Parasitol Res (2014) 113:1605–1624 DOI 10.1007/s00436-014-3791-2
ORIGINAL PAPER
Parasitization of invasive gobiids in the eastern part of the Central trans-European corridor of invasion of Ponto-Caspian hydrobionts Yuriy Kvach & Yuliya Kornyychuk & Katarzyna Mierzejewska & Nataliya Rubtsova & Violetta Yurakhno & Joanna Grabowska & Mykola Ovcharenko Received: 10 October 2013 / Accepted: 28 January 2014 / Published online: 9 March 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Four gobiid species, Babka gymnotrachelus, Neogobius melanostomus, Neogobius fluviatilis, and Proterorhinus semilunaris, were parasitologically studied in different localities of the Dnieper and Vistula river basins. The highest number of parasitic species was found in N. fluviatilis (35 taxa). The parasite fauna of N. melanostomus, B. gymnotrachelus, and P. semilunaris consists of 23, 22, and 15 taxa, respectively. The species accumulation curves show stable accumulation of parasite species by all four fish hosts along the studied part of the corridor, from the Dnieper Estuary to the Vistula River delta. The plot reveals also that the studied gobies lose the parasites common in the host native range and accept new parasites from the colonized area. In the
Y. Kvach (*) Odessa Branch of the Institute of Biology of the Southern Seas of the National Academy of Sciences of Ukraine, Pushkinska 37, Odessa 65011, Ukraine e-mail:
[email protected] Y. Kornyychuk : V. Yurakhno Institute of Biology of the Southern Seas of the National Academy of Sciences of Ukraine, Nakhimov Avenue 2, Sevastopol 99011, Ukraine K. Mierzejewska Department of Fish Biology and Pisciculture, University of Warmia and Mazury in Olsztyn, Oczapowskiego 2, 10719 Olsztyn, Poland N. Rubtsova Department of Biology, Zaporizhzhya National University, Zhukovskogo 66, Zhaporizhzhya 69600, Ukraine J. Grabowska Department of Ecology and Vertebrate Zoology, University of Łódź, Banacha 12/16, 90237 Łódź, Poland M. Ovcharenko W. Stefański Institute of Parasitology of the Polish Academy of Sciences, Twarda 51/55, 00818 Warsaw, Poland
case of N. melanostomus, it complies with the enemy release hypothesis, as the parasite load was low in the invaded area if compared to the native range. The three other alien gobies are vector for Gyrodactylus proterorhini in the Baltic basin. Moreover, populations of this alien monogenean tend to be more abundant in their new range in comparison with the Black Sea basin. In general, the number of parasite species in the colonized area was of the same rank as in the native one for N. fluviatilis, and even higher for B. gymnotrachelus. This results from accumulating new parasite species along the gobiid invasion route. In particular, the N. fluviatilis, B. gymnotrachelus, and P. semilunaris lost some of their native parasites and gained the local ones after entering the post-dam part of the Vistula River; it can be interpreted as a partial escape from parasites.
Introduction The Ponto-Caspian gobiids (Actinopterygii: Gobiidae: Benthophilinae) are among the most quickly widespread invasive species in Europe (Copp et al. 2005; Grabowska et al. 2008). They extend their ranges via the three invasion corridors of Ponto-Caspian hydrobionts described by Bij de Vaate et al. (2002). One of them, the so-called central corridor, comprises the Dnieper River; its tributary, i.e., the Prypiat River; the Bug River; and the Vistula River. It crosses three countries—Ukraine, Belarus, and Poland—then it extends westwards to Germany and the Netherlands through the system of inland canals connecting the Baltic and Northern sea basins. One of the crucial sections of this route is the DnieperBug Canal (also called Królewski Canal) that connects the Prypiat River (Black Sea basin) with the Bug River (Baltic Sea basin). The rate of the colonization process through that corridor was estimated as up to seven alien invasive species per 10 years (Panov et al. 2009).
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The four alien gobiids species, the racer goby Babka gymnotrachelus (Kessler, 1857), the round goby Neogobius melanostomus (Pallas, 1814), the monkey goby Neogobius fluviatilis (Pallas, 1814), and the western tubenose goby Proterorhinus semilunaris (Heckel, 1837), recorded so far in Polish inland waters differ in their pathways of introduction (Kostrzewa et al. 2004; Grabowska et al. 2008). The racer goby, the monkey goby, and the tubenose goby most probably used the central corridor of invasion. In the case of racer goby, data on that invasion route were supported by molecular analysis (Ohayon and Stepien 2007). Moreover, the species was detected for the first time in 1995 in the Bug River in a close vicinity of the Muchawiec River mouth, a tributary that joins the Dnieper-Bug Canal with Prypiat River (Danilkiewicz 1996). It cannot be coincident that 2 years later in the same section of the Bug River, the monkey goby was first noted (Danilkiewicz 1998). This locality indicates the central corridor as the most probable route of their expansion. Soon after their first records in Polish inland waters, all the gobies have spread farther downstream the Vistula River system, entering also some tributaries and reached the vicinity of the river delta by 2002 (Kostrzewa and Grabowski 2001; Kostrzewa et al. 2004; Grabowska et al. 2008; Grabowska et al. 2008). Finally, the western tubenose goby (mentioned as Proterorhinus marmoratus) was noted in the Lower Vistula (Włocławek Reservoir) in 2008 (Grabowska et al. 2008). The appearance of all the abovementioned species in Polish waters is a continuation of their gradual upstream migration in the Dnieper and in its tributary—Prypiat River (Pinchuk et al. 1985; Semenchenko et al. 2011). Five gobiid species (monkey goby, round goby, racer goby, western tubenose goby, and also the Black Sea tadpole-goby, Benthophilus nudus (Berg, 1898)) were recorded in the Middle Dnieper basin until the 1980s, when they were found near the City of Kiev (Pinchuk et al. 1985). They spread mostly through the active migration; however, short-distance passive migration with vessels in Ukraine and Belarus is also highly possible, considering high density of the gobies in the river harbors in Belarus (Semenchenko et al. 2011). On the other hand, the round goby was introduced most probably with ballast waters (Skóra and Stolarski 1993). However, despite investigations, the origin of N. melanostomus population introduced into the Gulf of Gdańsk remains unknown, as well as the route of the vessels that transported this species into the Gulf of Gdańsk. Three possible ways are considered. At the moment, the route from the Sea of Azov (through Don River) or from the Caspian Sea and then through Volga River, Rybinski Reservoir, Moscow River, and Onega Lake to the Gulf of Finland seems to be the most probable. The records of N. melanostomus in the Moscow River near Moscow from the middle of 1980s (Sokolov et al. 1989) support this supposition (Sapota 2004). It is worth mentioning that the round
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goby was recorded in Belarus, in Prypiat near Brest, so we can expect its invasion to Polish inland waters from the central invasion corridor in the nearest future. Less probable but still possible is a route around Europe, from the Sea of Marmara, through the Mediterranean, the Atlantic, and the North Sea into the Baltic. This way, the round goby could be transported to the Gulf of Gdańsk as fertilized eggs or juveniles in ballast waters. Comparing the longest possible time of round goby embryogenesis, the length of possible routes, and the average speed of ships from 5 to 17 km/h, it was estimated that survival of round goby embryos in ballast waters is highly possible for all the three abovementioned routes. It is also probable that round goby could hatch in ballast tanks of ships (Moskalkova 1996; Sapota and Skóra 2005). The round goby has spread along the Polish coast, entering also the lower section of some rivers. It was recorded as far as 130 km upstream in the Vistula (Kostrzewa and Grabowska 2002). Thus, the round goby invasion is a combination of passive dispersal in the first stage of invasion (the so-called arrival) and, later, an active dispersal to the adjacent waters. Thus, the round goby experienced quite different conditions during its journey to the invaded range than the other three species of Ponto-Caspian gobies. First, its translocation was rather rapid if compared to slow, taking years, seminatural dispersal of the other three gobies. Transport in ballast waters, probably in stage of eggs or newly hatched juveniles, could result in parasite loss. Even if some adults were transported in the same way, days spent in ballast water tanks could cause loss of their native parasites. The same “cleaning” effect could result also from a change in water salinity, from ca. 16–18 PSU in the Black Sea to 7–8 PSU in the Gulf of Gdańsk. The migration of racer and monkey gobies through the central corridor to Poland took decades (Semenchenko et al. 2011). The gobies are not good swimmers, and it is believed that their expansion in European waters has rather semi-natural character, facilitated by human alteration of the river flow and banks as well by inland water transport (Ahnelt et al. 1998; Wiesner 2005). The dam reservoirs seemed to play a particular role in this migration, as gobies reach higher densities in such water bodies than in the adjacent rivers (Pinchuk et al. 1985; Janković 1996; Harka and Biró 2007; Slynko et al. 2011). Such lentic sections in river systems are probably places of population growth and sources for a farther spread. There are six such reservoirs on the Dnieper River from the mouth of the Prypiat River to the Dnieper-Bug Canal (Slynko et al. 2011). In the Polish section of the central invasion corridor, gobies have passed through the dam on the Zegrzyński Reservoir and another one on the Włocławski Reservoir. The other places where gobies occur in greater densities are rip-rap constructions near river harbors (Wiesner 2005; Semenchenko et al. 2011). Such high densities attained in almost stagnant, muddy waters create ideal
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conditions for boosting the prevalence of both native and new parasite species in gobies. According to the “enemy release hypothesis” loss of parasites during invasion process is crucial for the host species as it determines the success or failure of its invasion (Prenter et al. 2004; Torchin et al. 2003). The hypothesis was supported by the study upon the invasive round goby and western tubenose gobies in the North American Great Lakes (Kvach and Stepien 2008). On the other hand, invasive species may introduce novel pathogens to the colonized area (Ovcharenko 2009; Ovcharenko et al. 2009). Such situation is favorable to the invader only if the introduced parasites cause a disproportionate harm to native species (Tompkins et al. 2003). Finally, invasive species can also acquire new parasites from local hosts. Boreal-Atlantic parasites were registered in the round goby in the Vistula Lagoon (Rolbiecki 2006). Local parasites may quickly evolve to infect the invading species, but temporal “release” may provide an early decisive advantage to the introduced species (Tanaka et al. 2007). Most papers relating to the role of parasites in the invasion success are based usually on studies upon change of parasite prevalence in native and invasive species co-occurring within the same habitat, or on biogeographical studies of parasite prevalence in native and introduced host populations (Colautti et al. 2004; Liu and Stiling 2006). Continuation of the studies upon parasites in the invasive gobiids is important as a background for the verification of the “enemy release hypothesis” and also for confirmation of using the corridors of migration by parasites. We believe that the different introduction pathways and dispersal types as well as the duration of the invasion processes should affect the parasite composition and prevalence in the round goby, monkey goby, racer goby, and tubenose goby along the central corridor. Thus, the aim of this study is to evaluate the prevalence and species richness of parasites in populations of four Ponto-Caspian gobiid invaders along their invasion route.
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Dnieper Estuary and delta); also, three individuals of the tubenose goby from the Lower Vistula River (7) were combined with the tubenose gobies from the Vistula delta (8; the locality “Lower Vistula and delta”). Then, for further statistical analyses, the localities were grouped according to the time of first records of the invasive gobies (see Table 1 for locality numbers): (1) native range (includes localities 1, 2); (2) old invasion, from 1985 (locality 3); (3) new invasion, from 1996, in the Vistula basin before the dam in Włocławek (localities 4– 6); and (4) current invasion, from 2001, in the Lower Vistula behind the dam in Włocławek (localities 7–8). The Vistula basin (as new invasive range) was provisionally divided into two parts, as the dam can be considered as an artificial barrier for hydrobionts migration. The parasitological terminology was accepted after Bush et al. (1997); the prevalence, intensity, and abundance (including their min-max values) were calculated. The mean infracommunity index was calculated as the mean number of parasite species in a host (Zander 2004). The standard deviation (SD) was calculated for the mean parameters; t test by group was used to verify the statistical significance of differences in abundance and values of the infracommunity index. The parameters of abundance of each parasite species in the infracommunities of studied gobies were used for the multifactor analysis. For the discriminant analysis, the fish were grouped according to the above-explained four categories. The Mahalanobis distance (MD) between categories was calculated; also, the plots of discriminant function were built for each host species. The species accumulation index was calculated according to Ugland et al. (2003). The fauna similarity level was evaluated using the Czekanowski-Sørencen index (Ics) (Sørensen 1948) and Bray-Curtis similarity index (BC) (Bray and Curtis 1957). The square root was retrieved from abundance parameters before BC calculation. The fauna similarity was considered high if the indices exceeded 50 %. The statistical analysis was done using Primer 6.0 (Copyright 2005 PRIMER-E Ltd) and Statistica 7.0 (Copyright StatSoft Inc. 1984–2004).
Materials and methods A total of 483 fishes representing four species (Babka gymnotrachelus, Neogobius melanostomus, Neogobius fluviatilis, Proterorhinus semilunaris) were parasitologically studied during 2010–2012 (Table 1). The gobies were caught at 25 sampling sites located within the Dnieper and Vistula basins. The sampling sites were grouped for further statistical analyses into eight main localities, according to their hydrographical and hydrobiological characteristics (Fig. 1). In two cases, when the number of sampled fish was too low for descriptive and statistical analysis, the neighboring localities were also included. In such way, one individual of racer goby from the Dnieper Estuary (1) was combined with the racer gobies from the Dnieper delta (2; the locality called
Results The monkey goby, Neogobius fluviatilis, was found to be a dominant invader: it occurred in all the localities studied, except the Dnieper River delta (Table 1). Racer goby, Babka gymnotrachelus, was the second widespread species. It was recorded in all localities except the Middle Dnieper (Table 1); in the Dnieper Estuary, we found a single specimen of this goby. Two other species occurred relatively rare. The western tubenose goby, Proterorhinus semilunaris, was caught in the Dnieper River delta (native range), in the Middle Dnieper, in the Włocławek Reservoir, and in all localities in the lower section of the Vistula River (Table 1). The round goby was
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Table 1 The number (n) and standard lengths (SL) of the studied fishes from different localities Locality 1. Dnieper Estuary 2. Dnieper River delta 3. Middle Dnieper 4. Bug River 5. Bugo-Narew 6. Włocławek Reservoir 7. Lower Vistula 8. Vistula River delta
Neogobius fluviatilis
Neogobius melanostomus
Babka gymnotrachelus
n
62
37
1
SL
7.8 (2.4–13.2)±2.9
8.0 (2.6–11.2)±1.6
4.5
Proterorhinus semilunaris
n
36
12
18
SL
5.7 (4.4–8.9)±1.0
4.1 (3.4–5.9)±0.8
2.7 (1.8–5.1)±0.7
n
24
6
SL
5.5 (2.8–8.6)±1.6
4.9 (4.1–5.8)±0.6
n
8
51
SL
7.6 (3.5–13.7)±3.0
5.7±2.3
n
58
24
SL
7.0 (5.6–9.5)±1.0
5.3 (2.5–6.9)±1.1
n
8
30
14
SL
6.7 (6.4–7.1)±0.3
3.7 (2.7–5.7)±0.7
4.0 (2.5–5.5)±1.1
n
24
16
3
SL
6.7 (5.5–9.3)±1.0
5.0 (3.1–7.7)±1.6
2.8 (1.9–3.4)±0.8
n
6
20
15
10
SL
6.7 (2.1–8.4)±2.4
6.5 (2.0–13.4)±2.9
3.6 (2.5–4.4)±0.5
2.6 (2.0–3.1)±0.4
rather numerous in the native range (Dnieper Estuary and delta), and farther, it was found only in the Vistula delta (Table 1). Parasite diversity The maximum parasite richness (35 taxa) was detected in the monkey goby (Table 2) (Figs. 2, b, c, d, e, g, h, l, m). The unicellular parasites were represented by two taxa of Microsporidia (Loma acerinae, Microsporidium sp.), Ichthyosporea (Dermocystidium sp.), Apicomplexa (Coccidia gen. sp.), and Ciliophora (Trichodina domerguei). The helminths comprised Monogenea (Gyrodactylus proterorhini), Cestoda (Proteocephalus gobiorum), 16 digenean taxa (including 11 taxa identified to species level, Diplostomum metacercariae identified to genus level, and four species of unidentified metacercariae), 8 species of nematodes (including 7 species and Agamonema sp. sensu Moravec and Ergens, 1971), and two acanthocephalan species (cystacanths of Pomphorhynchus laevis and adult Telosentis exiguus). In addition, the glochidia of Unionidae gen. sp. (part of them were identified as Anodonta anatina) parasitizing on gobies’ gills were found. The parasite fauna of round goby consisted of 23 taxa (Table 3; Figs. 2, a, f, k, n). The microparasites belonged to the same taxa as in the monkey goby, except for Dermocystidium sp. The myxozoan Kudoa nova was also registered in Dnieper Estuary zone (sampling point 1). The helminths were represented by two cestode species (Ligula pavlovskii and P. gobiorum), seven digeneans including four species, two taxa identified to genus level (Diplostomum sp. and Pronoprymna sp.), and unidentified Echinochasmidae
metacercariae, five taxa of nematodes including four identified to species level and Agamonema sp. as well as three acanthocephalan species (cystacanths of Polymorphus minutus and P. laevis, also T. exiguus). The unidentified unionid glochidia were found on fish gills. The parasite fauna of the racer goby consisted of 22 taxa (Table 4) (Fig. 2, i). The cysts of unidentified fungi were found on gills. Among the other microparasites, the ciliates (T. domerguei) and unidentified coccidians were found. The monogeneans were represented by G. proterorhini and cestodes by unidentified juvenile Caryophyllaeidae found in the guts. The digeneans were represented by 10 taxa, including five identified species, one taxon identified to genus level (Diplostomum sp. met), unidentified Echinochasmidae metacercariae, and also three unidentified species. Three species of nematodes were found in this host (Agamonema sp., Cosmocephalus obvelatus, and Eustrongylides excisus). The acanthocephalan P. laevis (both larvae and adult specimens) was also present. Two taxa of glochidia of Unionidae were also found (Anodonta anatina and another, unidentified, species). The poorest parasite fauna, 15 species, was noted in the tubenose goby (Table 5) (Fig. 2, j). Among microparasites, we found two taxa of microsporidians (Loma acerinae, Microsporidium sp.) and one species of ciliates (T. domerguei). The helminths were represented by one cestode species (P. gobiorum), eight digenean species (four identified species, including unidentified Diplostomum sp. and three unidentified metacercaria), two species of nematodes (Agamonema sp. and E. excisus), and one species of acanthocephalans (P. laevis). Monogeneans were not recorded. The glochidia of unidentified unionids were also found.
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Fig. 1 The schematic map of the sampling area. 1 Dnieper Estuary locality includes five sites: N 46○ 37.233′ E 31○ 49.241′, N 46○ 32.532′ E 31○ 33.675′, N 46○ 36.456′ E 31○ 31.499′, N 46○ 38.437′ E 32○ 36.456′, and N 46○ 38.437′ E 31○ 31.393′. 2 Dnieper delta (two sites): N 50○ 29.084′ E 30○ 32.449′ and N 50○ 42.456′ E 32○ 19.556′. 3 Middle Dnieper: N 50○ 42.454′ E 30○ 20.111′. 4 Bug River (four sites): N52° 23.594′ E 22° 41.52′, N 52° 36.975′ E 21° 35.897′, N 52° 35.37′ E 22°
25.53′, and N 52° 19.33′ E 23° 2.41′. 5 Lower Bug-Narew River (three sites): N 52° 26.04′ E 20°43.357′, N 52° 27.62′ E 21° 3.87′, and N 52° 27.265′ E 21° 4.099′. 6 Włocławek Reservoir (two sites): N 52° 31.924′ E 19° 41.28′ and N 52° 39.448′ E 19° 4.336′. 7 Lover Vistula (four sites): N 52° 46.205′ E 18° 55.191′, N 53° 50.04′ E 18° 50.187′, N 53° 55.708′ E 18° 50.569′, and N 54° 15.36′ E 18° 56.06′. 8 Vistula delta N 54° 18.927′ E 18°53.533′
Statistical analysis
Vistula River system (t=3.382, p=0.001). However, the parasite richness in the native range was lower than in the places of invasion (Table 6). The mean infracommunity index for the western tubenose goby in the post-dam part of the Vistula River was lower than in the Middle Dnieper River (old invasion; t=2.284, p=0.035) and the before-dam part of the Vistula basin (t=3.50, p=0.002). In addition, for two gobiids, the mean infracommunity index was significantly higher in the before-dam part of the Vistula River System than in the native range for the monkey goby (t=3.16, p=0.001) and for the western tubenose goby (t=2.404, p=0.022). The discriminant analysis revealed the significant difference between localities in almost all cases (Table 7; Fig. 3). The only case with no difference was between the parasitization of the tubenose goby in the post-dam part of the Vistula River and in the native range. In all the other cases, the
According to the t test, the parasite mean infracommunity index of gobiids inhabiting the Vistula River lower dam differed significantly in most cases from the one calculated for other regions (Table 6). Therefore, in spite of the same parasite richness, the parasite mean infracommunity index for the monkey goby in this region was significantly lower than in the Middle Dnieper River (old invasion; t=2.42, p=0.019). In addition, the mean infracommunity was lower than in the Vistula downstream from the dam (t=3.44, p=0.001). The round goby parasite mean infracommunity index in the postdam part of the Vistula River was lower than in the native range (t=5.327, p
