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Competitive Interactions for Food Resources Between Invasive Racer Goby Babka Gymnotrachelus and Native European Bullhead Cottus Gobio

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Competitive Interactions for Food Resources Between Invasive Racer Goby Babka Gymnotrachelus and Native European Bullhead Cottus Gobio Biol Invasions DOI 10.1007/s10530-013-0470-7 ORIGINAL PAPER Competitive interactions for food resources between invasive racer goby Babka gymnotrachelus and native European bullhead Cottus gobio Tomasz Kakareko • Jarosław Kobak • Joanna Grabowska • Łukasz Jermacz • Mirosław Przybylski • Małgorzata Poznan´ska • Dariusz Pietraszewski • Gordon H. Copp Received: 10 June 2012 / Accepted: 11 April 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com Abstract Racer goby is one of several Ponto– activity (time spent near or inside the feeder) recorded Caspian gobiids spreading throughout European rivers using video cameras and infrared illumination. Racer and concurrent with recent declines in threatened goby exhibited aggressive behaviour towards bullhead populations of a native species of similar biology, the (mean = 2.5 aggressive events h-1), but rarely the European bullhead. Although suggestive of compet- inverse (threatening only, mean = 0.05 events h-1), itive interactions, evidence thereof is scarce, so we significantly limiting bullhead foraging time (by examined behavioural interactions between racer 62 %) and being faster to reach food in the feeding goby and bullhead (single specimens of each species time in 76 % of cases. Gobies were more aggressive together, also pairs of each species) under experimen- during daylight (77 % of all aggressive events occur- tal conditions (shared space with two shelters) to ring in light), and both species spent more time on determine whether the invader displaces the native feeding activities in darkness (88 and 66 % of all time species when food resources are limited. Food (live spent in the feeder by bullheads and gobies, respec- chironomids) was added to a single feeder at rates tively). However, the adverse impact of goby on below satiation levels twice over 24 h (once in light bullhead was independent of light conditions. Our and once in darkness), with fish behaviour (aggressive results suggest that under natural conditions, racer interactions: attacks and threatening) and feeding goby are likely to displace bullhead during feeding, with potential consequences for foraging efficiency. T. Kakareko (&) Á Ł. Jermacz Keywords Ponto–Caspian gobiids Á Interspecific Department of Hydrobiology, Nicolaus Copernicus competition Á Aggressive behaviour Á Non-native University, Torun´, Poland species e-mail: [email protected] J. Kobak Á M. Poznan´ska Department of Invertebrate Zoology, Nicolaus Copernicus Introduction University, Torun´, Poland J. Grabowska Á M. Przybylski Á D. Pietraszewski Amongst the most impressive fish invasions in Department of Ecology and Vertebrate Zoology, European inland waters in recent decades are those University of Lodz, Lodz, Poland of the topmouth gudgeon Pseudorasbora parva, which occurred mainly as a contaminant of fish G. H. Copp Centre for Environment, Fisheries and Aquaculture transport (see Copp et al. 2005; Simon et al. 2011), Sciences, Lowestoft, Suffolk, UK and of the Ponto–Caspian gobies, which colonized 123 T. Kakareko et al. new areas mainly by natural dispersal via inter-basin barbatula from their preferred habitats by four connections, e.g. being transported by river ships (see gobiid species. However, racer goby was not Grabowska 2005 and Wiesner 2005). So far, six gobiid included in this study. species have been recorded in Europe as non-native In Polish inland waters, the gobiid species most species, including bighead goby Ponticola kessleri, likely to have deleterious consequences for the native Caspian bighead goby P. gorlap, monkey goby bullhead is the racer goby, which has established itself Neogobius fluviatilis, racer goby Babka gymnotrache- in parts of the River Vistula catchment where the lus, round goby N. melanostomus and Western tube- bullhead is native (Marszał et al. 2004; T. Kakareko, nose goby Proterorhinus semilunaris. These species personal observation). Both species are bottom dwell- have invaded or expanded their range in large ers of similar size, habitat use (crevices), and repro- European rivers such as the Danube (Ahnelt et al. ductive strategy (Tomlinson and Perrow 2003; Pinchuk 1998, 2001; Kautman 2001; Naseka et al. 2005), Rhine et al. 2003a) as well as similar dietary preferences, i.e. (Freyhof 2003; van Kessel et al. 2009), Vistula soft-bodied (non-mollusc) benthic invertebrates, espe- (Grabowska et al. 2008) and Volga (Copp et al. cially chironomid larvae and amphipods (Welton et al. 2005). The Ponto–Caspian gobies are relatively small 1991; Grabowska and Grabowski 2005; Kakareko et al. (up to 15–20 cm total length), bottom-dwelling spe- 2005). The bullhead is effectively the European cies that are usually associated with crevice habitats, equivalent of the North American cottid, the mottled though some invading populations have been reported sculpin Cottus bairdi, which in the Great Lakes has to have established in sandy areas (Sapota 2004). been demonstrated to be adversely affected by invading These species are territorial and aggressive, with nest- round goby populations (Corkum et al. 2004). There guarding males (Smirnov 1986; Charlebois et al. 1997; similarities makes the two species very likely compet- Pinchuk et al. 2003a, b), making them potential itors for space, spawning grounds, feeding areas and competitors to native European species of similar food types. environmental biology, such as Gobiidae in brackish The aim of the present study was to examine the waters (Corkum et al. 2004) and Cottidae in fresh interactions between these two species under exper- waters. This is particularly relevant to the European imental conditions in order to assess whether racer bullhead Cottus gobio, which is listed in Annex II of goby (henceforth referred to collectively as ‘gobies’) the European Habitats and Species Directive (92/43/ has an adverse impact on bullhead feeding behaviour EEC) because of declines in various parts of its range (time and location) when food resources are limited. (e.g. Lelek 1987; Knaepkens et al. 2004). This The working hypothesis was that racer goby would be includes Poland, where the European bullhead is more aggressive than native bullhead of comparable listed as vulnerable (Witkowski et al. 2009). The size, the former being a stronger competitor and threat of Ponto–Caspian gobies to native Cottidae displacing the latter from the profitable feeding areas, has already been demonstrated in the Laurentian and this is expected to have adverse consequences for Great Lakes, where invasive round goby have been bullhead foraging efficiency and fitness. found to out-compete native mottled sculpin Cottus bairdii for preferred habitat and to disrupt their reproduction (Dubs and Corkum 1996; Janssen and Material and methods Jude 2001). Reported declines in European bullhead populations, coinciding with goby invasions of the European bullhead were collected whilst SCUBA rivers Danube (Jurajda et al. 2005) and Rhine diving in a tributary of the lower River Vistula, the (Dorenbosch and van der Velde 2009) suggest that River Brda, near the city of Bydgoszcz (central Ponto–Caspian gobies are having a similar adverse Poland), where stones were overturned and bullhead impact on European as on North American Cottidae. specimens were captured by manoeuvring them into However, studies on the potential impacts of gobies an aquarium dip net. Racer gobies were collected by on European bullhead (henceforth simply ‘bull- electrofishing (IUP-12, Radet, Poznan´, Poland) from head’) are limited to one experimental study (van the Włocławek Reservoir, which is located in the Kessel et al. 2011), which focused on the potential lower River Vistula, central Poland about 100 km displacement of bullhead and stone loach Barbatula from the River Brda site. Immediately after capture, 123 Competitive interactions for food resources the fish were transported to the laboratory in aerated Samsung, South Korea, suspended & 45 cm above the plastic 5-L bottles (1.5 h transport time), immediately water level), and at one end a feeder, which consisted placed in 80-L tanks (filtered, aerated water at of a Petri dish (attached to the tank bottom with 17–19 °C; 20 % of water exchange per week), with silicone glue) and a transparent plastic hose (suspended 5–8 specimens per tank (segregated by species) and & 0.5 cm above the dish bottom). Food (30–60 mg of fed with live chironomid larvae. live chironomid larvae depending upon fish size; i.e. During the experiments, fish mean total length (TL) 3–4 9 below satiation level, as per preliminary obser- was measured from digital photographs (taken from vations) was flushed through a hose with a small the top view of the experimental aquaria) using image amount of water into the Petri dish, where they analysis software (ImageJ v1.40 g freeware by W.S. remained until taken by the fish. Fish were allowed to Rasband, U.S. National Institutes of Health, Bethesda, get used to these conditions in separate, segregated Maryland, USA, http://rsb.info.nih.gov/i). Fish mea- aquaria for 2 months prior to the experiments. surements were taken when the specimen was located Fish were tested in pairs of similar length (B1cm in front of an underwater scale situated on the tank difference in TL): (1) two bullheads (10 trials); (2) two bottom near the feeder, so as to ensure a constant gobies (11 trials); and (3) one goby and one bullhead measurement distance between the camera and all (16 trials; mean TLs not significantly different; measured fishes. Fish used in the experiments were not Student’s t test for dependent samples: t15 = 0.71, in spawning condition, exhibiting no symptoms such P = 0.490). Each pair of fish was tested in two light as dark colouration of males or courtships. Mean conditions (30 lux light vs. total darkness) during a lengths were 83 mm (min–max: 58–125 mm TL) and single trial, which lasted 24 h. The fish in both 81 mm (60–111 mm TL) for gobies and bullheads, experimental tanks and the stock tanks were held respectively. Capture and use in this study of European under the same light cycle, i.e.
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