New Record of Monogenean Parasites on Non-Indigenous Fishes in the Ukrainian Danube Delta

Home , Caucasian dwarf goby, Danube delta dwarf goby, Pumpkinseed, Pungitius

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) 1 0.6 Esociformes Fam. Esocidae Esox lucius L., 1758 7 3.9 Gasterosteiformes Fam. Gasterosteidae Gasterosteus aculeatus L., 1758 11 6.1 Pungitius platygaster (Kessler, 1859) 3 1.7 Syngnathiformes Fam. Syngnathidae Syngnathus abaster Risso, 1827 7 3.9 Atheriniformes Fam. Atherinidae Atherina boyeri Risso, 1810 1 0.6 Perciformes Fam. Centrarchidae Lepomis gibbosus (L., 1758) 2 1.1 Fam. Percidae Perca fluviatilis L., 1758 2 1.1 Fam. Odontobutidae Perccottus glenii Dybowski, 1877 75 41.4 Fam. Gobiidae Babka gymnotrachelus (Kessler, 1857) 7 3.9 Knipowitschia causacica (Berg, 1916) 1 0.6 Neogobius fluviatilis (Pallas, 1814) 1 0.6 Proterorhinus semilunaris (Heckel, 1837) 5 2.8 basin, Balaton basin, Vistula basin, Danube Delta (see Figure 2). Gyrodactylus avalonia Hanek and Threlfall, 1969 (Figure 3) Morphological measurements of the haptoral structures: Hamuli 42–43 µm long; base 30 µm; inner root 14.5– 16.0 µm; point 19 µm. Marginal hook sickles crescent- shaped, 4.5–5.0 µm long; handle 17–19 µm long. Ventral bar 5–6 µm long; 26–27 µm wide; ventral bar membrane of wide tongue shape. Type host: Gasterosteus aculeatus. Other hosts: Apeltes quadracus, Fundulus diaphanus, Gasterosteus wheatlandi, Lepomis gibbosus, Pungitius pungitius, Rhinichthys atratulus. Specimens deposited: IPCAS M-677. Distribution: Native range – freshwater lakes, Figure 1. Gyrodactylus perccotti ex Perccottus glenii, Danube Delta, Vylkove, Ukraine. A) complex of central anchors with brackish lagoons and estuaries of Newfoundland, Nova ventral and dorsal bar; B) marginal hook; Scale bar = 10 µm. Scotia (Hanek and Threlfall 1969, 1970a; Marcogliese

67 Y. Kvach et al.

Figure 2. Map of Gyrodactylus perccotti distribution in Europe (red circles – confirmed localities). 1. Ponds in Klyazma and Moscow rivers drainage (Reshetnikov et al. 2017); 2. Oka river drainage (Shershneva 2014); 3. Lake Krugloe (Sokolov et al. 2012); 4. Volgograd Reservoir drainage (Sokolov et al. 2013); 5. Włocławek Reservoir (Ondračková et al. 2012); 6. Lake Shaparnia (Zaichenko 2015); 7–8. River Tisza basin (Antal et al. 2015); 9. Zala River (Antal et al. 2015); 10. Danube Delta (current data).

1995), nearshore of Labrador (Hanek and Threlfall 1970b), also Lake Ontario (Hanek and Fernando 1971); invasive range – Danube Delta (current data, Figure 4). Onchocleidus similis Müller, 1936 (Figure 5) Morphological measurements of the haptoral and reproductive structures: Two pairs of hamuli: ventral hamuli 33–36 µm long; base 27–29 µm; inner root 8–10 µm; outer root 2.0–2.5 µm; point 13–14 µm. Dorsal hamuli 35.5–37.0 µm long; base 31 µm; inner root 7–9 µm; outer root 2–3 µm; point 14–15 µm. Marginal hooks similar in shape but slightly different in size, pair I–IV and VI–VII 19.0–22.5 µm long, pair V 11–12 µm long. Ventral bar 3.0–3.5 µm long; 20 µm wide; dorsal bar 2.5–3.0 µm long; 17–19 µm wide; not articulating with each other. Copulatory Figure 3. Gyrodactylus avalonia ex Lepomis gibbosus, Danube organ 27 µm long, comprising sclerotised, tubular penis Delta, Vylkove, Ukraine. A) complex of central anchors with with inflated base and two spiral filaments; tent-like ventral and dorsal bar; B) marginal hook; Scale bar = 10 µm. accessory piece. Type host: Lepomis gibbosus. Specimens deposited: IPCAS M-678. Danube basin, including delta, Lakes Balaton and Distribution: Native range – freshwaters of Atlantic Velence, Mediterranean coasts of France and Turkey, North America (Hoffman 1998); invasive range – subalpine lakes (Figure 4).

68 Monogeneans of non-indigenous Danube Delta fishes

Figure 4. European distribution map for non-native monogeneans of Lepomis gibbosus (red checkmark – confirmed locality of Gyrodactylus avalonia, black circle – confirmed locality of Onchocleidus similis). 1. River Danube, Corabia, Romania (Roman 1953); 2. River Danube, Drobeta-Turnu Severin, Romania (Roman 1955); 3. Lower Danube, Ukraine (Pashkevichute 1971); 4. River Danube and small tributaries in Slovakia (Moravec 2001; Ondračková et al. 2011); 5. River Hron, Slovakia (Moravec 2001); 6. River Tisza, Slovakia (Moravec 2001); 7. River Tisza, Hungary (Molnár 1968); 8. River Danube, Hungary (Molnár 1968); 9. Lakes Balaton and Velence, Hungary (Molnár 1968); 10. River Danube, Russe, Bulgaria (Margaritov 1968); 11. Danube Delta, Ukraine (Kulakovskaya and Koval 1973; current data); 12. Étang de Scamandre, France (Lambert 1977); 13. Subalpine lakes, Italy (Galli et al. 2003, 2005); 14. River Dyje drainage (Ondračková et al. 2011); 15. River Danube, Croatia (Ondračková et al. 2011); 16. River Danube, Koshava, Bulgaria (Ondračková et al. 2011); 17. River Durance, France (Havlátová et al. 2015); 18. Lake Sığırcı, Turkey (Çolak 2013).

Discussion

In this paper, we report the presence of an American gyrodactylid monogenean G. avalonia in Europe for the first time (though species identification is still awaiting molecular/genetic characterisation). In addition, our data confirm the presence of the ancy- rocephalid monogenean O. similis, a specific parasite of centrarchid fishes, in the Ukrainian stretch of the River Danube; and the presence of G. perccotti, a specific parasite of the Chinese sleeper, in the Danube Delta for the first time. Gyrodactylus avalonia was first described on the fins of a three-spined stickleback from the brackish waters of Witless Bay Estuary in Newfoundland, Canada (Hanek and Threlfall 1969). Later, the species was documented on the fins of pumpkinseed in the freshwater Bay of Quinte in Lake Ontario, Canada (Hanek and Fernando 1971). This parasite is described Figure 5. Onchocleidus similis ex Lepomis gobbisus, Danube as an extreme generalist among gyrodactylids, infecting Delta, Vylkove, Ukraine. A) dorsal anchors; B) dorsal bar; eight host species from five different orders (Bakke C) ventral anchors; D) ventral bar; E) marginal hooks; F) male et al. 2002). While G. avalonia is suspected of being copulatory organ; Scale bar = 10 µm.

69 Y. Kvach et al. a junior synonym of G. arcuatus Bychowsky 1933, 2011), O. similis from the Danube Delta exhibited it remains valid as a species until molecular/genetic smaller haptoral hard parts than those observed in characterisation is conducted (J. Lumme and S.D. the parasite’s native area (Hoffman 1998), probably King, pers. comm., in Rubio-Godoy et al. 2012). reflecting host size. According to the “parasite spillover” concept, an The Danube Delta region has a strong influence introduced host may serve as a source of new parasitic on waters of the Black Sea, with sea water reaching agents for native hosts (Kelly et al. 2009). As G. the town of Vylkove (Liashenko and Zorina-Sakharova avalonia displays broad halotolerance and halohabitat 2014, 2015) and branch waters and tributaries along distribution (Cone and Wiles 1985), shows low host the Ukrainian coast reaching an average salinity of specificity (Bakke et al. 2002) and its main host, G. around 0.29–0.81‰ (max. 4.72‰). This provides aculeatus, is relatively abundant in the Danube Delta, appropriate conditions for the survival of the parasite the consequent spread of this species in Europe is G. avalonia, whose natural range includes harbours highly likely. Moreover, as G. avalonia has been along the coastal waters of Newfoundland and shown to pass on pathogenic bacteria to its fish host, whose type host is the brackish-water three-spined further dispersal potentially represents a threat to stickleback (Hanek and Threlfall 1969). Two species local fish fauna (Cusack and Cone 1985). of Onchocleidus, O. similis and O. dispar, occur Gyrodactylus perccotti was recorded in Europe along the middle and lower stretch of the Danube for the first time in the Vistula Basin (Ondračková et (Ondračková et al. 2011), aside from the delta where al. 2012). The parasite was later documented in the only O. similis has been recorded (Kulakovskaya Middle Dnieper near Kiev, Ukraine (Zaichenko 2015) and Koval 1973; current data). Spreading of pump- and in the River Tisza Basin and the Lake Balaton kinseed in the Black sea region occurs during the drainage in Hungary (Antal et al. 2015) (Figure 2). spring floods, when riverine flood waters deliver fish The results of this study also confirm the presence of to the open sea and thence on to the deltas of other G. perccotti in the Ukrainian stretch of the Danube. rivers (Afanasyev et al. 2017). This same method Given the non-indigenous origin of this parasite and was the vector for pumpkinseed expansion into the its host specificity (Sokolov et al. 2012), its presence rivers Dniester and Dnieper, where pumpkinseed on the Chinese sleeper could point to the species’ fish populations are genetically identical to those in the host invasion history (Kvach et al. 2016b; Reshetnikov Danube (Slynko et al. 2014). At least one parasite et al. 2017). Gyrodactylus perccotti was not recorded species, O. dispar, has been co-introduced into the during a study investigating 70 individuals of the River Dnieper with its host (Rubtsova 2015). We Chinese sleeper in the River Prut drainage (Moldova) can therefore expect further range expansion of O. in 2012 (Sokolov and Moshu 2013). Therefore, it is similis into other river drainages in the Black Sea more likely that the Chinese sleeper was introduced basin along with its host, the pumpkinseed. (or expanded) into the Danube Delta from the Tisza basin via the main Danube channel. Acknowledgements The first study on pumpkinseed parasites in the This study received financial support through the European River Danube was undertaken by Roman (1953, Centre of Ichthyoparasitology under Grant Agency of the Czech 1955), who recorded two monogenean species Republic Centre of Excellence Grant No. P505/12/G112. We (Onchocleidus dispar Müller, 1936 and O. similis) in thank Dr Kevin Roche (Institute of Vertebrate Biology, Czech Academy of Sciences) for proofreading the English text. the lower Danube near Corabia and Drobeta-Turnu Severin, Romania. Both of these species were later References recorded in the Ukrainian stretch of the Danube (Pashkevichute 1971). The occurrence of O. similis Afanasyev SA, Gupalo YA, Manturova OV (2017) Distribution and on the pumpkinseed in our study corresponds with peculiarities of biology of the pumpkinseed Lepomis gibbosus the results of Kulakovskaya and Koval (1973), who (Perciformes: Centrarchidae) in the water bodies of Kyiv City. Hydrobiological Journal 53: 14–25, https://doi.org/10.1615/Hydrob also reported this species at Vylkove in the Danube J.v53.i3.20 Delta over 50 years ago. Since its first record in Aleksandrov B, Voloshkevich O, Kurakin A, Rybalko A, Gontar V Europe, O. similis has been documented from several (2014) The first finding of bryozoan Pectinatella magnifica (Lophopodidae) in Lower Danube. 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Supplementary material The following supplementary material is available for this article: Table S1. Records of Gyrodactylus perccotti ex. Perccottus glenii in Europe. Table S2. Records of Onchocleidus similis ex. Lepomis gibbosus in Europe. Appendix 1. List of references for annotated checklist. This material is available as part of online article from: http://www.reabic.net/journals/bir/2018/Supplements/BIR_2018_Kvach_etal_SupplementaryTables.xlsx