The Chinese sleeper,
The fish has negative impact on ecosystems in its non-native range, caused mostly by competition with local fauna and predation (Reshetnikov 2013; Rakauskas et al. 2016; Pupina et al. 2018), which could even lead to the elimination of the local fish fauna and the formation of monospecific communities (Kutsokon et al. 2021). Therefore, this fish has been listed as an Invasive Alien Species (IAS) of Union concern (European Commission 2017).
The Central European population of the Chinese sleeper shares the same haplotypes, originating from one of the few initial introductions from China into the Upper Dniester basin in Ukraine. From there, the species then spread to neighboring riverine basins, such as the Danube, the Dnieper, the Vistula and the Southern Bug basins (Grabowska et al. 2020). The history of this introduced population started in 1972, when the Chinese sleeper was introduced into the Velykyi Lubin fish farm (Dniester River basin) near Lviv, the Carpathian region of Ukraine (Fedoniuk 2005; Reshetnikov 2013; Kutsokon 2017). The population was therefore named the ‘Carpathian population’, as opposed to two others in Eastern Europe (Kvach et al. 2016a; Grabowska et al. 2020).
Parasites are commonly used as biological tags to distinguish fish populations (Mackenzie 1983
; Catalano et al. 2014; Poulin, Kamiya 2015). Four stenoxenous parasite species, specific to shovel-snouts (family Odontobutidae), were co-introduced with the Chinese sleeper from Asia to Europe, e.g. the coccidian
Sampling was conducted in five localities of the Lviv region in Ukraine in two different drainage basins (the Dniester and the Bug) in September–October 2017. A triangular trap (72 × 73 × 80 cm) with a 6 mm net mesh was used for sampling. In the Bug River basin (part of the Vistula drainage basin), fish were sampled in Lake Inzhenerne (50°00’52.7”N; 23°27’55.6”E), Lake on Znesinnia (49°50’54.1”N; 24°03’07.8”E) and Lake on Plastova (49°51’33.6”N; 24°04’47.7”E), while in the Dniester basin these were Lake Maliushevske (50°00’39.7”N; 23°41’00.6”E) and Lake on Stryiska (49°48’02.4”N; 24°01’00.1”E). Only Lake on Stryiska is a natural body of water, while the others are artificial reservoirs. Three of the lakes, Lake on Znesinnia, Lake on Plastova and Lake on Stryiska, are isolated from the mainstream of the river. Two of the reservoirs, Lake Inzhenerne and Lake Maliushevske, are aquaculture ponds built on small rivers. All the studied bodies of water are characterized by lush aquatic vegetation.
The fish were transported alive in aerated cans to the laboratory of Lviv University, where they were kept alive and then dissected two days after sampling, following a known protocol (Kvach et al. 2016b). The standard and total length of each fish was measured. A total of 120 individuals were examined for parasites (Table 1). In each fish, fins, skin, gills, eyes, muscles, viscera and internal organs (gut, liver, gall bladder, spleen, swimming bladder, kidneys, uterine bladder, gonads, mesentery and brain) were removed and examined under a microscope. Ciliates were examined alive under a light microscope. Monogeneans were removed from the host and preserved in GAP (ammonium picrate and glycerin mixture) as semi-permanent slides (Malmberg 1970). Cestodes, trematodes and nematodes were preserved in hot 4% formalin (Cribb, Bray 2010). Acanthocephalans were pressed between slides and fixed in 70% ethanol. Copepods and glochidia were preserved in 4% formalin. For species identification, cestodes and trematodes were stained in iron acetocarmine, dehydrated in ethanol and mounted in Canada balsam as permanent slides (Georgiev et al. 1986). Acanthocephalans, nematodes and copepods were mounted in glycerol as temporary slides for species identification.
Abundance and dimensions of the studied fish. n – number of fish, ind.; SL – standard length, mm; TL – total length, mm; m – mean parameters; SD – standard deviation
Parameters | Bug basin | Dniester basin | ||||
---|---|---|---|---|---|---|
Inzhenerne | Znesinnia | Plastova | Maliushevske | Stryiska | ||
n | 18 | 15 | 41 | 26 | 20 | |
SL, mm | m ± SD | 79.7 ± 19.3 | 53.6 ± 11.2 | 53.1 ± 21.4 | 121.9 ± 19.4 | 63.4 ± 4.4 |
min. – max. | 54 – 123 | 40 – 82 | 27 – 97 | 100 – 188 | 58 – 75 | |
TL, mm | m ± SD | 93.1 ± 20.9 | 65.1 ± 13.2 | 58.0 ± 28.9 | 142.2 ± 20.1 | 76.1 ± 3.7 |
min. – max. | 69 – 140 | 50 – 99 | 31 – 120 | 119 – 214 | 70 – 83 |
Indices of prevalence (P, %), mean intensity (MI), intensity range (IR) and mean abundance (A) were calculated for each parasite species according to Bush et al. (1997). Differences in parasite abundance and species richness between the sites were tested employing generalized linear models (GLM, Poisson distribution corrected for under-/overdispersion, i.e. quasipoisson), using fish size as a covariate. Differences in parasite assemblage composition were tested using permutational multiple analysis of variance (PERMANOVA, Anderson 2001) and visualized using non-metric multidimensional scaling (NMDS). Fish with no parasites were excluded from both PERMANOVA and NMDS. The response variable (distance matrix of samples, i.e. fish) for each PERMANOVA was calculated using (a) quantitative Bray–Curtis and (b) binary Jaccard dissimilarity as distance measures. PERMANOVA uses a multivariate analogue of Fisher’s F ratio to compare variability within groups versus variability between different groups, with P-values obtained using permutations (Anderson 2001). In this study, 999 permutations were conducted for each PERMANOVA. NMDS was conducted using the metaMDS function, which runs NMDS with several random starts and returns the best solution, rotated so that the largest variance of samples is on the first axis (Oksanen et al. 2019).
All analyses were conducted applying R 3.5.2, R Core Team 2018, using the
We identified eight taxa of parasites in the Lviv water bodies, including one ciliate, one monogenean, two cestodes, one digenean, one acanthocephalan, one parasitic crustacean and one unionid glochidium (Table 2). Only two parasite species, viz. the monogenean
Infection parameters of the Chinese sleeper (
Parasite species | Index | Bug basin | Dniester basin | |||
---|---|---|---|---|---|---|
Inzhenerne | Znesinnia | Plastova | Maliushevske | Stryiska | ||
CILIOPHORA | ||||||
P, % | 13.3 | 22.0 | 30.0 | |||
MI ± SD | 5.5 ± 6.4 | 21.1 ± 34.8 | 4.7 ± 5.3 | |||
IR | 1–10 | 1–113 | 1–15 | |||
A | 0.7 | 4.6 | 1.4 | |||
MONOGENEA | ||||||
P, % | 22.2 | 33.3 | 24.4 | 19.2 | 15.0 | |
MI ± SD | 1.3 ± 0.5 | 1.0 ± 0.0 | 2.7 ± 1.5 | 2.0 ± 1.2 | 7.3 ± 11.0 | |
IR | 1–2 | 1 | 1–5 | 1–4 | 1–20 | |
A | 0.3 | 0.3 | 0.7 | 0.4 | 1.1 | |
CESTODA | ||||||
P, % | 16.7 | 6.7 | 34.1 | 46.2 | 65.0 | |
MI ± SD | 3.3 ± 2.3 | 5.0 | 3.4 ± 3.5 | 7.0 ± 4.1 | 3.7 ± 2.1 | |
IR | 2–6 | 5 | 1–14 | 1–15 | 1–7 | |
A | 0.6 | 0.3 | 1.2 | 3.2 | 2.4 | |
P, % | 2.4 | |||||
MI ± SD | 2.0 | |||||
IR | 2 | |||||
A | 0.05 | |||||
DIGENEA | ||||||
P, % | 19.5 | |||||
MI ± SD | 2.5±1.4 | |||||
IR | 1–5 | |||||
A | 0.5 | |||||
ACANTHOCEPHALA | ||||||
P, % | 16.7 | |||||
MI ± SD | 2.3 ± 1.2 | |||||
IR | 1–3 | |||||
A | 0.4 | |||||
CRUSTACEA | ||||||
P, % | 11.1 | |||||
MI ± SD | 1.5 ± 0.7 | |||||
IR | 1–2 | |||||
A | 0.2 | |||||
BIVALVIA | ||||||
Unionidae gen. sp. | P, % | 77.8 | 14.6 | 7.7 | ||
MI ± SD | 5.2 ± 4.3 | 3.3 ± 2.4 | 1.5 ± 0.7 | |||
IR | 1–17 | 1–8 | 1–2 | |||
A | 4.1 | 0.5 | 0.1 | |||
Species richness | 5 | 3 | 6 | 3 | 3 |
There was a significant difference between the localities in parasite infracommunity species richness (GLM, df = 4.114, P = 0.002), but not in infracommunity abundance (GLM, df = 4.114, P = 0.315; Fig. 1). Parasite assemblage composition significantly differed between the sites in terms of both Bray–Curtis and Jaccard distances (PERMANOVA, both df = 4,78, both P = 0.001; Fig. 2).
Differences in assemblage species composition were significant in all pairs of localities (PERMANOVA, all P < 0.05), except for Lake on Stryiska and Lake Maliushevske (PERMANOVA, P = 0.498 and 0.676 for Jaccard and Bray–Curtis distances, respectively). Fish from Lake on Stryiska and Lake Maliushevske were typically parasitized by
Both
Another non-native parasite species, the copepod
Differences between the surveyed bodies of water were mainly due to their local seasonal conditions, and catchment characteristics. The geo-ecological conditions of lakes (both artificial and natural) in the Lviv region change every year depending on both natural and anthropogenic factors, e.g. precipitation, sewage discharge, etc. (Koinova, Chorna 2019). The most different water body (among the studied ones) is Lake on Plastova, which is an artificial pond with a muddy bottom, overgrown with macrophytes. This resulted in high infestation of the Chinese sleeper with trichodinids (Drobiniak et al. 2014) in this lake (see Table 2). The lake is characterized by a high concentration of organic matter in water (Koinova, Chorna 2019), and the presence of a large number of crustaceans, probably due to rich food resources (K. Nazaruk, unpublished data). This may be the source of a wider spectrum of parasites in this water body.
The second lake with good environmental conditions is Inzhenerne, where five parasite species occurred (see Table 2). It is an artificial lake used for fishing purposes. It is the only lake where the acanthocephalan
The similarities in the species composition of parasite assemblages from Lake Maliushevske and Lake on Stryiska (both located in the Dniester basin) were probably not due to their location in the same catchment, but due to the deterioration of environmental conditions in both lakes. Since the first intermediate hosts of
Invaders directly or indirectly affect the interactions between invasive and native parasite and host populations and their communities, which is manifested through various mechanisms (Goedknegt et al. 2016). The success of an invasion depends on the ability and chances of a parasite to complete its life cycle in the non-native environment. This is particularly important for parasites with complex life cycles, the invasional success of which depends on the presence of suitable intermediate hosts in the invaded ecosystem (Taraschewski 2006).
Usually, when several non-native species invade the same environment, this mutually increases the invasion success of each of them, which underlies the so-called ‘invasional meltdown hypothesis’ (Simberloff, von Holle 1999). This may also apply to parasite–host interactions, as invasive hosts may support the spread of non-native parasites introduced by other vectors (Taraschewski 2006; Emde et al. 2014). One piece of evidence for this hypothesis may be the find of the Asian crustacean
In general, the native parasite acquisition by the Chinese sleeper in the studied region is low. High abundance is mainly exhibited by non-native parasites (see Table 2). The current data confirm the presence of co-introduced populations of the monogenean (