Expansion of round gobies in a non-navigable river system

Limnologica 67 (2017) 27–36

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

Expansion of round gobies in a non-navigable river system Luděk Šlapanský a b

a,b,⁎

a

a

, Michal Janáč , Roche Kevin , Mikl Libor

a,b

, Jurajda Pavel

MARK a

Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, Brno 603 65, Czech Republic Institute of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 246/2, 611 37, Brno, Czech Republic

A R T I C L E I N F O

A B S T R A C T

Keywords: Impact Invasive species Neogobius melanostomus Pioneer fish Population characteristics Proterorhinus semilunaris

A number of Ponto-Caspian Gobiid species have greatly increased their geographical ranges over recent decades. Most expansion studies to date, however, have focused on navigable waterways. In this study, we present a summary of six-years (2008–2013) monitoring of round goby Neogobius melanostomus expansion along two connected non-navigable rivers. Contiguous range expansion was observed in both rivers, with dispersal rate ranging from 1.2 to 3.2 km/year. Gobies at newly invaded sites ranged from 20 to 117 mm, with both juveniles and adult fish observed. Though the data did not allow us to see any consistent pattern in the first years after 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 Several Ponto-Caspian gobiid species have greatly increased their ranges over recent decades (see Roche et al., 2013 for a review). Of these, the most successful has been the round goby Neogobius melanostomus, which has now spread throughout several major European river basins, including the Rhine (Borcherding et al., 2011) and Danube (spreading beyond their original range; Jurajda et al., 2005; Wiesner, 2005; Paintner and Seifert, 2006). In addition, round gobies have been introduced into the Laurentian Great Lakes Basin of North America and have gone on to colonise a number of major rivers and streams (Marsden and Jude, 1995). While this range expansion has been the subject of numerous studies in recent years, most have described expansion along navigable rivers and canals, presumably as transport in and on shipping is considered the main vector for 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). To date, relatively little has been written on ‘natural’ expansion (i.e. continuous range expansion by swimming alone) into and along non-navigable rivers and streams. Furthermore, most existing studies have concentrated on round goby occurrence in tributaries of the Great Lakes (Phillips et al., 2003; Krakowiak and Pennuto, 2008; Bronnenhuber et al., 2011; Brownscombe and Fox, 2012). To the best of our knowledge, just two studies have examined natural dispersal of round goby in non-navigable European tributaries, that of Brandner et al. (2013b), who reported rapid spread of round ⁎

gobies in an area immediately adjacent to (and partially overlapping with) the navigated section of the upper Danube, and Zarev et al. (2013), who documented round gobies 100 km upstream along nonnavigable tributaries of the Danube in the species’ native range (Bulgaria), though the authors provided no information on the rate of movement. Those studies that have examined expansion along non-navigable tributaries (USA or Europe) have noted considerable variation in the results. Speed of expansion, for example, was recorded at 0.5 km per year by Bronnenhuber et al. (2011) but at 17 km per year by Brandner et al. (2013b). There is also disagreement over the character of ‘pioneer’ fish found at the invasion front, with some studies reporting larger individuals (Gutowsky and Fox, 2011; Brandner et al., 2013b) and others suggesting that the driving force behind the invasion process are smaller (mainly male) fish that are forced into new areas through competition with larger individuals (Ray and Corkum, 2001; Brownscombe and Fox, 2012; Masson et al., 2016). On top of this, relatively little is known about how non-native gobies affect fish assemblages in rivers, despite this being one of the major concerns of gobiid invasion (Janssen and Jude, 2001; French and Jude, 2001; Balshine et al., 2005). Experimental studies suggest that round goby should have a negative impact on native fish assemblages via competition for shelter and food, spawning interference and predation on eggs and juveniles (e.g. Steinhart et al., 2004; Balshine et al., 2005; Bergstrom and Mensinger, 2009), with benthic species utilising similar 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.

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Republic (Fig. 1). Both the Morava, a main tributary of the Danube, and the Dyje, the Morava’s most important tributary, are non-navigable throughout (with the exception of occasional recreational canoes). The study covers a 44 km stretch of the Morava starting from the Czech border (70 km from its confluence with the Danube) and a 42 km stretch of the Dyje, starting from its confluence with the Morava (Fig. 1). Between 1968 and 1982, both rivers were channelised and their riverbanks stabilised with rip-rap, that on the Morava generally larger (30–80 cm max. diameter) than on the Dyje (15–25 cm; though stones of 40–60 cm are found at some locations). Channel width on the Morava varies between 40 and 60 m and depth ranges between 0.8 and 1.0 m. The Dyje is slightly narrower at 30–50 m, with depth similar at between 0.5 and 1.0 m. Annual mean discharge near the confluence is 61.1 m3 s−1 for the Morava and 41.7 m3 s−1 for the Dyje (Czech Hydrometeorological institute; http://portal.chmi.cz). Current speed along the banks rarely reaches 0.2 m s−1 on the Morava and 0.4 m s−1 on the Dyje. The bottom substrate of both rivers comprises sand, gravel and pebbles with patches of silt. Aquatic vegetation, woody debris, pools and riffles occur rarely. Prior to round goby invasion, both rivers supported a relatively diverse fish assemblage (Valová et al., 2006) dominated by native cyprinid species (e.g. 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 albipinatus (Jurajda and Peňáz, 1994), along with a stable population of non-native tubenose goby Proterorhinus semilunaris, which quickly became established after its introduction in the 1990s (Janáč et al., 2012). Round goby have been recorded in the middle Danube since 2000

includes not only native cottids (Verreycken, 2015) but also other nonnative gobiids. Valová et al. (2015), for example, suggested that tubenose goby Proterorhinus semilunaris, another, smaller Ponto-Caspian invader with a similar distribution to round goby, should prove an inferior competitor. Studies that have actually set out to determine impact at the population/assemblage level in the field are even rarer, with only three assessing round goby impact in rivers (Kornis et al., 2013; Janáč et al., 2016; Van Kessel et al., 2016). While studies from the Great Lakes have tended to document immediate and profound impacts on demersal fish communities following introduction of round goby (e.g. Janssen and Jude, 2001; Lauer et al., 2004), such an impact has only been observed in one (Van Kessel et al., 2016) of the three riverine studies thus far undertaken. Clearly, more studies are needed before population patterns prevalent at the goby invasion front can be generalised and actual impacts on native fish communities identified, both essential for the future management of this invasive species. In this paper, we present longterm data on the expansion of round goby along two connected nonnavigable European rivers. In doing so, we a) estimate speed of colonisation, b) describe population structure characteristics (body size, sex-ratio, proportion of juveniles) at first occurrence (along with any changes over the years following first occurrence), and c) assess possible impacts on the assemblage of fish captured in the nearshore riprap zone over time. 2. Material and methods 2.1. Study area This study took place on the Rivers Morava and Dyje in the Czech

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.

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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 D2 D3 D4 D5 D6

4.9 11.7 19 28 36 42.1

74.9 81.7 89 98 106 116

48.6412869 48.6914906 48.7340610 48.8277258 48.8277258 48.8572831

16.9268337 16.9170981 16.8849114 16.8594947 16.7731198 16.7245047

M1 M2 M3 M4 M5

73 74.3 78.7 85.7 93

48.6355256 48.6477614 48.6807642 48.7335697 48.7813386

16.9626603 16.9694194 16.9786092 17.0192761 17.0753558

(P) (P) (P) (S) (S) (N)

(see Roche et al., 2013). The first individuals caught in the Morava (Slovakia-Austria stretch; see Fig. 1) were found at several localities up to 19 km upstream of the confluence in 2006 (Lusk et al., 2008), with the first specimens in the Czech stretch being caught in 2008 below a weir at rkm 74.3 (Lusk et al., 2008; Fig. 1). In the same year, examples were also recorded at rkm 13.8 on the Dyje and below a weir near the town of Břeclav at rkm 22.3 (Lusk et al., 2008; Fig. 1).

(P) (S) (S) (N) (N)

shoreline (typically 200 m). The sampling effort in this study corresponds roughly with that of previous studies on gobiid impact on riverine fish communities (Kornis et al., 2013; Van Kessel et al., 2016). As sampling did not cover the whole width of the river, we only consider the fish assemblage captured along the rip-rap in our analysis of possible gobiid impact. 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 (Kornis et al., 2012). 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. All gobiid fish were then overdosed with clove oil and fixed in 4% formaldehyde for later analysis in the laboratory. Fish abundance was estimated using catch per unit effort (CPUE), measured as individuals captured per metre of shoreline (per 100 m in Tables 2 and 3).

2.2. Data collection The Institute of Vertebrate Biology, Czech Academy of Sciences, has monitored the progress of this round goby invasion since the first record in 2008. Sampling takes place each autumn when water discharge is more stable, fish are easily sampled and are old enough to be easily identified. Five sampling sites were initially established near the confluence of 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 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 are treated as ‘initial’ monitoring sites in the analysis). From 2009, sampling was extended with three further ‘secondary’ sites along the Dyje (D3-D6; Fig. 1) in order to allow repeated sampling of the fish community at sites at and above the invasion front. Following the reappearance of gobies at site M2 in 2011, three secondary upstream sites were also added to allow repeat sampling of the fish assemblage (M3M5; Fig. 1). Sampling always took place during the day (10:00-16:00) in autumn (from 20 October to 24 November). Conditions at the sampling sites remained relatively stable at each site between years, i.e. river discharge (maximum inter-annual divergence 11 m3 s−1) and mesohabitat (substrate, vegetation cover) changed little, leaving little room for inter-annual changes in fish assemblage attributable to habitat change. Fish were sampled by electrofishing using a portable backpack unit (SEN f. Bednář, Czech Republic; maximum output 225/300 V, frequency 75–85 Hz) fitted with an small elliptical stainless-steel anode (25 × 15 cm) with 4 mm mesh netting (Janáč et al., 2016). 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 all fish inhabiting the littoral rip-rap. Electrofishing of the nearshore zone is a reliable and commonly used method for sampling not only round goby assemblages (Brandner et al., 2013a) but also for describing riverine fish communities in general (Fame Consortium, 2004). Indeed, electrofishing was the method used in all three studies thus far published documenting round goby impact on native fish in rivers (i.e. Kornis et al., 2013; Van Kessel et al., 2016; Janáč et al., 2016). As the rivers are 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 almost the whole rip-rap zone in this stretch of river. Each sample site consisted of 100–400 m of rip-rap

2.3. Statistical analysis As gobies were already present at the four initial sites (D1, D2, D3, M1) in 2008, and as irregular sampling at these sites before 2008 failed to detect round goby, all sites were probably settled in the same year, i.e. 2008; hence, data from these four sites were pooled in order to better describe body size, sex-ratio and proportion of juveniles for each year after goby detection. The G-test was used to test for deviation of sex-ratio from parity in each year (exact binomial tests were used when expected frequencies were lower than five). Sex-ratio was expressed as number of females per male. Although our original aim was to statistically test for differences in fish-size, proportion of juveniles and proportion of females between years, we restricted ourselves to a simple description of any observable patterns as the sample sizes in the first years of invasion were too small (even when pooled across the initial sites) to provide more than indications. Due to the relatively low abundance and high turnover of native species (see Results), we restricted our analysis of impact on the fish assemblage to a) abundance (log-transformed) of tubenose goby (the only species showing a suitably high abundance) and the native fish pool, and b) native fish diversity indices (species richness, Shannon index, Simpson index, evenness). Effects on these response variables were tested using linear mixed models (LMM), with site as a random effect and measurements of round goby population status as fixed predictors. Three possible measurements of round goby population status were considered: a) simple abundance, b) abundance in the previous year (controlling for a possible time-lag in round goby effect) and c) phase of round goby establishment (categorical predictor with two levels: ‘non-established’, which merged years with no round goby and the first years after occurrence with few size classes present and relatively low goby density [ < 6 inds.100 m−1]; and ‘established’, which included years with many size-classes present and a relatively high goby density [ > 25 inds. 100 m−1]). As fish assemblage structure could also have been affected by environmental conditions in previous 29

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3.4. Body size

years (e.g. strong cohorts may arise from years with suitable environmental conditions), we controlled for the possible effect of calendar year by including calendar year as a fixed covariate (treated as a categorical factor).

Round gobies captured at the initial sites in 2008 were generally larger than those captured in subsequent years (Fig. 2A; note, however, the low sample size), with some fish being amongst the largest gobies 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). Length-frequency distribution at the initial sites appeared to stabilise, with clearly separated size categories apparent from 2010 on (Fig. 3). In contrast to the initial sites, the first fish colonising secondary sites were mostly smaller individuals, including juveniles (Fig. 4).

3. Results 3.1. Assemblage of fish captured along the rip-rap We caught 12 140 fish during the study (6 342 tubenose goby; 1 719 round goby and 4 079 other), comprising 31 species (29 on the Dyje, 27 on the Morava; Supplementary Tables S1 and S2). The fish assemblage along the rip-rap zone of both rivers was relatively similar (Supplementary Tables S1 and S2). Tubenose goby was the most common species on both the Morava and Dyje, representing between 10 and 94% of all fish caught each year (Supplementary Tables S1 and S2). Perch (Perca fluviatilis), burbot (Lota lota), roach and chub were the most common native species in the Dyje, and European bitterling, white-fine gudgeon, barbel, chub and perch in the Morava (Supplementary Tables S1 and S2). Within three years of detection, round gobies had become common in both rivers, representing between 14 and 75% of all fish caught.

3.5. Sex ratio During the early phase of invasion, the low numbers of fish caught were insufficient to state whether there was a clear trend in sex ratio at the initial sites, despite a significant female-dominated ratio in 2010 (1:8; G-test, P < 0.05; Table 2). While the sex ratio remained close to parity in 2011, there was an increasing trend towards female dominance from then on, with a significant deviation from parity observed in 2013 (1:1.6; G-test, P < 0.05; Table 2). At the secondary sites, the 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 caught were relatively low (Table 2).

3.2. Round goby dispersal The first round gobies caught along the Czech stretch of the Morava 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 M1 (rkm 73, Fig. 1), however, and no round gobies at M2 until 2011, despite regular sampling. In 2011, the invasion front moved a further 4.4 km upstream to site M3 (Fig. 1) and several specimens were recorded just under a weir at rkm 79.5 in 2012, approximately 1 km upstream of site M3 (Jurajda, unpublished data). No further occurrence of gobies has been recorded upstream of this apparent migration barrier since then. During this five-year period (2008–2013), round gobies colonised 5.8 km of the Morava, representing an average of 1.2 km upstream expansion per year. In doing so, the gobies overcame two migration barriers, the first a 1.5 m ogee-type weir (rkm 74.3; site M2) and the second an inoperable 0.5 m inflatable weir (rkm 77.4), neither of which had fish ladders. The first round gobies on the Dyje were also recorded in 2008 (Lusk et al., 2008), at rkm 13.8 close to our locality D2 (rkm 11.7) and near the town of Břeclav, close to our locality D3 (rkm 19; Fig. 1). Our own monitoring confirmed round goby presence at two downstream localities (D1 [rkm 4.9] and D2) later the same year. In 2010, a single specimen was captured 9 km upstream of D3 (site D4, rkm 28) and five specimens were collected 8 km upstream of site D4 in 2012, below a weir near the village of Bulhary (site D5, rkm 36). Round gobies have not progressed upstream of this point since 2012. Thus, the round goby invasion front moved 12.9 km over four years on the Dyje, representing an average movement of 3.2 km per year. During this time they overcame 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 boulder-ramp fish ladders.

3.6. Effect on the nearshore fish assemblage Round goby invasion appears to have had no significant effect on diversity or pooled abundance of the assemblage of native fish captured along the nearshore rip-rap zone (LMM, all P > 0.05; Table 3). On the other hand, there was a significant decline in tubenose goby abundance following round goby establishment (LMM, P < 0.05; Table 3), though with no direct correlation between abundance of the two species (LMM, P > 0.05; Table 3). An apparent decline in tubenose goby abundance following a sudden increase in round goby density is particularly visible at sites D1, D2, D3 and D5, with a weaker or no response visible at other sites (Fig. 5). 4. Discussion In the Czech Republic, we were lucky enough to identify invasive gobies entering the country at a very early stage. This has allowed us to accumulate long-term data on the expansion of the round goby population along two connected non-navigable rivers. In doing so, we were able to estimate speed of colonisation and, to some extent, document a range of population structure characteristics (i.e. body size, sex-ratio, proportion of juveniles) at first occurrence, along with any changes several years after first occurrence. Furthermore, multi-year sampling along the rip-rap provided data with the potential to reveal large detrimental changes in the native fish assemblage along the nearshore riprap zone attributable to round goby. 4.1. Range expansion Round goby expansion up (and down) navigable rivers has been rapid and wide-ranging thanks to long-distance transfer of fish via shipping and boat transport (Borcherding et al., 2011; Kalchhauser et al., 2013; Mombaerts et al., 2014; Roche et al., 2015), subsequently followed by natural expansion through swimming and downstream drift of juveniles (Janáč et al., 2013b). While studies on the Rhine have shown an average expansion rate of around 67 km/year (Manné et al., 2013), expansion rates in open waters or lentic systems tend to be lower, reaching around 6–10 km/year in the Baltic Sea (Rakauskas et al., 2013) and 14 km/year in Lake Michigan, USA (Bergstrom et al., 2008). The few studies to have monitored natural (i.e. swimming only)

3.3. Proportion of juveniles At the initial sites, lowest numbers of juveniles were recorded during 2008 (the year round gobies were first detected), though the proportion was still relatively high at 40% (Table 2; note the relatively low sample size, though). From 2009 on, the proportion of juveniles never dropped below 60%, peaking in 2010 at 93% (Table 2). At the secondary sites, the proportion of juveniles in the first year of occurrence varied widely, ranging from almost 100% at D4 to just 20% at D5 (Table 2). 30

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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 Initial D4 D5 M2 M3

40% – – – –

2009 (10) – – – –

79% – – – –

2010 (19) – – – –

93% 100% – – –

2011 (125) (1) – – –

77% – – 48% 26%

2012 (319) – – (31) (35)

60% 99% 20% 0% 74%

2013 (236) (82) (5) (1) (54)

66% 63% 81% 54% 78%

(280) (46) (27) (11) (49)

b) Sex ratio (number of females per male) 2008 Initial D4 D5 M2 M3

NA – – – –

2009 (1) – – – –

3.0 – – – –

2010 (4) – – – –

8.0 – – – –

2011 (9) – – – –

0.9 – – 1.0 1.0

2012 (74) – – (16) (26)

1.3 NA 1 NA 1.3

2013 (94) (1) (4) (1) (14)

1.6 16.0 4.0 4.0 1.2

(95) (17) (5) (5) (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 potential for rapid natural upstream migration, with weirs slowing the pace of upstream expansion but not necessarily preventing it (see also Bronnenhuber et al., 2011). We are convinced, based on our results and experience, that the ‘natural’ round goby expansion process is a combination of two components, i.e. rapid movement by pioneers from the source population over a relatively long distance, followed by a slow filling of the gap between the source and ‘invasion front’ sub-populations. The invasion front comprises just a small number of pioneers exhibiting high levels of movement activity compared to the rest of the population (Lynch and Mensinger, 2012; Masson et al., 2016). Indeed, Myles-Gonzales et al. (2015) demonstrated that individuals predisposed to behaviours associated with dispersal, such as high levels of exploration activity, are more likely to be located along an invasion front. Brownscombe and Fox (2012) suggested that these pioneers tend to disperse into high quality habitats during the initial stages of invasion. This was confirmed by our data from locality D5 (unpublished). Here, round gobies were first recorded over a relatively short stretch of rip-rap comprising rocks 40–60 cm in diameter (our past experience suggests that this size tends to be preferred by round goby), while an 8 km stretch downstream consisting of 10–20 cm rip-rap combined with gravel beaches and eroded banks remained uncolonised (L. Šlapanský, unpublished data).

Fig. 2. Fish size (standard length in mm) at initial sites, calculated (A) for the whole population and (B) for non-juvenile fish only. Solid bar = median, Box = quartiles, Whiskers = non-outlier range (1.5 * quartiles), point = outlier.

upstream migration have recorded much lower rates, typically ranging from 0.5 km to 5 km/year (Bergstrom et al., 2008; Bronnenhuber et al., 2011; Brownscombe and Fox, 2012). Our results fit into this latter range, with an average progress of 3.2 km/year on the Dyje and 1.2 km/year on the Morava. It should be noted, however, that all these studies, including our own, have estimated upstream dispersion rates using data based on first recording only, i.e. not through direct observation of tagged fish movements, for example. As such, none of these studies can exclude the possibility that the observed dispersion rate was facilitated, or even ensured, through anthropogenic means, e.g. through transfer in angler’s bait buckets. On the other hand, the order in which gobies passed the inter-weir sections in our study (never moving further than the next upstream section on each occasion) decreases the probability of human-mediated transfer, suggesting natural migration as a more probable option. Differences in the rate of expansion between rivers could be attributable to the type and number of migration barriers along their length. In our own case, weirs on the Dyje almost all have baffle or bypass fish 31

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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).

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The gap between pioneers at the invasion front and the source population is then filled via a) downstream drift of early life stages (Janáč et al., 2013a,2013) originating from the ‘invasion front’ sub-population, and/or b) slow upstream movement of (presumably) juveniles from the source sub-population. The combination of these phenomena will lead to stratified dispersal and an increasing rate of expansion into new areas (Bronnenhuber et al., 2011).

Table 3 Results for linear mixed models predicting the effect of round goby abundance on the abundance or diversity of native species and non-native tubenose goby. For each model, significance of round goby-related predictors (P values) and degrees of freedom are shown. Significant P values (P < 0.05) are in bold. Response variable/ Predictor Degrees of freedom

Abundance

Establishment phase

1,26

Abundance previous year 1,20

Native species richness Native species Shannon diversity Native species Simpson diversity Native species Shannon evenness Native species pooled abundance Tubenose goby abundance

0.613 0.298

0.543 0.591

0.305 0.515

0.409

0.496

0.901

0.437

0.549

0.336

0.415

0.956

0.833

0.625

0.208

0.010

1,26

4.2. Population characteristics In our study, round gobies tended to be either relatively small (< 50 mm, mostly corresponding to 0+ fish) when first detected at a site, or relatively large (> 90 mm, mostly corresponding to fish 2+ and older). Both cases have been documented in the literature. Ray and Corkum (2001), for example, reported a high proportion of small fish in the earliest years of colonisation, attributing this to displacement from 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.

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indicated no such dramatic impacts. Previous studies along the Morava and Dyje, at sites similar to ours, have also demonstrated i) a lack of any round goby impact on native fish young-of-the-year abundance or habitat use (Janáč et al., 2016), and ii) no sign of gobiid predation on native fish eggs or juveniles (Vašek et al., 2014; Všetičková et al.,2014). This, in combination with our own data, tends to support a growing consensus that the consequences of invasion in rivers such as the Dyje and Morava differ from those reported for the Great Lakes. In the Great Lakes (but not in their tributaries, see Kornis et al., 2013), round goby have been shown to have a strong negative effect on some native fish species, especially benthic fish such as cottids (Janssen and Jude, 2001; Lauer et al., 2004). Such species are absent along the lower Morava and Dyje, for example, and other native benthic species are relatively rare and tend to be found in different habitats than round goby (Janáč et al., 2016). The only documented impact by round goby in a European riverine system to date was indeed demonstrated on a cottid, Cottus perifretum from the River Meuse (Van Kessel et al., 2016). In contrast, our own unpublished data suggests that another common cottid, the European bullhead (Cottus gobio), can form viable populations on the Danube, even in the presence of invasive gobiids. Notably, Piria et al. (2016) recorded some correlations between the abundance of round goby and two native benthic species, zingel (Zingel zingel) and the Balkan spined loach (Sabanejewia balcanica). Clearly, therefore, while the round goby has the potential to affect native benthic fish assemblages (e.g. through competition for diet or shelter; Van Kessel et al., 2011; Piria et al., 2016; Števove and Kováč, 2016), things are not so straightforward, suggesting that local conditions may play a stronger role than once thought in determining whether such potential impacts are realised. It is conceivable that our system may have been previously impacted by tubenose goby, which colonised our sites ten years before the arrival of round goby. As no such effect has ever been reported elsewhere (e.g. Van Kessel et al., 2016), however, we consider this highly improbable. Instead, we suggest that round goby in these rivers are not outcompeting native fish but are, in effect, utilising a “vacant niche” (Janáč et al., 2016). River channelisation along the Morava and Dyje resulted in both rivers being straightened and the banks strengthened with rip-rap. While such a habitat alteration apparently provided a suboptimal habitat for most native species (Wolter, 2001), rip-rap appears to provide optimal habitat conditions for round and tubenose goby (Ray and Corkum, 2001; Erős et al., 2005; Young et al., 2010). In contrast to native fish, round gobies do appear to have had an at least partial effect on tubenose goby abundance. The relatively small tubenose goby is an inferior competitor to round goby and is expected to decrease in abundance at sites with other gobiid species (Valová et al., 2015), as appears to have been the case at some of our sites. Round and tubenose goby habitat and dietary requirements overlap to a large extent (Pettit-Wade et al., 2015; Janáč et al., 2016) and it is quite possible that some resources were restricted to the extent that direct competition occurred between the two species, resulting in tubenose goby being outcompeted. Such cases of out-competition between two invasive species are only rarely reported (e.g. Braks et al., 2004). We should stress here that there was no direct negative correlation between abundance of round and tubenose goby and that we only observed differences in tubenose goby abundance between periods prior to and after establishment of round goby (Fig. 5). Furthermore, the impact on tubenose goby appeared to vary between sites, probably as a result of site-specific environmental conditions such as resource richness or local fish assemblage. Such small-scale differences in the degree of impact of an invasive species are rarely considered and we suggest further studies on ecosystem-specific impacts could prove useful for improving predictions of invasive species impact generally. It should also be noted that, while our paper provides a view on direct impact on the nearshore native fish assemblage, round goby also have the potential to affect aquatic ecosystems through other direct or indirect routes. These may, for example, include a negative impact on

of round goby populations, with larger individuals (> 50 mm TL) moving outside of small home ranges only rarely (Lynch and Mensinger, 2012). Several other studies, however, have recorded large individuals during the initial phase of invasion; hence, their role as pioneers cannot be ruled out (Gutowsky and Fox, 2011; Brownscombe and Fox, 2012; Brandner et al., 2013b). Myles-Gonzales et al. (2015), for example, noted that a propensity for explorative behaviour in invasion-front gobies was independent of body size, sex or age. Overall, it is almost impossible to demonstrate empirically which fish are the invasion pioneers as the low numbers of fish at the invasion front lowers the probability of timely detection (Clapp et al., 2001). It is possible, for example, that the invasion pioneers are always large individuals, but their numbers are too low for early detection (VelézEspino et al., 2010), meaning they are missed during early surveys and first detection follows only after a lag of a year or more. In this case, the first individuals caught may be the progeny of the first large pioneers, juveniles being naturally dominant at the invasion front. A number of authors have also found contradictory results for sex ratio. Studies in the Great Lakes, for example, have recorded malebiased populations in both the core (source) area (Corkum et al., 2004; Young et al., 2010; Thompson and Simon, 2015) and at the invasion front (Gutowsky and Fox, 2011), which would be consistent with males tending to be the more mobile sex (Marentette et al., 2011). On the other hand, other studies (Brownscombe and Fox, 2012; Brandner et al., 2013b) have recorded a female-dominated population at the invasion front. Our samples showed no sex-bias in invasion front, with relatively large variability among sites. It is possible that the differences in sexratio are a reflection of the time (season) of sampling, with studies undertaken in autumn, when highest movement activity might be expected (Thompson and Simon, 2015), for example, showing fewer males due to increased mortality after spawning, as observed in the Black Sea (Miller, 1986). It is also possible that different sampling methods result in a sex bias in the catch (Clapp et al., 2001; Jurajda et al., 2013). Alternatively, differences in sex ratio at the invasion front could simply be the result of high levels of variation. We suggest that any future studies should concentrate on exactly which factors result in male or female-biased sex ratios at the invasion front. 4.3. Effect on the nearshore fish assemblage Although round goby have quickly dominated the nearshore fish assemblage (Supplementary Table S2), our data suggest no detrimental effect of round goby on native nearshore fish assemblage diversity or pooled abundance. However, this does not necessarily mean that there was no detrimental effect on the overall fish assemblage. As we sampled only the rip-rap zone (2–4 m from the bank), fish concentrating in the main channel (typically bleak, asp Aspius aspius (Linnaeus) and large specimens of barbel, common bream and nase Chondrostoma nasus (Linnaeus); Adámek et al., 2013) were not effectively sampled. On the other hand, round goby in the Morava and Dyje avoid the clean flat gravel and sandy bottom of the main channel (Jurajda, unpublished data). As goby occurrence is restricted almost exclusively to the nearshore rip-rap zone, any direct impact is likely to manifest itself on those species residing mainly along the banks, i.e. those residing the habitat we sampled (e.g. tubenose goby, chub, perch or burbot). Given the relatively low density of native fish species along the nearshore zone, even before round goby invasion (Adámek et al., 2013; this study), sampling effort may have been too low to provide data robust enough for assessing direct effects of invasion. While we are aware of such a limitation, we are also convinced that our sampling design (multiple years at multiple sites) would have revealed the dramatic impacts (i.e. complete failure of reproduction or abundance decrease in orders of magnitude) reported elsewhere (e.g. Janssen and Jude, 2001; Lauer et al., 2004; Van Kessel et al., 2016). Though we did not statistically test for effects on particular species, a simple visual check of nearshore native fish abundance (Supplementary Table S2) 34

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Neogobius melanostomus, in Great Lakes tributaries. Mol. Ecol. 20 (9), 1845–1859. http://dx.doi.org/10.1111/j.1365-294X.2011.05030.x. Brownscombe, J.W., Fox, M.J., 2012. Range expansion dynamics of the invasive round goby (Neogobius melanostomus) in a river system. Aquat. Ecol. 46 (2), 175–189. http://dx.doi.org/10.1007/s10452-012-9390-3. Cammaerts, R., Spikmans, F., van Kessel, N., Verreycken, H., Chérot, F., Demol, T., 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. http://dx.doi.org/10. 3391/ai.2012.7.2.011. Clapp, D.F., Schneeberger, P.J., Jude, D.J., Madison, G., Pistis, C., 2001. Monitoring round goby (Neogobius melanostomus) population expansion in eastern and northern Lake Michigan. J. Great Lakes Res. 27 (3), 335–341. http://dx.doi.org/10.1016/ S0380-1330(01)70649-1. Corkum, L.D., Sapota, M.R., Skora, K.E., 2004. The round goby, Neogobius melanostomus, a fish invader on both sites of the Atlantic Ocean. Biol. Invasions 6 (2), 173–181. http://dx.doi.org/10.1023/B:BINV.0000022136.43502.db. Erős, T., Sevcsik, A., Tóth, B., 2005. Abundance and night-habitat use patterns of PontoCaspian gobiid species (Pisces, Gobiidae) in the littoral zone of the River Danube, Hungary. J. Appl. Ichthyol. 21 (4), 350–357. http://dx.doi.org/10.1111/j.14390426.2005.00689.x. 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. 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. 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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 (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their nonnative area. Ecol. Freshw. Fish 22 (3), 430–438. http://dx.doi.org/10.1111/eff. 12037. Janáč, M., Valová, Z., Roche, K., Jurajda, P., 2016. No effect of round goby Neogobius 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 Calumet harbor, southern Lake Michigan, induced by the newly introduced round goby Neogobius melanostomus. J. Great Lakes Res. 27 (3), 319–328. http://dx.doi.org/ 10.1016/S0380-1330(01)70647-8. Johnson, T.B., Bunnell, D.B., Knight, C.T., 2005a. A potential new energy pathway in central Lake Erie: the round goby connection. J. 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Great Lakes Res. 39 (1), 182–185. http://dx.doi.org/10.1016/j.jglr.2012.12.002. Kalchhauser, I., Mutzner, P., Hirch, P.E., Burkhardt-Holm, P., 2013. Arrival of round goby Neogobius melanostomus (Pallas, 1814) and bighead goby Ponticola kessleri (Günther, 1861) in the high Rhine (Switzerland). Bioinvasions Rec. 2 (1), 79–83. http://dx.doi. org/10.3391/bir.2013.2.1.14. Klíma, O., 2009. Importance of permeability of migration barriers for fish community in the streams. Masaryk University, Faculty of Science, Brno (Bachelor thesis) 48p. Available from https://is.muni.cz/th/222900/prif_b. 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. J. Fish Biol. 80 (2), 235–285. http://dx.doi.org/10.1111/j.1095-8649. 2011.03157.x. Kornis, M.S., Sharma, S., Vander Zanden, M.J., 2013. Invasion success and impact of an invasive fish, round goby, in Great Lakes tributaries. 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the invertebrate assemblage (Lederer et al., 2008; Mikl et al., 2017), altering trophic pathways (Rush et al., 2012), pollution recycling (Johnson et al., 2005a; Kornis et al., 2012; Polačik et al., 2015) or parasite spillback/dilution (Poos et al., 2010; Ondračková et al., 2015; Šlapanský et al., 2016). The spreading of round goby into non-navigable rivers represents a secondary phase in the range expansion that has been ongoing in Europe and the US for a number of decades now. To date, population characteristics of invasive populations have shown high variation, probably connected with low numbers and specific environmental conditions found in individual streams and sites within them. As a result, it is still proving difficult to clearly define any specific age group, sex or body size of fish in relation to the invasion pioneers. What is certain, however, is that active movement upstream is neither limited by an absence of shipping nor necessarily by the presence of migration obstacles. To date, the consequences of this invasion have only been monitored for a relatively short period and further detailed monitoring is still needed in order to determine general population trends and longterm impacts on native fish assemblages in non-navigable river systems. Acknowledgements This study was supported by Czech Science Foundation (Grant Agency of the Czech Republic) Project no. P505/11/1768. We thank Z. Jurajdová, G. Konečná, M. Koníčková, M. Mrkvová, M. Pravdová and L. Všetičková for help with fieldwork. We are much indebted to representatives of the Moravian Angling Union (V. Habán) and the Židlochovice Forest Enterprise (J. Netik) for allowing research in their waters and grounds. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.limno.2017.09.001. References Adámek, A., Zahrádková, S., Jurajda, P., Bernardová, I., Jurajdová, Z., Janáč, M., Němejcová, D., 2013. The response of the benthic macroinvertebrate and fish assemblages to human impact along the lower stretch of the rivers Morava and Dyje (Danube basin, Czech Republic). Croat. J. Fish. 71, 93–115. http://hrcak.srce.hr/ 108849. Ahnelt, H., Bănărescu, P., Spolwind, R., Harka, A., 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 (5), 661–674. Balshine, S., Verma, A., Chant, V., Theysmeyer, T., 2005. Competitive interactions between round gobies and logperch. J. Great Lakes Res. 31 (1), 68–77. http://dx.doi. org/10.1016/S0380-1330(05)70238-0. Bergstrom, M.A., Mensinger, A.F., 2009. Interspecific resource competition between the invasive round goby and three native species: logperch, slimy sculpin, and spoonhead sculpin. Trans. Am. Fish. Soc. 138 (5), 1009–1017. http://dx.doi.org/10.1577/T08095.1. Bergstrom, M.A., Evrard, L.M., Mensinger, A.F., 2008. Distribution, abundance and range of the round goby, Apollina melanostoma, in the Duluth-Superior Harbor and St. Louis river estuary, 1998–2004. J. Great Lakes Res. 34 (3), 535–543. http://dx.doi.org/10. 3394/0380-1330(2008)34[535:DAAROT]2.0.CO;2. 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. J. Appl. Ichthyol. 27, 153–155. http://dx.doi.org/10.1111/j. 1439-0426.2010.01662.x. Braks, M.A.H., Honório, N.A., Lounibos, L.P., Lourenço-De-Oliveira, R., Juliano, S.A., 2004. Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. Ann. Entomol. Soc. Am. 97 (1), 130–139. http://dx.doi.org/10.1603/0013-8746(2004) 097[0130:ICBTIS]2.0.CO;2. Brandner, J., Pander, J., Mueller, M., Cerwenka, A.F., Geist, J., 2013a. Effects of sampling techniques on population assessment of invasive round goby Neogobius melanostomus. J. Fish Biol. 82 (6), 2063–2079. http://dx.doi.org/10.1111/jfb.12137. Brandner, J., Cerwenka, A.F., Schliewen, U.K., Geist, J., 2013b. Bigger is better: characteristics of round gobies forming an invasion front in the Danube River. PLoS One 8 (9), e73036. http://dx.doi.org/10.1371/journal.pone.0073036. Bronnenhuber, J.E., Dufour, B.A., Higgs, D.M., Heath, D.D., 2011. Dispersal strategies, secondary range expansion and invasion genetics of the nonindigenous round goby,

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