Introduction

Exotic species also may serve as sources for new parasite species to invade native host populations (Mack et al. 2000). Following a successful introduction, one would expect exotic species to become increasingly parasitized by the parasites harboured by ecologically similar native species. On the other hand, the release from parasites and pathogens, which is predicted to be greatest early in the invasion, forms part of the “enemy release hypothesis” (Keane and Crawley 2002; Torchin et al. 2003). It thus appears likely that sampling the parasite load of an exotic population over the time course following an introduction would yield increasing numbers of parasites, until the new hosts reach a parasite load similar to that of native species.

The round goby Neogobius (Apollonia) melanostomus (Pallas, 1814) is a bottom-dwelling fish native for the Ponto-Caspian basin (Smirnov 1986). The processes of invasion of the round goby were started by its introduction to Lake St. Clair (Great Lakes, North America) and the Gulf of Gdańsk (southern Baltic Sea) in 1990 (Skóra and Stolarski 1993; Jude et al. 1992). Now, it is widely distributed in all Great Lakes basin (Charlebois et al. 1997). Recently, the cases of the round goby invasion are mentioned in the Aegean Sea (Eryilmaz 2002), in the different parts of the Baltic Sea (Sapota and Skóra 2005), North Sea basin (van Beek 2006), and basins of the rivers Danube and Rhine (Jurajda et al. 2005; van Kessel et al. 2009). In the German part of the Baltic Sea, this fish was first noted in 1998 near the Rügen Island (Winkler 2006). Now, it is distributed along all southwestern Baltic coast and includes the Stettiner Haff (Szczecin Lagoon), the Unterwarnow (the estuary of the Warnow River), the mouth of the Trave River, and in the Nord-Ostsee (Kiel) Kanal.

In the Baltic Sea (Gulf of Gdańsk), the round goby N. melanostomus is entered to parasitic system that includes fish-eating birds, fishes of different ecological groups (predatory, planktivorous, bentivorous), and invertebrates (Kvach and Skóra 2007). Non-indigenous gobies colonizing the Baltic Sea and the Great Lakes apparently did not introduce new parasites to native fishes because they were introduced with ballast waters (Kvach and Stepien 2008). They were colonized by native parasite fauna. The processes of colonization of the invasive round goby by parasites in the Baltic Sea and the Great Lakes support the “enemy release hypothesis”. Opposite to these processes, in the Danube basin, the invasive round goby introduced the digenean Bucephalus polymorphus following the invasion of the first intermediate host Dreissena polymorpha into mid-European waters (Mühlegger et al. 2009, 2010). The parasite fauna of the round goby from the Gulf of Gdańsk is characterized by low similarity with one from the Black Sea. The southwestern part of the Baltic Sea is characterized by higher salinity and presence of the higher number of marine species in the parasite fauna of gobiids (Zander 1998; Zander 2004; Zander et al. 2000). In this view, the southwestern (SW) Baltic Sea is more similar to the Black Sea than the Gulf of Gdańsk. But the parasite communities of the round goby in the western Baltic are not yet studied.

The objectives of the study were:

  1. 1.

    To study the parasite communities of the invasive round goby N. melanostomus in the SW Baltic Sea.

  2. 2.

    To analyze the parasite fauna of the resident gobiids and compare it with the round goby. To study the processes of adaptation of local parasite system to the new host.

  3. 3.

    To compare it with the published data from the Gulf of Gdańsk, Great Lakes, and native habitats in the Black Sea basin.

Material and methods

The study was carried out between July 5 and September 5, 2010. The fish were sampled by fishermen using fyke nets and personally using seine. The fish were transported in buckets with the aerated water (water was got in the place of sampling) to the laboratory of the University of Rostock; then the fish were dissected in 3 days. The salinity of water from each locality was measured. The round goby N. melanostomus was caught in next localities in the SW Baltic Sea (Fig. 1): 1. Stettiner Haff (Szczecin Lagoon) in Ueckermünde, S = 0.3 PSU; 2. Peenemünde (the mouth of the Peene River) near Freest, S = 4.2 PSU; 3. Strelasund Strait, in Stralsund and near the Rügen Island coast opposite the Stralsund downtown, S = 6.9–7.1 PSU; 4. Unterwarnow (the estuary of the Warnow River) Rostock near Kleine Warnow and Peez, S = 9.1–9.3 PSU; 5. Nord-Ostsee Kanal (Kiel Canal) near Rade, S = 7.0 PSU. The sampling in the localities in the eastern coast of the Rügen Island showed no round gobies. But round gobies where caught later on (September) nearly everywhere in the Baltic Sea close to the Greifswalder Bodden and the Usedom Island.

Fig. 1
figure 1

Schematic map of investigated area in the SW Baltic Sea. Black circles with numbers are sampling localities

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In total, 148 individuals of the round goby were examined for parasites. The total weight and standard length of each goby were measured before dissection. The numbers of gobies from each locality and their weights and lengths are presented in Table 1. In addition, 33 individuals of the black goby Gobius niger L., 1758 (from the Greifswalder Bodden, near Thiessow, Rügen Island, and the Unterwarnow, Rostock), 19 individuals of the sand goby Pomatoschistus minutus (Pallas, 1770), and 20 individuals of the common goby Pomatoschistus microps (Krøyer, 1838) (both from the Unterwarnow) were examined for parasites for comparative study. The weight of Pomatoschistus spp. was not measured due to the small sizes.

Table 1 The parasitization of the round goby by parasites in the different regions of the SW Baltic Sea
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The parasitological indices were calculated according to Bush et al. (1997): prevalence (P %), intensity (presented as min–max), mean intensity (MI), and abundance (A). The importance of parasites was judged by an altered core-/satellite concept according to their abundance: >2 = core species, 0.6–2 = secondary species; 0.2–0.6 = satellite species; and <0.2 = rare species (Zander et al. 2000). The tendency to join the infracommunity was evaluated according to the Infracommunity Index, ICI; the great tendency to join the community was determined by the ICI level more then 0.30 (Zander 2004). To compare the parasite faunas, the Index of Czekanowski-Sørensen, ICS (Czekanowski 1909; Sørensen 1948), was used.

Results

In total, 86 individuals of examined fishes (58.1%) were infected with parasites (Table 1). The maximal prevalence was in the Stettiner Haff (96%), but minimal in the Nord-Ostsee Kanal (40.1%). The round goby in the SW Baltic Sea was infected with 12 parasite species (Table 1): 1 species of Microsporidia, 1 species of Monogenea, 1 of Cestoda, 3 species of Trematoda, 3 species of Nematoda, 2 of Acanthocephala, and 1 species of Bivalvia. The maximal number of parasite species was registered in the Stettiner Haff near Ueckermünde—six species. Also, almost the same number of parasite species was in the Peenemünde—five species. Only one parasite species, Microsporidia gen. sp., occurred in the Strelasund.

The core of the round goby parasite community consists of two species: Diplostomum spathaceum and Unionidae gen. sp. glochidia (Table 1). Metacercariae of D. spathaceum occurred in eyes of fishes from the Stettiner Haff and Peenemünde. It was most abundant parasite of the round goby in the SW Baltic Sea. Another abundant parasites were glochidia of Unionidae, located in gills of gobies from the Stettiner Haff. Only microsporidians played the role of secondary species. These parasites were found in all localities (Table 1). The taxonomic status of these microsporidia is unclear, but the preliminary investigation shows that they are differs from the microsporidia infest gobiids in the Black Sea. This is most prevailed parasite species. The larvae of Pomphorhynchus laevis played a role of satellite species in the Stettiner Haff and Peenemünde. All other species were rare.

The infracommunity of the invasive round goby in the SW Baltic Sea consists of one to four species (Table 2). The infracommunities formed by one species are prevailed in the Strelasund, Unterwarnow, and the Nord-Ostsee Kanal, but in the Stettiner Haff the infracommunity formed by three species was prevailed (Fig. 2). In the Peenemünde the prevailed communities were two and three components. In total, 19 types of infracommunities were registered. One-component community, composed by microsporidians only, was most common. According to ICI, the great tendency to join the infracommunity have microspiridians (Table 3). Only in the Stettiner Haff, the great tendency has D. spathaceum met and Unio sp. glochidia.

Table 2 Composition of infracommunities of different types (number of cases/% to total number of fish infected)
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Fig. 2
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The percentage of different types of infracommunities of parasites of the round goby in different localities of the SW Baltic Sea

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Table 3 Infracommunity index
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Ten parasite species occurred in resident gobiids (Table 4). Six species were found in the black goby, four in the sand goby, and nine in the common goby. All these parasites were registered in the SW Baltic Sea earlier.

Table 4 The parasite of three species of native gobiids in SW Baltic Sea
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Discussion

Communities of parasites of the invasive round goby in the SW Baltic Sea

The microsporidians, which are most prevailed parasites in the round goby in the SW Baltic Sea, had the great tendency to join the infracommunity (Table 3). The parasite community, consisting of only microsporidians, was also most common in the region (Table 2). This tendency was common for all localities accept the Stettiner Haff, where microsporidians were presented only in composition with other species (Table 2). In this locality, the great tendency to join infracommunity has limnetic parasite species, such as D. spathaceum met and Unio sp. glochidia. The Stettiner Haff is the estuary of the Oder River, connected with the Baltic Sea via the rivers Peene, Swina, and Dziwna. This waterbody has low instable salinity from 0.3 to 4.5 PSU (mean salinity 1.4 PSU) (Radziejewska and Schernewski 2008). In the sampling place, the salinity was 0.3 PSU; this is the locality with the lowest salinity between the waterbodies studied. The limnetic parasites, such as B. polymorphus met, Tylodelphys sp. met, Unio sp. glochidia, occurred only in these waterbody and absent in all other localities (Table 1). Another locality with low salinity was the Peenemünde, the mouth of the Peene River (one of the rivers, which connect the Stettiner Haff with the main Baltic Sea)—S = 4.2 PSU. Some of limnetic parasite species (D. spathaceum met, E. excisus L3) were presented here (Table 1). But metacercariae of D. spathaceum lost the tendency to join infracommunity (Table 3).

In the localities, such as the Strelasund, Unterwarnow, and the Nord-Ostsee Kanal, the parasite community was rather poor. Also, the percent of infected fishes was lower there (Fig. 2). These waterbodies have “normal” Baltic salinity, from 6.9 to 7.1 PSU in the Strelasund and Nord-Ostsee Kanal to 9.1–9.3 PSU in the Unterwarnow. In all these localities, the microsporidians have very high tendency to join infracommunity (in the Strelasund, it was only parasite occurred) (Table 3). The marine species, such as monogeneans Gyrodactylus rugiensis and cestodes Bothriocephalus scorpii pl, occurred only in the Unterwarnow (Table 1).

Parasite fauna of resident gobiids and its comparing with the round goby one

All parasites found have local origin and common in another species of Baltic fishes. The parasites specific for the Ponto-Caspian gobiids did not occur. Most of the parasites are generalists and can infest many of fish hosts. Only exception is the monogenean G. rugiensis. This is the most interesting finding, because of its host specificity; it is a specific parasite of the common goby (Huyse et al. 2003). This is a case of occasional infestation of the round goby, but shows the possibility of G. rugiensis to switch to alien gobiid species. Most of the parasites registered in the round goby were not found in local gobiids (Table 2).

Only four parasite species occurred in both round goby and another gobiids: Microsporidia gen. sp., G. rugiensis, B. scorpii, and D. spathaceum. The Czekanowski-Sørensen Index (ICS) shows the low similarity between the parasite faunas of the round goby and local gobiids in the total SW Baltic. So, the similarity between the round goby and the black goby was 22.2%; between the round goby and the sand goby, it was 12.5%, but between the round goby and the common goby, it was 28.6%. Comparing the parasite fauna in the same locality (all three species occurred together in the Unterwarnow), we found the similarity higher: round goby/black goby—ICS = 44.4%, round goby/common goby—ICS = 50.0%. But it was no similarities in the parasite fauna of the round goby and the sand goby in the Unterwarnow (Table 2).

The parasites, such as D. spathaceum met, B. scorpii pl, Proteocephalus sp. pl, Echinorhynchus gadi, P. laevis have been already noted in different gobiid species in the SW Baltic Sea according to the published data (Zander et al. 1999; Zander 2004; Josten et al. 2009). The larvae of Cosmocephalus obvelatus were registered in the common goby from the Flensburg Fjord (Josten et al. 2009).

Role of the round goby in the parasite life cycles

Three of the parasite species were presented by adult stages: G. rugiensis, E. gadi, P. laevis. The acanthocephalan P. laevis was presented by both adults and larvae. G. rugiensis is viviparous ectoparasite, very specific to fish host. The acanthocephalans found in the round goby are parasites of different fish species in the Baltic Sea. The infestation of fish comes due to consumption of the gammarids infected with cystacanths (Petrochenko 1956).

Five parasite species are parasites of fish-eating birds in adult stages, but larvae are in fishes: D. spathaceum, Tylodelphys sp., C. obvelatus, Eustrongylides excisus, and Paracuaria adunca. D. spathaceum, Tylodelphys sp., and C. obvelatus are generalists, which infest many species of fish-eating birds (Gaevskaya et al. 1975; Anderson 2000). They are also generalists in larval stages. Both larvae and adults are common in different parts of Europe. The nematode E. excisus is specific parasite of cormorants Phalacrocorax carbo (Anderson 2000). The first intermediate host is the freshwater oligochaets Tubifex sp., which is dietary item for gobiids. For the digeneans, the round goby plays a role of the second intermediate host. For nematodes fishes are paratenic hosts.

Another three species are parasites of fishes in adult stage, but the larvae are also in fishes: B. scorpii, B. polymorhus, and P. laevis. The cestode B. scorpii is a parasite of scorpionfishes Myoxocephalus sp. and flounders Platichthyes flesus (Renaud et al. 1984). Intermediate hosts are planktonic crustaceans, but small-sized gobiids (mostly Pomatoschistus spp.) play the important role in the realization of the life cycle to be hosts of post-pleurocercoids (Robert et al. 1988). The round goby got the same ecological niche in the Baltic Sea, to be the host of the post-pleurocercoids of B. scorpii, which located in the gut of fishes. The trematode B. polymorphus in adult stage is parasite of zanders Sander lucioperca, sometime another predatory percids (like perch Perca fluviatilis). The gobiids, which plays important role in the diet of the zander, are second intermediate hosts (Gaevskaya et al. 1975). In the case of P. laevis, the round goby plays a role of definitive host and also paratenic. The encysted larvae of this acanthocephalan were located in the intestinal walls of gobies.

Unionidae are free-living mussels in adult stages, but parasites as larvae. The glochidia have no host specificity, located in the gills of many of fish species. Microsporidia were presented by xenomas, which located in the mesentery of gobiids.

Comparing with the data from the other sites of the Baltic Sea, Great Lakes, and the Black Sea basin

According to the data of Czekanowski-Sørensen Index, the similarity with the other part of the Baltic Sea is rather low, less than 50% (Table 5). In total, five species of parasite found in the round goby in the SW Baltic Sea were already mentioned in this host species in the other parts of this water basin (Table 6). The similarity with the Black Sea is also low. The parasite fauna of the round goby in the SW Baltic Sea consists of only two parasites, which were registered in the northwestern (NW) Black Sea (Table 6; Kvach 2005): B. polymorphus met and E. excisus L3. Both of these parasites were never mentioned in the round goby in the Baltic Sea earlier. Another two parasite species, D. spathaceum met and P. adunca L3, were not mentioned in the NW Black Sea, but registered in the other parts of the Black Sea basin (Chernyshenko 1957; Korniychuk et al. 2008).

Table 5 The Czekanowski-Sørensen Index between the parasite fauna of the round goby in different part of the Baltic Sea and the NW Black Sea (native area)
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Table 6 Parasites of the round goby in the different parts of the Baltic Sea comparing to the Black Sea data
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Between 25 parasite species found in the Great Lakes according to the published data (Muzzall et al. 1995; Pronin et al. 1997; Camp et al. 1999; Kvach and Stepien 2008), only one species, Diplostomum spp. met was registered in the Baltic Sea (Ics = 5.4%). In general, the parasite fauna of the round goby in the Great Lakes consists of local species and not similar to the European one (Kvach and Stepien 2008).

Processes of colonization of the invasive round goby by parasites

In the SW Baltic Sea, the round goby was colonized by seven new parasites species, did not found in this fish in the Baltic Sea earlier: Microsporidia gen. sp., G. rugiensis, B. polymorphus, C. obvelaus L3, E. excisus L3, P. adunca L3, Unio sp. glochidia. Microsporidia gen. sp., G. rugiensis, and Unio sp. are new parasites for the round goby.

The processes of colonization have same tendency as in the Gulf of Gdańsk. The typical gobiid parasites, like the trematode Cryptocotyle concavum met and the nematode Dichelyne minutus, which are common in the round goby in the Black Sea (Kvach 2005; see Table 6), were not registered in the round goby from the SW Baltic. Both of these parasites are presented in resident gobiids (see Table 4; Zander 2004; Zander et al. 1999, 2000). The same situation was in the Gulf of Gdańsk in 2001, at the beginning of the study of the invasive round goby parasites (Kvach 2002; Rokicki and Rolbiecki 2002). Later, both these parasites occurred in the parasite fauna of the round goby in Polish waters (Rolbiecki 2006; Kvach and Skóra 2007).

The introduction of the Ponto-Caspian round goby to the SW Baltic Sea makes the life cycles of the digenean B. polymorphus and the nematode E. excisus in this waterbody identical to that in the Ponto-Caspian region. On the other hand, due to the presence of these parasites in the SW Baltic Sea, the invasive round goby starts to play the same role in this ecosystem, as in their native habitats. The presence of this invasive component in the life cycles supports the further distribution and spreading of B. polymorphus and E. scisus at the colonized area.