The effect of flow on the competition betweenthe alien racer goby and native EuropeanbullheadŁukasz Jermacz1, Jarosław Kobak1, Anna Dzier_zy�nska1, Tomasz Kakareko21Department of Invertebrate Zoology, Nicolaus Copernicus University, Toru�n, Poland2Department of Hydrobiology, Nicolaus Copernicus University, Toru�n, Poland

Accepted for publication May 27, 2014

Abstract – The racer goby is an invasive Ponto-Caspian fish spreading throughout Europe. They threaten a nativespecies of similar biology, the European bullhead, by displacing them from shelters. These shelters are necessaryfor reproduction as well as for protection against predators and hydrodynamic forces. However, abiotic conditionsmay strongly modify the outcome of an interspecific competition in the wild. Nevertheless, little is known of theeffect of flow velocity on the competition between these rheophilic species, although this factor is crucial for theirdistribution in the field. We video-recorded fish behaviour for 2 h in single-species and mixed-species pairs in thepresence of single shelters at three flow velocities: 0, 10 (a velocity preferred by the racer goby) and 30 cm�s�1 (avelocity greater than preferred by the racer goby) to determine whether the invader can deprive the native species ofits shelter. At the flow of 0 and 10 cm�s�1, the racer goby exhibited aggressive behaviour towards bullhead, andthis restricted the time spent by the bullhead in the shelter. Moreover, although the flow of 30 cm�s�1 inhibitedracer goby aggression, the time spent by the bullhead in the shelter in interspecific competition was still reducedwhen compared to intraspecific controls. Our results suggest that under natural conditions, the racer goby displacebullheads from their shelters even at flow velocities greater than optimal for the racer goby.

Key words: interspecific aggression; flow velocity; biological invasion; Babka gymnotrachelus; Cottus gobio; shelter

Introduction

Biological invasions are regarded as one of the major(Allendorf & Lundquist 2003; Thiele & Otte 2008),if not the greatest (Lambertini et al. 2011) threats tothe world biodiversity. The appearance of alien spe-cies in the environment may lead to a significantreduction of the occurrence of native species or eventheir extinction due to the interference competition ofa more aggressive invader (Barbaresi & Gherardi1997; Martin et al. 2010). One of the fundamentalfactors determining the result of interspecific interfer-ence competition is abiotic conditions. In aquaticecosystems, such factors as salinity (Wijnhoven et al.2003), hydrodynamics (Genin & Karp 1994; Krassoiet al. 2008), temperature (Taniguchi & Nakano 2000)and type of substrate (Palmer & Ricciardi 2004) mayinfluence the outcomes of direct fights. Consequently,abiotic conditions influence displacement of one

species by another, their coexistence in the same habi-tat or their separation in space. Hence, there is a needfor a thorough examination of the potential results ofbehavioural interactions between native and invasiveorganisms under a wide range of abiotic conditions.This would allow for the more precise predictions ofecological consequences of biological invasions inspecific environments.Ponto-Caspian neogobiid fish (Gobiidae, Percifor-

mes) belong to the most impressive vertebrate invad-ers in freshwater aquatic ecosystems (Copp et al.2005; Roche et al. 2013). They are bottom-dwellingbenthivorous fish with a developed system of pater-nal care of eggs, aggressively competing for territo-ries and breeding sites (crevices in the bottom) withconspecifics and congener species (Dubs & Corkum1996; Van Kessel et al. 2011; Copp et al. 2013;Kakareko et al. 2013a). Their opportunistic foragingstrategy (Kostrzewa & Grabowski 2003; Grabowska

Correspondence: Łukasz Jermacz, Lwowska 1, 87-100 Toru�n, Poland. E-mail: lukasjermacz@gmail.com

doi: 10.1111/eff.12162 467

Ecology of Freshwater Fish 2015: 24: 467–477 � 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

ECOLOGY OFFRESHWATER FISH

& Grabowski 2005), broad environmental tolerance(Pinchuk et al. 2003) and effective reproduction(Kostrzewa et al. 2004; Grabowska 2005) contributeto their high invasive potential. The increasing expan-sion of gobiids in Europe may threaten native specieswith similar behaviour, like the European bullheadCottus gobio – a species listed in Annex II of theEuropean Council Directive on the conservation ofnatural habitats and of wild fauna and flora (CouncilDirective 92/43/EEC). So far, the disappearance ofbullhead has been observed in waters inhabited bygoby in the River Danube (Jurajda et al. 2005). Thecause of this phenomenon has been speculated to bestrong interference competition for space and food,particularly for the limited number of available shel-ters used as breeding areas, exerted by the goby.Indeed, one of the representatives of the Ponto-Cas-pian gobiids in the Baltic Sea catchment area, racergoby Babka gymnotrachelus (formerly Neogobiusgymnotrachelus, Neilson & Stepien 2009), has beenfound to be an effective competitor displacing bull-head from feeding areas (Kakareko et al. 2013a) andhiding places (Copp et al. 2013) under laboratoryconditions. However, to be able to extrapolate theresults of such experimental studies to natural condi-tions, water velocity, which may strongly affect thebehaviour and interspecific relationships of both spe-cies, must be taken into account. The cited studieswere conducted in stagnant water conditions, whereasboth species live in running waters and, moreover,differ in their flow preferences (Knaepkens et al.2002; Kakareko 2011). The bullhead occur mainly inthe areas of rapid flow, available to specialised fishonly (Smyly 1957). On the other hand, the racer gobyoccur in both reservoirs and rivers, but mainlyoccupy nearshore areas with slow current (Bryli�nska2000; Pinchuk et al. 2003; our own observations).An underwater study conducted in a medium-sizedEuropean river by Kakareko et al. (2013b) has showna significant degree of habitat separation between thespecies; however, they did not exclude the possibilityof a negative impact of the racer goby upon bullheadin the field, leaving the question of the potential dis-placement of the native species by the invading racergoby open. It can be expected that different prefer-ences of both species to water flow can modify theresults of interactions between them. Nevertheless,these differences have never been taken into accountin studies on behavioural interactions between theracer goby and bullhead.Therefore, the aim of our study was to check

experimentally the effect of flow velocity on the out-come of the competition for the shelter between theracer goby and European bullhead. We hypothesisedthat the bullhead, as a species occurring at higherflow velocities, would compete more effectively for

the shelter under rapid flow conditions which areunfavourable for the racer goby. We tested ourhypothesis by studying shelter occupancy as well asintra- and interspecific aggression level and formsdisplayed by the racer goby and European bullheadindividuals exposed in two-species and single-speciespairs to various flow velocities in the laboratory.

Methods

Experimental animals

Racer goby were caught in the Włocławek Reservoir(the lower River Vistula, central Poland) nearDobiegniewo village by electrofishing (IUP-12; Ra-det, Pozna�n, Poland). Bullhead were collected fromstony bottom in the River Brda in the city of By-dgoszcz (central Poland) by a diver equipped with anaquarium dip net. All fish were caught in summerand autumn of 2012 (nonreproductive period). Imme-diately after capture, they were transported in 10-lcontainers (transport time: ca. 1.5 h) to 100-l stocktanks located in an air-conditioned room with a con-stant temperature of 17 °C. Each species was keptseparately in groups of 4–5 animals of similar bodysize. The water in the stock tanks was constantlyoxygenated and filtered using standard aquarium fil-ters. We exchanged weekly 20% of the capacity ofwater. The fish were fed once a day with live or fro-zen chironomid larvae. Shelters made of PVC tubescut in the middle (U shaped) were put into the breed-ing tanks. Their shape and size were the same asthose of the shelters used in the experiment, and theirnumber matched the number of the fish in the aquar-ium, so that each individual could accustom to theartificial shelter. The fish were used in the experi-ments after at least 3 months spent in the laboratoryconditions. Our preliminary observations made dur-ing everyday caretaking of the animals show that 1–2 days after placing them in the stock tanks, individ-uals did not exhibit any signs of stress, moved freelyaround the tank, occupied the shelter and took food.After a few days, the fish accustomed to the presenceof the experimenter and showed no symptoms of dis-tress during manipulations in the stock tank.Capture and use of European bullhead, which is a

legally protected species in Poland, was under permit(no. DOPozgiz-4200/V-20/3068/10/ls), as was theexperimental procedure (Statement no. 6/2010 of theLocal Ethics Committee in Bydgoszcz, Poland).

Experimental conditions

The experiment was carried out in an acrylic flow-through tank, 150 cm long, 40 cm high and 15 cmwide, with regulated water flow velocity. Water was

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pumped upwards by a pump (OmniGene TP 550 BW,�Swiezcice, Poland, maximum output: 150 l�min�1, lift-ing height of the water column: 7 m) from an 800-lcontainer to an inlet of the experimental flow-throughtank and then flowed down back to the container(Fig. 1). The water depth during the experiments wasca. 8 cm. In the centre of the tank, a 45-cm-longworking arena was confined with plastic mesh barriers(diameter: 1 mm), in which test fish were placed.Inside the working arena, a single shelter was placed.It was made of a U-shaped PVC half-tube 10 cm longand 7 cm wide, like those used in the breeding tanks(Fig. 1). The shelter was only open from one side,opposite to the flow direction, ensuring darkness andstill water inside. The flow velocity was set using twoball valves installed between the pump and the inlet ofthe experimental tank (Fig. 1). This allowed for pre-cise regulation of the flow velocity in the experimentaltank up to 1 cm�s�1. A desired flow velocity wasdetermined based on a series of at least 20 measure-ments made by an ultrasonic gauge (Greyline Instru-ments Inc., Massena, NY, USA).Experiments were conducted at following flow

velocities: 0 (no flow), 10 and 30 cm�s�1. Previouslaboratory experiments have shown that the racer gobyprefer flow velocity of 10 cm�s�1 but not those ofabove 20 cm�s�1 (Kakareko 2011). Bullhead are usu-ally found at flow velocities of 20–100 cm�s�1 (Bless1982, 1990 after Knaepkens et al. 2002). However,we observed racer goby individuals co-occurring withbullheads in a river at flow velocities of 30 cm�s�1

and lower (T. Kakareko, personal observation). Thus,

our experiments were carried out under optimum andsuboptimum conditions for one or both of the selectedspecies, within the range in which the bullhead may bepotentially endangered by the racer goby.During the tests, the sides of the experimental tank

were curtained off with foamed polystyrene screensto isolate the area from the surrounding environmentand ensure a uniform illumination. The water temper-ature in the tank during the experiments was 17.4–17.9 °C [sustained by air conditioning and Teco R20aquarium cooler (Teco S.l.r., Ravenna, Italy), andoxygenation was 8.8 mg O2 dm�3 (96.8–98.0%)(measured with a multimeter Multi340i; WTWGmbH, Weilheim, Germany]. The experimental tankwas illuminated from the top by fluorescent lightwith the intensity of 170–280 lx (luxometer L-20A,Sonopan Ltd., Białystok, Poland).

Experimental protocol

In each trial, two fish of similar body size were testedsimultaneously. The mean lengths of the used fishwere 8.2 cm (min–max: 6.5–10.0 cm TL,SD � 1.35 cm) for racer goby and 7.4 cm for bull-head (min–max: 5.5–10.7 cm TL, SD � 2.10 cm).The maximum difference between the body lengthsof the individuals making up a pair was 1 cm. Allindividuals were measured immediately after theexperiment with a ruler to the nearest 1 cm. The fishwere tested in single-species combinations (eight tri-als for each species) and two-species treatments (15trials). Both fish were put into the arena simulta-

(a)

(b) (c)

Fig. 1. Experimental set-up. Thick arrows indicate the direction of water flow. Dimensions are given in mm.

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neously in order not to favour any of the individuals.Each test was preceded by a 2-h period of adaptation,intended to acclimate the fish to the conditions of theexperimental tank (constant flow, one shelter and lowwater level). This allowed us to evaluate the periodafter establishing the preliminary domination struc-ture between both fish and determine the final resultof their interference competition. Duration of theexperiment was set for 2 h following the adaptationperiod. The whole experiment was recorded using aLogitech QuickCam Pro 9000 webcam (LogitechEurope S.A., Lausanne, Switzerland) placed abovethe tank. The video camera was connected to a PC,which allowed recording and constant monitoring ofthe experiment.A series of tests was carried out in March and

April 2013. This is the time around the spawning per-iod of both species in the field (Tomlinson & Perrow2003; Grabowska 2005); however, the fish did notshow any symptoms of spawning readiness (withregard to morphology, colouration or behaviour) inthe laboratory. The bullhead used in the experimentwere released at the place of capture; the racer gobywere euthanised by anaesthetic overdose.

Data analysis

During the video-recording analysis, the followingevents were noted for each fish: (1) consecutiveentrances and exits from the shelter and (2) acts ofaggression in the form of (i) attacks (dynamicapproach of one individual towards the other associ-ated with biting and/or chasing) and (ii) threateningevents (stretching the dorsal fins to frighten a com-petitor and drive it from an occupied zone withoutany physical contact between the individuals).Single-species treatments were designed to check

the typical behaviour of each species not restricted bythe presence of a competitor species. We assumedthat dominating individuals from each single-speciespairs (i.e., the ones spending more time in the shelterand being more aggressive) would show species-spe-cific behaviour, not limited by the presence of a com-peting species. Thus, the data for the dominatingindividuals from single-species treatments were usedin all analyses described below.The following comparisons were carried out in sep-

arate analyses: (i) dominating gobies versus dominat-ing bullheads from single-species treatments, to checkfor the differences in the behaviour of both speciesindependent of their interspecific interactions; (ii)dominating bullheads from single-species treatmentversus bullhead from two-species treatment, to checkfor the effect of racer goby on the behaviour of bull-head and (iii) dominating gobies from single-speciestreatment versus gobies from two-species treatment,

to check for the effect of bullhead on the behaviourof racer goby. The data were analysed with two-wayANOVAs with species (in comparisons between single-species treatments) or accompanying species (in com-parisons of single-species treatments with two-speciestreatments) and current velocity (0, 10 or 30 cm�s�1)as factors. The analyses were followed by sequentialBonferroni-corrected Fisher LSD tests used whennecessary as a post hoc procedure for significanteffects. Dependent variables tested in analyses wereas follows: (i) time spent by fish in the shelter(expressed as the percentage of the total observationtime); (ii) number of entries of fish into the shelter;(iii) number of entries of fish into the shelter alreadyoccupied by the other individual; (iv) number ofattacks during the experiment duration and (v) num-ber of threatening events. The percentage data (#1)were arcsine transformed, and the count data (#2–5)were square root transformed to decrease the violationof normality and homoscedasticity assumptions in ANO-

VA. Only the gobies (comparison iii) were analysedwith regard to the entries to the occupied shelter vari-able (#3), as only the gobies kept with bullheads dis-played this behaviour often enough. Also, only theaggression of gobies (variables #4 and 5) was tested,as the bullheads did not display any aggressive eventsat all during the entire study. Any differences in thenumbers of aggressive interactions displayed by thefish could result either from the change in their aggres-sion level caused directly by water flow, and/or fromthe differences in the time spent by them in the shelterat various flow velocities (as we could only observeaggressive events taking place outside the shelter). Tocheck this, we carried out another ANOVA using thenumber of aggressive interactions (attacks or threaten-ing events) per a unit of time spent by both fish out-side the shelter as a dependent variable. Only thecases in which both fish were present together outsidethe shelter for at least 10 min were used in this analy-sis. Due to the insufficient number of availablereplicates, we had to drop 30 cm�s�1 treatment fromthis analysis, as at this flow velocity, many fish tendedto spent nearly all the time in the shelter. Additionally,we analysed the time spent in the shelter together byboth individuals using the data from all three treat-ments (single-species goby, single-species bullheadand two-species treatment).

Results

Time spent in the shelter

Time spent in the shelter by dominating individualsfrom single-species pairs depended on the fish spe-cies and flow rate, as evidenced by a significant spe-cies 9 current interaction (F2,49 = 3.39, P = 0.042,

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full details of the statistical analysis are given in thesupplementary materials, Table S1A). The racer gobyspent less time in the shelter than bullhead. Onlyracer goby significantly increased their time spent inthe shelter with increasing water velocity (Fig. 2).The presence of racer goby reduced the residence

time of bullhead inside the shelter (Fig. 2) regardlessof flow velocity (accompanying species effect:F1,66 = 11.47, P = 0.001, Table S1B). On the otherhand, the racer goby did not respond significantly tothe presence of bullhead (accompanying specieseffect: F1,67 = 2.53, P = 0.116, Table S1C). How-ever, at 30 cm�s�1, a tendency to reduce time spentin shelter by the racer goby in the presence of bull-head could be observed (Fig. 2).The analysis of time spent by both fish together in

the shelter (Fig. 2) showed that this behaviour wasdisplayed most often by the pairs consisting of twobullheads. The mixed pairs spent significantly lesstime in the shelter, whereas the pairs formed by twogobies were almost never found together in the shel-ter (pair of species effect: F2,91 = 24.93, P < 0.001,Table S1D).

Aggression acts

The racer goby turned out to be definitely moreaggressive towards both conspecifics and individualsof a competing species, compared to the bullhead(Fig. 3). The bullhead did not exhibit any aggressionacts against any fish in our study. In the combina-tions involving the racer goby, one of the individualsalways clearly dominated the other one. A flowvelocity of 30 cm�s�1 caused a complete inhibitionof attacks by the racer goby (current effect:F2,66 = 6.86, P = 0.002, Table S1E). At lower flowvelocities, the number of attacks depended on thecompetitor species (accompanying species effect:F1,66 = 6.15, P = 0.016, Table S1E). The number ofattacks of the racer goby against bullhead at 10 and20 cm�s�1 was significantly lower than that displayedduring intraspecific competition (Fig. 3a).Threatening acts displayed by the racer goby with-

out any physical contact with the other individualwere directed almost exclusively against conspecificsand occurred at the flow velocities lower than30 cm�s�1 (Fig. 3b), resulting in a significant accom-

Fig. 2. Time spent by gobies (filled circles) and bullheads (open circles) in the shelter. G1 and B1 indicate dominating gobies and bull-heads in single-species treatments, respectively, whereas G2 and B2 indicate subordinated fish. Error bars are standard errors of the mean.Grey diamonds indicate the time spent in the shelter by both fish together. Asterisks indicate the cases in which the behaviour of fish dif-fered between the single-species and two-species treatments (Table S1B-C). The same letters (a, b) above the circles indicate the flowvelocities which did not differ from one another (P > 0.05) with regard to the time spent in the shelter by a given species (Table S1A-C).The same letters (x, y, z) above the diamond symbols indicate the flow and fish treatments which did not differ from one another withregard to the time spent by both fish together in the shelter (Table S1D). ‘#’ marks indicate significant differences between gobies and bull-heads from the single-species treatments (Table S1A)

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panying species 9 current interaction (F2,66 = 8.54,P = 0.001, Table S1F).The analysis of aggression acts expressed per unit

of time spent by both fish outside the shelter(Fig. 3c,d) showed no significant differences amongthe flow rates and competitor species except for thefact that threatening acts were directed primarilyagainst individuals of their own species (accompany-ing species effect: F1,21 = 8.90, P = 0.007, TableS1H). This means that the differences observed in theprevious analyses can be accounted for by the differ-ent residence times of fish in shelters in various flowconditions. However, this analysis should be treatedwith care due to the low number of replicates leftafter excluding unsuitable cases (i.e., those withinsufficient amount of time spent by both individualsoutside the shelter).

Entries to the shelter

The racer goby was more active than bullhead, oftenleaving the shelter and returning to it again (Fig. 4),as shown by a significant species effect in the analy-sis of single-species treatments (F1,46 = 40.61,

P < 0.001, Table S1I). The presence of the racergoby reduced the number of entries to the shelterexhibited by the bullhead (accompanying specieseffect: F1,66 = 4.55, P = 0.037, Table S1J), whereasthe presence of the bullhead had no effect on the fre-quency of this behaviour shown by the racer goby(accompanying species effect: F1,67 = 1.29, P =0.261, Table S1K). The racer goby never attemptedto enter the shelter when it had already been occupiedby another goby (Fig. 4), whereas they regularlyentered the shelter occupied by a bullhead (accompa-nying species effect: F1,67 = 23.16, P < 0.001, TableS1L). Entries of bullheads to the occupied shelterwere rarely observed (Fig. 4). However, it should benoted that the fish of this species tested in runningwater often spent most of the observation timetogether in the shelter (Fig. 3), to which they musthave entered during the adaptation time (before arecording was started).

Discussion

The experimental studies on the competition betweenthe Ponto-Caspian gobiids and native species for lim-

(a)

(c)

(b)

(d)

Fig. 3. Numbers of attacks (a, c) and threatening acts (b, d) displayed by gobies against conspecifics and bullheads during the entire exper-iment duration (a–b) and per 1 h of time spent by both fish outside the shelter (c–d). G1 and G2 indicate dominating and subordinatedgoby individuals, respectively. Error bars are standard errors of the mean. The same letters above the symbols indicate the treatments inwhich fish behaviour did not differ from one another.

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ited environmental resources, such as food (Kakarekoet al. 2013a) and shelter/habitat (Dubs & Corkum1996; Balshine et al. 2005; Van Kessel et al. 2011;Copp et al. 2013) have shown the potential outcomeof their competition under controlled conditions instagnant water only (aquaria). However, in Europe,the foremost potential areas of their competition withthe bullhead Cottus gobio in the field seem riversconstituting corridors for the spread of gobies (Coppet al. 2005; Grabowska et al. 2008; Roche et al.2013). Given that the bullhead seems better adaptedto life in the fast-flowing parts of rivers, we hypoth-esised that it should effectively compete with theracer goby for the shelter under high-flow conditions.However, our results did not confirm the hypothesis.Conversely, we have shown that the racer goby is aversatile invader that can effectively compete forshelters even in suboptimal conditions, like higherthan preferred flow velocities. The bullheads weredisplaced from the shelter by the competing racergoby regardless of the flow velocity up to 30 cm�s�1,thus also above the range preferred by the racer goby(>20 cm�s�1) (Kakareko 2011). The racer gobyclearly reduced their activity and remained in theshelter for a longer time at the flow of 30 cm�s�1,which suggests that such conditions were suboptimalfor this species. In general, the fish from Gobiidae

family seem not well adapted to deal with strongwater current as most or all of their sensory organs(neuromasts) responsible for perception of watermovements are located on the surface of the skinrather than in the canals of the lateral line, which isusually typical for fish associated with quiet environ-ments (Janssen 2004). Nevertheless, the racer gobyappeared to be an efficient competitor for space infaster than preferred flowing water. Thus, the presentstudy gives valuable insight into our understandingof invasiveness of the racer goby in lotic environ-ments.Factors responsible for shaping the relationship

between the species are probably associated predomi-nantly with aggression intensity and form, whichdiffered interspecifically. In our study, the racer gobyrepeatedly showed acts of aggression against otherfish regardless of species. However, the quality andquantity of these acts depended on the species, aswell as on the flow velocity. The predominating formof aggression exhibited by gobiids was a direct attackassociated with biting and/or chasing the rival. Suchattacks were directed towards both species, but thehighest number was recorded during intraspecificrelationships. Strong intraspecific competition con-nected with direct aggression in the goby confirmsthe results obtained by Dubs & Corkum (1996) as

Fig. 4. The number of entries of gobies (filled circles) and bullheads (open circles) into the shelter. G1 and B1 indicate dominating gobiesand bullheads in single-species treatments, respectively, whereas G2 and B2 indicate subordinated fish. Grey diamonds show the numbersof entries to the occupied shelter. Error bars are standard errors of the mean. Asterisks indicate the cases in which the total number ofentries differed between single-species and two-species treatments (Table S1J-K). ‘$’ marks show the cases in which the number of entriesto the occupied shelter differed between gobies from the single-species and two-species treatment (Table S1L). ‘#’ marks indicate signifi-cant differences between gobies and bullheads from the single-species treatments (Table S1I).

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well as Savino et al. (2007) who showed that theround goby more frequently attacked conspecificsthan individuals of the mottled sculpin (Cottus bairdi)and ruffe (Gymnocephalus cernuus). This corrobo-rates with the fact that intraspecific aggression is usu-ally stronger than in the case of interspecific relations(Connell 1983). Nevertheless, aggression directedtowards heterospecifics is quite common in nature(Peiman & Robinson 2010) and may shape speciesdistribution (Maruyama et al. 2010) as well as theoutcome of interspecific competition (Barbaresi &Gherardi 1997; Warnock & Rasmussen 2013).Interestingly, at the lower flow velocities, including

that preferred by the racer goby (10 cm�s�1)(Kakareko 2011), the level of aggression remainedconstant, whereas almost all acts of aggression disap-peared at the value of 30 cm�s�1. This is probablyrelated to the limited possibilities of gobies to handlefast flow velocities and increased time spent by themin the shelter under such conditions. A reduction ofinterspecific aggression in more demanding environ-mental conditions has been observed in various spe-cies of trout, in which water flow modified theoutcome of a competition between the bull trout(Salvelinus confluentus) and the brook trout (S. fonti-nalis) (Warnock & Rasmussen 2013). Nevertheless,it should be emphasised that in our study, despite thereduction of aggression, the presence of the racergoby still restricted the residence time of the bullheadin the shelter at the high flow velocity. At a strongerflow, this influence can be even more important thanin stagnant water, because the success of the bull-head, being a relatively poor swimmer (Tudoracheet al. 2008) devoid of a swim bladder, depends onthe availability of shelters in the strong current(Tomlinson & Perrow 2003).In contrast to the behaviour of the racer goby, we

did not record any direct attacks of bullheads againstthe racer goby or conspecifics. It has been reportedthat the intraspecific hierarchy in bullhead is mainlybased on sound waves of a specific frequency, aswell as behavioural postures such as fin stretchingand head shaking. Direct acts of aggression by bull-head in intraspecific competition are rare (Ladich1989; Tomlinson & Perrow 2003). On the contrary,in the racer goby, the aggression in the form of bit-ing, threatening acts and attacks seems to be anessential element of establishing a hierarchy in thepopulation, as well as of interspecific competition forlimiting shelter resources. Direct aggression formsseem more likely to be efficient in interspecific inter-actions, when similar species have to compete forlimited environmental resources (Peiman & Robinson2010). Such behavioural patterns might have evolvedin an organism co-occurring in its native range withseveral species utilising similar environmental

resources. Evolution in a highly competitive multi-species community has been postulated as a cause ofa great invasion success of the group of Ponto-Cas-pian amphipods (Devin & Beisel 2008). Perhaps,sympatric Ponto-Caspian neogobiid fishes constitutea similar type of community.The time spent in the shelter by the dominating

fish was influenced by the species and flow velocity.At lower flow velocities, the racer goby tended tospend more time outside the shelter than the bull-head, but in both species, there was a noticeable ten-dency for a longer stay in hiding with the increasingflow velocity. This was particularly evident for themaximum flow speed when both species spent mostof time inside the shelter. There were, however,between-species differences in behaviour under high-flow conditions. The bullhead, in contrast to the racergoby, tolerated conspecifics inside the shelter. In sin-gle-species treatments, both individuals entered theshelter during the adaptation period and did not leaveit until the end of observation. This phenomenon wasnot observed in the racer goby, which occupied theshelter with the bullhead, but never with another con-specific. This can be explained by strong intraspecificcompetition and aggression exhibited by the racergoby. It was confirmed by the fact that in each pairconsisting of two racer gobies, one clear dominantappeared, prevailing over its competitor in terms ofboth residence time in the shelter and aggressivebehaviour.Another trait strongly differentiating between both

species is their predisposition to take over a shelterthat has already been occupied by a competitor andthe ability to defend their own shelter. The bullheadallowed conspecifics to enter the shelter and wasunable to defend a shelter against racer goby intrud-ers. It was also unable to enter the shelter inhabitedby a goby. The racer goby, on the other hand,showed a remarkably different behaviour, effectivelydefending its shelter against competitors, as well aseasily displacing the bullhead individuals from theshelters occupied by them. Such a strategy may be afactor giving it a significant advantage over ‘defence-less’ species, unaccustomed to physical competitionfor shelter.Invasive species, newly occurring in the environ-

ment, can cause a complete removal or significantreduction of the distribution range of species withsimilar ecological niches (MacNeil et al. 2004).However, the competitors often exhibit a great levelof plasticity, allowing them to coexist at the expenseof a partial change or reduction of the width of theniche (Robinson & Wilson 1996; Platvoet et al.2009; Maruyama et al. 2010). The outcome of suchan encounter between two species may depend onlocal environmental conditions, shaping their behav-

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iour and aggression level of both competitors(Taniguchi & Nakano 2000; Warnock & Rasmussen2013). The possibility of displacement or coexistenceof populations in the case of the racer goby and bull-head remains an open question. In the LaurentianGreat Lakes of North America, a local bullhead spe-cies Cottus bairdii has been effectively displaced bythe round goby Neogobius melanostomus, which winthe interspecific competition for spawning sheltersand consume bullhead eggs (Dubs & Corkum 1996;Janssen & Jude 2001). Our results showed that racergoby was able to compete with European bullhead insuboptimal conditions, like running waters, at leastup to 30 cm�s�1. Our experiment and other recentstudies (Copp et al. 2013; Kakareko et al. 2013a)have definitely shown the superiority of the racergoby in the competition for limited environmentalresources. Nevertheless, to further validate this state-ment, it is necessary to test the interactions betweenthe species thoroughly in the field, in the locations oftheir shared occurrence. In Europe, the racer gobyrapidly colonised the Vistula River system (Grab-owska 2005), but they do not occur in other rivercorridors (Roche et al. 2013). So far, only Kakarekoet al. (2013b) have conducted a field research in theplace of the occurrence of the European bullheadshortly after the invasion of the racer goby in thearea. The results indicate a significant habitat parti-tioning between species, with the bullhead primarilyoccupying sites with fast water flow. However,within the sites co-occupied by both species, signifi-cant negative relationships have been observed. Thefurther fate of the bullhead population experiencingthe pressure of invasive gobies is difficult to predict.It might be able to survive in lotic habitats, or afurther increase of the racer goby abundance mayresult in their expansion also to areas with strongerflow, where, as indicated by our current results, theymay also threaten the bullhead. This phenomenon isoften observed in the case of two invasive dreissenidspecies, Dreissena polymorpha and D. rostriformisbugensis. The latter, being a more efficient competi-tor, after its appearance in the water body inhabitedby the former species, first begins to dominate in thedeeper parts, on soft sediments, where its competitivesuperiority is most pronounced, but over time, itgradually dominates all areas and totally displacesD. polymorpha (Nalepa et al. 2010). In the case ofthe racer goby and European bullhead, this questionrequires further complementary studies in the labora-tory and field.

Acknowledgements

Our research was supported by a Grant of the Polish Ministryof Science and Higher Education No. N N304 371539. We

are grateful to Małgorzata Pozna�nska for her assistance in thefield, as well as to John Janssen and an anonymous reviewerfor their valuable comments which helped greatly improve ourarticle.

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Supporting Information

Additional Supporting Information may be found inthe online version of this article:Table S1. Two-way ANOVA of the variables tested

in the study. SS – single-species treatments, TS –two-species treatments.

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