ISSN 1995-0829, Inland Water Biology, 2009, Vol. 2, No. 4, pp. 377–382. © Pleiades Publishing, Ltd., 2009. Original Russian Text © S.K. Zaostrovtseva, 2009, published in Biologiya Vnutrennikh Vod, No. 4, 2009, pp. 87–92.
PARASITOLOGY OF HYDROBIONTS
Analysis of Fish Parasitofauna in Vistula Lagoon (the Baltic Sea) S. K. Zaostrovtseva Kaliningrad State Technical University, Sovetskii pr. 1, Kaliningrad, 236000 Russia e-mail:
[email protected] Received May 13, 2008
Abstract—The characteristics of parasitofauna (81 species) of 15 fish species from Vistula Lagoon (the Baltic Sea) are given. Parasites with a direct developmental cycle dominate. Parasites with a complicated developmental cycle are represented mainly by species developed through zoobenthos. Some of the parasites testify to the deterioration of the ecological state of the lagoon. A zoogeographic analysis of fish parasitofauna has shown the presence of five faunistic complexes. In Vistula Lagoon freshwater species dominate, but marine species are also recorded. Species that appeared in the lagoon as a result of human commercial activity are also registered. Key words: parasitofauna, parasite, host, invasion extensiveness, invasion intensity, index of abundance. DOI: 10.1134/S1995082909040130
munity and the inhibition of species that are more demanding of clear natural waters. Our task was to study ecologically analyze the fish parasitofauna in Vistula Lagoon.
INTRODUCTION In Vistula Lagoon (the Baltic Sea), which is a shallow estuary water body, marine salty and fresh waters mix; as a result, a peculiar hydrofauna is formed. Zooplankton of the Russian part of the Vistula Lagoon is represented by euryhaline species and subspecies of marine and freshwater origin that belong to three taxonomic groups: Rotatoria (27), Cladocera (10), and Copepoda (14 species). In some periods of the vegetative season, representatives of other taxa, mainly nauplii Cyrripedia and metatrochophores Polychaeta, were recorded [21]. Over a 30-year period, considerable changes occurred in this community structure. In 1963, 58 species were counted in the bay. In 1995 there were 51; 25 species disappeared from this community and 18 species were recorded in the water body for the first time [12, 13, 21, 23]. The zoobenthos of Vistula Lagoon is not distinguished by a high taxonomic diversity; it is made up of euryhaline species of marine and freshwater origin and a small number of brackish-water species. Studies of the first two-thirds of the 20th century [1, 2, 22] indicate that the composition of bottom fauna at that time was noticeably different than the current composition [6–8]. The species composition of zoonbenthos considerably decreased from that of the 1960s (Table 1). A decrease was recorded in the numbers of oligochaetes, gastropods, crustaceans, and larval insects that serve as intermediate hosts for fish parasites. The decrease in species diversity can be explained by the pollution of the bay, mostly of organic matter and biogenic elements [15, 16]. This leads to an increase in the β-mesosaprobic component of the com-
Table 1. Number of zoobenthos species in Vistula Lagoon [1, 7] Years Group 1952–1958 1965–1973 1996–2001 Sponges
1
1
1
Coelenterata
4
5
3
Flatworms
4
4
1
Nemertines
1
1
1
31
0
0
Polychaeta
1
1
6
Oligochaeta
20
18
11
Hirudinea
10
11
2
Crustaceans
26
23
18
1
1
1
Insects (without chironomids)
22
18
2
Chironomids
24
24
3
Gastropoda
22
22
5
Bivalves
16
15
5
Bryozoa
1
0
1
184
144
60
Round worms
Arachnida
Total 377
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Table 2. Number of studied fish and parasite species in fish in Vistula Lagoon Number, individuals Fish Pike Esox lucius L. Bream Abramus brama (L.) Gudgeon Gobio gobio (L.) Rudd Scardinius erythrophtalmus (L.) White bream Blicca bjoerkna (L.) Bleam Alburnus alburnus (L.) Asp Aspius aspius (L.) Crucian carp Carassius carassius (L.) Roach Rutilus rutilus (L.) Eel Anguilla anguilla (L.) Zander Stizostedion lucioperca (L.) Perch Perca fluviatilis L. Ruff Acerina cernua (L.) Burbot Lota lota (L.) Flounder Pleuronectes platessa (L.)
of parasite species
of fish 4 150 -----------1989 10 18
12 34 9 15
18 15 15 12 55 --------970 64 24 37 10 15 13
21 8 4 4 22 13 15 21 11 6 8
Note: Above the line are fish studied by the method of complete parasitological analysis; below the line are those studied by the method of incomplete parasitological analysis.
Table 3. Distribution of fish parasites in Vistula Lagoon according to systematic group Systematic group of parasite
Number of species
Microsporidia
1
Myxosporidia
18
Infusorians
4
Monogeneans
16
Cestodes
9
Trematodes
12
Nematodes
9
Proboscis worms
6
Leeches
1
Mollusks (glochidia)
1
Crustaceans
4
MATERIAL AND METHODS From 1989 to 2005, the parasitofauna of 15 fish species (460 specimens) from different areas of the lagoon was studied (Table 2). Collection, fixation, and processing of the material was performed using common methods. The invasion extensiveness and intensity and the index of abundance were calculated for each fish species.
An incomplete parasitological autopsy of 2959 fish individuals was made to study their infection with ligule. RESULTS We found 81 species of ichthyoparasites (Table 3); among them, parasites with a direct developmental cycle dominate. Myxosporidians were attributed to this group, because there have been no significant proofs so far of the obligatory presence of oligochaetes in their life cycles [20]. Parasites with a direct developmental cycle are present to a greater degree in cyprinids. This is related to the fact that their juveniles stay together (in “small schools”) and infusorians, the oncomiracidia of monogeneans, and larval stages of parasitic copepods easily pass from one host to another. A fish is infected with parasites with a complicated development cycle when its diet includes intermediate or reservoir parasite hosts. The environment affects all stages of the life cycle of fish parasites directly or via the host. All parasitic organisms found in the studied fish have at least one free-living stage. At this stage, the parasite is most vulnerable and dependent on all ecological environmental factors. The more adapted the parasite is to the host, the more sensitive its free-living stages are to environmental exposures. For survival, parasites have developed several strategies throughout their evolution: R, S, and K strategies [19]. In the fish parasitofauna of the lagoon, 18 species of microsporidia were found: 8 with rapidly descending spores; 6 with slowly descending spores; and 4 with spores that occupy an intermediate position according to the rate of descent. However, in fish of different systematic groups, the distribution of species of Microsporidia with different spore buoyancies is different. For instance, cyprinids are infected mainly with microsporidians with rapidly descending spores. These fish have only one species of Microsporidia with slowly descending spores and one species of Microsporidia with spores that have an intermediate position according to the rate of descent. In representatives of other fish families in the lagoon, nine species of Microsporidia have been found: five with slowly descending spores and two with spores that occupy an intermediate position with respect to the rate of descent and rapidly descending. Since pike is a predator that ambushes its prey and is immobile for a long time, it is infected with microsporidians with slowly descending spores. The active vertical movement of the perch in the water column promotes its infection with microsporidians with slowly descending spores and spores that occupy an intermediate position with respect to the rate of descent. In eels, which lead a near-bottom mode of life, Myxobolus macrocapsularis Reuss with rapidly descending spores and Myxidium giardi Cepede with slowly descending spores were found. Finding of a speINLAND WATER BIOLOGY
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ANALYSIS OF FISH PARASITOFAUNA IN VISTULA LAGOON
cies with rapidly descending spores is possible because eels spends a considerable amount of time hiding on the bottom of the water body. Myxolobus dispar Theloban, a species with rapidly descending spores, was found on the zander, an active predator that moves rapidly in the water column. The ability of the zander to collect food from the bottom, feeding on bottom organisms, makes it possible for M. dispar to be a parasite on it. All microsporidians that are present in fish of Vistula Liman correspond to the specific features of the feeding of the host and its behavior in the water body. Our study of the fauna of Microsporidia on fish in Vistula Lagoon indicates that the most widespread species in it include M. bramae Reuss, M. dispar, M. muelleri Bütschli, and M. pseudodispar Gorbunoba. They infect 33 to 82% of fish, but their invasion intensity is singular. A great number of M. muelleri was recorded only on gills of roach. Other species of Microsporidia of this genus were found in small amounts. It is likely that a decrease in the invasion extensiveness and intensity of fish with microsporidians is a response to toxic substances of different natures that get into the lagoon. M. muelleri, M. muelleriformis Donec et Tozyjakova, sp.n., and M. dispar had deformed spores. In the bream and roach in the northeastern part of the lagoon (in the area of the water drift from the Pregolya River), along with normal spores, spores of M. muelleri with curved and atypically located polar capsules were found. The number of deformed spores is 12–15%. This, along with species composition, may be an indicator of the ecological situation in the lagoon. Spores of microsporidians have compact valves and protect ameboid embryos well. However, upon descending to the bottom, they may lose their invasion capacity. Single infection of fish with many species of Microsporidia, especially with rapidly descending spores, may be related to the accumulation of silty deposits on the bottom of Vistula Lagoon [15–17]. A very rarefied population of oligochaetes in the lower reaches of the Pregolya River and the adjacent part of the lagoon (up to its complete disappearance) may also lead to the absence of species of Myxosporidia that use them in their life cycle. In Vistula Lagoon, four species of parasitic infusorians have been found. They include Chilodonella piscicola (Zacharias) Jankowski, Ichthyophthirius multifiliis Fouquet, Trichdina jadranica Raabe, and Paratrichodina incisa (Lom) found on the gills and skin of the crucian carp, white bream, perch, roach, bream, zander, and flounder. In different fish species, the invasion extensiveness is ≤30% and the invasion intensity is always singular. Infusorians were localized to a greater degree on gills and to a smaller degree on the skin of fish. In the fauna of monogeneans of fish from Vistula Lagoon, eight species belong to the genus Dactylogyrus, three to Paradiplozoon, two to Diplozoon, and one to the genera Gyrodactylus, Tetraonchus, and Ancyrocephalus, each. Every species of monogeneans found are of freshINLAND WATER BIOLOGY
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water origin. Cyprinids are the most infected with monogeneans; the invasion intensity in them is low. The invasion extensiveness in representatives of the genera Diplozoon and Paradiplozoon reaches 98% in bream and 94.4% in white bream and rudd. Species of monogeneans of the genera Diplozoon and Paradiplozoon exhibit a specificity to cyprinids, but occur on other fish species as well [14]. The author of this paper found Diplozoon paradoxum Nordmann in perch and eel. According to the opinion of some authors [3, 4, 11], this species can be used as a pollution indicator in water bodies. On zander and pike, species Ancyrocephalus paradoxus Creplin and Tetraonchus monenteron (Wagener) were found specific for them. Of the genus Gyrodactylus, a single species-specific parasite of gudgeon G. gobii Schulman was found. Four species of the class Cestoda belong to the family Caryophyllaeidae, two belong to the family Proteocephalidae; and one belongs to the families Triaenophoridae, Amphicotylidae, and Ligulidae, each. Four species of Caryophyllaeidae that parasitize in the intestine of the final host— cyprinids, were found in the southeastern part of the lagoon. The first intermediate host of caryophyllids are oligochaetes. The remaining cestodes use plankton organisms as the first intermediate hosts (Copepoda). In the lagoon, a small number of trematodes were found for which fish is a final host. All of them are of freshwater origin. Four species of trematodes (Azygia lucii (Müller), Bunodera luciopercae (Müller), Allocreadium isoporum (Looss), and Nicolla skrjabini (Iwanitzky) parasitize on fish at the stage of marita and were found in the southeastern part of the lagoon and in the area of islands located along the navigable canal. At the stage of metacercarium, seven species of the family Diplostomidae (the genera Diplostomum and Tylodelphys) and one species Ichthyocotylurus variegatus (Creplin) (fam. Strigeidae) are found in fish. Metacercaria were recorded in fish throughout the water area of the lagoon. Cyprinids and predatory fish are infected with these parasites to nearly equal degree. Cercaria infect fish that prefer the zone of aquatic vegetation to a greater extent. One specific feature of the fauna of trematodes in fish of the lagoon is the considerable number of species of the genus Diplostomum in them. Since trematodes are specific to the first intermediate host (mollusk) [18], their fauna is closely related to the species composition of malacofauna. Of the nine species of nematodes found, four are marine (Anguillicoda crassum Kuwahara, Cucullanellus minutus (Rudolphi), Cucullanus cirratus Müller, and Hyterothylacium aduncum Ward et Magath); the remaining are freshwater. Most species develop using the copepodite group of zooplankton. Larval forms parasitize in bream and small perch. Nematodes of marine origin are brought to the lagoon by final hosts (eel and flounder). Anguillicola crassum was recorded in eel from Vistula Lagoon in 1989.
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Table 4. Distribution of fish parasitofauna of Vistula Lagoon according to faunistic complexes Faunistic complex Boreal-plain Ecological group: palearctic amphiboreal Ponto-Caspian Arctic freshwater Arctic marine Atlantic boreal Pacific Not cleared up
Number of species total, individuals
% of total
62
76.54
43 – 19 4 1 7 1 6
69.35 – 30.65 4.94 1.23 8.64 1.23 7.42
The fauna of proboscis worms is represented by six species that have a freshwater origin (Metechinorhynchus salmonis (Müller), Acanthocephalus anguillae (Müller), A. lucii (Müller), Pomphorhynchus laevis (Müller), Acanthocephalus clavula (Dujardin, 1845), and Pseudoechinorhynchus borealis (Linstow, 1901). The maximum number of species of proboscis worms, sufficiently low indices of invasion extensiveness (3.7– 21.8%) and invasion intensity (1–3), and index of abundance (0.04–0.90) suggest that the number of bottom crustaceans is low in the lagoon benthofauna. The fauna of crustaceans that parasitize on fish in the lagoon includes four species, of which Ergasilus gibbus Nordmann and Lernaeocera branchialis (Linne) are marine and Ergasilus sieboldi Nordmann and Achtheres percarum Nordmann are freshwater species. A. percarum was found on a host specific for it (zander). Infection with it is rather high (invasion extensiveness 54.2%, invasion intensity 2–35, and index of abundance 4.75). This species has resistance to water pollutants [3]. Ergasilus sieboldi, found on gills of the eel and pike, is an indicator of the increased trophicity of the water body. DISCUSSION These studies of fish parasitofauna from Vistula Lagoon have demonstrated that there is a mixing of freshwater (81.5%) and marine (11.1%) parasite species. The richest parasitofauna is in the bream (34), roach (22), perch (21), white bream (21), rudd (15), zander (15), eel (13), and pike (12 species) (Table 2). Other fish species are infected considerably less. Multi-term studies of the infectiousness of bream with plerocercoids of cestode Ligula intestinalis (Linnaeus) showed that the invasion extensiveness and intensity of the host are different in the water area of the water body [5, 9, 10]. The main focus of ligulosis of the
bream in Vistula Lagoon is its northeastern part, where invasion extensiveness reaches 66% and invasion intensity reaches up to 4 individuals of the parasite in the host. In this area, an extended period of invasion of bream up to five years old was recorded. Ligulosis of the bream in the lagoon is related to the intensification of processes of water body eutrophication. An increase in the invasion of the eel with nematode Anguillicola crassum has been observed for several years. Invasion extensiveness from 1989 to 2002 increased from 9.1 to 40% and invasion intensity increased from 2 to 36 individuals of parasites in the host; the index of abundance increased from 0.18 to 11.6. First and second intermediate hosts suitable for the parasite (cyclops, small fish) and essential for its life cycle occur in the lagoon; in connection with this, A. crassum is a serious threat for the eel stock. The zoogeographic analysis of parasitofauna of fish from Vistula Lagoon demonstrated the presence of five faunistic complexes (Table 4). The boreal-plain complex is represented by the maximum number of species. Representatives of marine origin are also present in the bay. The nematode Cucullanellus minutus belongs to the arctic marine complex. The Atlantic boreal faunistic complex consists of species that parasitize on fish (Baltic herring, eel, flounder, etc.) that enter the lagoon from the sea. The simplest—microsporidium Glugea stephani Hagenmuller and microsporidium Myxidium giardi—are specific to their hosts (the first to flounder and the second to eel). Other species of this complex have a wide specificity and parasitize on many marine fish of the basin of the Atlantic Ocean. These are cestode Proteocephalus macrocephalus (Creplin), nematodes Hysterothylacium aduncum, Cucullanus cirratus, and crustaceans Ergasilus gibbus and Lernaeocera branchialis. Nematode Anguillicola crassum belongs to the Pacific faunistic complex; it got entered the Baltic Sea together with its host (eel) due to commercial human activity. The distribution of parasites with a direct developmental cycle is directly affected by environmental factors (temperature, current, salinity, water turbidity, pollution, etc.). In their life cycles, endoparasites of fish have at least one free living stage in water and the environment exerts a direct impact on it. Parasites that inhabit intermediate or final hosts are exposed to environmental effect through their hosts. A poor species composition of zooplankton has determined a decrease in the number of parasite species for which copepods serve as intermediate hosts (Table 3). Most fish parasites in the lagoon use zoobenthos in their life cycles. Mollusks of the fam. Lymneidae are intermediate hosts of trematodes of the genera Diplostomum, Tylodelphys, and Posthodiplostomum. The high invasion extensiveness and intensity of fish with these trematodes correlates with the large numbers of limneid mollusks. The latter indicates the intensification of processes of eutrophication in the water body, because these molINLAND WATER BIOLOGY
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ANALYSIS OF FISH PARASITOFAUNA IN VISTULA LAGOON Table 5. Number of species of fish endoparasites that use different hydrobionts in their life cycle Group of hydrobionts
Number of species total, individuals
Zooplankton Zoobenthos:
% of total
14
38.9
22
61.1
oligochaetes
4
18.2
mollusks (the genera Galba, Sphaerium, Unio, Anodonta) mollusks (fam. Lymneidae) bottom crustaceans
4
18.2
8
36.4
6
27.2
5.
6.
7.
lusks are detritophages and develop in mass at dead aquatic vegetation. A small number of trematode species at the stage of marita in fish of the lagoon suggests that, in the fauna of mollusks, the number of species of the genera Gabda and Sphaerium decreased or completely disappeared. A noticeably smaller number of species of fish endoparasites is used in their life cycle by other organisms of zoobenthos (oligochaetes, gammaruses, hog slates, etc.) (Table 5). The colonization of intermediate hosts by parasites occurs along the historically formed canals. The impoverishment of the benthofauna of the lagoon entailed a decrease in the number of parasite species.
8.
9.
10. 11.
CONCLUSIONS In Vistula Lagoon there are parasite species in fish that indicate the intensification of processes of eutrophication of the water body. The formation of fish parasitofauna in the water body is affected by natural (current, water temperature, etc.) and anthropogenic factors (pollution, eutrophication, etc.). REFERENCES
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