BioInvasions Records (2018) Volume 7, Issue 1: 65–72 Open Access DOI: https://doi.org/10.3391/bir.2018.7.1.10 © 2018 The Author(s). Journal compilation © 2018 REABIC Research Article New record of monogenean parasites on non-indigenous fishes in the Ukrainian Danube Delta Yuriy Kvach1,2,*, Markéta Ondračková1, Yuliya Kutsokon3 and Nataliya Dzyziuk4 1Institute of Vertebrate Biology, Czech Academy of Science, Květná 8, 60365 Brno, Czech Republic 2Institute of Marine Biology, National Academy of Science of Ukraine, Vul. Pushkinska 37, 65011 Odessa, Ukraine 3Schmalhausen Institute of Zoology, National Academy of Science of Ukraine, Vul. B. Khmelnytskoho 15, 01030 Kiev, Ukraine 4Department of Zoology, Ivan Franko National University of Lviv, Vul. Hrushevskoho 4, 79005 Lviv, Ukraine *Corresponding author E-mail: [email protected] Received: 26 June 2017 / Accepted: 13 November 2017 / Published online: 1 December 2017 Handling editor: Pamela J. Schofield Abstract The Danube Delta is a recognised hot-spot for non-indigenous aquatic species, with 11 new species recorded over the last 20 years. The North-American pumpkinseed (Lepomis gibbosus L., 1758), has been common in the Ukrainian Danube Delta since 1918, while the Chinese sleeper (Perccottus glenii Dybowski, 1877) has only recently been introduced. In April 2017, 21 fish species were recorded during a study of the fish fauna around Vylkove (Ukraine, Danube Delta). The Chinese sleeper was the dominant sampled fish from the studied locality, comprising 41.4% of the fish community, while pumpkinseed comprised only 1.1%. Three non-indigenous monogenean parasites were registered: Gyrodactylus perccotti Ergens and Yukhimenko, 1973 infecting the Chinese sleeper; and Gyrodactylus avalonia Hanek and Threlfall, 1969 and Onchocleidus similis Müller, 1936 infecting pumpkinseed. The American monogenean G. avalonia is reported for the first time in Europe though further molecular/genetic characterisation is needed for species validation. Likewise, G. perccotti, a specific parasite of the Chinese sleeper, is recorded in the Danube Delta for the first time. Finally, our data confirm the presence of the monogenean O. similis, a specific parasite of centrarchid fishes, in the Ukrainian part of the Danube. Key words: Ancyrocephalidae, first finding, Gyrodactylidae, non-indigenous species, parasite spillover Introduction broader ecological and physiological parameters (Machkevskyi et al. 2015). Non-indigenous host-species can introduce alien The Danube Delta is a recognised hot-spot for parasites into its new range or play a role in distri- non-indigenous aquatic species, with 11 new species buting local parasites into new habitats (Taraschewski recorded over the last 20 years (Alexandrov 2004; 2006). Many non-native parasites are co-introduced Năstase 2007; Aleksandrov et al. 2014). The North- with their original host species. Such parasites often American pumpkinseed (Lepomis gibbosus L., 1758), remain a part of the host’s parasite fauna and are has been common in the Ukrainian Danube Delta spread only as the host increases its range (Lymbery since 1918 (Pavlov and Bilko 1962), while the Chinese et al. 2014). Some co-introduced parasites can also sleeper (Perccottus glenii Dybowski, 1877) has only switch to new native host species, however, greatly recently been introduced (Kvach 2012). increasing the speed at which it spreads through the The Chinese sleeper is an Asian fish species that new environment (Galli et al. 2005). In this case the was first introduced into the Danube basin via the parasite forms a complicated bicomponent parasitic upper River Tisza drainage in Ukraine in 1995 system, where parasite success in the new environment (Sivokhop 1998) and is now invasive in many Euro- depends on the predisposition of the new hosts to pean waters (Kottelat and Freyhof 2007). In Europe, 65 Y. Kvach et al. the fish hosts two co-introduced helminth species: in the laboratory; all other species being released the monogenean Gyrodactylus perccotti Ergens and alive where they were caught. The fish were kept in Yukhimenko, 1973 in the River Vistula, Poland aerated water and transported to the laboratory of the (Ondračková et al. 2012); and the cestode Institute of Marine Biology, National Academy of Nippotaenia perccotti (Akhmerov, 1941) in the River Sciences of Ukraine in Odessa. Tisza, Slovakia (Košuthová et al. 2004). Moreover, Eleven Chinese sleeper (standard length [SL]; G. perccotti has been reported from the River mean ± S.D. = 69 ± 8.3; range 50–83 mm) and two Dnieper in Ukraine and the River Tisza in Hungary pumpkinseed (SL 42 and 44 mm) were examined for (Antal et al. 2015; Zaichenko 2015) and N. perccotti parasites within 48 h of capture (Kvach et al. 2016a). from the Rivers Dniester and Tisza (Kvach et al. Monogeneans were mounted in glycerine-ammonium- 2013, 2016b; Antal et al. 2015), and in the River picrate solution (GAP) in accordance with Malmberg Vistula in Poland (Mierzejewska et al. 2010). (1970). The slides were then studied under an Olympus Pumpkinseed, which is one of the most widespread BX50 light microscope equipped with phase contrast, non-native fish species in Europe, has been found in differential interference contrast and Olympus around 30 different countries (Copp and Fox 2007). MicroImage™ Digital Image Analysis software In Ukraine, the species has a range stretching from (Olympus Optical Co.). The voucher material has the Kalmius river basin in the east (Diripasko et al. been deposited in the Helminthological Collection of 2008) to the Middle Dnieper basin near Kiev in the the Institute of Parasitology, Biology Centre of the north (Tsyba 2011; Afanasyev et al. 2017). Specific Czech Academy of Sciences, České Budějovice, monogenean species are known to parasitise pump- Czech Republic (acronym IPCAS). kinseed in different parts of Europe, such as France (River Durance; Havlátová et al. 2015), the Ukraine Results (Rubtsova 2015), Italy (subalpine lakes; Galli et al. 2003, 2005), Norway (ponds; Sterud and Jørgensen A total of 21 fish species were recorded in the fish 2006) and in southwestern England (Hockley et al. sample (Table 1), with the invasive Chinese sleeper 2011). In addition to the co-introduced monogeneans, dominant at the sampling locality (41.4% of the fish pumpkinseed act as host to the American digenean, sample), followed by native bleak Alburnus alburnus Posthodiplostomum minimum centrarchi Hoffmann, (L., 1758) (7.2%), loach Cobitis elongatoides Băcescu 1958, which has also been recorded in the Danube and Mayer, 1969 (6.1%) and three-spined stickleback basin (Kvach et al. 2017; Stoyanov et al. 2017). All Gasterosteus aculeatus L., 1758 (6.1%). Pumpkinseed other pumpkinseed parasites registered in Europe are represented just 1.1% of the fish sample. One of the of local origin. 11 Chinese sleepers caught was found to be infected The aim of the present study was to describe the with a specimen of an Asian monogenean, G. perccotti presence of non-indigenous parasites co-introduced (Gyrodactylidae). Both pumpkinseed were infected along with their non-indigenous fish hosts, the with North-American monogeneans, one with two Chinese sleeper and the pumpkinseed, in the Ukrainian specimens of Gyrodactylus avalonia Hanek and part of the Danube Delta. Threlfall, 1969 (Gyrodactylidae) and the second with two specimens of Onchocleidus similis Müller, 1936 Material and methods (Ancyrocephalidae). On 25.04.2017, we sampled the fish community in a Gyrodactylus perccotti Ergens and Yukhimenko, 1973 canal connected with the River Danube at the town (Figure 1) of Vylkove, Danube Delta, south-western Ukraine (45º24′N; 29º35′E). The canal has muddy bottom Morphological measurements of the haptoral struc- overgrown with submerged aquatic vegetation. Fish tures: Hamuli 86 µm long; base 56 µm; inner root 39 were sampled using a 10-m beach-seine at a depth of µm; point 35 µm. Marginal hook sickles 12 µm long; around 1 m. The seine was towed about 50 m along handle 24 µm long. Ventral bar 2.5 µm long; 18 µm the shore with about 50% capture (in total of 250 m2 wide; ventral bar membrane of long tongue shape. was covered by sampling). All fish were identified to Type host: Perccottus glenii. species, counted and species dominance calculated Specimens deposited: IPCAS M-139. as the percentage of all species caught. There are no Distribution: Native range – Far East Asia (Ergens published studies of fish samples in this region, so and Yukhimenko 1973; Wu et al. 2000; Ermolenko we present the data from the sample in Table 1. Two 2004), Sakhalin (Sokolov and Frolov 2012); invasive invasive fish species, the Chinese sleeper and the range in Asia – Baikal basin, Western Siberia (see pumpkinseed, were caught and individuals larger references in Sokolov et al. 2014); invasive range in than 20 mm were taken for further parasite analysis Europe – Volga river basin, Middle Dnieper, Tisza river 66 Monogeneans of non-indigenous Danube Delta fishes Table 1. Fish density (number of fish per 250 m2) and dominance (in %) at Vylkove, Danube Delta, Ukraine. Fish species Density Dominance Cypriniformes Fam. Cyprinidae Rhodeus amarus (Bloch, 1782) 2 1.1 Carassius gibelio (Bloch, 1782) 10 5.5 Pseudorasbora parva (Temminck and Schlegel, 1846) 4 2.2 Blicca bjoerkna (L., 1758) 5 2.8 Alburnus alburnus (L., 1758) 13 7.2 Leucaspius delineatus (Heckel, 1843) 5 2.8 Scardinius erythrophthalmus (L., 1758) 9 5.0 Fam. Cobitidae Cobitis elongatoides Băcescu and Mayer, 1969 11 6.1 Misgurnus fossilis (L., 1758)