4th August 2015, a round goby was caught for the first time in the upper Elbe at ◦ ′ ′′ ◦ ′ ′′ 36 Svádov (Czech Republic), near the city of Ústí nad Labem (50 39 38 N, 14 031 56 E; Fig- 37 ure 1), 603 r. km upstream of Geesthacht, during an ecotoxicological examination by the 38 Czech Angling Union (T. Kava, Czech Angling Union, Pers. Comm.). Up to that date, there 39 had been no report of gobies above Geesthacht. On the 17th August, a fish was accidentally 40 caught during sampling of zoobenthos (Bu riˇ cˇ et al. , 2015 ) and a further individual was re- ◦ ′ ′′ ◦ ′ ′′ 41 ported by an angler close to the previous site (village of Povrly; 50 40 23.3 N, 14 09 38.3 E)

33p2 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

Figure 1 Map of the upper Elbe illustrating: a) ﬁrst ﬁnding of round goby (4.8.2015), b) second individual caught (20.8.2015), 1) the Dolní Žleb sampling site, 2) the D eˇ cínˇ sampling site, 3) the Svádov sampling site, and 4) the Nu cniceˇ sampling site (1-4 all 26.8.2015); see Table I for coordinates.

on the 20th August (Skalický in litt. ). Very soon after (see below), while undertaking manda- 1 tory ichthyological monitoring of the upper Elbe under the EU Water Framework Directive, 2 members of the Institute of Vertebrate Biology, Czech Academy of Sciences, caught multi- 3 ple specimens at several locations along the river. An identical survey by the Academy and 4 the Angling Union in 2013 (Jurajda et al. , 2013 ; unpublished report) found no goby presence 5 along the same stretch, suggesting introduction sometime within the last two years. 6 Here, we provide the ﬁrst data on population characteristics (size, sex ratio, proportion of ju- 7 veniles) for this new population, along with morphometric measurements and a discussion on 8 the possible source of the population. In addition, we provide data on the native ichthyofauna, 9 thus providing background data for assessing any future impact of this non-native species on 10 local ﬁsh populations. 11

METHODS

Fish sampling was conducted at four sites on the River Elbe between Dolní Žleb (5 km up- 12 stream of the Czech/German border) and Nu cniceˇ on the 26th August 2015 (Figure 1; see 13 Table I for coordinates). The riverbank throughout this stretch has been modiﬁed and sta- 14 bilised with 10 −50 cm stony rip-rap. The river bottom in the section from Dolní Žleb to Svádov 15 has a natural stony substrate and, during periods of very low discharge (as during this sam- 16 pling period), some parts of the bank consist of sand-gravel beaches. Aquatic vegetation was 17 absent throughout the stretch. The Nu cniceˇ site lies above a weir and water ﬂow is much 18

33p3 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

1 reduced. As a result, the river bottom is covered with mud and nearshore aquatic vegetation 2 is commonly present.

3 Fish were caught along the river bank (depth not exceeding 80 cm, mean sampled width 4 ca. 1.2 m) during the day using single pass continual electrofishing (SEN battery-powered 5 backpack electrofishing gear, Bedná r,ˇ Czech Republic) fitted with a 2 mm mesh anode, with 6 100 m of shoreline generally being sampled. Details on the actual sampling methods used 7 are described in more detail in Pola cikˇ et al. (2008 ). All fish sampled (native and non-native) 8 were identified and measured, native species being immediately returned alive to the water. −2 9 Fish data are presented as relative percentage and estimated total density (fish ·m ) at each 10 site (Table I).

11 All round gobies were sacrificed with an overdose of clove oil then placed in ice for transport 12 to the laboratory. In the laboratory, the fish were measured to the nearest 0.01 mm using 13 digital callipers, weighed to the nearest 0.01 g (total weight) and fin clips taken and stored 14 in 96% ethanol for further genetic analysis. Sex was determined during fish dissection based 15 on the type of gonads present and on external genitalia. Fish with absent or indistinguishable 16 gonads were considered as juveniles and those with clearly distinguishable gonads as adults. 17 The proportion of each sex (juveniles excluded) was used to calculate the adult sex-ratio.

Table I Geographic characteristics (GPS coordinates and river km) and fish assemblage structure (relative %) for the four sites monitored on the upper Elbe on 26th August 2015. Site Dolní Žleb Deˇ cínˇ Svádov Nu cniceˇ River km 363 353 333 295 Coordinates N 50 ◦50 ′33.14 ′′ 50 ◦46 ′53.66 ′′ 50 ◦39 ′57.27 ′′ 50 ◦30 ′23.66 ′′ Coordinates E 14 ◦13 ′04.16 ′′ 14 ◦12 ′26.30 ′′ 14 ◦06 ′00.83 ′′ 14 ◦13 ′33.72 ′′ Common name Scientific name Roach Rutilus rutilus 21.6 7.4 27.6 24.4 Dace Leuciscus leuciscus 1.1 5.5 Chub Leuciscus cephalus 55.7 25.2 17.2 45.3 Ide Leuciscus idus 2.5 3.0 2.9 Nase Chondrostoma nasus 3.4 6.7 Gudgeon Gobio gobio 4.9 10.4 12.2 White-fin Gobio albipinnatus 1.1 1.2 1.5 gudgeon Stone morocco Pseudorasbora parva 0.7 Barbel Barbus barbus 13.6 21.5 17.9 Bleak Alburnus alburnus 2.5 0.6 Vimba Vimba vimba 4.7 Bitterling Rhodeus amarus 8.1 Goldfish Carassius auratus 0.6 Stone loach Barbatula barbatula 1.8 Wells Silurus glanis 0.6 Three-spined Gasterosteus stickleback aculeatus Perch Perca fluviatilis 1.1 11.0 7.5 0.6 Ruffe Gymnocephalus 2.3 6.1 6.7 cernuus European bullhead Cottus gobio 0.6 0.7 Round goby Neogobius 3.1 6.7 melanostomus Total density (fish ·m−2) 44.0 81.5 167.5 172.0

33p4 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

0.02

0.01 A

Pec 0.00 Pel BUL SVK D1 CZE

MDS Axis 2 GER

-0.01

-0.02

20.0- 00.0 0.02 MDS Axis 1

Figure 2 MDS ordination showing similarities in meristic characteristics (in bold) of four round goby populations. Number of ﬁn rays: Pec = pectoral, Pel = pelvic, D1 = 1st dorsal, D2 = 2nd dorsal, A = anal. Populations: BUL = Bulgarian Danube, SVK = Slovakian Danube, CZE = Czech Elbe, GER = German Elbe.

Morphological characteristics (data presented in Supplementary Table I) were compared with 1 those originating from the tidal Elbe (data obtained from Hempel and Thiel, 2013 ) and non- 2 native and native Danubian populations from Slovakia and Bulgaria, respectively (described 3 in Pola cikˇ et al. , 2012 ). Only meristic characteristics were taken into account due to allometric 4 growth in round gobies (L’avrin cíkováˇ et al. , 2005 ) and a mismatch in ﬁsh length between pop- 5 ulations. Multiple analysis of variance (MANOVA) and multidimensional scaling were used to 6 compare and visualise the meristic characters, using the R statistical software, version 3.2.1 7 (R Core Team, 2015 ). 8

RESULTS

Round goby were present at both Svádov (r. km 333) and D eˇ cínˇ (r. km 353) but not at Dolní 9 Žleb (r. km 363) or Nu cniceˇ (r. km 295) (see Figure 1; Table I). Fourteen fish were caught at 10 −2 −2 Svádov (equivalent to 0.11 fish ·m ) and five at D eˇ cínˇ (equivalent to 0.03 fish ·m ). At both 11 positive sites, native species were present in high abundance, with gobies representing a 12 minor part of the assemblage (Table I). 13 All five gobies caught at D eˇ cínˇ were <46 mm SL, presumably representing young-of-the- 14 year fish. On the other hand, most gobies sampled at Svádov (13 ind.) had fully-developed 15 gonads and were classed as adults. Most of these fish were between 40 and 65 mm SL, with 16 one individual measuring 78 mm SL and one 102 mm SL (in the absence of further aging 17 evidence ( e.g. scale readings), we estimate that these correspond with 1+, 2+ and 3+ fish, 18 respectively). The overall male:female sex ratio at Svádov was 1.83:1. 19 There was no significant difference in meristic characteristics between round gobies from the 20 tidal Elbe and the upper Elbe (MANOVA, P = 0.24; Figure 2). There was, however, a significant 21 difference between both Elbe populations and the two Danubian populations (MANOVA, all 22 P < 0.001; Figure 2). 23

33p5 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

DISCUSSION

1 In this study, the detection of a newly established round goby population far from any source 2 population provides compelling new evidence supporting the rapid spread of round gobies in 3 European river networks through port-to-port transfer by shipping. Several lines of evidence 4 strongly suggest that the upper Elbe population originated through boat-mediated transport 5 from the port at Hamburg on the tidal Elbe. 6 Both the upper and lower Elbe populations share statistically similar morphological (meristic) 7 characteristics. While such evidence could be considered indirect as a) meristic character- 8 istics are not fully heritable (Hermida et al. , 2002 ) and (b) morphological characteristics can 9 change significantly due to environmental factors within just a few weeks (Olsson and Eklöv, 10 2005 ; Heerman et al. , 2007 ), it is certainly compelling. The morphological analysis also dis- 11 credits the possibility that the fish originated from within the Czech Republic through overland 12 transport ( e.g. in an anglers bait bucket) from the Rivers Morava and Dyje, until now the only 13 established round goby population in the Republic. The Morava/Dyje population, which origi- 14 nated through natural migration up the Morava from the Danube, should share morphological 15 characteristics with Danubian gobies, which in turn display distinct morphological differences 16 to those on both the upper and lower Elbe. Moreover, despite being closer geographically 17 (290 km), gobies have no possibility of migrating naturally between the Morava/Dyje and Elbe 18 as they are situated in different watersheds, unconnected by any artificial canal. 19 Secondly, the rate of spread appears too fast for natural dispersal to have taken place ( i.e. by 20 swimming). As we are unaware of any further surveys reporting goby occurrence upstream of 21 Geesthacht since the single observation in 2012, gobies would have to have swum 600 km 22 upstream in just three years. This is far beyond the rate of natural upstream migration ob- 23 served in recent studies (estimates range from 1 −15 km per year; see Marentette et al. , 2011 ; 24 Lynch and Mensinger, 2012 ; Janá cˇ et al. , 2012 ). 25 Finally, the upper Elbe population appears to be restricted to the area immediately surround- 26 ing the inland port at Ústí nad Labem, which lies approximately 1.5 km upstream of Svádov. 27 Our data suggest that gobies have not yet penetrated St rekovˇ weir, 4 km upstream of the 28 port (first weir on the Elbe upstream of Geesthacht), as no gobies were found at Nu cnice.ˇ 29 Furthermore, no gobies were caught 30 km downstream of the port at Dolní Žleb. The five 30 fish found at D eˇ cínˇ (20 km downstream of the port) were all juveniles and, while it is possible 31 that they represent new arrivals, it is more probable that they colonised the site as drifting 32 early life-stages from the near-port stretch (see Janá cˇ et al. , 2013 ). D eˇ cín,ˇ therefore, in addi- 33 tion to representing the furthest downstream extent of the population also provides evidence 34 of reproduction and expansion from an upstream site. This same pattern of restricted dis- 35 tribution near ports has also been observed in other isolated round goby ‘populations’ ( e.g. 36 Vienna/Bratislava; Roche et al. , 2013 ). 37 Thus far, the upper Elbe round goby population represents a minor part of the local fish as- 38 semblage (note, however that local fishermen have reported high densities around the port 39 itself [not sampled during our survey]; T. Kava, pers. comm.). Based on previous experience, 40 it is highly likely that gobies will come to dominate the local fish assemblage, as they have 41 elsewhere (see Kornis et al. , 2012 ). Furthermore, as drift of early life-stages has been shown 42 to greatly increase the rate at which gobies spread downstream (Janá cˇ et al. , 2012 ), coloni- 43 sation of the German stretch of the Elbe, with eventual connection with the downstream tidal 44 population, would appear inevitable. Upstream migration is likely to be much slower, in part 45 due to the presence of multiple weirs along this upper stretch. 46 Previous studies, and particularly those from the Laurentian Great Lakes, have reported round 47 gobies directly affecting native fish assemblages through predation of eggs and juveniles 48 (Chotkowski and Marsden, 1999 ; Roseman et al. , 2006 ), competition for shelter and spawn- 49 ing interference (Janssen and Jude, 2001 ; Balshine et al. , 2005 ; Bergstrom and Mensinger, 50 2009 ). To date, however, none of these has been confirmed as having a major impact in 51 European rivers (Vašek et al. , 2014 ; Všeti ckováˇ et al. , 2015 ; Janá c,ˇ unpublished data). In- 52 stead, we suspect that round gobies will affect the native fish assemblage through effects 53 on other ecosystem components, e.g. by providing a reservoir for native parasites ( i.e. the

33p6 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33 spill-back effect; Ondra ckováˇ et al. , 2015 ), strongly impacting local invertebrate communi- 1 ties (Lederer et al. , 2008 ; Kipp and Ricciardi, 2012 ) and through incorporation into food-webs 2 (Rush et al. , 2012 ; Pola cikˇ et al. , 2015 ), with subsequent alterations to food-web structure 3 and energy and pollutant transfer (Rogers et al. , 2014 ). 4 This newly established population highlights the speed with which this species has been able 5 to colonise wide areas of Europe via establishment of widely-separated populations through 6 port-to-port transfer and rapid inter-site connection through downstream drift and natural 7 migration. Its recent establishment and presently isolated status provides an ideal opportu- 8 nity for long-term monitoring in order to assess rates of colonisation and actual impacts on 9 recipient ecosystems. 10

ACKNOWLEDGEMENTS

We would like to express our thanks to Ing. Tomaš Kava, manager of the North Bohemian 11 Anglers Union, for alerting us to the presence of round goby on the Elbe, for enabling us to 12 survey in their ﬁshing grounds and for kind help in the ﬁeld. We also thank Matej Pola cikˇ for 13 providing data on Danubian goby morphometry. Finally, we thank two anonymous reviewers 14 for their valuable comments on a previous version of the manuscript. This study was sup- 15 ported by the Grant Agency of the Czech Republic, Grant No. P505/11/1768. 16

REFERENCES

Ahnelt H., Banarescu P., Spolwind R., Harka A. and Waidbacher H., 1998. Occurrence and distribution 17 of three gobiid species (Pisces, Gobiidae) in the middle and upper Danube region – examples of 18 different dispersal patterns? Biologia , 53 , 665–678. 19 Balshine S., Verma A., Chant V. and Theysmeyer T., 2005. Competitive interactions between round 20 gobies and logperch. J. Gt. Lakes Res. , 31 , 68–77. 21 Bergstrom M.A. and Mensinger A.F., 2009. Interspecific resource competition between the invasive 22 round goby and three native species: logperch, slimy sculpin, and spoonhead sculpin. Trans. Am. 23 Fish. Soc. , 138 , 1009–1017. 24 Borcherding J., Staas S., Kruger S., Ondra ckováˇ M., Šlapanský L. and Jurajda P., 2011. Non-native 25 Gobiid species in the lower River Rhine (Germany): recent range extensions and densities. J. 26 Appl. Ichthyol. , 27 , 153–155. 27 Brunken H., Castro J.F., Hein M., Verwold A. and Winkler M., 2012. First records of round goby 28 Neogobius melanostomus (Pallas, 1814) in the river Weser. Lauterbornia , 75 , 31–37. 29 Bu riˇ cˇ M., Bláha M., Kouba A. and Drozd B., 2015. Upstream expansion of round goby ( Neogobius 30 melanostomus ) – first record in the upper reaches of Elbe river. Knowl. Manag. Aquat. Ecosyst ., 31 416, 32 32 Chotkowski M.A. and Marsden J.E., 1999. Round goby and mottled sculpin predation on lake trout eggs 33 and fry: Field predictions from laboratory experiments. J. Gt. Lakes Res. , 25 , 26–35. 34 Grabowska J., Kotusz J. and Witkowski A, 2010. Alien invasive fish species in Polish waters: an 35 overview. Folia Zool. , 59 , 73–85. 36 Hayden T.A. and Miner J.G., 2009. R apid dispersal and establishment of a benthic Ponto-Caspian goby 37 in Lake Erie: diel vertical migration of early juvenile round goby. Biol. Invasions , 11 , 1767–1776. 38 Heerman L., Beeck P. and Borcherding J., 2007. Two size classes of 0+ perch: is phenotypic plasticity 39 based on food resources? J. Fish Biol. , 70 , 1365–1377. 40 Hempel M. and Thiel R., 2013. First records of the round goby Neogobius melanostomus (Pallas, 1814) 41 in the Elbe River, Germany. BioInvasions Rec. , 2, 291–295. 42 Hermida M., Fernandez C., Amaro R. and San Miguel E., 2002. Heritability and “evolvability” of meristic 43 characters in a natural population of Gasterosteus aculeatus . Can. J. Zool. , 80 , 532–541. 44 Janá cˇ M., Valová Z. and Jurajda P., 2012. Range expansion and habitat preferences of non-native 0+ 45 tubenose goby ( Proterorhinus semilunaris ) in two lowland rivers in the Danube basin. Fundam. 46 Appl. Limnol. , 181 , 73–85. 47

33p7 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

1 Janá cˇ M., Šlapanský L., Valová Z. and Jurajda P., 2013. Downstream drift of round goby ( Neogobius 2 melanostomus ) and tubenose goby ( Proterorhinus semilunaris ) in their non-native area. Ecol. 3 Freshw. Fish , 22 , 430–438.

4 Janssen J. and Jude D.J., 2001. Recruitment failure of mottled sculpin Cottus bairdi in Calumet Harbor, 5 southern Lake Michigan, induced by the newly introduced round goby Neogobius melanostomus . 6 J. Gt. Lakes Res. , 27 , 319–328.

7 Jude D.J., Reider R.H. and Smith G.R., 1992. Establishment of Gobiidae in the Great-Lakes Basin. Can. 8 J. Fish. Aq. Sci. , 49 , 416–421.

9 Jurajda P., Cernýˇ J., Pola cikˇ M., Valová Z., Janá cˇ M., Blažek R. and Ondra ckováˇ M., 2005. The recent 10 distribution and abundance of non-native Neogobius ﬁshes in the Slovak section of the River 11 Danube. J. Appl. Ichthyol. , 21 , 319–323.

12 Jurajda P., Jurajdová Z., Roche K. and Šlapanský L. 2013. Survey of ﬁsh communities in the lower Czech 13 Elbe. Report of the Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic. 14 (In Czech; Unpublished data)

15 Kalchhauser I., Mutzner P., Hirsch P.E. and Burkhardt-Holm P., 2013. Arrival of round goby Neogobius 16 melanostomus (Pallas, 1814) and bighead goby Ponticola kessleri (Günther, 1861) in the High 17 Rhine (Switzerland). BioInvasions Rec. , 2, 79–83.

18 Kipp R. and Ricciardi A., 2012. Impacts of the Eurasian round goby ( Neogobius melanostomus ) on 19 benthic communities in the upper St. Lawrence River. Can. J. Fish. Aq. Sci. , 69 , 469–486.

20 Kornis M.S., Mercado-Silva N. and Vander Zanden M.J., 2012. Twenty years of invasion: a review of 21 round goby Neogobius melanostomus biology, spread and ecological implications. J. Fish Biol. , 22 80 , 235–285.

23 L’avrin cíkováˇ M., Ková c,ˇ V. and Katina, S., 2005. Ontogenetic variability in external morphology of round 24 goby Neogobius melanostomus from Middle Danube, Slovakia. J. Appl. Ichthyol. , 21 , 328–334.

25 Lederer A.M., Janssen J., Reed T. and Wolf A., 2008. Impacts of the Introduced round goby ( Apollonia 26 melanostoma ) on dreissenids ( Dreissena polymorpha and Dreissena bugensis ) and on macroinver- 27 tebrate community between 2003 and 2006 in the littoral zone of Green Bay, Lake Michigan. J. Gt. 28 Lakes Res. , 34 , 690–697.

29 Lynch M.P. and Mensinger A.F., 2012. Seasonal abundance and movement of the invasive round goby 30 (Neogobius melanostomus ) on rocky substrate in the Duluth-Superior Harbor of Lake Superior. 31 Ecol. Freshw. Fish , 21 , 64–74.

32 Marentette J.R., Wang G., Tong S., Sopinka N.M., Taves M.D., Koops, M.A. and Balshine S., 2011. 33 Laboratory and ﬁeld evidence of sex-biased movement in the invasive round goby. Behav. Ecol. 34 Sociobiol. , 65 , 2239–2249.

35 Michalek M., Puntila R., Strake S. and Werner M., 2012. Abundance and distribution of round goby 36 (Neogobius melanostomus ). HELCOM Baltic Sea Environment Fact Sheets. http://www.helcom.ﬁ/ 37 baltic-sea-trends/environment-fact-sheets/ .

38 Miller P.J., 2004. The Freshwater Fishes of Europe, Vol 8/II Gobiidae 2. Aula-Verlag, Wiesbaden. 478 p.

39 Olsson J. and Eklöv P., 2005. Habitat structure, feeding mode and morphological reversibility: factors 40 inﬂuencing phenotypic plasticity in perch. Evol. Ecol. Res. , 7, 1109–1123

41 Ondra ckováˇ M., Hudcová I., Dávidová M., Adámek Z., Kašný M. and Jurajda P., 2015. Non-native gobies 42 facilitate the transmission of Bucephalus polymorphus (Trematoda). Parasit. Vectors , 8, 382.

43 Painter S. and Seifert K., 2006. First record of the round goby, Neogobius melanostomus (Gobiidae), in 44 the German Danube. Lauterbornia , 58 , 101–107.

45 Pola cikˇ M., Janá cˇ M., Jurajda P., Vassilev M. and Trichkova T., 2008. The sampling efficiency of elec- 46 trofishing for Neogobius species in a riprap habitat: a field experiment. J. Appl. Ichthyol. , 24 , 47 601–604.

48 Pola cikˇ M., Janá cˇ M., Vassilev M. and Trichkova T., 2012. Morphometric comparison of native and non- 49 native populations of round goby Neogobius melanostomus from the River Danube. Folia Zool. , 50 61 , 1–8.

51 Pola cikˇ M., Jurajda P., Blažek R. and Janá cˇ M., 2015. Carcass feeding as a cryptic foraging mode in 52 round goby Neogobius melanostomus . J. Fish Biol. , 87 , 194–199.

53 R Core Team, 2015. R: A language and environment for statistical computing. R Foundation for 54 Statistical Computing, Vienna, Austria. http://www.R-project.org/ .

33p8 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33

Ray W.J. and Corkum L.D., 2001. Habitat and site affinity of the round goby. J. Gt. Lakes Res. , 27 , 1 329–334. 2 Roche K.F., Janá cˇ M. and Jurajda P., 2013. A review of Gobiid expansion along the Danube-Rhine 3 corridor - geopolitical change as a driver for invasion. Knowl. Manag. Aquat. Ecosyst., 411 , 01. 4 Rogers M.W., Bunnell D.B., Madenjian C.P. and Warner D.M., 2014. Lake Michigan offshore ecosystem 5 structure and food web changes from 1987 to 2008. Can. J. Fish. Aq. Sci. , 71 , 1072–1086. 6 Roseman E.F., Taylor W.W., Hayes D.B., Jones A.L. and Francis J.T., 2006. Predation on walleye eggs 7 by fish on reefs in western Lake Erie. J. Gt. Lakes Res. , 32 , 415–423. 8 Rush S.A., Paterson G., Johnson T.B., Drouillard K.G., Haffner G.D., Hebert C.E., Arts M.T., McGoldrick 9 D.J., Backus S.M., Lantry B.F., Lantry J.R., Schaner T. and Fisk A.T., 2012. Long-term impacts of 10 invasive species on a native top predator in a large lake system. Freshwater Biol. , 57 , 2342–2355. 11 Sapota, M.R. and Skora, K.E., 2005. Spread of alien (non-indigenous) fish species Neogobius melanos- 12 tomus in the Gulf of Gdansk (south Baltic). Biol. Invasions , 7, 157–164. 13 Schomaker C. and Wolter C., 2014. First record of the round goby Neogobius melanostomus (Pallas, 14 1814) in the lower River Oder, Germany. BioInvasions Rec. , 3, 185–188. 15 Skóra K.E. and Stolarski J., 1993. New fish species in the Gulf of Gdañsk. Neogobius sp. [ cf . Neogobius 16 melanostomus (Pallas, 1811)]. Bull. Sea Fish. Inst., 1 , 83–84. 17 van Beek G.C.W., 2006. The round goby Neogobius melanostomus first recorded in the Netherlands. 18 Aquat. Inv. , 1, 42–43. 19 Vašek M., Všeti ckováˇ L., Roche K. and Jurajda P., 2014. Diet of two invading gobiid species 20 (Proterorhinus semilunaris and Neogobius melanostomus ) during the breeding and hatching sea- 21 son: No field evidence of extensive predation on fish eggs and fry. Limnologica , 46 , 31–36. 22 Vseti ckováˇ L., Janá cˇ M., Roche K. and Jurajda P., 2015. Assessment of possible diel and sex-related 23 differences in round goby ( Neogobius melanostomus ) diet. Folia Zool. , 64 , 104–111. 24 Wiesner C., 2005. New records of non-indigenous gobies ( Neogobius spp.) in the Austrian Danube. 25 J. Appl. Ichthyol. , 21 , 324–327. 26

Cite this article as: K. Roche, M. Janá c,ˇ L. Šlapanský, L. Mikl, L. Kope cek,ˇ and P. Jurajda, 2015. A newly established round goby ( Neogobius melanostomus ) population in the upper stretch of the river Elbe. Knowl. Manag. Aquat. Ecosyst. , 416, 33. 27

33p9 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33 F VI 13 I;14 I;12 II;10 8.15 6.22 6.97 1.57 3.90 5.04 3.64 10.66 17.94 18.71 19.94 32.41 14.39 15.23 67.55 57.29 11.05 17.02 10.52 11.34 11.26 18 (+1) Svádov VI 12 I;15 I;11 JUV II;10 7.04 12.2 9.73 6.91 6.57 6.95 4.55 4.54 4.68 8.05 1.07 2.93 2.61 0.66 12.22 38.62 13.54 22.33 10.75 46.67 10.30 18 (+1) Svádov VI M 18 11 I;15 I;13 II;10 8.57 6.86 4.95 4.99 3.85 2.09 8.03 11.24 19.08 13.75 60.75 17.60 19.83 21.42 32.67 11.71 15.79 72.36 11.96 10.80 12.45 Svádov VI M 18 10 I;11 I;14 II;10 8.83 11.8 1.80 8.78 7.78 8.10 3.85 5.59 3.20 1.17 5.11 6.00 9.13 14.19 13.79 14.87 11.30 54.82 45.97 12.39 25.57 Svádov 9 VI M 20 I;12 I;15 II;10 67.7 55.8 8.32 7.30 6.48 3.64 4.62 3.55 1.77 10.65 11.27 16.60 11.17 10.93 17.72 17.84 18.82 30.35 13.58 11.04 14.33 Svádov 8 VI M 19 I;12 I;15 II;10 8.81 6.81 9.65 3.36 1.92 8.01 3.63 5.21 55.92 10.93 16.89 16.52 19.08 31.13 15.19 11.25 15.05 66.11 16.81 10.97 11.01 Svádov 7 F VI 18 I;12 I;15 II;10 9.51 7.15 9.08 4.72 5.80 4.14 2.32 14.17 18.30 74.50 64.02 10.91 17.99 18.94 21.32 35.87 16.10 12.59 18.93 11.85 11.32 Svádov 6 F VI 19 I;15 I;12 II;10 7.76 6.02 3.50 4.88 3.95 2.17 8.22 10.55 15.17 19.90 16.97 15.82 66.19 56.22 10.42 16.19 10.44 10.99 16.83 31.34 12.18 Svádov om the upper stretch of the River Elbe. 5 F VI 18 I;15 I;11 II;10 9.23 6.81 8.93 4.57 6.02 3.96 2.29 11.16 61.08 17.95 19.15 20.81 33.86 17.20 16.04 71.36 10.77 17.27 10.81 11.16 13.47 Svádov 4 VI M 18 I;14 I;11 II;10 4.23 7.06 5.09 78.77 10.31 10.31 15.57 19.98 22.08 26.03 45.22 10.79 20.24 16.67 20.64 91.30 11.48 13.87 21.24 15.31 16.48 Svádov 3 F VI 18 II;9 I;15 I;12 8.83 6.83 3.76 2.07 7.37 4.34 5.27 70.63 59.74 12.18 16.56 12.47 18.91 18.29 20.54 31.67 15.16 12.08 17.75 11.33 11.55 Svádov 2 VI M 18 I;12 I;14 II;10 8.11 6.99 8.06 3.75 4.93 3.71 3.48 11.07 16.93 17.25 19.05 13.78 16.86 66.85 56.06 11.85 16.22 10.27 11.73 32.48 12.20 Svádov 1 VI M 18 I,12 I,16 II,10 6.98 5.86 1.58 6.20 8.79 2.67 9.28 8.81 3.48 2.50 10.63 47.86 12.86 14.19 16.49 28.31 11.36 15.63 55.63 10.50 14.24 Svádov Morphological characteristics for round gobies sampled fr Characteristics / individual no. Site Total length Standard length Total weight First dorsal fin spines Second dorsal fin spines and rays Anal fin spines and rays Pelvic fin spines and rays Pectoral fin rays Sex Body depth Head length Head depth Head width Snout length Postorbital head length Orbit diameter Interorbital width Caudal peduncle depth Caudal peduncle length Pre-pectoral length Pre-pelvic length Pre-dorsal length Pre-anal length First dorsal fin height Pectoral fin length Pelvic fin length Pelvic fin insertion to anal fin origin Supplementary Table I.

33p10 K. Roche et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 33 F VI 18 24 I;15 I;12 II;10 7.29 5.08 3.82 22.11 20.65 22.39 95.43 81.30 11.19 10.26 16.48 26.22 45.87 21.54 13.52 19.27 21.10 16.69 19.21 10.54 16.15 Svádov* ˇ cín ˇ VI 18 23 e I;14 I;12 JUV II;10 8.06 6.23 7.94 0.74 5.81 9.50 5.17 6.01 2.78 4.70 2.37 0.41 3.70 4.37 7.01 33.82 10.50 10.30 11.78 40.86 17.95 D ˇ cín ˇ VI 18 22 e I;14 I;10 JUV II;10 4.82 1.14 5.17 7.21 5.26 9.18 1.52 7.42 7.13 7.48 3.27 3.05 11.99 51.09 42.17 10.96 13.56 13.79 14.59 24.50 10.33 D ˇ cín ˇ VI 18 21 e I;15 I;12 JUV II;10 5.80 4.90 7.64 5.70 1.61 7.77 7.78 7.61 4.07 3.02 1.16 9.13 12.12 45.36 14.49 14.03 14.45 25.54 10.54 55.03 12.25 D ˇ cín ˇ VI 17 20 e I;15 JUV II;10 2.54 4.80 5.19 9.72 1.51 7.86 6.59 7.62 4.01 2.97 1.50 I;112 13.16 10.14 11.82 50.20 43.04 11.97 12.45 14.50 23.09 11.80 D ˇ cín ˇ VI 17 19 e I;14 I;11 JUV II;10 5.90 4.87 7.24 1.44 5.74 9.35 1.53 7.79 8.07 7.60 3.01 2.90 12.25 40.99 12.61 12.29 14.96 10.90 48.56 11.47 23.79 D VI M 17 18 I;14 I;11 II;10 6.43 5.02 9.12 5.52 2.04 8.73 8.27 8.27 3.81 2.67 1.25 15.05 47.96 13.21 14.73 16.32 26.06 14.05 55.45 13.00 10.36 Svádov VI M 19 17 I;15 I;12 II;10 9.31 7.59 2.65 8.81 5.54 5.92 3.47 16.80 11.71 63.81 17.31 20.98 36.31 16.41 13.02 76.76 12.75 19.94 12.02 12.66 220.07 Svádov F VI 18 16 I;15 I;11 II;10 6.04 4.44 31.56 14.23 12.48 20.93 30.06 28.46 32.75 35.11 58.57 12.20 28.20 19.02 21.10 19.52 20.58 23.26 10.25 120.44 102.77 Svádov VI M 17 15 I;16 I;12 II;10 6.41 5.34 9.56 6.14 2.00 9.21 8.58 8.34 3.68 3.34 1.49 8.67 13.98 14.06 15.28 16.62 10.82 56.90 47.25 13.38 27.26 Svádov VI M 19 14 I;16 I;12 II;10 6.50 5.76 9.52 1.62 5.58 2.47 9.02 8.29 9.67 4.28 3.35 14.70 49.50 15.08 15.41 16.85 26.09 11.92 10.36 60.37 12.89 Svádov Continued. Characteristics / individual no. Site Total length Standard length Total weight First dorsal fin spines Second dorsal fin spines andAnal rays fin spines and rays Pelvic fin spines and rays Pectoral fin rays Sex Body depth Head length Head depth Head width Snout length Postorbital head length Orbit diameter Interorbital width Caudal peduncle depth Caudal peduncle length Pre-pectoral length Pre-pelvic length Pre-dorsal length Pre-anal length First dorsal fin height Pectoral fin length Pelvic fin length Pelvic fin insertion to anal fin origin Supplementary Table I. *First specimen captured on the river.

33p11 Publikace D

Downstream drift of round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their non- native area

Janáč, M., Šlapanský, L., Valová, Z. & Jurajda, P. (2013)

Ecology of Freshwater Fish, 22 (3), 430-438

Ecology of Freshwater Fish 2013 Ó 2013 John Wiley & Sons A/S ECOLOGY OF FRESHWATER FISH

Downstream drift of round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their non-native area

Michal Janac, Ludek Slapansky, Zdenka Valova, Pavel Jurajda Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Kvetna 8, Brno, 603 65, Czech Republic

Accepted for publication January 19, 2013

Abstract – Several Ponto-Caspian gobiid species have recently expanded their ranges in Europe and North America. This is the first study to demonstrate passive downstream dispersal (drift) of the round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in newly colonised areas (River Dyje, Danube basin), a factor that could play an important role in their dispersal. Drift duration (i.e. number of dates on which the species was caught) in round goby was longer than that of both native species and tubenose goby, providing a possible advantage. Size of drifting fish was restricted to a narrow range of 6–8 mm and 5–8 mm for round and tubenose goby, respectively. Drift in both species occurred almost completely during hours of darkness (<1 lux) and fish size did not vary throughout the night. In both species, drift density increased significantly during the first hour after dusk. Round goby density gradually decreased up to dawn, while tubenose goby density varied throughout the night with no clear pattern. Drift of early life stages appears to be an important phenomenon that has not received adequate attention in studies of round and tubenose goby ecology and dispersal.

Key words: invasive species; dispersal; drift; round goby; tubenose goby; Gobiidae

fish, with results suggesting relatively low movement Introduction activity for these benthic, swim bladder-lacking, fish The round goby Neogobius melanostomus (Pallas (Cookingham & Ruetz 2008; Bronnenhuber et al. 1814) and tubenose goby Proterorhinus semilunaris 2011; Marentette et al. 2011; Lynch & Mensinger (Heckel 1837) are two Ponto-Caspian gobiid species 2012; but see Tierney et al. 2011). Passive movement that have recently expanded their ranges in Europe of early ontogenetic stages, however, may represent and North America (for reviews of recent distribution an important dispersal mechanism. Both round and see; Kocovsky et al. 2011; Vasek et al. 2011; Kornis tubenose goby have been documented as undergoing et al. 2012). These species have become a subject of downstream drift in their first weeks of life within interest for fish biologists, mostly due to the detri- their historic range (Vassilev 1994; Zitek et al. mental impact of round goby in the Laurentian Great 2004). Recent studies have proposed that drift may Lakes (Kornis et al. 2012). If we are to understand, help in the spread of these species from points of and potentially block, expansion of these fish, it is anthropogenic introduction (Hayden & Miner 2009; critical that we determine their dispersal mechanisms Kocovsky et al. 2011; Janac et al. 2012). No study to (Hayden & Miner 2009; Kornis et al. 2012). date, however, has documented such downstream Studies on dispersal of Ponto-Caspian gobiids have drift for Ponto-Caspian gobiids in newly colonised focussed almost exclusively on movement of adult areas.

Correspondence: Michal Janac, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Kvetna 8, 603 65, Brno, Czech Republic. E-mail: [email protected] doi: 10.1111/eff.12037 1 Janac et al.

While basic knowledge on aspects of goby drift (e. The first appearance of round goby at the study g., size range and seasonal or diel pattern) is central site (and its first record in the Czech Republic) dates to efforts aimed at preventing further expansion and from 2008 (Lusk et al. 2010), with the population facilitating future research on drift in these species, stable since 2009. The species presently ranges from existing information is scarce. Zitek et al. (2004) the confluence with the Morava to approximately have provided information on seasonal pattern and 8 km upstream of the study site (Jurajda, unpublished size range of drifting tubenose goby near the edge of data). Both species were abundant in the study stretch the species’ historical range (downstream of Vienna; in 2011 (Jurajda, unpublished data). River Danube); however, their results may not be widely applicable as (i) the study took place in a Data sampling man-made channel, and (ii) a recent study on passage of tubenose goby from a reservoir to a river (Janac Samples were obtained over 16 sampling dates at et al. 2013) suggested that fish of larger sizes than weekly intervals from late May to early September those reported by Zitek et al. (2004) may also drift. 2011 (Table 1; Fig. 1). On each sampling date, eight Vassilev (1994) documented drift of round and tube- samples were taken, each consisting of a 30 min nose gobies in their native range along the Bulgarian exposure of four drift nets (see below; note that the Danube, though few individuals were sampled (56 expression ‘sample’ henceforth refers to a single round gobies and three tubenose gobies) and no exposure of four nets). Fish drift, in general, is driven information on seasonal pattern was provided. Both by light intensity (Pavlov 1994; Reichard et al. authors observed greater drift during the night rather 2002b), with gobiids drifting mostly during the night than day (Vassilev 1994; Zitek et al. 2004). No infor- (Pavlov et al. 1977; Zitek et al. 2004). Sampling, mation is available, however, on drift during crepus- therefore, was mainly aimed at describing differences cular periods or on how drift patterns vary over the in drift density during the crepuscular and dark per- dark period, despite drift density in other species iod, with samples symmetrically distributed around being known to vary during the night (Persat & civil dusk and dawn (Table 2). Time of civil dusk Olivier 1995; Sonny et al. 2006). and dawn were obtained from http://calendar.zoznam. In this study, we aim to (i) assess whether tubenose sk/sunset-en.php. Timing of dusk and dawn varied and round gobies undergo downstream drift in their substantially during the sampling season (Table 1), non-native area, (ii) identify the life stages that stressing the importance of setting sampling time rel- undergo drift (through determination of the size ative to dusk and dawn and not to a fixed sample range(s) of drifting fish), and (iii) determine the sea- hour. sonal and diel (or, more specifically, night-time) drift Four conical drift nets were used (3 m long, mouth patterns and compare them between species. diameter 58 cm, mouth area 0.264 m3, 0.5 mm mesh size), each leading to a 2 l plastic collection bottle at the cod end. Each net was stabilised with steel rods Material and methods hammered into the river bottom. On each bank, two nets were positioned simultaneously at a distance of Study site 1–3 m parallel to the bank. Fish from each collection The study took place on the River Dyje (Czech bottle were preserved separately in 4% formaldehyde. Republic; Danube basin), near the town of Breclav In the laboratory, fish were identified according to (48°44′30.079″N, 16°53′31.366″E), 22 km from its Koblickaya (1981) and our own collection of com- confluence with the River Morava, a main tributary parative material and measured to the nearest to the River Danube. The river is channelised along 0.01 mm (standard length; SL). the study stretch, with a riverbank consisting of rip- At the beginning of the first and last sample on rap with stones of 10–50 cm width. Wet-width is each sampling date, we measured current velocity 45 m, maximum depth 1.5 m and mean annual dis- (mÁsÀ1) at the mouth of each net using a MiniAir20 charge 41 m3ÁsÀ1. flow measurement device (Schiltknecht, Switzerland) Tubenose goby have been present at the study site and, in cases where the net was not submersed com- since 1998, and have formed a stable population (i.e., pletely, distance from the water’s surface to the upper all age classes present) since 2000 (Prasek & Jurajda end of the net (used to calculate area of net opening 2005; Janac et al. 2012). The species is now abun- submersed, and hence volume of water filtered). As dant all along the Dyje from the NoveMlyny reser- neither submersed area nor current velocity differed voir, (original introduction point of the species in the substantially between the first and last samples (max- Czech Republic; Prasek & Jurajda 2005), 23 km imum difference 3 cm and 0.04 mÁsÀ1, respectively), upstream of the study site, down to its confluence the mean of the two values was considered to be with the Morava. common for all samples within a sampling date.

2 Downstream drift of non-native gobies

Table 1. Sampling dates, time of civil dusk and civil dawn (CET), and environmental parameters measured during drift sampling in 2011.

Sampling date

# Date Dusk Dawn Transparency (cm) Temperature (°C) Discharge (m3ÁsÀ1)

1 May 23 21:14 4:22 70 20 26 2 May 30 21:24 4:15 86 22 38 3 June 07 21:31 4:09 47 23 27 4 June 13 21:37 4:06 47 23 33 5 June 20 21:41 4:06 65 22 19 6 June 27 21:42 4:08 70 22 23 7 July 3 21:40 4:12 100 19 17 8 July 11 21:36 4:19 60 23 20 9 July 18 21:29 4:28 50 22 16 10 July 25 21:20 4:37 46 19 20 11 August 1 21:10 4:48 48 19 23 12 August 8 20:58 4:58 47 20 33 13 August 15 20:45 5:09 90 21 23 14 August 22 20:31 5:20 100 24 20 15 August 29 20:16 5:31 100 23 19 16 September 5 20:00 5:40 110 23 16

25 160 Data analysis 140 20 Inter-species differences in frequency of occurrence 120 ) over the 16 sampling dates were tested using a gener- –1 ·s 15 100 3 alised linear model (GLM, binomial [Bernouilli] 80 distribution), with comparisons made between round and tubenose goby and the most common native 10 60 species (dominance >1%) only. Density of drifting Temperature (°C) 40 Discharge (m 5 fish on each sampling date (pooled for all samples 20 and nets) was calculated as the number of individuals 3 0 0 per 1000 m of filtered water (volume of filtered March April May June July August water was calculated as current velocity multiplied by Date exposure time and area of net opening submersed). Fig. 1. Seasonal course of water temperature (solid line) and dis- As the volume of water filtered did not differ charge (dotted line) on the River Dyje in 2011. The x-axis ranges between samples within a sampling date (see above), from March 15 to September 5. Sampling dates are drawn as solid circles on the temperature curve. raw abundance data were used when comparing inter-sample differences in drift density. Differences in abundance between samples were also tested Table 2. Timing of samples for each sampling date and the median (with using a GLM as the response parameter (abundance) range in parentheses) illumination value. The two illumination values was Poisson distributed. As data were repeatedly presented in samples B and G represent measurements at the start and measured over 16 sampling dates, we used the gen- end of the sample. eralised estimating equations (GEE; geeglm function in the geepack package (Hojsgaard et al. 2006)) to Sample Timing Illumination (lux) control pseudoreplication. GEE are a common A 1 h before dusk 2780 (767–8700) approach to analysing correlated non-normal data B Dusk 35 (9–148); 1 (1–4) (see Zuur et al. 2009) and can be understood as an C 1 h after dusk 0 (0–0) D 2.5 h after dusk 0 (0–0) analogy to the mixed model (in which sampling date E 2.5 h before dawn 0 (0–0) would be a random parameter and sample a fixed F 1 h before dawn 0 (0–0) parameter). The model was simplified by combining G Dawn 1(1–8); 90(12–300) similar levels of the ‘sample’ factor (i.e., levels that H 1 h after dawn 2595 (967–6500) possessed similar abundance), where available [i.e., a non-significant difference between the model with original levels and that with new levels (analysis of At the start of each sample, we also measured light Walds’ statistic, P > 0.05)]. Multiple post-hoc com- intensity (in lux) using a LX-103 digital light metre, parisons were then conducted in order to reveal (Lutron Electronic Enterprise Co., Taiwan). differences between separate samples (significance

3 Janac et al. level in post-hoc tests corrected using the Bonferroni Table 3. List of species captured during drift sampling in 2011, with method). number of individuals sampled (N), relative proportion in assemblage (%), number of sampling dates with species occurrence (f; total number 16), When conducting common statistical tests (i.e., and range of drifting season (r; as sampling dates; see Table 1). Kruskal-Wallis test and multiple Kolmogorov-Smir- nov tests), both inter-sample and inter-sampling date Common name Scientific name N % fr comparisons of fish size provided many significant differences that lacked meaningful biological expla- Cyprinidae < Roach Rutilus rutilus 598 18.51 9 1–9 nations (e.g., a significant difference for a 0.2 mm Chub Leuciscus cephalus 3 0.09 2 1–2 difference between two sampling dates). As we are Dace Leuciscus leuciscus 1 0.03 1 2 convinced that the differences occurred due to our Ide Leuciscus idus 12 0.37 2 2–3 large sample size, we used an effect size index Asp Aspius aspius 27 0.84 3 1–3 ’ Nase Chondrostoma nasus 9 0.28 2 2–3 (Cohen s d; Cohen 1988) to measure differences in Topmouth Pseudorasbora parva 21 0.65 7 1–15 fish size. Effect size indices measure the magnitude gudgeon* of a treatment effect independently of sample size. Barbel Barbus barbus 160 4.95 10 1–12 – Cohen’s d is computed as the difference between two Bleak Alburnus alburnus 146 4.52 14 1 16 Silver bream Abramis bjoerkna 37 1.15 7 4–11 means divided by the pooled standard deviation and Common bream Abramis brama 215 6.66 10 1–13 its absolute value can range from 0 (perfect overlap Bitterling Rhodeus amarus 216 6.69 11 2–12 between two distributions) to infinity. Commonly, a Siluridae Wells Silurus glanis 1 0.03 1 3 d value of 0.8 is considered as a large effect size, Percidae corresponding to non-overlap of 47.3% between two Perch Perca fluviatilis 6 0.19 2 1–2 distributions and, therefore, we set this value as a Pikeperch Sander lucioperca 31 0.96 6 1–8 threshold. Only samples or sampling dates compris- Ruffe Gymnocephalus cernuus 2 0.06 1 2 Gobiidae ing at least five fish were considered in fish size anal- Tubenose goby* Proterorhinus semilunaris 325 10.06 8 1–9 ysis. All statistical analyses were conducted using R Round goby* Neogobius melanostomus 1420 43.96 16 1–16 2.14.2 (R Foundation for Statistical Computing, Vienna, Austria). *Denotes non-native species.

very start of the study, followed by a notable decline Results from the beginning of June (Fig. 2). The last tube- In total, 3 230 individuals of 18 species were cap- nose goby individuals were observed on the ninth tured, belonging to four families (Table 3). Round sampling date in mid-July (Fig. 2). goby were the most common fish in drift samples Most native fish species (roach, bream and barbel) (comprising over 40% of sampled fish), followed by also showed a decline in density following an initial native roach Rutilus rutilus and tubenose goby peak in late May/early June, with drift ceasing from (Table 3). Other native fish were less common, with mid-July (ninth sampling date; Fig. 2). Only bitter- only bitterling Rhodeus amarus, common bream ling and bleak showed multiple peaks and ceased Abramis brama, barbel Barbus barbus, bleak Albur- drifting later, though they both occurred in low densi- nus alburnus and silver bream Abramis bjoerkna ties from August onward (Fig. 2). comprising more than 1% of captured fish. Round gobies drifted almost exclusively at sizes Round goby were the only fish captured on all 16 ranging from 6 to 8 mm (Fig. 3), with no significant sampling dates, occurring in significantly more sam- change in size throughout the sampling season pling dates than both tubenose goby and all native (Fig. 3). All paired comparisons displayed an effect species (GLM, all d.f. = 1,30 and P <0.01), with the size of d < 0.8, with the exception of that between exception of bleak (GLM, d.f. = 1,30, P > 0.05). dates 1 and 12 with an effect size of d = 0.83 (most From mid-June (fourth sampling date) round goby likely the result of stochastic effects with no biologi- were the most common fish and from the start of cal explanation). Round gobies larger than 8 mm August (11th sampling date) were almost the only appeared in drift samples sporadically, with their fish found (Fig. 2). Round goby density displayed proportion increasing at the end of the season. multiple peaks that occurred throughout the study Drifting tubenose gobies mostly ranged from 5 to (Fig. 2). 8 mm (Fig. 3), with no change in size between May Tubenose goby were found on eight out of 16 23 and June 13 (sampling dates 1–4, Fig. 3; effect dates, and occurred at similar frequencies as native size d < 0.8 for all paired comparisons). Larger indi- species (GLM, all d.f. = 1,30 and P > 0.05), with viduals of tubenose goby occurred more frequently the exception of bleak that occurred more frequently than for round goby and were found in more sam- (GLM, d.f. = 1,30, P < 0.05). Tubenose goby pling dates (starting from the second sampling date, displayed a single peak in density in late May at the Fig. 3).

4 Downstream drift of non-native gobies

70 Neogobius melanostomus N. melanostomus ) –3 60 Rutilus rutilus 30

50 Proterorhinus semilunaris 10 40

10 Drift density (inds.1000 m

0 Fish size (SL, in mm) 0 2 4 6 8 10 12 14 16 May June July August 456789 16 12 3 4 5 67 8 910111213141516

) 14 May June July August –3 Rhodeus amarus 12 Abramis brama P. semilunaris 10 Barbus barbus 30 Alburnus alburnus 8 6 4 2 Drift density (inds.1000 m 0 0246810121416 May June July August Fish size (SL, in mm) Fig. 2. Seasonal patterns in density of fish drifting on the River Dyje in 2011. Species with dominance >10% are shown in the upper panel, species with dominance 2–10% in the lower panel, 45678910 species with dominance <2% are not shown. Note that different 123456789 scales are used on the y-axes. Sampling date number is presented May June July on the x-axis. Vertical lines separate months. Fig. 3. Size of N. melanostomus (upper panel) and P.semilunaris (lower panel) drifting on the River Dyje in 2011. Central lines = median, boxes = inter-quartile range, whiskers = non-out- Significant diel differences were recorded in drift lier range, points = outliers (i.e., points beyond 1.5 times the of round goby (GEE GLM, d.f. = 7,120, P < 0.001), inter-quartile range). On sampling dates with <5 fish caught, all with most fish drifting during the night (samples C, fish are drawn as points. Sampling date number is presented on D, E, and F; Fig. 4). Most drifting round gobies were the x-axis. Vertical lines separate months. Please note that the y-axes are denser above the 10 mm threshold (marked by dotted caught during the first night-time sample (C), with line) and that the x-axes differ between panels. numbers decreasing as the night progressed (Fig. 4). Drift intensity during the final night-time sample (F) drift had previously been suggested by Hayden & was similar to that for the sunset sample (B). Drift Miner (2009) based on the presence of young round intensity in daylight (A and H) and dawn (G) gobies in the pelagic zone of the Laurentian Great samples varied from low to none (Fig. 4). Lakes. The high drift frequency and abundance Significant diel differences were also observed in observed indicates that drift in these species was not drift of tubenose goby (GEE GLM, d.f. = 7,120, the result of an episodic catch of several individuals P < 0.001), with almost no fish drifting in daylight but a stable and large-scale phenomenon. Down- (A and H) or crepuscular samples (B and G), and stream drift of early life stages, therefore, may well relatively rich drift in night-time samples (Fig. 4). represent an effective dispersal mechanism in gobies, Significantly lower numbers of tubenose goby were as it is for non-native aquatic invertebrates (Stoeckel observed drifting in the second night-time sample (D) et al. 2004; Van Riel et al. 2011) and plants (Dawson compared to other night-time samples, none of which & Holland 1999; Jacquemyn et al. 2010). differed from each other (Fig. 4). For both round and Our results (Fig. 2) indicate that we missed the tubenose goby, size of drifting fish did not differ start of the sampling season and, therefore, the % among samples (effect size d < 0.8 for all paired proportion of fish drifting early (e.g., tubenose goby, comparisons in both species). common bream and barbel) may have been underestimated. Nevertheless, we are convinced that species proportion within the sampled assemblage was only Discussion slightly biased. The start of sampling season (May To our knowledge, this is the first comprehensive 23) was determined based on the results of our study to describe drift of early life stages of round preceding drift study in the Dyje (Janac et al. 2013). and tubenose goby in newly colonised rivers. Such It appears that higher water temperatures in 2012,

5 Janac et al.

120 A single density peak was recorded in late May for

100 N. melanostomus tubenose goby; however, the similarity in fish size between sampling dates suggests that tubenose goby 80 f spawned continuously, though for a shorter period

60 compared to round goby. The tubenose goby seasonal drift pattern did not differ from that of native 40 fish, which is in opposition to the findings of Zitek e d 20 ccet al. (2004) and our data on drift from the Nove a b b Mlyny reservoir into the River Dyje (Janac et al.

Number of drifting fish per sample 0 ABCDEFGH 2013). Both of these studies also showed a single 60 peak in tubenose goby drift density; however, both P. semilunaris noted protracted drift (at least 2 months) lasting 50 longer than that of other cyprinid and percid species. 40 Round goby were absent in these studies, suggesting

30 that the presence of this species may somehow limit the spawning of tubenose goby (e.g., through compe- 20 d d tition for spawning habitat, which is identical in both d 10 c species; Miller 2004a,b). This assumption is sup- a a a b ported by the complementarity in drift season

Number of drifting fish per sample 0 ABCDEFGH between these species; the tubenose goby peak end- Sample ing in early June just as the round goby peak starts. Fig. 4. Numbers of fish drifting in separate samples (estimates It should be noted, however, that the observed pattern resulting from generalised estimating equations GLM). Samples could also originate from different spawning or were collected 1 h before dusk (A), at dusk (B), 1 h after dusk developmental times. Moreover, some of the tube- (C), 2.5 h after dusk (D), 2.5 h before dawn (E), 1 h before dawn nose gobies caught may have originated from the = (F), at dawn (G), and 1 h after dawn (H). Bars mean values, upper sections of the Dyje, where round gobies are whiskers = confidence intervals. Different letters above bars indicate significant differences according to multiple post-hoc com- absent (see below), and for which competition is not parisons. a factor. The size of drifting round goby in the Dyje was however, triggered earlier spawning and drift. Based similar to that in its native range (Vassilev 1994). on water temperature measurements obtained later, Moreover, the size range matched the size of round we back-calculated that sampling started 50 days gobies sampled from the pelagic zone of the Lauren- after the water temperature reached 10 °C (Fig. 1). tian Great Lakes (Hensler & Jude 2007; Hayden & Drifting patterns in nearby rivers (Reichard et al. Miner 2009), suggesting that movement to the pela- 2002a; Zitek et al. 2004; Reichard & Jurajda 2007; gic zone and riverine drift are closely related (see Janac et al. 2013) suggest drift starts approximately Pavlov et al. 2002). The narrow size range of drifting 40 days after water temperatures consistently reach round goby was maintained throughout the drifting 10 °C. Thus, we are convinced that the drift season season, documenting that drift is restricted to a began no earlier than around ten days before the start specific ontogenetic stage defined by an interval of of our study and that all density peaks were covered several days. The minimum size observed in this by the study. study was just above that determined by Logachev & Unlike native fish, round gobies drifted at high Mordvinov (1979) for round gobies 3 days after densities throughout most of the sampling season hatching. Similarly, the size range of drifting tube- (from late May to late August). As drift is generally nose gobies did not differ substantially from that considered to be a function of when fish spawn observed in the Danube (Vassilev 1994; Zitek et al. (Brown & Armstrong 1985), the round goby drift 2004), corresponding to several days after hatching pattern suggests multiple spawning events, or rather (Miller 2004b). The limitation of drift to a specific continuous spawning throughout the season as ontogenetic stage appears to be more relaxed in the drifting fish were caught within a narrow size interval tubenose goby as their size range was larger com- during all sampling dates. This would give the round pared to round goby, with larger individuals also goby an advantage over native species (with the occurring more frequently (see also Zitek et al. exception of bleak, whose drift densities were, how- 2004). ever, low) as an extended spawning period would The larger size range of tubenose goby may also increase the probability of a proportion of drifting reflect fish range in the river stretch above our study young encountering optimal conditions for recruit- site. The range of occurrence of round goby ends ment (Zitek et al. 2004). approximately 8 km upstream of our site, while that

6 Downstream drift of non-native gobies of tubenose goby extends much further upstream. drift cessation due to negative buoyancy has not yet Larger tubenose gobies may have originated from been proved, however, and some studies question its beyond the range of round goby, having had longer occurrence (Maeda & Tachihara 2010). to grow. This hypothesis, however, relies on gobies Third, night-time drift patterns were not species drifting for long distances. Drifting for tens to hun- specific (as suggested by the previous scenarios), but dreds of km has been documented in pelagic spawn- reflect species’ range upstream from the study site. ing fish (e.g., Widmer et al. 2012), but no data on Assuming that all individuals react concurrently to a drift distances are available for negatively-buoyant drift stimulus, were equally likely to cease drifting, gobiids; thus stressing the importance of further stud- and could drift at least several kilometres during one ies dealing with gobiid drift. night, then the expected night-time drift pattern Goby drift was limited during the crepuscular peri- would match that observed in our study. Combining ods, a major increase in drift density being observed data on dark period duration (approximately 7.28 h) in the first night-time sample for both species. Sev- and range of water velocity measured at the nets eral previous studies have observed the same pattern (approximately 0.2–0.4 mÁsÀ1), the distance travelled in other species, with largest numbers of drifting fish by drifting gobies along the Dyje can be roughly always being captured during the first hour following established at 5.2–10.4 km per night, suggesting that a drop in light intensity below 1 lux (Pavlov et al. the hypothesis is at least possible. While such esti- 1977; Iguchi & Mizuno 1990; Persat & Olivier mates serve as a theoretical ‘exercise’ only (Hayden 1995). Indeed, for many species, a drop in light & Miner 2009), they highlight the need for ‘actual’ intensity below a threshold value is considered to be data on drift distance. the stimulus that activates either an ontogenetically- This study documented that young round and specific ascent to the water’s surface and/or ceasing tubenose gobies commonly undergo a downstream of rheoreaction, resulting in downstream drift (Pavlov drift in the newly colonised rivers. Further studies et al. 1968; Pavlov 1994). should reveal the population consequences of goby In round goby, the vast majority of fish were drift (see Lutscher et al. 2010 for the theoretical con- observed drifting during the first night-time sample, cept) and its role as regards dispersal into new areas. with a gradual decrease from then on, whereas tube- As an example, drifting fish may support down- nose gobies drifted at similar densities throughout the stream dispersal from points of anthropogenic intro- night. The trend for round goby corresponds well duction (see Borcherding et al. 2011; Janac et al. with night-time drift patterns for other species (e.g., 2012). On the other hand, in areas where gobies are Pavlov et al. 1977; Bardonnet et al. 1993; Johnston dispersing upstream (majority of cases, see for 1997; Oesmann 2003; Maeda & Tachihara 2010), example Poos et al. 2010), downstream drift of early while literature support for the tubenose goby trend is life stages can lead to (a) deceleration of population lower (Gale & Mohr 1978; Brown & Armstrong establishment at the front of the migration wave and/ 1985; Bardonnet et al. 1993). We suggest that three or (b) filling of gaps between long-distance dispers- scenarios could be responsible for the differences in ing ‘pioneers’ and the slower-dispersing population night-time drift pattern in round and tubenose gobies. behind (see Bronnenhuber et al. 2011 for dispersal First, fish did not react concurrently to a drift stim- patterns of round goby). In the latter case, the move- ulus, but individuals reacted at different times and ment of long-distance pioneers (moving as much as the proportion of such fish differed between the two 50 m per day; Bronnenhuber et al. 2011; Lynch & species. Individual differences in propensity to drift Mensinger 2012) and subsequent drift of their prog- have been indicated by Pavlov et al. (1968), who eny may result in establishing populations over large suggested they were connected with changing size of areas in a relatively short period. To address such drifting fish (see also Sonny et al. 2006). Note, how- predictions, it is essential that three questions are ever, that the size of drifting fish did not differ during answered: (i) what is the distance that can be cov- the night in the present study. ered by drifting fish, (ii) what proportion of a cohort Second, individuals of both species reacted concur- undergoes downstream drift, and (iii) what is the rently to a drift stimulus, but differed in drift cessa- mortality level in drifting gobies. Further studies, tion due to differences in negative buoyancy (Iguchi therefore, should focus on answering these ques- & Mizuno 1991). The concurrent response of all indi- tions. viduals to a stimulus is a plausible hypothesis as drift studies conducted in the laboratory, or in very short Acknowledgement rivers, have shown both a rapid increase and rapid decline in drift density (i.e., in terms of hours; Iguchi This study was supported by the Grant Agency of the Czech & Mizuno 1990; Persat & Olivier 1995; Maeda & Republic, Grant No. P505/11/1768, and through institutional Tachihara 2010; but see Bardonnet et al. 1993). Early support grant no. RVO:68081766. We thank M. Vasek,

7 Janac et al.

G. Konecna, M. Konickova, L. Vsetickova, K. Roche, the exotic plant species Sisymbrium austriacum: evidence M. Konecna, K. Halacka, I. Slovackova, and V. Michalkova for long-distance seed dispersal. Biological Invasions 12: for help with fieldwork, and K. Roche for valuable comments 553–561. and help in preparing the English version of the manuscript. Janac, M., Valova, Z. & Jurajda, P. 2012. Range expansion and We thank three anonymous reviewers for their comments on a habitat preferences of non-native 0+ tubenose goby (Protero- previous version of the manuscript. We are much indebted to rhinus semilunaris) in two lowland rivers in the Danube representatives of the Moravian Angling Union for allowing basin. Fundamental and Applied Limnology 181: 73–85. research in their waters. River discharge and temperature data Janac, M., Jurajda, P., Kruzikova, L., Roche, K. & Prasek, P. were obtained from the Czech Hydrometeorological Institute 2013. Reservoir-to-river passage of 0+ fish – indication of a in Brno. dispersion pathway for a non-native species. Journal of Fish Biology, DOI: 10.1111/jfb.12037. Johnston, T.A. 1997. Downstream movements of young-of- References the-year fishes in Catamaran Brook and the Little Southwest Bardonnet, A., Gaudin, P. & Thorpe, J.E. 1993. Diel rhythm of Miramichi River, New Brunswick. Journal of Fish Biology – emergence and of 1st displacement downstream in trout 51: 1047 1062. (Salmo trutta), Atlantic salmon (S. salar) and grayling Koblickaya, A.F. 1981. Key for identifying young freshwater (Thymallus thymallus). Journal of Fish Biology 43: 755–762. fishes. Moscow: Light and Food Industry Publishing House. Borcherding, J., Staas, S., Kruger, S., Ondrackova, M., 208 pp. Slapansk y, L. & Jurajda, P. 2011. Non-native Gobiid species Kocovsky, P.M., Tallman, J.A., Jude, D.J., Murphy, D.M., in the lower River Rhine (Germany): recent range extensions Brown, J.E. & Stepien, C.A. 2011. Expansion of tubenose and densities. Journal of Applied Ichthyology 27: 153–155. gobies Proterorhinus semilunaris into western Lake Erie Bronnenhuber, J.E., Dufour, B.A., Higgs, D.M. & Heath, D. and potential effects on native species. Biological Invasions – D. 2011. Dispersal strategies, secondary range expansion 13: 2775 2784. and invasion genetics of the nonindigenous round goby, Kornis, M.S., Mercado-Silva, N. & Vander Zanden, M.J. Neogobius melanostomus, in Great Lakes tributaries. Molec- 2012. Twenty years of invasion: a review of round goby ular Ecology 20: 1845–1859. Neogobius melanostomus biology, spread and ecological – Brown, A.V. & Armstrong, M.L. 1985. Propensity to drift implications. Journal of Fish Biology 80: 235 285. downstream among various species of fish. Journal of Fresh- Logachev, V.S. & Mordvinov, Y.E. 1979. Speed swimming water Ecology 3: 3–17. and activity of larvae of the round goby Neogobius melano- Cohen, J. 1988. Statistical power analysis for the behavioral stomus Pall, and some predatory crustaceans of the Black – sciences. Hillsdale, NJ: Lawrence Earlbaum Associates. 569 Sea. Biologia Morya 3: 77 80. pp. Lusk, S., Luskova, V. & Hanel, L. 2010. Alien fish species in Cookingham, M.N. & Ruetz, C.R. 2008. Evaluating passive the Czech Republic and their impact on the native fish – integrated transponder tags for tracking movements of round fauna. Folia Zoologica 59: 57 72. gobies. Ecology of Freshwater Fish 17: 303–311. Lutscher, F., Nisbet, R.M. & Pachepsky, E. 2010. Population Dawson, F.H. & Holland, D. 1999. The distribution in bank- persistence in the face of advection. Theoretical Ecology 3: – side habitats of three alien invasive plants in the UK in rela- 271 284. tion to the development of control strategies. Hydrobiologia Lynch, M.P. & Mensinger, A.F. 2012. Seasonal abundance 415: 193–201. and movement of the invasive round goby (Neogobius mela- Gale, W.F. & Mohr, H.W. 1978. Larval fish drift in a large nostomus) on rocky substrate in the Duluth-Superior Harbor – river with a comparison of sampling methods. Transactions of Lake Superior. Ecology of Freshwater Fish 21: 64 74. of the American Fisheries Society 107: 46–55. Maeda, K. & Tachihara, K. 2010. Diel and seasonal occur- Hayden, T.A. & Miner, J.G. 2009. Rapid dispersal and estab- rence patterns of drifting fish larvae in the Teima stream, – lishment of a benthic Ponto-Caspian goby in Lake Erie: diel Okinawa Island. Pacific Science 64: 161 176. vertical migration of early juvenile round goby. Biological Marentette, J.R., Wang, G., Tong, S., Sopinka, N.M., Taves, Invasions 11: 1767–1776. M.D., Koops, M.A. & Balshine, S. 2011. Laboratory and Hensler, S.R. & Jude, D.J. 2007. Diel vertical migration of field evidence of sex-biased movement in the invasive round – round goby larvae in the Great Lakes. Journal of Great goby. Behavioral Ecology and Sociobiology 65: 2239 2249. Lakes Research 33: 295–302. Miller, P.J. 2004a. The Freshwater Fishes of Europe, Vol 8/I Hojsgaard, S., Halekoh, U. & Yan, J. 2006. The R Package Gobiidae. Wiesbaden: Aula-Verlag. 404 pp. geepack for Generalized Estimating Equations. Journal of Miller, P.J. 2004b. The Freshwater Fishes of Europe, Vol 8/II Statistical Software 15: 1–11. Gobiidae 2. Wiesbaden: Aula-Verlag. 478 pp. Iguchi, K.I. & Mizuno, N. 1990. Diel changes of larval drift Oesmann, S. 2003. Vertical, lateral and diurnal drift patterns among amphidromous gobies in Japan, especially Rhinogo- of fish larvae in a large lowland river, the Elbe. Journal of – bius brunneus. Journal of Fish Biology 37: 255–264. Applied Ichthyology 19: 284 293. Iguchi, K.I. & Mizuno, N. 1991. Mechanisms of embryonic Pavlov, D.S. 1994. The downstream migration of young fishes drift in the amphidromous goby, Rhinogobius brunneus. in rivers - mechanisms and distribution. Folia Zoologica 43: – Environmental Biology of Fishes 31: 295–300. 193 208. Jacquemyn, H., Van Looy, K., Breyne, P. & Honnay, O. Pavlov, D.S., Sbikin, Y.N. & Mochek, A.D. 1968. The effect 2010. The Meuse river as a corridor for range expansion of of illumination in running water on the speed of fishes in

8 Downstream drift of non-native gobies

relation to features of their orientation. Voprosy ikhthiologii in a small tributary of the Meuse River, Belgium. Folia Zoo- 8: 250–255. logica 55: 75–85. Pavlov, D.S., Pakhorukov, A.M., Kuragina, G.N., Nezdolii, Stoeckel, J.A., Rehmann, C.R., Schneider, D.W. & Padilla, D. V.K., Nekrasova, N.P., Brodskii, D.A. & Ersler, A.L. 1977. K. 2004. Retention and supply of zebra mussel larvae in a Some peculiarities of downstream migrations of young large river system: importance of an upstream lake. Fresh- fishes in the Volga and Kuban rivers. Voprosy ikhthiologii water Biology 49: 919–930. 17: 415–428. Tierney, K.B., Kasurak, A.V., Zielinski, B.S. & Higgs, D.M. Pavlov, D.S., Lupandin, A.I. & Kostin, V.V. 2002. Down- 2011. Swimming performance and invasion potential of the stream migration of fish through dams of hydroelectric round goby. Environmental Biology of Fishes 92: 491–502. power plants. Oak Ridge, Tennessee: Oak Ridge National Van Riel, M.C., Van der Velde, G. & De Vaate, A.B. 2011. Laboratory. 249 pp. Dispersal of invasive species by drifting. Current Zoology Persat, H. & Olivier, J.M. 1995. The first displacements in the 57: 818–827. early stages of Chondrostoma nasus under experimental con- Vasek, M., Juza, T., Cech, M., Kratochvõl, M., Prchalova, M., ditions. Folia Zoologica 44: 43–50. Frouzova, J., RIha, M., Tuser, M., Sed’a, J. & Kubecka, J. Poos, M., Dextrase, A.J., Schwalb, A.N. & Ackerman, J.D. 2011. The occurrence of non-native tubenose goby Protero- 2010. Secondary invasion of the round goby into high diver- rhinus semilunaris in the pelagic 0+ year fish assemblage of sity Great Lakes tributaries and species at risk hotspots: a central European reservoir. Journal of Fish Biology 78: potential new concerns for endangered freshwater species. 953–961. Biological Invasions 12: 1269–1284. Vassilev, M. 1994. On the downstream migration of ichthyo- Prasek, V. & Jurajda, P. 2005. Expansion of Proterorhinus plankton along the Bulgarian shore of the Danube river. Vie marmoratus in the Morava River basin (Czech Republic, Et Milieu 44: 273–280. Danube R. watershed). Folia Zoologica 54: 189–192. Widmer, A.M., Fluder, J.J., Kehmeier, J.W., Medley, C.N. & Reichard, M. & Jurajda, P. 2007. Seasonal dynamics and age Valdez, R.A. 2012. Drift and retention of pelagic spawning structure of drifting cyprinid fishes: an interspecific compari- minnow eggs in a regulated river. River Research and Appli- son. Ecology of Freshwater Fish 16: 482–492. cations 28: 192–203. Reichard, M., Jurajda, P. & Ondrackova, M. 2002a. Interannu- Zitek, A., Schmutz, S. & Ploner, A. 2004. Fish drift in a Dan- al variability in seasonal dynamics and species composition ube sidearm-system: II. Seasonal and diurnal patterns. Jour- of drifting young-of-the-year fishes in two European low- nal of Fish Biology 65: 1339–1357. land rivers. Journal of Fish Biology 60: 87–101. Zuur, A.F., Ieno, E.N., Walker, N., Saveliev, A.A. & Smith, Reichard, M., Jurajda, P. & Ondrackova, M. 2002b. The effect G.M. 2009. Mixed Effects Models and Extensions in Ecol- of light intensity on the drift of young-of-the-year cyprinid ogy with R. New York: Springer-Verlag. 574 pp. fishes. Journal of Fish Biology 61: 1063–1066. Sonny, D., Jorry, S., Watriez, X. & Philippart, J.C. 2006. Inter-annual and diel patterns of the drift of cyprinid fishes

9 Publikace E

Early life stages of exotic gobiids as new host for unionid glochidia

Šlapanský, L., Jurajda, P. & Janáč, M. (2016)

Freshwater Biology, 61, 679-690.

Freshwater Biology (2016) 61, 979–990 doi:10.1111/fwb.12761

Early life stages of exotic gobiids as new hosts for unionid glochidia

1,2 1 1 LUDEK SLAPANSKY , PAVEL JURAJDA AND MICHAL JANAC 1Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Brno, Czech Republic 2Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic

SUMMARY

1. Introduction of an exotic species has the potential to alter interactions between fish and bivalves; yet our knowledge in this field is limited, not least by lack of studies involving fish early life stages (ELS). 2. Here, for the first time, we examine glochidial infection of fish ELS by native and exotic bivalves in a system recently colonised by two exotic gobiid species (round goby Neogobius melanostomus, tubenose goby Proterorhinus semilunaris) and the exotic Chinese pond mussel Anodonta woodiana. 3. The ELS of native fish were only rarely infected by native glochidia. By contrast, exotic fish displayed significantly higher native glochidia prevalence and mean intensity of infection than native fish (17 versus 2% and 3.3 versus 1.4 respectively), inferring potential for a parasite spillback/ dilution effect. Exotic fish also displayed a higher parasitic load for exotic glochidia, inferring potential for invasional meltdown. Compared to native fish, presence of gobiids increased the total number of glochidia transported downstream on drifting fish by approximately 900%. 4. We show that gobiid ELS are a novel, numerous and ‘attractive’ resource for unionid glochidia. As such, unionids could negatively affect gobiid recruitment through infection-related mortality of gobiid ELS and/or reinforce downstream unionid populations through transport on drifting gobiid ELS. These implications go beyond what is suggested in studies of older life stages, thereby stressing the importance of an holistic ontogenetic approach in ecological studies.

Keywords: ﬁsh larvae, Gobiidae, host–parasite interaction, invasive species, Unionidae

parasites typically achieve high densities (Dunn, 2009). Introduction An exotic host, therefore, can act as a reservoir for Introduction of a new species inevitably results in alternative parasites, increasing the likelihood of native host ations to previously established interactions, including infection (‘parasite spillback’; Kelly et al., 2009a). Alter- those between hosts and parasites. The enemy release natively, if it is an unsuitable host (i.e. the parasite hypothesis (Mitchell & Power, 2003; Torchin et al., 2003) attaches but fails to develop to its next life stage), exotic suggests that establishment of some exotic species is species can act as an infection sink, reducing the pool of supported by insufficient regulation by native predators parasites that could potentially infect native hosts (‘dilu- and parasites. Exotic species are thought to benefit from tion effect’; Kelly et al., 2009b). Exotic parasites, on the a loss of parasite diversity as a consequence of leaving other hand, may take advantage of native host naivety parasites behind and the inability of native-specialised to become successful in the novel system (‘parasite pol- parasites (i.e. those that require specific hosts for suc- lution’; Daszak, Cunningham & Hyatt, 2000). Presence cessful development) to infect the exotic host. As a of a previously established exotic host may also facilitate result, exotic hosts tend to be parasitised by a low num- establishment of exotic parasites (‘invasional meltdown’; ber of generalist native parasite species (Kennedy & Simberloff & Von Holle, 1999), particularly when native Bush, 1994; Poulin & Mouillot, 2003), though these parasites utilise this novel resource suboptimally.

Correspondence: Michal Janac, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Kvetna 8, Brno, 603 65, Czech Republic. E-mail: [email protected]

© 2016 John Wiley & Sons Ltd 979 980 L. Slapansky et al. Testing of such theoretical approaches is typically facilitated through ecosystem changes caused by an ear- restricted to ontogenetic stages that are easy to capture, lier large-scale invasion by the zebra mussel, Dreissena breed, observe and/or identify. Life stages not comply- polymorpha, which forms one of its major food sources ing with these conditions (e.g. larval stages) are usually (Simberloff & Von Holle, 1999). At the same time, it was ignored (see Rius et al., 2014 for an exception), despite believed that the gobiids threatened numerous popula- the likelihood that their traits and/or niche may differ tions of native unionids with specialised glochidia by from more easily studied stages. Fish early life stages outcompeting and reducing populations of their specific (ELS), for example, often differ in physiology, behaviour glochidial fish hosts (Strayer, 1999; Poos et al., 2010). and habitat preference from the older life stages (Garner, Gobiid invaders in both Europe and North America are 1997), meaning that inter-stage differences may exist in known to act as hosts to generalist glochidia of native probability of parasite encounter or transfer. Despite the bivalves, suggesting the potential for a parasite spillback important contribution of fish ELS to the success of the and/or dilution effect, with unknown effects on both species as a whole (Garner, 1997), they are only rarely host and parasite populations (Muzzal, Peebles & Tho- included in parasitological studies (see Grutter et al., mas, 1995; Ondrackova et al., 2005; Kvach & Winkler, 2010 for exception). This motivated us to focus on fish 2011). This situation is further complicated as invasion ELS while studying the role of exotic species in a fish- of exotic unionid bivalves may also alter fish-bivalve bivalve host–parasite system. interactions. The successful worldwide invasion of the Unionid bivalves (Unionidae) are among the world’s freshwater Chinese pond mussel, Anodonta (Sinanodonta) most endangered animal taxa (Lydeard et al., 2004), with woodiana, for example, has been attributed to its broad habitat degradation, pollution, excessive harvesting and host generalism (Douda et al., 2012). As a direct conse- introduction of exotic species all contributing to their quence, presence of this unionid has completely unfavourable conservation status (Bogan, 1993; Cope reversed the host– et al., 2008). Unionid populations are particularly vulner- parasite relationship between European bitterling, able due to their dependence on fish, which play an Rhodeus amarus, and native unionid bivalves (Reichard essential role in the unionid life cycle (Barnhart, Haag & et al., 2012). Roston, 2008). Unionid larvae, known as a ‘glochidia’ , Previous studies of fish-bivalve interactions have are an obligate external parasite of fish. After release tended to consider the relationship between bivalves from the maternal mussel, the glochidia must rapidly and adult fish only. Fish ELS have usually (and in gobi- attach to a fish’s skin or gill, where it encapsulates and ids, always) been omitted in parasitological studies (see lives on the host’s body fluids (Haag & Staton, 2003). Kelly et al., 2010a,b; Timi, Luque & Poulin, 2010 for The glochidium will then develop into a juvenile mussel exceptions), despite representing an important target over several days to months (Zimmerman & Neves, due to their abundance and the increased impact of each 2002). Though the parasitic period may be short relative parasite on each individual (Grutter et al., 2010). More- to the typical lifespan of a unionid (ranging from 6 to over, gobiid ELS display different dispersal patterns to 100 years Aldridge, 1999), this stage is central to both older fish, with ELS passively dispersing downstream the survival and dispersal of mussel populations (Sch- by drifting with the current (Hayden & Miner, 2009; walb & Pusch, 2007), especially considering the very low Janac et al., 2013 a,b) and older fish tending to be more dispersal ability of adult mussels. sedentary or showing a preference for moving upstream Several Ponto-Caspian gobiids, a large family of bot- (Bronnenhuber et al., 2011). tom-dwelling fish, have spread from their native area In this study, we examine glochidial infection of both into numerous major water systems across Europe and native (mostly cyprinid) and exotic (gobiid) fish ELS in a North America since 1990s (Jude, Reider & Smith, 1992; river recently colonised by two gobiid species, N. me- Roche, Janac & Jurajda, 2013). It is generally believed lanostomus and the Western tubenose goby, Proterorhinus that the invasion of gobiids into new ecosystems threat- semilunaris, and an exotic unionid species, A. woodiana ens native species (e.g. Poos et al., 2010; Kornis, Mer- (colonising events independent of each other). We test cado-Silva & Vander Zanden, 2012). Indeed, there is whether exotic gobiids are able to host native and exotic some evidence that interactions between invading gobi- mussel glochidia, and whether exotic mussel glochidia ids and bivalve communities may play an important role are able to infect native and exotic hosts. We predict that in their overall effect on the native ecosystem. For exam- (i) gobiid ELS will demonstrate a higher parasitic load ple, invasion of the round goby, Neogobius melanostomus, of native mussel glochidia than native ELS, raising the into the Laurentian Great Lakes is believed to have been potential for parasite spillback/dilution in this age

© 2016 John Wiley & Sons Ltd, Freshwater Biology, 61, 979–990 Glochidia on gobiid early life stages 981 group; (ii) exotic mussel glochidia will be more success- examined under a stereomicroscope, whereupon any ful at infecting naive native hosts than glochidia of glochidia were identiﬁed according to Pekkarinen & native mussels and (iii) exotic mussel glochidia will be Englund (1995) and our own comparative material (ripe able to utilise exotic hosts, raising the potential for inva- glochidia collected from the gills of adult ﬁsh at the sional meltdown (i.e. gobiid ELS will be infected by all study stretch), counted and location on the host’s body generalist glochidia, whether exotic or native). noted.

Data analysis Methods For the purposes of data analysis, all native fish spe- Study site cies and both gobiid species captured were pooled as This study took place on the River Dyje (Czech Repub- ‘native fish’ and ‘exotic fish’, respectively, as we lic), near the town of Breclav (48°44030.079″N, wanted to stress the differences between the pool of 16°53031.366″E), 22 km from its confluence with the native fish hosts available before gobiid invasion and River Morava, a main tributary of the River Danube. the novel hosts available as a consequence of the inva- The study stretch is channelised and the bank is sion. strengthened with 10–50 cm rip-rap. The river has a In order to highlight the different roles played by wet-width of 45 m, a maximum depth of 1.5 m and a native and gobiid ELS in glochidial transport, we quanti- mean annual discharge of 41 m3 s 1. fied density of glochidia transported downstream on Proterorhinus semilunaris colonised the study site in these two types of fish host on each sampling date as 1998 (Janac, Valova & Jurajda, 2012) and N. melanostomus the number of individuals per 1000 m3 of filtered water. in 2008 (Lusk, Luskova & Hanel, 2010). Both species were Density (d) was calculated as d = n/V, where n = the abundant by 2011 and their ELS were the most abundant total number of glochidia recorded on all fish from a in the fish ELS assemblage (Janac et al., 2013a). The native net, and V = the volume of water filtered during net fish assemblage comprised mostly cyprinids (Rutilus ruti- exposure in m3 (for more details on calculation of V, see lus, Rhodeus amarus, Abramis brama, Barbus barbus and Janac et al., 2013a). Alburnus alburnus; for common names see Table 1). Three glochidial infection parameters were deter- Anodonta woodiana reached the study site around 2006 mined: (i) prevalence – the proportion of infected hosts (Beran, 2013), with mussel colonisation being indepen- among all hosts examined; (ii) mean intensity of infec- dent of gobiid colonisation. Malacological studies (e.g. tion – the mean number of parasites found on infected Beran, 2013) have confirmed the presence of a unionid hosts and (iii) distribution of glochidia on host bodies community at the study site, consisting of swollen river – the total number of glochidia recorded on pectoral mussels, Unio tumidus Philipsson 1788, and duck mus- fins, ventral fins (or sucking disc in the case of gobi- sels, Anodonta anatina Linnaeus, 1758 (both native), along ids), anal fin, caudal fin, dorsal fin, mouth and opercu- with the exotic A. woodiana. lae. No glochidia were found attached to any other body part. Differences in prevalence and intensity of infection Data sampling were tested using generalised linear models (GLM), with Samples were obtained at weekly intervals from 23 May binomial (Bernoulli) distribution detected for prevalence to 5 September, 2011 (16 sampling dates). On each sam- and Poisson distribution (for analyses corrected for over- pling date, four drift nets were exposed for a total of dispersion, i.e. quasi-Poisson) for intensity of infection. 240 min (see Janac et al., 2013a for details) spread over To demonstrate whether glochidial load differs between the course of the night (fish drift occurring mainly at exotic and native fish ELS, we tested for differences in night; Janac et al., 2013a,b). All fish from each net were prevalence and intensity of infection between the groups overdosed with clove oil and preserved separately in 4% (corresponding to the categorical predictor ‘fish origin’) formaldehyde. In the laboratory, the fish were identified separately for exotic mussel, native mussels and all glo- according to Koblickaya (1981) and our own collection chidia together. In these models, ‘fish size’ (SL; centred of comparative material and measured to the nearest and scaled before analysis) was added as a covariate 0.01 mm [standard length, SL; gobiid ELS ranged in size based on the known relationship between infection rate from 4.1 to 15.1 mm (median 6.8 mm) and native ELS and fish size. To demonstrate whether native or exotic from 5.1 to 41.5 mm (median 13.2 mm)]. The fish were glochidia are more successful in infecting fish ELS, we

Table 1 Glochidia infection on fish drifting in the River Dyje in 2011. Number of fish examined (n), number infected (n inf), prevalence (prev, in %) and mean intensity of infection (MII) are shown for native Unio tumidus, exotic Anodonta woodiana and both (Total). Note that some fish were infected by both bivalve genera concurrently. Species for which >40 individuals were examined (minimum number required to precisely estimate infection parameters; Marques & Cabral, 2007) are marked in bold.

Total A. woodiana U. tumidus

Common name Scientiﬁc name n n inf prev MII n inf prev MII n inf prev MII

Round goby Neogobius melanostomus* 1395 290 20.8 3.0 149 10.7 1.6 178 12.8 3.7 Roach Rutilus rutilus 525 54 10.3 1.1 48 9.1 1.1 7 1.3 1.0 Tubenose goby Proterorhinus semilunaris* 320 132 41.3 3.0 44 13.8 2.4 109 34.1 2.7 European bitterling Rhodeus amarus 212 5 2.4 1.4 4 1.9 1.5 1 0.5 1.0 Common bream Abramis brama 206 8 3.9 1.1 4 1.9 1.0 4 1.9 1.3 Barbel Barbus barbus 155 19 12.3 1.2 17 11.0 1.2 2 1.3 1.5 Bleak Alburnus alburnus 134 7 5.2 1.0 5 3.7 1.0 2 1.5 1.0 White bream Blicca bjoerkna 34 2 5.9 2.0 2 5.9 2.0 Pikeperch Sander lucioperca 27 9 33.3 1.9 5 18.5 1.6 4 14.8 2.3 Asp Aspius aspius 25 1 4.0 1.0 1 4.0 1.0 † Topmouth gudgeon Pseudorasbora parva 20 2 10.0 1.5 2 10.0 1.5 Ide Leuciscus idus 12 3 25.0 1.3 3 25.0 1.3 – Nase Chondrostoma nasus 9 1 11.1 3.0 1 11.1 3.0 Perch Perca ﬂuviatilis 6 2 33.3 1.0 2 33.3 1.0 Chub Leuciscus cephalus 4 Ruffe Gymnocephalus cernuus 2 – Dace Leuciscus leuciscus 1 Native 1372 113 8.2 1.2 91 6.6 1.2 23 1.7 1.4 Exotic* 1715 422 24.6 3.0 193 11.3 1.8 287 16.7 3.3 Total 3087 535 17.3 2.7 284 9.2 1.6 310 10.0 3.1

† Species not native to the system but long established (>25 years); not counted as an exotic in this study. * Exotic species. tested for the differences in prevalence and intensity of Prevalence and intensity of infection infection on native fish and exotic fish separately, with glochidial origin (exotic versus native mussels) being the Exotic fish displayed significantly higher prevalence and only predictor considered. Separate models were then intensity of glochidial infection than native fish (GLM, both constructed for each combination of native fish, exotic P < 0.001; Tables 1 & 2). The same results were obtained fish and mussel, to demonstrate the relationships when testing separately for A. woodiana (GLM, both between fish size and prevalence or mean intensity of P < 0.001; Tables 1 & 2) and U. tumidus glochidia (GLM, infection. Differences in distribution of glochidia on the prevalence P < 0.001, intensity P < 0.05; Tables 1 & 2). host’s body were assessed using Chi squared (v2) tests. A. woodiana glochidia infected native fish significantly All statistical analyses were conducted using R version more often than native U. tumidus glochidia (prevalence 2.14.2 (R Core Team 2012). 6.6 and 1.7% respectively; GLM, P < 0.001; Table 2). Both glochidia species displayed similar intensity of infection on native fish (A. woodiiana 1.2 and U. tumidus Results 1.4 glochidia per infected fish; GLM, P > 0.05, Table 2). Overall, we examined 3087 fish of 17 species, of which In contrast, U. tumidus glochidia displayed significantly 535 fish of 14 species were infected with glochidia higher prevalence and intensity of infection than (17.3%; see Table 1 for species-specific infection rates). In A. woodiana glochidia on exotic fish (A. woodiana 11.3% total, 460 A. woodiana glochidia were detected on 284 prevalence and 1.8 mean intensity of infection, U. tu- fish of 12 species and 959 U. tumidus glochidia on 310 midus 16.7% and 3.3; GLM, both P < 0.001; Table 2). fish of 10 species. We counted 1281 glochidia on gobiids No effect of fish size was observed for prevalence and and 138 glochidia on native fish. Fifty-nine fish had glo- intensity of U. tumidus infection on exotic fish (GLM, chidia of both A. woodiana and U. tumidus concurrently, P = 0.472 and 0.492; Figs 1 & 2). On the other hand, of which 37 were N. melanostomus,21P. semiunaris and prevalence and intensity of A. woodiana infection on exo- one R. rutilus.NoA. anatina glochidia were detected on tic fish increased significantly with increasing body any fish examined. length (GLM, both P < 0.001). Both prevalence and

Table 2 Parameters of generalised linear models testing for differences in prevalence and intensity of infection between native and exotic fish and bivalves. Degrees of freedom (d.f.), deviance explained (dev) and significance (P) of each predictor in the model is shown, as well as null deviance and null d.f. Significant values (P < 0.05) are in bold.

A. woodiana U. tumidus Total

Predictor d.f. dev P d.f. dev P d.f. dev P

(a) Native versus exotic ﬁsh: prevalence # null 3087 1896.5 3087 2013.0 3087 2847.2 Fish length 1 0.4 0.510 1 109.1 <0.001 1 29.4 <0.001 Fish origin 1 50.4 <0.001 1 135.1 <0.001 1 160.0 <0.001 (b) Native versus exotic ﬁsh: intensity of infection # null 283 2847.2 309 1035.9 534 1442.8 Fish length 1 0.4 0.506 1 8.0 0.192 1 26.0 0.007 Fish origin 1 42.4 <0.001 1 27.8 0.015 1 145.1 <0.001

Gobiid Native Total

Predictor d.f. dev P d.f. dev P d.f. dev P

(c) Native versus exotic bivalves: prevalence # null 3429 2777.3 2745 948.6 6175 3910.7 Bivalve origin 1 21.5 <0.001 1 45.2 <0.001 1 1.3 0.261 (d) Native versus exotic bivalves: intensity of infection # null 479 1286.0 113 22.5 593 1406.8 Bivalve origin 1 100.5 <0.001 1 0.8 0.090 1 152.9 <0.001 intensity of A. woodiana and U. tumidus infections difference of 900%). The density of A. woodiana glochidia increased significantly with increasing body length in on exotic fish was consistently higher than on native fish native fish (GLM, both P < 0.001; Fig. 1 & 2). (mean density 2.6 versus 0.2 glochidia 1000 m 3; Fig. 3). Glochidia of U. tumidus were transported downstream almost exclusively by exotic fish, with a density peak in Distribution on the host mid-June (101.9 glochidia 1000 m 3; Fig. 3). With the There were significant differences in distribution of glo- exception of A. woodiana glochidia on exotic fish, trans- chidia between native and exotic fish (v2 test, native glo- port of glochidia on drifting fish ceased around the end chidia v2 = 60.3, d.f. = 6, P < 0.001; exotic glochidia of July. v2 = 333.2, d.f. = 6, P < 0.001). While exotic fish were mainly infected on the ventral part of the body (pectoral Discussion and ventral fins accumulating over 50% of glochidia; Table 3), native fish were infected mostly around the As far as we are aware, this is the first study to report mouth (46% of glochidia; Table 3). glochidial infection on gobiid ELS, and the first to report A. woodiana glochidia were distributed differently than glochidia on any fish as small as 4.1 mm SL (minimal those of U. tumidus in both exotic and native fish (v2 test, size of fish infected in our study). Previous parasitologi- exotic fish v2 = 204.2, d.f. = 6, P < 0.001; native fish cal studies have generally ignored fish ELS (see Young v2 = 43.2, d.f. = 5, P < 0.001). In both native and exotic & Williams, 1984 or Kelly et al., 2010a,b for exceptions). hosts, A. woodiana glochidia were more abundant around Omitting ELS, however, means losing information on an the mouth (Table 3). The ventral parts of exotic fish were important aspect of a species’ ecology. Our study, for similarly infected by both A. woodiana and U. tumidus glo- example, demonstrated the importance of fish ELS in chidia; however, A. woodiana were less abundant than studies of exotic introductions, demonstrating that novel U. tumidus on the ventral parts of native fish (Table 3). fish-bivalve interactions were introduced at the ELS level following invasion by exotic fish and bivalve species. While native fish ELS largely avoided infection by Density of glochidia transported on drifting fish native glochidia, (a) invasion of an exotic mussel intro- The density of glochidia transported downstream was duced glochidia more able to attach to native fish and much greater on drifting exotic fish ELS than native fish (b) invasion of exotic fish species provided ELS hosts ELS (mean density 20.2 versus 2.2 glochidia 1000 m 3;a that were easily infected.

N |||||||||||||||||||||||||||||||||||||||||||| ||||||||||| ||||||||| ||| | | | | || || | | | | | E ||||||||||||| |||||||||||||||||||||||||||| |||||||||||||||||||||||||||||||||||||||||| ||||||||| ||||||| | ||||| | ||| | | ||| | |||| | |

(a)

Fig. 1 Prevalence of (a) Anodonta woodi- 0.0E 0.2||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||| |||||||||||||| ||||| |||||||||||||| ||||||||||||| |||||||||| ||||||||||||| 0.4||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||||||||||||| |||||||||||||||||| |||||||||| |||||||||||| ||||||||| ||||||||||||| ||||||||| | |||||||| | |||||||| | |||||| | | | | | | | | || | | | 0.6 | 0.8 | | 1.0 | N |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||||||||||||||||||||| |||||||| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||||||||||||||||||||||||||||||| |||||||||||||||||| ||||||||||||||||||||||||||||||||||| |||||||||||||||| ||||||||||||||||||||||||||||||||||||||||||||||||||| |||||||| ||||||||||| |||||||||||||||| ||||||||||| ||||||||||||||||||||| ||||||| | ||||||||||||||| | |||| |||||||||||||| | ||||| |||| |||||||||||||||||| | ||| |||||| ||| | |||||||| ||||||||| ||||| ||||||||||||||| ||| || | | ||||| ||| | | ||| | ||| || ||| |||| | | | | |||| || | | ||||| || || | |||| |||| | || || || || | || | | | || || | | | | | | | || | | || ||| | || | || | | | | | | ana and (b) Unio tumidus glochidia as an effect of fish size in exotic gobiid (E, solid line) and native fish (N, dashed Prevalence line) early life stages. Bold and weaker N ||||||||||||||||| | | | | | | E ||||||||||||||||||||| ||||||||||||| ||||||||||||| |||||||||||||||||||| |||||||||||||||||| |||||||||||||||||| ||||||||||||||||||| ||| | |||| ||| ||| ||| || | | lines represent curves and 95% confidence intervals respectively, as predicted (b) by generalised linear models. Vertical lines above and below the graph represent individuals with and without glochidia respectively. Model formulae and parameters: (a) exotic fish: y = 1/(1 + e^ (5.738–0.536* SL), d.f. = 1,1713, var (% of variability explained) = 4.7%; native fish: † y = 1/(1 + e^(3.652–0.067 * SL), d.f. = 1,1372, var = 2.3%; (b) exotic fish (†): y = 1/(1 + e^(1.932–0.048* SL), d.f. = 1,1714, var (% of variability 0.0E 0.2|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| |||||||| ||||| ||||| ||||||||||||| || |||||| |||||||||||||||||| ||||||||||||||||| 0.4||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||||||||||||||||||||| ||||||| ||||||||| |||||||||||||| |||||||||| |||||| ||||||||| |||||| ||| |||||| | |||||||| ||| | | | ||| | || | | || | | | 0.6| | 0.8 | | || 1.0 | | =< = N |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||||||||||||||||||||| ||||||||| ||||||||||||||||| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||||||||||||||||||||||||||| |||||||||||||||| |||||||||||||||||||||||||||||||||||| |||||||||||||| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||| ||||||||| |||||||| |||||||||||| ||||||||||| ||||||||||||||||||| |||| ||||||| |||||||||||| ||| |||||| ||||||||||||||| ||||| |||| | ||||||| ||||||||||| |||| | ||||||||| || ||||||| ||||||||| ||||| ||||||||||||||| ||| || | | ||||| ||| | | ||| | ||| || ||| ||| | ||| ||||| || | | ||||| || || | ||||| |||| | || || | || | || | || | | | || ||| | | | | | | | || | | | || | | ||| | |||| | ||| | | | | explained) 0.1%; native fish: y 1/ (1 + e^(5.724–0.102* SL), d.f. = 1,1372, 10 20 30 40 var = 6.1%.†–model slope is not signifi- Fish standard length (mm) cantly different from 0.

(neither genera having evolved active host attraction). Mechanisms ... Thus, higher rates of glochidial infection are more likely In this study, the influx of two exotic gobiid fish species in benthic dwellers (Schwalb, Poos & Ackerman, 2011) introduced new and ‘attractive’ fish hosts for unionid such as adult gobiids (Ondrackova et al., 2009; Francova glochidia, at least in contrast to the native fish pool. We et al., 2011) and, presumably, gobiid ELS. Indeed, the suggest two possible reasons for the high ELS parasite increased level of infection observed on the ventral parts loads observed. First, it may simply represent the typical of gobiid bodies (Table 3) corresponds well with infec- response observed when exotic species are introduced tion by bottom-dwelling glochidia observed in other into a novel area, i.e. heavy infection by a few generalist benthic species (Martel & Lauzon-Guay, 2005). parasite species. Second, high glochidial prevalence in Similarly, the presence of exotic A. woodiana intro- gobiid ELS may be a direct result of the specific life- duced parasitic glochidia that were significantly more styles of glochidia and gobiid ELS. Both N. melanostomus apt to infect native fish ELS than native bivalve glochi- and P. semilunaris are guarding cavity spawners (Miller, dia. The probable reason for this is again to be found in 1986), newly hatched gobiid embryos staying several the lifestyle and morphology of both fish ELS and glo- days in the nest before moving down to the substrata, chidia. In native fish, A. woodiana glochidia were mostly with sandy substratum preferred (Leslie & Timmins, found around the mouth region. As previously docu- 2004). This is in contrast to native fish (mainly cyprinid) mented in other fish species (Zale & Neves, 1982), glo- ELS, which swim more-or-less freely in the water col- chidia often attach themselves to the mouthparts when umn, using aquatic vegetation and/or shallow micro- fish attempt to eat them. Large numbers of A. anatina, habitats with moderate flow for shelter (Garner, 1996). closely related to A. woodiana, have also been observed In both U. tumidus and A. woodiana, a high proportion of around the mouthparts of juvenile and adult native fish the glochidia discharged sink to the bottom substrata (Blazek & Gelnar, 2006). Note, however, that while

Fig. 2 Intensity of (a) Anodonta woodiana and (b) Unio tumidus glochidia infection as an effect of fish size in exotic gobiid (solid line) and native fish (dashed line) early life stages. Bold and weaker lines represent curves and 95% confidence intervals respectively, as predicted by generalised linear models. Model formulae: (a) exotic fish: y = e^(0.864 + 0.190 * SL), d.f. = 1,192, var = 35.6%; native fish: y = e^(0.244 + 0.023 * SL), d.f. = 1,90, var = 24.1%; (b) exotic fish (†): y = e^(0.955 + 0.035 * SL), d.f. = 1,286, var = 0.2%; native fish: y = e^(0.310 + 0.031 * SL), d.f. = 1, 22, var = 36.3%. †–model slope is not significantly different from 0.

Table 3 Distribution of glochidia (A. woodiana, U. tumidus) on their respective ﬁsh hosts expressed as a percentage (%) of the total count (n) for each locality.

Pectoral fins Ventral fins Anal fin Caudal fin Dorsal fin Mouth Operculae n

Gobiid fish 27.6 21.6 6.9 17.7 9.6 12.8 3.7 1281 Native fish 10.9 0.7 2.9 22.5 16.7 45.7 0.7 138 U. tumidus on exotic fish 29.2 20.2 8.0 18.5 11.3 9.0 3.8 930 A. woodiana on exotic fish 23.4 25.4 4.3 15.7 5.1 22.8 3.4 351 U. tumidus on native fish 24.1 3.4 3.4 37.9 31.0 0.0 0.0 29 A. woodiana on native fish 7.3 0.0 2.8 18.3 12.8 57.8 0.9 109

A. anatina are abundant at the study site (Beran, 2013), item than A. woodiana glochidia, which may be being infection of fish ELS was not observed due to a temporal taken preferentially as a result. This is supported by the mismatch in hatching (Hinzmann et al., 2013). Unlike very low presence of U. tumidus glochidia in the near- A. anatina, which mostly release glochidia in spring or mouth area. Indeed, previous studies have shown that autumn (Watters & O’Dee, 2000), A. woodiana glochidia Unio spp. glochidia almost always attach themselves to are released during summer, which coincides with the the gills in both juvenile and adult fish (Smith et al., occurrence of both native fish and, to an even greater 2004; Blazek & Gelnar, 2006). Both glochidia genera in extent, exotic gobiid ELS. On the other hand, while our study were too large to attach to the gills of fish release of native U. tumidus glochidia coincided with the ELS; however, we suggest that fish ELS fin tissue may presence of native fish ELS (Aldridge, 1999), we be sufficiently soft for attachment of U. tumidus glochi- observed a very low infection rate. We suggest that the dia in its place. Lack of attraction as a potential food smaller (approx. 50%) U. tumidus glochidia are less dis- item suggests that U. tumidus infection on the fins of fish cernible and potentially represent a less attractive food ELS relies more on ‘passive’ contact with the host’s

) Exotic –3 12 Native

6 glochia density (1000 m 4

2 A.woodiana 0 May June July August

120 Exotic ) –3 100 Native

glochia density (1000 m 40

Fig. 3 Seasonal density patterns of both 20 exotic (upper panel) and native (lower panel) glochidia transported downstream U. tumidus 0 on drifting early life stages of native ﬁsh May June July August (dashed line, empty square) and exotic gobiids (solid line, empty circle).

body, a situation common in benthic gobiid ELS but rare to earlier glochidial attack; Dodd et al., 2005). The proba- in native fish ELS (see above). bility of A. woodiana and U. tumidus glochidia encapsulating is further increased by their ability to complete development on a wide spectrum of hosts (Trdan & ... and possible consequences Hoeh, 1982; Douda et al., 2012). Presence of a parasite on a host’s body does not neces- Even then, successful encapsulation does not guaran- sarily mean that it will successfully encapsulate and tee survival of the glochidium. As glochidia cannot com- complete its development. Several host-specialised plete their development on a dead host, and are unable unionid bivalves attached to juvenile N. melanostomus to re-attach to another host, death of the host results in (total length ≥40 mm), for example, were largely unsuc- death of the parasite (Smith Trail, 1980). The detrimental cessful in encapsulating (Tremblay, 2012). As no infor- effect of parasitic infection decreases with fish size mation is available on the course of infection for gobiid (Tucker, Sommerville & Wootten, 2002) and the proba- ELS parasitised by A. woodiana and U. tumidus, we can bility of lethal infection is thus highest in fish ELS. As only extrapolate from such related studies. fish ELS were just 6 mm long (mean SL), it is highly As the fish ELS in our study were only days old (Janac likely that several large glochidia would decrease et al., 2013a), they were clearly encountering glochidia for manoeuvrability, increase energy expenditure and, in the first time. The probability that glochidia will encapsu- the case of glochidia attached to the mouth, decrease late (and successfully complete their development) is energy intake to such an extent that predation and star- highest in these fish as they have no inbuilt resistance vation rates would be increased. As such, gobiid ELS (resistance being attributed to an immunological response would act as a sink for a proportion of the attached

© 2016 John Wiley & Sons Ltd, Freshwater Biology, 61, 979–990 Glochidia on gobiid early life stages 987 glochidia, either through gobiid resistance or death. In proportion underestimated in our samples. On the other this case, exotic gobiids act as an ‘ecological trap’ (sensu hand, the assumption that there is a time lag between Robertson, Rehage & Sih, 2013), whereby a proportion infection and death would appear logical. Furthermore, of bivalve progeny are lost through attachment to an we observed no conspicuous outlier values in our data- abundant ‘false-host’, as previously reported by Trem- set, which was based only on fish several days old. We blay (2012) for North American host-specialist bivalves. are optimistic, therefore, that our data mirror actual That attraction of glochidia to fish ELS is maladaptive is infection rates. indirectly supported by the very low levels of native Those gobiid ELS that survive infection and allow glo- glochidial infection on native fish ELS in this study. It is chidia to develop will increase the importance of exotic unlikely, however, that such an ecological trap would gobiids as glochidial hosts, and perhaps even increase significantly threaten bivalve populations, given the the possibility of future effects from parasite spillback. presence of other, more suitable hosts and the high Notably, gobiid ELS may also enhance establishment of number of glochidia released. However, as we are exotic mussels (i.e. A. woodiana) in the same way. Just unable to define the ratio of glochidia attached to gobiid such a beneficial interaction between two exotic species ELS in relation to all glochidia, the magnitude of any is predicted by the invasional meltdown theory of Sim- dilution effect induced through attraction to gobiid ELS berloff & Von Holle (1999). Gobiid invasion would also must remain speculative. result in a large number of both native and exotic glo- It is worth noting here that the terms ‘parasite spill- chidia being transported downstream on the bodies of back’ and ‘dilution effect’ are often applied with some drifting gobiid ELS. Assuming that downstream transform of positive or negative connotation, e.g. a dilution port was not present before gobiid invasion (note the effect implies a lowered parasitic load for native hosts very low infection rate in native fish ELS), downstream and spillback threatens native hosts. Our study is a good bivalve populations may be reinforced as a result and example for showing that always viewing interactions local and upstream populations potentially weakened. If from the host’s standpoint can be inappropriate. In our proven, colonisation of new downstream areas by case, the native glochidial parasite (U. tumidus)isan A. woodiana via ‘hitchhiking’ on drifting gobiid ELS endangered species and, from the viewpoint of mussel would represent a new invasional meltdown phe- conservation management, the implications of the terms nomenon in this system. spillback and dilution are reversed. Fish ELS will play a key role in determining the future From another viewpoint, the detrimental effect of glo- development of fish communities on the Dyje, with chidial infection on fish ELS will contribute to an interactions taking place at the ELS level being reflected increase in (already high) fish ELS mortality (Houde, later on at the population-level. We have to stress, how- 2002). Through glochidial infection, therefore, bivalves ever, that the changes observed form only part of the may decrease gobiid recruitment and impede expansion, overall changes that may be occurring in fish-bivalve contributing to biotic resistance of the system against the interactions following introduction of exotic species to exotic gobiids. Stage-specific prevalence and mortality the system. Hence, future studies should not concentrate will determine the extent to which infection will affect solely on gathering information on the ‘evolving’ ELS gobiid populations. While prevalence may reach very level of the interaction but also on providing supple- high rates (prevalence of A. woodiana, e.g., reached over mentary data on glochidia infection in older fish. In our 80% in gobiids >12 mm in this study), the mortality rate study area, for example, there are no data available in gobiid ELS is largely unknown. While we tried to regarding glochidial-induced mortality in older gobiids, estimate the rate of infection-related mortality in gobiid or on the probability of glochidial encapsulation in this ELS in a pilot study, difficulties associated with keeping species. Despite this lack of information, we can such small fish alive over the course of the experiment presume that studies on older life stages only would prevented us from obtaining any reliable estimates, have missed some of the patterns observed in this study though we were able to confirm that at least some and/or some of the consequences predicted (e.g. the role infected gobiid ELS were able to survive for at least of bivalves in biotic resistance to gobiids or the role of 7 days. gobiid ELS in bivalve dispersal). We believe that our Theoretically, fish ELS mortality resulting from glochi- results have highlighted a previously overlooked aspect dial infection could also have introduced some bias into of fish-bivalve interaction, therefore, emphasising that our study. If, for example, heavily infected fish die all ontogenetic stages should be included when studying quickly, then they may have been missed or their the effects of exotic introductions (see Rius et al., 2014).

© 2016 John Wiley & Sons Ltd, Freshwater Biology, 61, 979–990 988 L. Slapansky et al. Acknowledgments Douda K., Vrtılek M., Slavık O. & Reichard M. (2012) The role of host specificity in explaining the invasion success This study was supported by the Czech Science Founda- of the freshwater mussel Anodonta woodiana in Europe. tion (GA CR), Project No. P505/12/G112: ECIP (funding Biological Invasions, 14, 127–137. for field sampling, MJ and PJ) and P505/11/1768 (fund- Dunn A.M. (2009) Parasites and biological invasions. ing for LS and for laboratory work). We thank M. Vasek, Advances in Parasitology, 68, 161–184. G. Konecna, M. Konıckova, L. Vsetickova, K. Roche, M. Francova K., Ondrackova M., Polacik M. & Jurajda P. (2011) Konecna, K. Halacka, I. Slovackova and V. Michalkov a Parasite fauna of native and non-native populations of for help with fieldwork; R. Blazek for help with glochidia Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the determination and K. Roche for help in preparing the longitudinal profile of the Danube River. Journal of – English version of the manuscript. R. Blazek, M. Polacik, Applied Icthyology, 27, 879 886. Garner P. (1996) Microhabitat use and diet of 0 + cyprinid M. Reichard and K. Roche also provided valuable com- fishes in a lentic, regulated reach of the River Great Ouse, ments on an earlier version of the manuscript. We are England. Journal of Fish Biology, 48, 367–382. much indebted to representatives of the Moravian Garner P. (1997) Habitat use by 0 + cyprinid fish in the Angling Union for allowing research in their waters. River Great Ouse, East Anglia. Freshwater Forum, 8,2–27. Grutter A.S., Cribb T.H., McCallum H., Pickering J.L. & References McCormick M.I. (2010) Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccen- Aldridge D.C. (1999) The morphology, growth and repro- sis. Coral Reefs, 29,31–40. duction of Unionidae (Bivalvia) in a Fenland waterway. Haag W.R. & Staton J.L. (2003) Variation in fecundity and Journal of Molluscan Studies, 65,47–60. other reproductive traits in freshwater mussels. Freshwater Barnhart M.C., Haag W.R. & Roston W.N. (2008) Adapta- Biology, 48, 2118–2130. tions to host infection and larval parasitism in Unionidae. Hayden T.A. & Miner J.G. (2009) Rapid dispersal and estab- Journal of the North American Benthological Society, 27, 370– lishment of a benthic Ponto-Caspian goby in Lake Erie: 394. diel vertical migration of early juvenile round goby. Bio- Beran L. (2013) Freshwater molluscs of the Dyje (Thaya) logical Invasions, 11, 1767–1776. river and its tributaries – the role of these water bodies in Hinzmann M., Lopes-Lima M., Teixeira A., Varandas S., expansion of alien species and as a refuge for endangered Sousa R., Lopes A. et al. (2013) Reproductive cycle and gastropods and bivalves. Folia Malacologica, 21, 143–160. strategy of Anodonta anatina (L., 1758): notes on hermaph- Blazek R. & Gelnar M. (2006) Temporal and spatial distri- roditism. Journal of Experimental Zoology, 319, 378–390. bution of glochidial larval stages of European unionid Houde E.D. (2002) Mortality. In Fishery Science: The Unique mussels (Mollusca: Unionidae) on host fishes. Folia Para- Contributions of Early Life Stages (Eds L.A. Fuiman & R.G. sitologica, 53,98–106. Werner), pp. 64–87. Blackwell Science, Oxford. Bogan A.E. (1993) Freshwater bivalve extinctions (Mollusca: Janac M., Jurajda P., Kruzıkova L., Roche K. & Prasek V. Unionidae): a search for causes. American Zoologist, 33, (2013b) Reservoir to river passage of age-0 + year fishes, 599–609. indication of a dispersion pathway for a non-native spe- Bronnenhuber J.E., Dufour B.A., Higgs D.M. & Heath D.D. cies. Journal of Fish Biology, 82, 994–1010. (2011) Dispersal strategies, secondary range expansion Janac M., Slapansky L., Valova Z. & Jurajda P. (2013a) and invasion genetics of the nonindigenous round goby, Downstream drift of round goby (Neogobius melanostomus) Neogobius melanostomus, in Great Lakes tributaries. Molec- and tubenose goby (Proterorhinus semilunaris) in their ular Ecology, 20, 1845–1859. non-native area. Ecology of Freshwater Fish, 22, 430–438. Cope W.G., Bringolf R.B., Buchwalter D.B., Newton T.J., JanacM.,Valova Z. & Jurajda P. (2012) Range expansion and Ingersoll C.G., Wang N. et al. (2008) Differential expo- habitat preferences of non-native 0 + tubenose goby sure, duration, and sensitivity of unionoidean bivalve life (Proterorhinus semilunaris) in two lowland rivers in the stages to environmental contaminants. Journal of the North Danube basin. Fundamental and Applied Limnology, 181,73–85. American Benthological Society, 27, 451–462. Jude D.J., Reider R.H. & Smith G.R. (1992) Establishment of Daszak P., Cunningham A.A. & Hyatt A.D. (2000) Emerg- Gobiidae in the Great Lakes basin. Canadian Journal of ing infectious diseases of wildlife – threats to biodiversity Fisheries and Aquatic Sciences, 49, 416–421. and human health. Science, 287, 443–449. Kelly D.W., Paterson R.A., Townsend C.R., Poulin R. & Dodd B.J., Barnhart M.C., Rogers-Lowery C.L., Fobian T.B. Tompkins D.M. (2009a) Parasite spillback: a neglected & Dimock R.V. Jr (2005) Cross-resistance of largemouth concept in invasion ecology? Ecology, 90, 2047–2056. bass to glochidia of unionid mussels. Journal of Parasitol- Kelly D.W., Paterson R.A., Townsend C.R., Poulin R. & ogy, 91, 1064–1072. Tompkins D.M. (2009b) Has the introduction of brown

trout altered disease patterns in native New Zealand fish? Ondrackova M., Davidov a M., Blazek R., Gelnar M. & Jura- Freshwater Biology, 54, 1805–1818. jda P. (2009) The interaction between an introduced fish Kelly D.W., Poulin R., Tompkins D.M. & Townsend C.R. host and local parasite fauna: Neogobius kessleri in the (2010b) Synergistic effects of glyphosate formulation and middle Danube River. Parasitology Research, 105, 201–208. parasite infection on fish malformations and survival. Ondrackova M., Davidov a M., Pecınkova M., Blazek R., Journal of Applied Ecology, 47, 498–504. Gelnar M., ValovaZ. et al. (2005) Metazoan parasites of Kelly D.W., Thomas H., Thieltges D.W., Poulin R. & Tomp- Neogobius fishes in the Slovak section of the River kins D.M. (2010a) Trematode infection causes malforma- Danube: a preliminary study. Journal of Applied Ichthyol- tions and population effects in a declining New Zealand ogy, 21, 345–349. fish. Journal of Animal Ecology, 79, 445–452. Pekkarinen M. & Englund P.M. (1995) Description of union- Kennedy C.R. & Bush A.O. (1994) The relationship between acean glochidia in Finland, with a table aiding in their pattern and scale in parasite communities: a stranger in a identification. Archiv fur€ Hydrobiologie, 134, 515–531. strange land. Parasitology, 109, 187–196. Poos M., Dextrase A.J., Schwalb A.N. & Ackerman J.D. Koblickaya A.F. (1981) Key for Identifying Young Freshwater (2010) Secondary invasion of the round goby into high Fishes. Light and Food Industry Publishing House, Mos- diversity Great Lakes tributaries and species at risk hot- cow. spots: potential new concerns for endangered freshwater Kornis M.S., Mercado-Silva N. & Vander Zanden M.J. species. Biological Invasions, 12, 1269–1284. (2012) Twenty years of invasion: a review of round goby Poulin R. & Mouillot D. (2003) Host introductions and the Neogobius melanostomus biology, spread and ecological geography of parasite taxonomic diversity. Journal of Bio- implications. Journal of Fish Biology, 80, 235–285. geography, 30, 837–845. Kvach Y. & Winkler H.M. (2011) The colonization of the R Core Team (2012) R: A Language and Environment for Sta- invasive round goby Neogobius melanostomus by parasites tistical Computing. R Foundation for Statistical Comput- in new localities in the southwestern Baltic Sea. Parasito- ing, Vienna. ISBN: 3-900051-07-0. Available at: http:// logical Research, 109, 769–780. www.R-project.org/ Leslie J.K. & Timmins C.A. (2004) Description of age-0 Reichard M., Vrtılek M., Douda K. & Smith C. (2012) An round goby, Neogobius melanostomus Pallas (Gobiidae), invasive species reverses the roles in a host-parasite rela- and ecotone utilization in St. Clair lowland waters, Ontar- tionship between bitterling fish and unionid mussels. Bio- io. Canadian Field Naturalist, 118, 318–325. logical Letters, 8, 601–604. Lusk S., Luskova V. & Hanel L. (2010) Alien fish species in Rius M., Potter E.E., Aguirre J.D. & Stachowicz J. (2014) Czech Republic and their impact on the native fish fauna. Mechanisms of biotic resistance across complex life Folia Zoologica, 59,57–72. cycles. Journal of Animal Ecology, 83, 296–305. Lydeard C., Cowie R.H., Bogan A.E., Bouchet P., Cum- Robertson B.A., Rehage J.S. & Sih A. (2013) Ecological nov- mings K.S., Frest T.J. et al. (2004) The global decline of elty and the emergence of evolutionary traps. Trends in nonmarine mollusks. BioScience, 54, 321–330. Ecology and Evolution, 28, 560. Marques J.F. & Cabral H.N. (2007) Effects of sample size on Roche K.F., Janac M. & Jurajda P. (2013) A review of Gobiid fish parasite prevalence, mean abundance and mean inten- expansion along the Danube-Rhine corridor – geopolitical sity estimates. Journal of Applied Ichthyology, 23, 158–162. change as a driver for invasion. Knowledge and Manage- Martel A.L. & Lauzon-Guay J.S. (2005) Distribution and ment of Aquatic Ecosystems, 411, 01. density of glochidia of the freshwater mussel Anodonta Schwalb A.N., Poos M.S. & Ackerman J.D. (2011) Move- kennerlyi on fish hosts in lakes of the temperate rain forest ment of logperch – the obligate host fish for endangered of Vancouver Island. Canadian Journal of Zoology, 83, 419– snuffbox mussels: implications for mussel dispersal. 431. Aquatic Sciences, 73, 223–231. Miller P.J. (1986) Gobiidae. In Fishes of the Northeastern Schwalb A.N. & Pusch M. (2007) Horizontal and vertical Atlantic and the Mediterranean (Eds P.J.P. Whitehead, M.L. movements of unionid mussels (Bivalvia: Unionidae) in a Bauchot, J.C. Hureau, J. Nielson & E. Tortonese), pp. lowland river. Journal of the North American Benthological 1019–1085. UNESCO, Paris. Society, 26, 261–272. Mitchell C.E. & Power A.G. (2003) Release of invasive Simberloff D. & Von Holle B. (1999) Positive interactions of plants from fungal and viral pathogens. Nature, 421, 625– nonindigenous species: Invasional meltdown? Biological 627. Invasions, 1,21–32. Muzzal P.M., Peebles C.R. & Thomas M.V. (1995) Parasites Smith C., Reichard M., Jurajda P. & Przybylski M. (2004) of the round goby, Neogobius melanostomus and tubenose The reproductive ecology of the European bitterling (Rho- goby, Proterorhinus marmoratus (Perciformes, Gobiidae), deus sericeus). Journal of Zoology, 262, 107–124. from the St. Clair River and Lake St. Clair, Michigan. Smith Trail D.R. (1980) Behavioural interactions between Journal of the Helminthological Society of Washington, 62, parasites and hosts: host suicide and the evolution of 226–228. complex life cycles. The American Naturalist, 116,77–91.

Strayer D.L. (1999) Effects of alien species on freshwater ectoparasite of Atlantic salmon Salmo salar. Diseases of mollusks in North America. Journal of the North American Aquatic Organisms, 49, 145–152. Benthological Society, 18,74–98. Watters G.T. & O’Dee S.H. (2000) Glochidial release as a Timi J.T., Luque J.L. & Poulin R. (2010) Host ontogeny and the function of water temperature: beyond bradyticty and temporal decay of similarity in parasite communities of tachyticty. In Proceedings of the Conservation, Captive Care, marine ﬁsh. International Journal for Parasitology, 40,963–968. and Propagation of Freshwater Mussels Symposium (Eds R.A. Torchin M.E., Lafferty K.D., Dobson A.P., McKenzie V.J. & Tankersley, D.I. Warmolts, G.T. Watters, B.J. Armitage, Kuris A.M. (2003) Introduced species and their missing P.D. Johnson & R.S. Butler), pp. 135–140. Special Publica- parasites. Nature, 421, 628–630. tion of the Ohio Biological Survey, Columbus. Trdan R.J. & Hoeh W.R. (1982) Eurytopic host use by two Young M. & Williams J. (1984) The reproductive biology of congeneric species of freshwater mussel (Pelecypoda: the freshwater pearl mussel in Scotland. 1 Field Studies. Unionidae: Anodonta). American Midland Naturalist, 108, Archiv fur€ Hydrobiologie, 99, 405–422. 381–388. Zale A.V. & Neves R.J. (1982) Fish hosts of four species of Tremblay M. (2012) An Effect of The Invasive Round Goby lampsiline mussels (Mollusca: Unionidae) in Big Moc- (Neogobius melanostomus) on The Recruitment of Unionid casin Creek, Virginia. Canadian Journal of Zoology, 60, Mussel Species at Risk (Bivalvia: Unionidae). MSc thesis, The 2535–2542. University of Guelph, Guelph. Available at: https:// Zimmerman L.L. & Neves R.J. (2002) Effects of temperature atrium.lib.uoguelph.ca/xmlui/bitstream/handle/10214/ on duration of viability for glochidia of freshwater mus- 5111/Tremblay_Maude_201212_MSc.pdf?sequence=1 sels (Bivalvia: Unionidae). American Malacological Bulletin, Tucker C.S., Sommerville C. & Wootten R. (2002) Does size 17,31–35. really matter? Effects of ﬁsh surface area on the settle- ment and initial survival of Lepeophtheirus salmonis,an (Manuscript accepted 2 March 2016)

Publikace A

Šlapanský, L., Janáč, M., Roche, K., & Jurajda, P. (2019). Round goby movement patterns in a non-navigable river. Odesláno do Canadian Journal of Fisheries and Aquatic research 11. 12. 2018.

Sbíral jsem materiál v terénu, zpracoval jsem terénní materiál a s připomínkami spoluautorů jsem napsal finální verzi rukopisu. Můj podíl na tomto rukopise byl 65%.

Publikace B

Šlapanský, L., Janáč, M., Roche, K., Mikl, L. & Jurajda, P. (2017). Expansion of round gobies in a non-navigable river systém. Limnologica, 67, 27-36.

Sbíral jsem materiál v terénu, zpracoval jsem získaný materiál a s připomínkami spoluatorů jsem napsal finální verzi rukopisu. Můj podíl na této publikaci byl 65%.

Publikace C

Zpracovával jsem materiál nasbíraný v terénu a podílel jsem se na psaní rukopisu. Můj podíl na této publikaci byl 15%.

Publikace D

Podílel jsem se na sběru materiálu v terénu, zpracoval jsem získaný materiál a podílel jsem se na psaní finální verze rukopisu. Můj podíl na této publikaci byl 40%.

Rukopis E

Šlapanský, L., Jurajda, P. & Janáč, M. (2016). Early life stages of exotic gobiids as new host for unionid glochidia. Freshwater Biology, 61, 679-690.

Podílel jsem se na sběru materiálu v terénu, zpracoval jsem získaný materiál a s připomínkami spoluatorů jsem napsal finální verzi rukopisu. Můj podíl na této publikaci byl 60%.

7.3 Seznam impaktovaných publikací

PUBLIKOVANÉ

Borcherding, J., Staas, S., Krüger, S., Ondračková, M., Šlapanský, L. & Jurajda, P. (2011). Non-native Gobiid species in the lower River Rhine (Germany): recent range extensions and densities. Journal of Applied Ichthyology, 27(1), 153-155.

Roche, K., Janáč, M., Šlapanský, L., Mikl, L., Kopeček, L. & Jurajda, P. (2015). A newly established round goby (Neogobius melanostomus) population in the upper stretch of the river Elbe. Knowledge and Management of Aquatic Ecosystems, 416 (33), 1-11.

Šlapanský, L., Jurajda, P. & Janáč, M. (2016). Early life stages of exotic gobiids as new host for unionid glochidia. Freshwater Biology, 61, 679-690.

Adámek, Z., Mrkvová, M., Zukal, J., Roche, K., Mikl, L., Šlapanský, L., Janáč, M. & Jurajda, P. (2016). Environmental quality and natural food performance at feeding sites in a carp (Cyprinus carpio) pond. Aquaculture International, 24, 1591-1606.

Šlapanský, L., Janáč, M., Roche, K., Mikl, L. & Jurajda, P. (2017). Expansion of round gobies in a non-navigable river systém. Limnologica, 67, 27-36.

Mikl, L., Adámek, Z., Všetičková, L., Janáč, M., Roche, K., Šlapanský, L. & Jurajda, P. (2017). Response of benthic macroinvertebrate assemblages to round (Neogobius melanostomus) and tubenose (Proterorhinus semilunaris) goby predation pressure. Hydrobiologia, 785, 219-232.

Mikl, L., Adámek, Z., Roche, K., Všetičková, L., Šlapanský, L. & Jurajda, P. (2017). Invasive Ponto-Caspian gobies in the diet of piscivorous fish in a European lowland river. Fundamental and Applied Limnology, 192 (2), 157-171.

Janáč, M., Roche, K., Šlapanský, L., Polačik, M. & Jurajda, P. (2018). Long-term monitoring of native bullhead and invasive gobiids in the Danubian rip-rap zone. Hydrobiologia, 807, 323-337.

ODESLANÉ NA RECENZI

Šlapanský, L., Janáč, M., Roche, K., & Jurajda, P. (2019). Round goby movement patterns in a non-navigable river. Odesláno do Canadian Journal of Fisheries and Aquatic research 11.12. 2018.

7.4 Příspěvky na konferencích

MEZINÁRODNÍ

Šlapanský L., Jurajda P., Janáč M.: New kids on the block: A case study of how invasives can alter early-life stage fish-mussel interactions. 8th International Conference of Biological Invasions from understanding to action, Turecko 2014 (přednáška).

DOMÁCÍ

Šlapanský L., Janáč M., Jurajda P.: Drift hlaváčovitých ryb. XIII. Česká ichtyologická konference, Červená nad Vltavou 2012 (přednáška).

Šlapanský L., Janáč M., Jurajda P.: Hlaváči v našich vodách – Je čeho se bát?. Zoologické dny, České Budějovice 2016 (přednáška).

Šlapanský L., Janáč M., Mikl L., Jurajda P.: Interakce raných vývojových stádií nepůvodních hlaváčovitých ryb a unioidních mlžů. XV. Rybářská a ichtyologická konference, Praha 2016 (poster).

Šlapanský L., Janáč M., Mikl L., Jurajda P.: Hlaváč černoústý v ČR: dvě řeky, dva osudy?. XVI Rybářská a ichtyologická konference, Brno 2018 (poster).

7.5 Ostatní výzkumná činnost

VÝZKUMNÉ ZPRÁVY

Ondračková M., Šlapanský L., Janáč M., Jurajda P., Mikl L., Kvach Y., Fojtů J. (2018): Ichtyologické studie na dolní Moravě a Dyji za roky 2016-2017. Lesy ČR; Lesní závod Židlochovice, polesí soutok a Moravskýrybářský svaz.

Jurajda P., Janáč M., Šlapanský L., Mikl L. (2018): Monitoring hlaváče černoústého (Neogobius melanostomus) v Labi na území ČR. Český rybářský svaz.

Jurajda P., Adámek Z., Všetičková L., Jurajdová Z., Šlapanský L. (2018): Ichtyologický a hydrobiologický průzkum ramene domovina a Mlýnského potoka u jezu u Sokolovny v Olomouci. Odbor životního prostředí magistrátu města Olomouce.

Jurajda P., Jurajdová Z., Mikl L., Šlapanský L. (2018): Vyhodnocení druhového složení a početnosti společenstev juvenilních ryb ve vazbě na hodnocení dobrého stavu vod na vybraných profilech v povodí Odry. Povodí Odry, státní podnik.

Jurajda P., Janáč M., Roche K., Šlapanský L. (2018): Příprava podkladů pro aktualizaci metodiky hodnocení ekologického stavu toků podle biologické složky ryby. Výzkumný ústav vodohospodářský TGM.

Mikl L., Adámek Z., Šlapanský L. (2017): Vliv technických úprav na společenstvo makrozoobentosu malých vodních toků – hydrobiologický a hydrologický průzkum.

Jurajda P., Jurajdová Z., Šlapanský L., Mikl L. (2017): Vyhodnocení druhového složení a početnosti společenstev juvenilních ryb ve vazbě na hodnocení dobrého stavu vod na vybraných profilech v povodí Odry. Povodí Odry, státní podnik.

Jurajda P., Adámek Z., Mikl L., Šlapanský L., Všetičková L., Jurajdová Z. (2017): Ichtyologický a hydrobiologický průzkum mrtvého ramene a řeky Moravy. Odbor životního prostředí magistrátu města Olomouce.

Jurajda P., Jurajdová Z., Janáč M., Šlapanský L., Mikl L., (2017): Monitoring hlaváče černoústého (Neogobius melanostomus) v Labi na území ČR v roce 2016. Český rybářský svaz.

Jurajda P., Jurajdová Z., Šlapanský L., Mikl L., (2016): Vyhodnocení druhového složení a početnosti společenstev juvenilních ryb ve vazbě na hodnocení dobrého stavu vod na vybraných profilech v povodí Odry.

Jurajda P., Adámek Z., Mikl L., Šlapanský L., Všetičková L., Jurajdová Z. (2016): Mrtvé rameno a Holické pískovny: ichtyologický a hydrobiologický průzkum.

Jurajda P., Jurajdová Z., Šlapanský L., Mikl L., Roche K., Janáč M. (2014): Vyhodnocení druhového složení a početnosti společenstev juvenilních ryb ve vazbě na hodnocení dobrého stavu vod na vybraných profilech v povodí Odry.

Jurajda P., Jurajdová Z., Mrkvová M., Janáč M., Šlapanský L., Mikl L. (2013): Ichtyologický průzkum poříčních tůní a lagun řeky Labe v úseku Střekov – Hřensko.

Jurajda P., Jurajdová Z., Mrkvová M., Roche K., Šlapanský L. (2013): Vyhodnocení druhového složení a početnosti společenstev juvenilních ryb ve vazbě na hodnocení dobrého stavu vod na vybraných profilech v povodí Odry.