The Parasite Fauna of Ecological Forms of the European Smelt, Osmerus Eperlanus L

ПАРАЗИТОЛОГИЯ, 51, 5, 2017

УДК 576.89:597.552.3

THE PARASITE FAUNA OF ECOLOGICAL FORMS OF THE EUROPEAN SMELT, OSMERUS EPERLANUS L.

12 Institute of Biology, Karelian Research Centre RAS 11 Pushkinskaya St., 185910 Petrozavodsk, Republic of Karelia 3 Zoological Institute RAS 1 Universitetskaya Nab., 199034 St Petersburg 1 E-mail: [email protected] Submitted 19.05.2017

Three ecological forms of smelt have been analyzed: an anadromous (marine) form from the North Sea drainage basin and two freshwater forms — smelt proper from lakes Ladoga, Onego and Pyaozero, and dwarf (lake) smelt from lakes Beloye, Vozhe and Peipus (Pskov-Chudskoye). It is demonstrated that ecological forms of smelt feature their specific sets of parasites and the taxonomic structure of their diversity as represented by the composition of higher taxa. It is shown that ecological forms of smelt are characterized by a specific set of parasites and systematic structure of its diversity, which is assessed on the composition of the higher taxa. Most significant differences were detected between the anadromous form inhabiting waters of varying salinity and the freshwater form. These characteristics of the parasite fauna stem from smelt's high ecological plasticity, which enables the fish to inhabit both marine and fresh waters. Key words: smelt Osmerus eperlanus, ecological forms, parasite species composition, diversity structure.

ПАРАЗИТОФАУНА ЭКОЛОГИЧЕСКИХ ФОРМ ЕВРОПЕЙСКОЙ КОРЮШКИ OSMERUS EPERLANUS L.

12 Институт биологии Карельского научного центра РАН ул. Пушкинская, 11, Петрозаводск, Республика Карелия, 185910 3 Зоологический институт РАН Университетская наб., 1, Санкт-Петербург, 199034 1 [email protected] Поступила 19.05.2017

Проведен анализ паразитофауны трех экологических форм европейской корюш- ки: проходной (морской) из бассейна Северного моря и двух пресноводных форм — собственно корюшки из озер Ладожское, Онежское и Пяозеро и снетка из озер Белое,

369 Воже и Псковско-Чудское. Показано, что экологические формы корюшки характери- зуются специфичным набором паразитов и систематической структурой его разнооб- разия, которое оценивается по составу высших таксонов. Максимальные различия выявлены между проходной, обитающей в водоемах с разным градиентом солености, и пресноводной формами корюшек. Эти особенности паразитофауны являются ре- зультатом большой экологической пластичности корюшки, которая позволяет ей обитать в морских и пресноводных водоемах. Ключевые слова: корюшка Osmerus eperlanus, экологические формы, видовой со- став паразитов, структура разнообразия.

The European smelt has a wide North European range from France (the Loi- re) to the Baltic, White and Barents Seas, including the south-eastern part of the Scandinavian Peninsula and southwestern Ireland. The Russian range spans the catchments of all of these seas. The species occurs in the Kola Peninsula, is widespread in Karelia, and waterbodies from the Northern Dvina to the Pechora rivers and lakes of Bolshezemelskaya tundra (Fishes..., 2010). Smelt have disper- sed widely across Northern Europe after the last deglaciation and adapted to a variety of ecological conditions, having differentiated into anadromous, lacustrine-riverine, and lacustrine forms. Anadromous smelt are quite widespread in the drainage basins of the Baltic and the North Seas, as well as along North At- lantic coasts. They spend most of their lives in marine coastal waters, ascending rivers to spawn. The freshwater form comprises 2 groups: smelt proper (lacustrine-riverine) — large-sized form passing from a planktonic diet to predation during the life cycle, and dwarf (lake) smelt — small-sized precocious fish that remain planktivorous throughout their life (Petrov, 1940; Berg, 1948; Klyuka- nov, 1977; Atlas..., 2003; Fishes..., 2010). The origins of the ecological forms of the European smelt have been poorly investigated. The composition and structure of the species have been discussed and revised for decades (Atlas..., 2003; Sendek et al., 2005; Kovpak et al., 2010; Skurikhina et al., 2010; Kottelat and Freyhof 2007, etc.). A key reason for studying the parasite fauna of smelt is to assess the specific characteristics of its life and habitat conditions in various waterbodies. Trophic connections between the hosts of parasites with a complex life cycle create the background for using them as indicators of fish nutrition. The aim of this study was to analyze and compare the parasite fauna in different ecological forms of smelt to assess the species' structure and distinctions between the ecological forms.

MATERIALS AND METHODS

The paper is based on the authors' own materials and published data on smelt parasites. We analyzed the species composition of parasites in smelt from waters of Karelia (lakes Ladoga, Onego, Pyaozero), Vologda and Pskov Regi- ons (lakes Beloye, Vozhe, Peipus), and the North Sea drainage basin. Lakes La- doga, Onego, and Pyaozero are inhabited by the lacustrine-riverine form of smelt, lakes Beloye, Vozhe, Peipus by dwarf smelt, the North Sea basin by anadromous smelt (Berg, 1948; Smirnova-Stefanovskaya, 1967; Ivanova, 1982; At- las..., 2003).

370 The similarity of the species composition of smelt parasites was estimated by the principal component analysis method (Korosov, Gorbach, 2010). In addition, archival materials from the Laboratory of Animal and Plant Parasitology at the Institute of Biology, Karelian Research Centre RAS were used.

RESULTS

The parasite fauna of anadromous smelt from the North Sea drainage basin comprises 29 species (Kahl, 1936; Voigt, 1975; Jarling, 1982; Möller and Klatt, 1990; Obickezie et al., 1992; Anders and Wiese, 1993; Palm et al., 1999; Kuhn et al., 2013). Ten species belong to the freshwater ecological group. This group is heterogeneous, represented by parasites differing in host specificity. Three species mainly occur in smelts — protozoa Pleistophora ladogensis Voronin, 1978 and Eimeria osmeri Molnar, Fernando, 1974, as well as the cestode Prote- ocephalus tetrastomus (Rudolphi, 1810); 2 species predominantly parasitize sal- monoids — the cestode Diphyllobothrium ditremum (Creplin, 1825), and the nematode Cystidicola farionis Fischer, 1798; and 6 species are wide generalists — metacercariae of the genus Diplostomum Nordman, 1832, nematode Cammalanus truncatus (Rudolphi, 1814), crustacean Ergasilus sieboldi Nord- mann, 1832, leech Piscicola geometra Linnaeus, 1761, glochidium Anodonta anatina L., 1758. Nineteen species belong to the marine ecological group. They are widespread parasites with a complex life cycle. The number of species is the highest for nematodes. The list of parasites for the North Sea drainage basin includes all species of marine nematodes and acanthocephalans known from smelt in its entire species range (Anikieva and Ieshko, 2017). The number of species in the parasite fauna of lacustrine-riverine smelt inhabiting lakes of Karelia is similar to that of anadromous smelt from the North Sea basin. The greatest number of species (29) was found in smelt from Lake Lado- ga (Rumyantsev et al., 1979, 1984, 2001; Rumyantsev, Permyakov, 1994; Ru- myantsev, Ieshko, 1997; Anikieva, 1998; Rumyantsev, 2007). Differences between parasite faunas of anadromous and lacustrine-riverine smelts consist in the ratio of ecological groups of parasites and the number of species within these groups. Lacustrine-riverine smelt host only 2 marine species — relict acanthocephalans of the genus Corynosoma Lühe, 1904, whose definitive host include the ringed seal Pusa hispida (Schreber, 1775) — a marine relict and endemic species of Lake Ladoga. All other parasites in lacustrine-riverine smelt belong to the freshwater ecological group. Smelt in Onego and Ladoga Lakes have similar species compositions of parasites typical of the freshwater ecological group. Smelt from these lakes had the highest number of freshwater parasite species. This group included all specific parasites of smelts — protozoans Eimeria osmeri Molnar, Fernando, 1974, Pleistophora ladogensis, and Glugea hertwigi Weissenberg, 1921, the monoge- nean Gyrodactylus osmeri Rumyantsev, Schulman, Iyeshko, 1998, and the cestode Proteocephalus tetrastomus. A substantial component of the parasite fauna are species whose development involves zooplankton, spezialist smelt parasite Proteocephalus tetrastomus, salmonoid parasites P. longicollis, Diphyllobo- thrium ditremum, Eubothrium salvelini Schrank, 1790. A few plerocercoids of the broad tapeworm Diphyllobothrium latum (Linnaeus, 1758) have been found.

371 There is a wide representation of parasites developing through a stage involving zoobenthos. These are trematodes of the genus Diplostomum, Ichtyocotylurus erraticus (Rudolphi, 1809) Odening, 1969, and the nematode Raphidascaris acus (Bloch, 1779) — broad generalists. The life cycles of Echinorhynchus salmonis Mueller, 1780, Cystidicola farionis, Corynosoma are linked with relict crustaceans. The smelt parasite fauna from Lake Pyaozero differs from that of Ladoga and Onego Lakes in a smaller total number of species, fewer species in certain taxonomic groups, and absence of crustaceans. It does however com- prise a majority of parasite species typical in lacustrine-riverine smelt. The parasite fauna of the dwarf smelt comprises fewer species being compa- red to lacustrine-riverine and anadromous forms (Kogteva, 1957; Izyumova, 1974; Radchenko, 1999, 2002). Protozoa within it are few. The dwarf smelt from Lake Beloye hosted only two species of protozoans, a specialist parasite Glugea hertwigi at a low prevalence (1.7 %) and generalist infusorians of the genus Capriniana Mazzarelli, 1906 (not identified to species). Dermocystidium sp. was found in the dwarf smelt from Lake Beloye — 6.6 % (Radchenko, 1999). In this lake, Radchenko (1999) also retrieved Dermocystidium from perch and pike, and identified it as D. percae Reichenbach-Klinke, 1950. The rest of parasites have a complex life cycle and either occur in a wide range of fish hosts or specialize in another taxonomic group of hosts. Of the 16 parasite species found in the dwarf smelt from Lake Beloye, five species were parasites of salmonoid fish — Eubothrium crassum (Bloch, 1779), Diphyllobothrium ditremum, Proteocephalus longicollis, Phyllodistomum umblae (Fabricius, 1780) Bake, 1982, and Ichthyocotylurus erraticus, 3 species had cyprinids and 2 species had percids as their preferred hosts, and the rest were broad generalists. The parasite fauna of the dwarf smelt from Lake Vozhe includes species with a complex life cycle — parasites of salmonoid, percid and cyprinid fish. Among the total 8 parasite species, there were 2 species of cestodes (Proteoce- phalus longicollis, Triaenophorus crassus Forel, 1868), 3 trematodes (Diplosto- mum baeri, Ichthyocotylurus variegatus (Creplin, 1825), and I. erraticus), and 3 nematodes (Cystidicola farionis, Camallanus lacustris (Zoega, 1776), and Raphidascaris acus). There were no specialist parasites. Two cestode species (T. crassus, and Eubothrium crassum) found in dwarf smelts from lakes Vozhe, and Beloye (Radchenko, 1999, 2002) were atypical for freshwater eco- forms of the smelt. Two T. crassus plerocercoids were isolated from muscles of two 0 + dwarf smelt from Lake Vozhe in autumn (Radchenko, 2002, p. 25). T. crassus was found in Lake Ladoga in smelt of the lacustrine-riverine form — 7 % (Baryscheva and Bauer, 1957; Rumyantsev, 2007). Rybak (1982) postula- ted that finding of T. crassus in smelt from Lake Segozero was the result of the parasite's invasion in the smelt stocked into the lake as eggs from Lake Ladoga. There are several reasons to doubt findings of E. crassum in dwarf smelt from Lake Beloye. For this lake, E. crassum has been reported also from Volga pike-perch, Sander volgensis (Gmelin, 1788) — a species of the family Perci- dae. Identification of larval stages of the genus Eubothrium cestodes to species is complicated by the lack of reliable discriminating traits. The life cycle of E. crassum can occur as two alternative patterns. The first one involves two intermediate hosts (the first intermediate host is represented by copepods, the second one, by the vendace). The second pattern includes a single intermediate host. In the latter case, the parasite's plerocercoid and adult stages are combined

372 Ordination onto the axes on the principal components of differences in the parasite fauna of smelt from. 1 — North Sea drainage basin, 2 — Lake Ladoga, 3 — Lake Onego, 4 — Lake Pyaozero, 5 — Lake Vozhe, 6 — Lake Peipus, 7 — Lake Beloye. within a single host species (vendace) (Kuperman, 1979; Anikieva et al., 2016). Since the only suitable definitive host for E. crassum in Lake Beloye is vendace, and the parasite has not been detected in this fish species, plerocercoids of the genus Eubothrium found in dwarf smelt and Volga pike-perch from this lake should rather be reported as parasites not identified to species level. The parasite fauna of dwarf smelt in Lake Peipus comprises 7 species: salmonoid parasites Ichthyocotylurus erraticus, Proteocephalus longicollis, and Diphyllobothrium ditremum, predominantly percid parasites Triaenophorus no- dulosus (Pallas, 1781), Camallanus lacustris, a cyprinid parasite Bucephalus polymorphus Baer, 1827, and a broad generalist Ergasilus sieboldi. Noteworthy is the absence in Lake Peipus of a parasite causing epizootic events in dwarf smelt, the myxosporidian Glugea hertwigi, which has been reported from lakes Seliger, Ilmen and Pestovo (Kogteva, 1957). Principal component analysis was employed to estimate the differentiation of the ecological forms of smelt by species composition of its parasites (see figure). The analysis was performed on 59 parasite species retrieved from smelt from the waters in question. Factor loadings for component 1 are represented by a set often parasite species associated with salmonoid fish — Pseudocapillaria salvelini, Eubothrium salvelini, Echinorhynchus borealis, E. salmonis, broad generalists — Capriniana piscium, Trichodina pediculus, Tripartiella copiosa, Tylodelphys clavata, and 2 specialist parasites of smelt Eimeria osmeri and Gyrodactylus osmeri (Anikieva and Ieshko, in press). This set of species is res- ponsible for the distinctness of waterbodies harboring the lacustrine-riverine form of smelt: lakes Ladoga, Onego and Pyaozero. Factor loadings for component 2 are generated by 5 parasite species, including Corynosoma strumosum, C. semerme, Proteocephalus tetrastomus, which survived in fresh water as a re- licts, Pleistophora ladogensis — a parasite found also in the burbot in addition to the smelt, and a generalist Diplostomum spathaceum. In the coordinates of two principal components which explain 71 % of variation of the parasite species diversity the investigated smelt populations form three discrete clusters (see figure). One of the clusters is represented by lacustrine-riverine forms of smelt from lakes Onego, Ladoga and Pyaozero. The lowest difference in the parasite fauna was observed between smelt from Lake Onego

373 and Lake Pyaozero, whose genesis was higher that of periglacial lakes. The pre- sence of endemic acanthocephalans of the genus Corynosoma in the parasite fauna of fish from Ladoga created some distinction from lakes Onego and Pyao- zero. The second cluster comprises dwarf smelt from lakes Vozhe, Peipus and Be- loye. This form of smelt hosts few protozoa and specialist parasites. In this cluster, helminth species with a complex life cycle dominate. Differences between smelt from lakes Vozhe and Peipus in the composition of parasites were minor. The only somewhat isolated member in this cluster was the dwarf smelt from Lake Beloye. The third cluster is represented by the anadromous form of smelt from coastal waters of the North Sea, and a major share in the parasite fauna belongs to marine species. Anadromous smelt is the furthest from both freshwater forms in terms of the species composition of parasites and their taxonomic diversity.

DISCUSSION

Numerous observations of the life style and population structure of the Euro- pean smelt have revealed the species' outstandingly wide-ranging ecological variability and plasticity. Within its distribution range, smelt are represented by populations differing in abundance patterns, maturation time, spawning characteristics, dietary range and other parameters. In almost «every body of water smelt has a peculiar form shaped by the specific conditions in this waterbody» (Ivanova, 1982; p. 12). The properties of freshwater forms of smelt are not here- ditary. When environmental conditions change, «dwarf smelt» populations can acquire the traits typical of «smelt proper» populations, and vice versa (Kriksu- nov, Shatunovsky, 1979). The ability to modify biological characters to adapt to habitat conditions was demonstrated the most vividly when dwarf smelt was int- roduced in Volga reservoirs and when eggs of large-sized smelt from the Olon- ka River were stocked in Segozerskoye reservoir with the following dispersal to Lake Vygozero (Volodin, Ivanova, 1973; Ivanova, 1982). Studies of the genetic diversity and population structure of European smelt by allozyme electrophoresis and mitochondrial DNA restriction fragment length polymorphism (RFLP), analysis of variation in nucleotide sequences in mitochondrial and nuclear DNA revealed a high genetic diversity and a poor population genetic structuring (Gordeeva et al., 2005, 2009; Kovpak, 2010). In spite of the poor genetic differentiation, statistically significant differences between populations were observed in allele frequencies at some polymorphic loci. For ins- tance, populations of anadromous smelt from the Gulf of Finland, lacustrine smelt from Lake Ladoga and dwarf smelt from Lake Beloye reliably differed on two out of four polymorphic genes (GPI-2 and PGM). The percentage of polymorphic loci was the lowest for dwarf smelt from Lake Beloye. This same population was the most distant from anadromous smelt from the Gulf of Finland and lacustrine smelt from Lake Ladoga in terms of both genetic distances and F index values, which indicate the degree of reproductive isolation of populations (Sendek et al., 2005). Analysis of the species composition of parasites confirmed the differentiation of European smelt into anadromous and freshwater ecotypes (Atlas..., 2003;

374 Sendek et al., 2005; Fishes..., 2010). It was demonstrated that various ecological forms possess their own specific sets of parasites. The greatest differences were found between anadromous smelt, inhabiting waters with a gradient of salinities, and freshwater forms of smelt. Anadromous smelt live in high salinity waters and enter brackish river channels for spawning. The assortment of its parasites reflects the smelt's ability to live under a wide range of abiotic conditions and its broad dietary spectrum, the bulk of it made up of mysids, side-swim- mers, decapods, with a smaller contribution of insect larvae, mollusks, polycha- etes, and other benthic organisms. The freshwater form of smelt had adapted to living in fresh water. The diverse composition of its parasite fauna also points to quite a wide dietary spectrum. The predominant component of the diet, however, is represented by planktonic crustaceans: cladocerans, copepods, and mysids. Common items in smelt's diet are Eudiaptomus, Limnosida, Limnocala- nus, Bosmina, Cyclops, and Mysis. A comparison of the species composition of zooplankton with the diet composition of smelt showed that the latter accurately modeled the abundance of zooplankton in a waterbody (Maltseva, 1983; Niko- laev, 1983). Differences in the parasite fauna between freshwater forms of smelt (lacustrine-riverine vs. dwarf smelt) also originate from the specific features of their life in individual lakes. Lacustrine-riverine smelt live in cold and deep oligotrophic waters, such as lakes Ladoga, Onego, Pyaozero, inhabited by diverse composition of aquatic organisms. The parasite fauna of lacustrine-riverine smelt resembles that of anadromous smelt in the number of species, but differs in the set of species and the taxonomic diversity of parasites. The diversity of the parasite fauna reflects the wide dietary spectrum of lacustrine-riverine smelt. Smelt in lakes Ladoga, Onego and Pyaozero belong to the same ecological group — a large-sized form, but differ in the size-age composition, rates of length and weight increment, dietary characteristics and other parameters. In cold- and deep-water oligotrophic lakes young smelt grow and develop slowly. Maturation takes place relatively late. The age structure of the smelt population is complex, with a maximum life span of 6—10 years. Ladoga smelt (at spawning) is 100 to 252 mm long. The bulk of the catches is made up of 1+ to 3+ fish 110—180 mm long. Onego smelt are smaller. The length of mature individuals ranges from 90 to 160 mm (Ivanova, 1982). The average length of Pyaozero smelt is 120 mm, average weight is 12 g. According to Kudersky (Kudersky, 2005), smelt had arrived to the large North European lakes Ladoga and Onego from different sources: to Ladoga from the Baltic Ice Lake, to Onego from the Upper Volga system of ice lakes. The parasite fauna of smelt in these lakes has a similar composition of specialist and common species but differs in rare species. Dwarf smelt is a precocious small-sized form of smelt. Lake Beloye is a mesotrophic, mesohumic waterbody. The fish fauna is that of a classic zan- der-smelt lake. Lake Vozhe is an extensive shallow-water mesotrophic lake of the 'bream type'. Lake Peipus is a highly eutrophied shallow-water lake. Dwarf smelt in these lakes are typical representatives of a small-sized form of smelt. They mature at 1—2 years of age, 3—7 cm length and 0.4—3.1 g weight, rarely live as long as 4 years of age, and have an average length of 6—10 cm and weight of up to 6 g. The dominant component of dwarf smelt's dietary spectrum are cladocerans, with more diversity in autumn, when the food bolus of the fish contains up to 78 % (by weight) of copepods (Radchenko, 1999, 2002). The pa-

375 rasite fauna of dwarf smelt in these lakes is rather poor and made up of broad generalists. Thus, the analysis of the parasite fauna of European smelt revealed differences in the species composition and structure of the taxonomic diversity of parasites among ecological forms. The distinctions found in the parasite fauna ref- lect smelt's adaptations to a wide variety of environmental conditions. High ecological plasticity enables smelt to inhabit waters on a gradient of salinities and trophic levels. Conditions in the waterbodies and the life patterns of smelt in them are the factors providing differences in the parasite fauna between the various ecological forms of smelt.

ACKNOWLEDGEMENTS

The authors are grateful to Yu. S. Reshetnikov (Severtsov Institute of Ecolo- gy and Evolution RAS) for support and valuable advice. The research was funded from the federal budget through allocations to imp- lementation of state order (N 0221-2014-0030).

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