Fish helminths in Lithuanian inner waters

INTRODUCTION

There are far more kinds of parasitic than non-parasitic organisms in the world and parasites may be one of the factors that regulate host populations (Roberts, Janovy, 2008). Parasitic diseases decrease fish growth rate and fertility, influence development of anomaly, decrease the quality of fish meat, and can cause mass death of fish. Manifestation of parasites can be different. Infected by digestive tract parasites, fish cannot assimilate a great part of nutrients and become exhausted. Parasites of the digestive tract, gill, and skin cause mechanical injuries with their attachment organs sometimes leading to necrosis. Sites of injuries are a favourable medium for bacteria and fungi, which cause infectious diseases. Gill lamella hypertrophy, tumour formation, tissue injuries, and emergence of haemorrhages caused by monogenean infestation lead to a decrease of the respiratory surface and fish death because of hypoxia or anaemia. In aquaculture, diseases are among the most serious threats to commercial success (Noga, 2010). All these facts make the study of fish helminths relevant.

In Lithuania, investigation into fish helminths started at the beginning of the twentieth century. In 1909, Wegener studied helminths and other parasites in the Curonian Lagoon. Later, Szidat (1926, 1944) studied fish parasites in the Curonian Lagoon. In the Soviet period, a number of researchers studied fish parasites in natural water bodies and aquacultures: Sabina Gecevičiūtė, Rostislavas Krotas, S. A. Paškevičiūtė, Edvardas Rauckis, Vytautas Kemėža, A. D. Žaliūnienė, V. V. Marazas, V. A. Dogel, G. K. Petrushevskij, E. A. Bogdanova, B. E. Kazakov, E. N. Protasova, V. A. Rojtman, D. G. Tsejtlin, D. Kh. Khussein, A. A. Shigin and others. The bibliography of these works can be found in Rauckis’s (1988) book in which the author provided an overview of fish parasites in Lithuania. Vytautas Oškinis (1993) studied fish helminths in the Lake Drūkšiai. The following researchers studied fish parasites in the Curonian Lagoon and the coastal region of the Baltic Sea: Stankus (1996), Bacevičius (2002, 2003, 2004, 2009), Bacevičius and Karalius (2008), Rakauskas et al. (2008), and Bagdonas et al. (2011). Bacevičius (2003) provided an overview of the studies on fish parasites in the Curonian Lagoon and the costal region of the Baltic Sea. Pilecka-Rapacz and Kesminas (2006) investigated the occurrence and intensity of the nematode Anguillicola crassus infection in eels in Lake Dringis. Rakauskas and Blaževičius (2009, 2010) studied parasites of the roach (Rutilus rutilus).

However, the composition of helminths may have undergone changes over time. The aim of the present study is to investigate helminths of freshwater fish in Lithuanian inner waters.

MATERIALS AND METHODS

Fish were sampled from June to November 2005 using electro-fishing and fyke nets at 55 study sites in 20 lakes, the Kaunas Hydroelectric Power Plant reservoir, the Curonian Lagoon and 13 different rivers (Figure). In total, 947 individuals of 23 fish species were examined for helminths:ten brown trouts Salmo trutta morpha fario L., 1758, two European whitefish Coregonus lavaretus (L., 1758), two vendaces Coregonus albula (L., 1758), 193 Northern pikes Esox Lucius L., 1758, 217 roaches Rutilus rutilus (L., 1758), 41 chubs Squalius cephalus (L., 1758), 42 common daces Leuciscus leuciscus (L., 1758), 140 rudds Scardinius erythrophthalmus (L., 1758), five belicas Leucaspius delineatus (Heckel, 1843), 28 tenches Tinca tinca (L., 1758), four gudgeons Gobio gobio (L., 1758), three bleaks Alburnus alburnus (L., 1758), 37 white breams Blicca bjoerkna (L., 1758), 16 freshwater breams Abramis brama (L., 1758), four vimba breams Vimba vimba (L., 1758), 12 crucian carps Carassius carassius (L., 1758), ten Prussian carps Carassius gibelio (Bloch, 1782), five stone loaches Barbatula barbatula (L., 1758), four weatherfish Misgurnus fossilis (L., 1758), five burbots Lota lota (L., 1758), 29 ruffes Gymnocephalus cernua (L., 1758), 132 European perches Perca fluviatilis L., 1758, and six bullheads Cottus gobio L., 1758.

Lithuanian water bodies are divided into lakes, rivers, and the Curonian Lagoon; the Kaunas Hydroelectric Power Plant reservoir was considered as part of the Nemunas River. Fish distribution in different types of Lithuanian water bodies in samples for helminthological studies is provided in Table 1.

Before necropsy, fish were killed by severing the spinal cord. Skin, fins, gills, mouth cavity, eyes, and viscera (intestine, mesentery, gall-bladder, gonads, liver, and kidney) were examined under a stereomicroscope following conventional methods described by Bykhovskaya-Pavlovskaya (1969).

Helminths were identified to the lowest possible taxa according to fish parasite keys (Bauer, 1985, 1987). Helminths were identified to the taxonomical level of species or at least genus. A small number of nematodes were not identified.

Table 1. Fish distribution in different types of Lithuanian water bodies in sample for helminthological studies

Helminthological terms were used according to the recommendations of Bush et al. (1997). The 95% confidence intervals for prevalence were calculated as described by Rojtman and Lobanov (1985).

A generalized linear mixed model (GLMM) with negative binomial distribution and a log link was used to model particular helminth abundance data in 23 fish species. The GLMM was performed using IBM SPSS Statistics, version 20. Fish species was used as fixed effects and the type of Lithuanian inner water (lake, river or the Curonian Lagoon) was used as random effects. The primary statistical analysis using non-parametric χ² criteria shows that it is possible to create a GLMM for just three helminths (Diplostomum sp. metacercariae, Posthodiplostomum cuticola (Nordmann, 1832) metacercariae, Tylodelphys clavata (Nordmann, 1832) metacercariae).

RESULTS AND DISCUSSION

In two examined C. lavaretus, two C. albula, four G. gobio, and five B. barbatula, no helminths were found. The examined fish of all other species were infected with helminths (Table 2). Sixty-three taxa of helminths were found. The largest number of helminth taxa was found in predatory fish E. lucius and P. fluviatilis, 20 and 18, respectively. A relatively high number of helminth taxa was also found in abundant cyprinids R. rutilus and S. erythrophthalmus, 15 and 17, respectively. From two to 11 helminth taxa were found in fish of other species.

Helminths of three phyla were found: 56 taxa of Plathyhelminthes (17 Trematoda, 27 Monogenea, 12 Cestoda), five Nematoda, and two Acanthocephales. Monogenea was the most diverse taxon of the class rank.

Host numbers varied among the found helminths. Metacercariae of flukes Diplostomum sp., P. cuticola and T. clavata were found in the biggest number of host species; 16, 11, and 12, respectively. All other helminths were found in hosts of 1–7 species.

All helminths identified to species taxonomic level, except Gyrodactylus truttae Glaser, 1974, had already been found in Lithuania and mentioned by Rauckis (1988). Fluke Rhipidocotyle campanula (Dujardin, 1845) was mentioned by Rauckis (1988) under the name of Rhipidocotyle illense (Ziegler, 1883). Tapeworm Neogryporhynchus cheilancristrotus (Wedl, 1855) was mentioned by Rauckis (1988) under the name of Gryporhynchus cheilancristrotus (Wedl, 1855). Valipora campylocristrota (Wedl, 1855) was registered by Rauckis (1988) under the name of Valipora unilateralis (Rudolphi, 1819) Spasssky 1965.

Fluke Bucephalus polymorphus Baer, 1827 is a widespread fish parasite in Eurasia. The adult stage of this fluke parasitises predatory fish. The first intermediate host of the parasite is bivalve molluscs of the genera Unio, Anodonta and also Dreissena polymorpha (Pallas, 1771), metacercariae are found in different fish, mostly in cyprinids (Bykhovskaya-Pavlovskaya, Kulakova, 1987; Rauckis, 1988). In this study, B. polymorphus were found in E. lucius, R. rutilus, S. cephalus and P. fluviatilis.

Fluke R. campanula is a widespread fish parasite in Eurasia (Bykhovskaya-Pavlovskaya, Kulakova, 1987; Rauckis, 1988). The adult stages of the species parasitise predatory fish. The first intermediate host is bivalves (Rauckis, 1988), metacercariae are found in different fish, mostly in cyprinids (Bykhovskaya-Pavlovskaya, Kulakova, 1987). In this study, fluke R. campanula was found in E. lucius.

Phyllodistomum folium (Olfers, 1816) was found in fish of three species, E. lucius, R. rutilus, and P. fluviatilis. Intermediate hosts of the genus Phyllodistomum flukes are molluscs of the Anodonta and Dreissena genus and the Spheridae family (Rauckis, 1988). For the genus Phyllodistomum, encystment of cercariae inside sporocysts in an intermediate host is typical (Shultz, Gvozdev, 1972). P. folium is a characteristic parasite of E. lucius, yet it is found in other fish as well and its distribution coincides with the distribution of E. lucius in the Northern hemisphere (Bykhovskaya-Pavlovskaya, Kulakova, 1987).

Table 2. Freshwater fish infection with helminths in 2005 in Lithuania. A±SD – mean abundance ± standard deviation; P (%) (CI95%) – prevalence (95% confidence interval)

Two species of the genus Asymphylodora were found. Fluke Asymphylodora imitans (Mühling, 1898) was found in the intestines of A. brama. Asymphylodora tincae (Modeer, 1790) was found in the intestines of R. rutilus and T. tinca. Intermediate hosts of flukes of the genus Asymphylodora are molluscs of Bithynia, Radix and other genera (Rauckis, 1988). The metacercarial stage is absent in the life cycle of A. tincae and the definitive host becomes directly infected after the ingestion of snails harbouring rediae with mature cercariae (Našincová & Scholz 1994). The distribution of A. tincae coincides with the distribution of T. tinca, yet this parasite is also found in others host species (Bykhovskaya-Pavlovskaya, Kulakova, 1987). A. imitans is found in basins of the Baltic, Black, Azov and Caspian seas (Bykhovskaya-Pavlovskaya, Kulakova, 1987).

Palaeorchis incognitus Szidat, 1943 was found in two species of fish, R. rutilus and S. cephalus. Intermediate hosts of flukes of the genus Palaeorchis are molluscs of Bithynia genus. These flukes parasitise mainly cyprinids. P. incognitus is distributed in the basins of the Baltic, Black, and Azov seas (Rauckis, 1988; Bykhovskaya-Pavlovskaya, Kulakova, 1987). Snails Bithynia are the intermediate hosts of the genus Palaeorchis (Rauckis 1988).

Bunodera luciopercae (Müller, 1776) was found in E. lucius and P. fluviatilis. It is a widespread parasite in Eurasia and North America. Nuclear ribosomal DNA studies revealed possible existence of a cryptic species complex within the nominal species B. luciopercae (Petkevičiūtė et al., 2010). The first intermediate hosts of this fluke are clams of the genera Sphaerium and Pisidium, the second intermediate hosts are Bosmina, Chydorus, Daphnia, Simocephalus, Eurycercus, Notodroma, and others (Bykhovskaya-Pavlovskaya, Kulakova, 1987; Ieshko, 1988; Rauckis, 1988). Planktivorous fish are infected by eating the second intermediate hosts. Predatory fish can be infected by eating planktivorous fish. Because of cannibalism, in P. fluviatilis population fluke B. luciopercae is transferred from one size-age group to another (Ieshko, 1988). In Lithuania, two subspecies of the fluke are found: B. luciopercae luciopercae (Müller, 1776) and B. luciopercae acerinae Rojtman et Sokolov, 1999 (Sokolov et al., 2006).

Plagioporus sp. was found in two of the six studied specimens of C. gobio. According to Rauckis (1988), two species of this genus are found in Lithuania: Plagioporus angusticolle (Hausmamm, 1899) and Plagioporus occidentalis Szidat, 1944. For some species of the Plagioporus genus, e.g. P. sinitsini Mueller, 1934, there are three potential pathways: a three-host life cycle involving molluscan, arthropod, and piscine hosts, a two-host life cycle involving only molluscan and piscine hosts, and a one-host life cycle involving only the snail host (Barger, Esch, 2000).

Fluke Sphaerostomum bramae (Müller, 1776) was found in R. rutilus. The definitive hosts of the flukes of the genus Sphaerostomum are cyprinids, but they are also found in fishes of other families (Zhokhov, 2002). The first intermediate host of S. bramae is mollusc Bithynia tentaculata and the second is leech Herpobdella (Bykhovskaya-Pavlovskaya, Kulakova, 1987). The range of S. bramae covers Europe (except for Scandinavia) and Western Siberia to the River Ob basin inclusive. Its northern boundary extends from the Ob Bay to lakes Onega and Ladoga. The southern boundary in Europe lies between the Greater and Lesser Caucasus. In Asia, it extends along the Emba and Irgiz rivers to Lake Zaisan and then ascends to the Verkhne-Chulymskie lakes in the Altai piedmonts (Zhokhov, 2002).

Fluke Azygia lucii (Müller, 1776) was found in predatory fish, E. lucius and P. fluviatilis. The main definitive host of this fluke is E. lucius, but it is also found in other fish. The range of the fluke coincides with the range of E. lucius (Bykhovskaya-Pavlovskaya, Kulakova, 1987). Intermediate hosts of fluke A. lucii are molluscs Anisus vortex, Radix ovata, Galba palustris, Planorbis planorbis, Gyraulus acronicus (Barskaya et al., 2008; Shultz, Gvozdev, 1972). Cercariae of this fluke are similar to larvae of Culicidae and are eaten by fry. In E. lucius, they develop into adult flukes; in fish that are not definitive hosts, they develop to metacercariae and reach maturity when these fish are eaten by E. lucius (Shultz, Gvozdev, 1972).

Metacercariae of three species of the genus Ichthyocotylurus were found. Ichthyocotylurus pileatus (Rudolphi, 1802) metacercariae were found in E. lucius, Ichthyocotylurus platycephalus (Creplin, 1825) metacercariae were found in S. erythrophthalmus, and Ichthyocotylurus variegatus (Creplin, 1825) metacercariae were found in fish of three species: S. erythrophthalmus, G. cernua and P. fluviatilis. Metacercariae of the genus Ichthyocotylurus not identified to the species level were found in P. fluviatilis. The first intermediate hosts of flukes of the genus Ichthyocotylurus are molluscs of Valvatidae (Rauckis, 1988). Metacercariae are found in fish. The definitive hosts of these flukes are piscivorous birds (Rauckis, 1988; Niewiadomska, 2001b).

Diplostomum sp. metacercariae were found in eye lens of 16 fish species: S. trutta morpha fario, E. lucius, R. rutilus, S. cephalus, L. leuciscus, S. erythrophthalmus, T. tinca, A. alburnus, B. bjoerkna, A. brama, V. vimba, C. carassius, C. gibelio, L. lota, G. cernua and P. fluviatilis. Systematics of the genus Diplostomum is still debated; species identification based only on morphology is complicated and molecular studies revealed a high level of species diversity (Niewiadomska, Laskowski, 2002; Galazzo et al., 2002; Locke et al., 2010a, b; Haarder et al., 2013). Because of this, we did not identify these metacercariae to the species level. Eyeflukes of the genus Diplostoma have three host life cycles. Definitive hosts are piscivorous birds. The first intermediate hosts are freshwater snails. In the case of Diplostomum spaethaceum, one of the species in which metacercariae are found in fish eye lens, the first intermediate hosts are limneids. Fish are the second intermediate hosts (Shultz, Gvozdev, 1972). Eyeflukes can be pathogenic to the fish host and cause poor growth, blindness, and, in certain situations, mass mortality in aquaculture of salmonids and cyprinids (Chappell et al., 1994).

The GLMM shows that six cyprinid species – R. rutilus, S. erythrophthalmus, L. leuciscus, S. cephalus, B. bjoerkna, and A. brama – have greater probability of infection with Diplostomum sp. metacercariae (or have a positive statistical significant impact (p < 0.05) on the parasite appearance) (Table 3). In these cyprinids, high infection prevalence and mean abundance values were identified; the highest values were registered in B. bjoerkna (Table 2). In order to determine the homogeneity of infection prevalence in the six selected fish species (R. rutilus, S. erythrophthalmus, L. leuciscus, S. cephalus, B. bjoerkna and A. brama), a non-parametric χ² test was performed. The obtained results (χ² = 37.106, p = 0.00) showed that there were statistically significant infection prevalence differences.

In addition, the GLMM shows that the random effect (the type of Lithuanian inner water) is also statistically significant at 0.05 level (Table 4). Different water body types differ in the structure of fish community, and infection parameters of some species are different in different water body types. Based on the data in Table 1, the homogeneity of the distribution of the six selected fish species (R. rutilus, S. erythrophthalmus, L. leuciscus, S. cephalus, B. bjoerkna and A. brama) in types of water bodies was evaluated using a non-parametric χ² test. The obtained results (χ² = 189.173, p = 0.000) showed that there was a statistically significant difference between fish distribution in Lithuanian inner water body types. This can be related with various habitat preferences of different fish species (Virbickas, 2000).

Table 3. GLMM parameters for Diplostomum sp. metacercariae

^a This coefficient is set to be zero because it is redundant.

Differences of the prevalence of infection with Diplostomum sp. metacercariae in different types of water bodies were assessed using χ² test. For some fish, species prevalence differences are significant, e.g., S. erythrophthalmus and B. bjoerkna (Table 5). Higher prevalence of infection in S. erythrophthalmus in rivers compared to lakes was ascertained. Prevalence in B. bjoerkna was higher in lakes.

P. cuticola metacercariae were found in skin and fins of 11 fish species: E. lucius, R. rutilus, S. cephalus, L. leuciscus, S. erythrophthalmus, L. delineatus, T. tinca, B. bjoerkna, A. brama, G. cernua, and P. fluviatilis. Flukes of the genus Posthodiplostomum have three-host life cycles (Shultz, Gvozdev, 1972). Definitive hosts are Ciconiiformes, metacercariae are found in cyprinids and other fish species, the genus is distributed universally (Niewiadomska 2001a; Bykhovskaya-Pavlovskaya, Kulakova, 1987).

Table 4. GLMM random effect for Diplostomum sp. metacercariae

^a This parameter is redundant.

Table 5. Infection with Diplostomum sp. metacercariae in fish in different types of water bodies in Lithuania in 2005. N – number of fish studied; P(%) – prevalence, p – asymptotic significance level (2-sided)

The GLMM did not reveal any statistically significant dependencies for P. cuticola metacercariae.

Using χ² test, significant differences of prevalence of infection with P. cuticola metacercariae in various water body types were established for E. lucius, G. cernua and P. fluviatilis (Table 6). In fish of these species P. cuticola metacercariae were found only in rivers.

T. clavata metacercariae were found in vitreous humour of 12 fish species: E. lucius, R. rutilus, S. cephalus, S. erythrophthalmus, L. delineatus, T. tinca, B. bjoerkna, A. brama, V. vimba, M. fossilis, G. cernua and P. fluviatilis. The definitive hosts of T. clavata are grebes, the first intermediate hosts are snails Radix ovata and others. Metacercariae are found in cyprinids and other fish (Shultz, Gvozdev, 1972; Bykhovskaya-Pavlovskaya, Kulakova, 1987).

The GLMM did not prove any statistically significant dependencies for T. clavata metacercariae.

Using χ² test, significant differences in the prevalence of infection with T. clavata metacercariae in various water body types were established for R. rutilus, S. erythrophthalmus and P. fluviatilis (Table 7). In fish of these species, higher prevalence meanings were established in lakes or the Curonian Lagoon. Higher prevalence of infection in R. rutilus with T. clavata metacercariae in lakes compared to rivers has been already mentioned by Rakauskas and Blaževičius (2009) and explained by the lower numbers of Grebes in rivers compared with those in lakes.

Twenty-seven monogeneans were found, each on 1–4 host species. This is in agreement with the known fact that monogeneans are highly host specific, so that a given parasite species infects a single host species or a restricted number of host species (Šimková and Morand, 2008). The life cycles of monogeneans are direct without involvement of intermediate hosts. They are viviparous (Gyrodactylus) or oviparous (all other genera) (Shultz, Gvozdev, 1972). All monogenean species, except G. truttae, have already been found in Lithuania and are mentioned by Rauckis (1988). Monogenea G. truttae was found on the skin of S. trutta morpha fario. The species is a widespread parasite in S. trutta morpha fario and rainbow trout Oncorhynchus mykiss (Walbaum, 1792) (Ergens, 1985).

Table 6. Infection with Posthodiplostomum cuticola metacercariae in fish in different types of water bodies in Lithuania in 2005. N – number of fish studied; P(%) – prevalence, p – asymptotic significance level (2-sided)

Table 7. Infection with Tylodelphys clavata metacercariae in freshwater fish in different types of water bodies in Lithuania in 2005. N – number of fish studied; P(%) – prevalence, p – asymptotic significance level (2-sided)

Two species of the genus Caryophyllaeus were found: tapeworm Caryophyllaeus laticeps (Pallas, 1781) was found in A. brama and tapeworm Caryophyllaeus fimbriceps Annenkova-Chlopina, 1919 was found in S. erythrophthalmus. Tapeworms of the Caryophyllaeus genus have two-host life cycles. The main definitive hosts of C. laticeps are A. brama, B. bjoerkna, white-eye bream Ballerus sapa (Pallas, 1814), V. vimba, and R. rutilus; it also parasitises S. cephalus, ide Leuciscus idus (L., 1758), S. erythrophthalmus, asp Leuciscus aspius (L., 1758), barbel Barbus barbus (L., 1758), and other cyprinids; intermediate hosts of the species are annelids Tubifex tubifex, T. barbatus, and Limnodrilus claperedeanus (Shultz, Gvozdev, 1972; Dubinina, 1987). The definitive hosts of tapeworm C. fimbriceps are wild and domesticated common carps Cyprinus carpio L., 1758, more rarely A. brama, but this parasite also parasitises T. tinca, S. cephalus, and R. rutilus. Intermediate hosts of tapeworm C. fimbriceps are annelids T. tubifex, T. barbatus, Psammoryctes albicola, and Limnodrilus udekemianus (Shultz, Gvozdev, 1972; Dubinina, 1987).

Adult tapeworms Triaenophorus nodulosus (Pallas, 1781) were found in the intestines of E. lucius and P. fluviatilis. Plerocercoides of the species were found in livers of E. lucius. This tapeworm has free living coracidium which is swallowed by crustaceans, the first intermediate hosts: Cyclops strenuus, Microcyclops varicans, Mesocyclops oithonoides, Macrocyclops fuscus, Acanthocyclops bicuspidatus, Eucyclops serrulatus, Eudiaptomus gracilus, and others. In the body cavity of crustaceans, procercoids are formed. When crustaceans are eaten by fish, the second intermediate host, plerocercoids, form in them. Definitive hosts are infected when they eat the second intermediate hosts. The definitive hosts of T. nodulosus are E. lucius and other predatory fish. The second intermediate hosts are the same predatory fish and also other fish species (Shultz, Gvozdev, 1972; Dubinina, 1987; Rauckis, 1988).

Plerocercoids of Ligula intestinalis (L., 1758) were found in R. rutilus and B. bjoerkna. The definitive hosts of L. intestinalis are gulls and other piscivorious birds. The tapeworm has a free-living stage, coracidium. Procercoids develop in crustaceans, the first intermediate hosts: Cyclops strenuus, Acanthocyclops bicuspidatus, A. viridis, Mesocyclops oithonoides, Eudiaptomus gracilus, and E. graciloides. Fish represent the second intermediate host. Plerocercoids are found in body cavities of R. rutilus, L. leuciscus, S. cephalus, L. idus, Eurasian minnow Phoxinus phoxinus (L., 1758), S. erythrophthalmus, G. gobio, B. barbus, chirruh snowtrout Schizothorax esocinus Heckel, 1838, A. alburnus, schneider Alburnoides bipunctatus (Bloch, 1782), B. bjoerkna, A. brama, B. sapa, and other species (Shultz, Gvozdev, 1970; Dubinina, 1987).

Five tapeworm species of the genus Proteocephalus were found. Proteocephalus cernue (Gmelin, 1790) were found in G. cernua, Proteocephalus esocis (Schneider, 1905) in E. lucius, Proteocephalus percae (Müller, 1780) in P. fluviatilis, Proteocephalus sagittus (Grimm, 1872) in M. fossilis, and Proteocephalus torulosus (Batsch, 1786) were found in S. erythrophthalmus, A. alburnus, and A. brama. These tapeworms are parasites of freshwater fish. There are one or two intermediate hosts and definitive hosts in the life cycle of the genus Proteocephalus. Procercoids develop in crustaceans, the first intermediate hosts: Cyclops, Eucyclops, Macrocyclops and others. The development in a piscine host depends on the fish species. If a procercoid occurs in the intestine of a definitive host, it can develop into a plerocercoid and then into an adult tapeworm. If a procercoid occurs in the intestine of a non-specific host, it develops into a plerocercoid and remains in this stage until its access to the specific definitive host. The life cycle may also include paratenic hosts (Shultz, Gvozdev, 1972; Dubinina, 1987).

Plerocerci of tapeworm Neogryporhynchus cheilancristrotus (Wedl, 1855) was found in fish of five species: S. erythrophthalmus, T. tinca, A. brama, C. carassius, and G. cernua. The definitive hosts of this cestode are herons (Dubinina, 1987). Their life cycle includes two intermediate hosts: cercoscoleci develop in cyclopid copepods Mesocyclops oithonoides (Jarecka, 1970) and plerocerci in the intestines of freshwater fish, particularly cyprinids (Dubinina, 1987). In zope Ballerus ballerus (L., 1758) from the Oder River, N. cheilancristrotus metacestodes are found throughout the year, but the dynamics of infection parameters indicates that there are two main periods of new infections: spring and late autumn-early winter (Pietrock, Scholz, 2000). Unlike the majority of cestodes inhabiting the gut lumen of fish and attaching to the gut epithelium, N. cheilancristrotus intrudes into deeper layers of the gut wall. Histological findings show that N. cheilancristrotus is a pathogenic species causing degeneration and inflammation in the intestinal wall (Molnár, 2005). According the review by Scholz et al. (2004), the geographic distribution of N. cheilancristrotus covers Belarus, Bulgaria, the Czech Republic, Germany, Hungary, Italy, Lithuania, Moldova, Poland, Romania, Russia, Slovakia, and Ukraine in Europe and Azerbaijan, Georgia, Iraq, Japan, Kazakhstan, Tajikistan, Turkmenia, and Uzbekistan in Asia. The morphological descriptions of N. cheilancristrotus (e.g., length of rostellar hooks) provided by most authors differ from those provided by Dubinina (1987) and some uncertainty in the taxonomy of gryporhynchid metacestodes exists (Pietrock, Scholz, 2000).

Cestodes Valipora campylancristrota (Wedl, 1855) and Valipora sp. were found in gall bladders of E. lucius. The definitive hosts of this cestode are herons (Dubinina, 1987). Their life cycle includes two intermediate hosts: the first intermediate hosts are crustaceans and the second intermediate hosts are fish. The most common host of the cestode are T. tinca, but parasites are found in many cyprinids and predatory fish. According to the review by Scholz et al. (2004), the geographic distribution of V. campylocristrota covers: Czech Republic, Germany, Hungary, Italy, Latvia, Lithuania, Moldavia, Poland, Romania, Russia, Slovakia, the Ukraine, former Yugoslavia (Monte Negro) in Europe; Iraq, Japan, Kazakhstan, Mongolia, Tajikistan, Uzbekistan in Asia; Canada and Mexico in North America; and Brazil in South America. In Lithuania, V. campylocristrota were registered under the name of Valipora unilateralis (Rauckis, 1988). In pond fisheries V. campylocristrota cause decrease in the fish mass and growth and if it occurs in high intensities, it may cause fish death (Dubinina, 1987; Ermolenko, 2000).

Nematodes Raphidascaris acus (Bloch, 1779) were found in E. lucius. R. acus is a widely distributed parasite in various predatory fish in the Holarctic; in Europe, the most frequent definitive hosts are E. lucius and S. trutta morpha fario but it also occurs in other fish species (Moravec, 1994). Various invertebrate (oligochaetes, crustaceans and aquatic insects) are preintermediate paratenic hosts of the second stage larvae (Moravec, 1994). There is an opinion that these invertebrates are to be considered as the first intermediate hosts (Vismanis et al., 1987). Various species of fish and cyclostomes, and more rarely, amphibians are intermediate hosts; the third stage larvae in the liver of an intermediate host are infective to a definitive host (Moravec, 1994). Some invertebrate (e.g., Gammarus fussarum) may also serve as true intermediate hosts (Moravec, 1996), but most invertebrates play a role as paratenic hosts only (Moravec, 2004). The maturation cycle of R. acus is seasonal, but it may be different in different ecological conditions (Moravec, 2004).

Desmidocercella sp. larvae were found in fish of three species: R. rutilus, S. erythrophthalmus and P. fluviatilis. Larvae parasitise in ocular vitreous of Cyprinidae and Percidae in the lakes of Lithuania and Belarus (Vismanis et al., 1987; Rauckis, 1988). Adults of the Desmidocercella genus parasitise in air sacks of herons, bitterns and cormorants (Vismanis et al., 1987).

Nematodes Camalanus lacustris (Zoega, 1776) were found in the intestines of fish of three species: E. lucius, S. erythrophthalmus and P. fluviatilis. The definitive hosts of this nematode are fish of the Percidae and Esocidae families and also many other fish (Vismanis et al., 1987; Rauckis 1988). Females of the nematode are viviparous, larvae with faeces of fish get into the water and are swallowed by intermediate hosts – copepods, in the body cavity of which C. lacustris develop; larvae moult two times and become infective for definitive hosts (Vismanis et al., 1987).

Nematodes Skrjabillanus scardinii Molnár, 1966 (syn. Agrachanus scardinii) were found in kidneys of S. erythrophthalmus. Adults of this nematode parasitise on the serosa of swimbladder, kidneys, and intestine and on the mesentery of S. erythrophthalmus (Vismanis et al., 1987; Anderson, 2000). The first-stage larvae are carried in blood to the skin, where small accumulations from five to 50 individuals could be found. Intermediate hosts – the ectoparasitic brachiurans, Argulus coregoni and A. foliaceus – ingest larvae while feeding. Larvae move to haemocoel of crustaceans and later resettle to the legs, where two moults take place. The third-stage larvae leave the mouth parts of brachiurans while the latter are feeding. Larvae invade the fish, migrate to the serous membranes and mature (Tikhomirova 1971, 1975, 1980 cited according Anderson 2000; Vismanis et al., 1987).

Acanthocephalan Neoechinorhynchus rutili (Müller, 1780) was found in S. erythrophthalmus. The species is a wide spread parasite of many species of fish, mostly cyprinids in Eurasia and North America (Bauer, Skryabina, 1987) also found in Africa e.g. Nigeria (Olurin, Somorin, 2006). Intermediate hosts are alderflies Sialis sp. (possibly paratenic host) and ostracods, Candona spp. and Cypria spp. (Bauer, Skryabina, 1987).

Acantacephalus lucii (Müller, 1776) was found in fish of five species: E. lucius, A. brama, L. lota, G. cernua and P. fluviatilis. The species parasitises a wide range of carnivorous and benthofagous fish. The intermediate host is Asellus aquaticus (Bauer, Skryabina, 1987).

CONCLUSIONS

Sixty-three species or higher taxa of helminths were identified in fish of 23 species. Fifty-six taxa of Plathyhelminthes, five Nematoda, and two Acanthocephales were found. Monogenea Gyrodactylus truttae were registered in Lithuania for the first time. For the identified helminths, fish are the only hosts (monogeneans), definitive hosts (part of trematodes, some cestodes, some nematodes and all acanthocephalans), intermediate and definitive hosts (some trematodes, some cestodes and some nematodes), and intermediate hosts (part of trematodes, some cestodes and some nematodes); where fish are intermediate hosts, piscivorous birds are the definitive hosts.

The highest number of helminth taxa was found in predatory fish: E. lucius and P. fluviatilis, 20 and 18, respectively. A relatively large number of helminth taxa were also found in cyprinids: R. rutilus and S. erythrophthalmus, 15 and 17, respectively. In fish of other species, from two to 11 helminth taxa were found.

Metacercariae of flukes Diplostomum sp., Posthodiplostomum cuticola and Tylodelphys clavata were found in the biggest number of host species; 16, 11, and 12, respectively. All other helminths were found in hosts of 1–7 species.

The GLMM shows that six cyprinid species – R. rutilus, S. erythrophthalmus, L. leuciscus, S. cephalus, B. bjoerkna and A. brama – have a greater probability of infection with Diplostomum sp. metacercariae. In addition, the GLMM shows that the random effect (the type of Lithuanian inner water) is also statistically significant. There is a statistically significant difference between the fish distribution in Lithuanian inner water body types. The differences in the prevalence of infection in different water body types are significant for some fish species, e.g., for S. erythrophthalmus and B. bjoerkna. Higher prevalence of infection in S. erythrophthalmus with Diplostomum sp. metacercariae was established in rivers compared to lakes. The prevalence in B. bjoerkna was higher in lakes.

Significant differences of prevalence of infection with P. cuticola metacercariae in different water body types were established for E. lucius, G. cernua and P. fluviatilis. In these hosts, P. cuticola metacercariae were found only in rivers.

Significant differences of prevalence of infection with T. clavata metacercariae in various water body types were established for R. rutilus, S. erythrophthalmus, and P. fluviatilis. In fish of these species, higher prevalence values were established in lakes or the Curonian Lagoon. This can be explained by the fact that definitive hosts of the parasite (grebes) live in standing waters.

Vytautas Mažeika, Saulius Petkevičius,
Egidijus Pumputis, Ričardas Krikštolaitis

ŽUVŲ HELMINTAI LIETUVOS VIDINIUOSE VANDENYSE