CC BY
22
Biosystems
Diversity
ISSN 2519-8513 (Print) ISSN 2520-2529 (Online) Biosyst. Divers., 2019, 27(3), 214-220 doi: 10.15421/011929
Parasitofauna of pike Esox lucius of the Lower Tobol (Russia)
E. L. Liberman*, E. L. Voropaeva*' **, S. A. Kozlov*
*Tobolsk Complex Scientific Station UrB RAS, Tobolsk, Russia
**A. N. Severtsov Institute of Ecology and Evolution ofthe RAS, Moscow, Russia
Article info
Received 10.03.2019 Received in revised form
13.04.2019 Accepted 15.04.2019
Tobolsk Complex Scientific Station UrB RAS, Y. Osipova st., 15, Tobolsk, 626152, Russia. Tel.: +7-905-826-23-47. E-mail: eilat-tymen@mail.ru
A. N. Severtsov Institute of Ecology and Evolution ofthe RAS, Leninsky Prospect, 33, Moscow, 119071, Russia. Tel.: +7-925-509-40-96. E-mail: kts2@yandex.ru
Liberman, E. L., Voropaeva, E. L., & Kozlov, S. A (2019). Parasitofauna ofpike Esox lucius of the Lower Tobol (Russia). Biosystems Diversity, 27(3), 214-220. doi:10.15421/011929
One of the predators of the ichthyofauna of the Lower Tobol is Esox lucius (Linnaeus, 1758) (Esociformes, Esocidae). The purpose of this work is to study the current state of the E. lucius parasite fauna in the lower reaches of the Tobol River. In the present study 47 individuals of the northern pike of different sex aged from 2+ to 8+ years were examined by the method of complete parasitological dissection. As a result of the research, 23 types of parasites were found in the pike. The largest number of species of parasitic organisms - 20 - were found in May, 12 were found in December and 11 in September. Of these, 10 species are specific to northern pike: Haemogregarina esoci (Nawrotzky, 1914), Chloromyxum esocinum (Dogiel, 1934), Myxidium lieberkuhni (Biitschli, 1882), Myxosoma anurum (Cohn, 1895), Henneguyapsorospermica (Thelohan, 1995), Tetraonchus monenteron (Wagener, 1857), Gyrodactylus lucii (Kulakowskaja, 1951), Triaenophorus nodulosus (Pallas, 1781), Azygia lucii (Miiller, 1776), Raphidascaris acus (Bloch, 1779). For the first time an intraerythrocyte parasite - H. esoci - was found in pike in the Lower Tobol, the extensiveness of invasion was 18.7% in December, and 6.2% in May. Epistylis sp. and Trichodinella epizzotica parasitized on the surface of the body of fish only in May, whereas members of the genus Trichodina were found in winter and spring. In all seasons, parasitization by M. anurum and H. psorospermica was established on the gills. The greatest occurrence of spores ofM. lieberkuhni and C. esocinum was observed in the spring. Myxosporidia parasitized in the kidneys and T. monenteron parasitized on the gills during all periods of the study (the latter with an extensivity of invasion of 100.0%). All examined fish are infected with T. nodulosus 100.0% of cases. In May, other types of cestodes were found: P. esocis and Dibothriocephalus latus. Three pike were infected with proteocephalis. The larval stage of diphyllobothriid was found in one fish in the liver and gonads in an amount of 139 individuals. In the pikes' stomach, during all periods of the study, A. lucii was found in all the fish examined. In the autumn period of the study immature R. campanula were found in in the intestine of 4 fish specimens. The nematode R. acus was found in pike only in spring. This nematode was found in fish aged 4+-8+. In May, glochidia with a high intensity of invasion were found on fins, gill covers and gills of fish. E. sieboldi copepods were found on the gills; in May, one specimen was found in one pike and in September in 6 with AI of 0.7. Tetraonchus monenteron was a dominant species, in May its degree of dominance decreased with the greatest uniformity of species in this study period. Having considered the age dynamics of pike infection by various types of parasites, it was found that in the age group 4+-5+ the number of species of parasites was greatest (20), while in groups 2+-3+ and 6+-8+ it was 14. In the pike, the core parasitic fauna were M. anurum, H. psorospermica, T. monenteron, T. nodulosus, A. lucii. Seasonality has virtually no effect on the degree of infection with specific parasites. The age of fish largely determines the qualitative and quantitative composition of the parasite fauna.
Keywords: Northern pike; parasitic community; Haemogregarina esoci; Tetraonchus monenteron; Triaenophorus nodulosus; Azygia lucii.
Introduction
Northern pike Esox lucius (Linnaeus, 1758) is a broadly distributed predatory fish in fresh waters of Eurasia and North America. Also it is found in fresh-water marine areas: in bays of the Baltic and Azov seas. In water bodies where no intensive fishing is done, pike can reach up to 180 cm in length (usually length of caught fish is up to 1 meter) and weigh up to 40 kg (usually up to 8 kg) (Crai, 1996). E. lucius lives in areas with slow flow, preferring to keep in thickets of aquatic vegetation. The diet of pike is significantly affected by biotopic, seasonal and size variation (Grunin, 2009). In the Ob river, the basis of diet of adult fish comprises carp, and also whitefish (Coregoninae), European perch, ruffe, burbot, and young pike.
The main factors which determine the qualitative and quantitative composition of parasitofauna are the age of the host and seasonal changes in natural conditions. Over its lifetime, the host undergoes changes in body structure, behaviour and range of food. In turn, extensi-ty and intensity of many species of parasites increase the older the host becomes (Alvarez et al., 2006; Iyaji et al., 2010).
Water temperature is the main abiotic factor that affects the cycle of the development of ectoparasites - protozoans and monogeneans. Out
of them, a large number of species was found to have a clearly manifested spring-summer maximum of the development, and did not have an active state in winter. Kennedy (1975) reported that many endopara-sites of fish were observed to have clearly manifested seasonal changes in number over the year. Thus, extensity and intensity of infestation with Triaenophorus nodulosus cestode, which parasitizes in pike, remain at a relatively constant level over the year due to dynamic balance between constant replenishment of the population and mortality (death of mature cestodes after breeding). Aspects of seasonal changes in fauna of parasites of fish are broadly studied by many authors (Lamkova et al., 2007; Abdel-Aziz et al., 2012; Kondo et al., 2016).
Study of species composition of parasitic organisms in fish has great practical significance for assessment of the epizootic condition of water bodies. Studies on parasitofaunua allow one to find distribution of fish parasites dangerous for humans. In the Ob-Irtysh basin, pike is a source of the dibothriocephalus pathogen.
Detailed study of parasitofauna of E. lucius has been conducted by many scientists in our country (Malahova, 1961; Mitenev, 1998; Ieshko & Korosov, 2012; Chugunova et al., 2014), as well as abroad (Watson & Dic, 1980; Colak, 2013; Fallah et al., 2015). Detailed data on parasites of pikes in the Ob-Irtysh basin have been published in a number of
large studies in the second half of the XX century (Petrushevskij et al., 1948; Titova, 1965; Agapova, 1966; Pugachev, 1984).
The objective of our research was to establish the current condition of species composition of parasites of northern pike in the Lower Tobol.
Materials and methods
Material for our study was collected on 10-21 December of 2017, 14-19 May and 17-22 September of 2018 from the lower flow of the Tobol River (Karachino village, 58°02'50'' N, 68°06'35'' E). Catching was performed using gillnets and fixed gillnets (on stakes) with 2438 mm cells. The fish were transported to the laboratory alive in special live-fish tanks. Using the method of parasitologic autopsy (Byhovskaya-Pavlovskaya, 1985), a total of 47 individuals of E. lucius (L = 31.269.2, M = 142.2-1224.0) were examined, 2+ to 8+ year old males, females and juvenile individuals. Biological and morphometric parameters of the fish were determined according to generally accepted methods (Pravdin, 1966). Fixation of found parasitic organisms, and preparing temporary and constant preparations of parasites were made using standard methods (Byhovskaya-Pavlovskaya, 1985). We identified the species of parasites (Skarlato, 1984, 1985, 1987; Fiala et al., 2015), calculated extensity of infestation (percent of individuals of hosts in which a species of parasite was found, EI) with standard mean error, intensity of infestation (minimum and maximum number of specimens of parasite per each infested individual, II), index of abundance (mean number of specimens of a parasite species per one examined individual of host, AI) with standard mean error. For determining the dominance of species in the parasite fauna, we used the Berger-Parker index of dominance (d) (Mehgarran, 1992). Statistical analysis of the results was made using Statistica 10 software (StatSoft Inc., 2011).
Results
As a result of the studies we conducted, in northern pike from the Nyzhny Tobol, 23 species of parasites (Table 1) were determined (Sporo-zoa - 1, Kinetoplastida - 1, Cnidosporidia - 2, Oligohymenophorea - 4, Myxosporea - 5, Monogenea - 2, Cestoda - 3, Trematoda - 2, Nematoda -1, Copepoda - 1, Bivalvia - 1). Out of them, 10 species are specific to pike: H. esoci, C. esocinum, M. lieberkuhni, M. anurus, H. psorospermi-ca, T. monenteron, G. lucii, T. nodulosus, A. lucii, R. acus. The highest number of species, 20, was determined in May, 12 were found in December, and 11 parasitic species in September (Table 1, 2).
The endoglobular parasite H. esoci (Fig. 1a) was found in blood smears of 3 specimens (spec.) of fish in December and in 1 fish in May. Trypanosoma sp. (Fig. 1b) was recorded in the bloodstream of 2 pikes in May and in 10 in September. Epistylis sp. and T. epizzotica parasitized the body surface of fish only in May, extensity of infestation was 6.2% and 62.5% respectively. T. esocis (Fig. 2a), T. rectangle (Fig. 2b) and T. pediculus (Fig. 2c) were found on the body surface of pikes in the winter and spring period of study, total EI equaled 31.2% in December and 100.0% in May. M. anurus (Fig. 3a) and H. psorospermica (Fig. 3b) parasitized the gills of fish during all periods of study with increase in infestation towards autumn (Table 1).
The highest abundance of spores of M. lieberkuhni, which parasitizes the bladder of pike, and C. esocinum found in the bladder was observed in the spring period. In September, infestation with spores of these microsporidians decreased, and in December they were not found. In the kidneys, in all studied periods, Myxosporidia was found. In May, highest values of infestation were observed. Apiosoma sp. was found on the gills, fins and the body surface of the examined fish only in September with extensity of 37.5%.
The monogenean T. monenteron parasitized the gills over all periods of study with high abundance index. In September, AI reached 225.3 spec., and 161 spec. over all periods of study. Another representative of monogeneans - G. lucii was found only on the fins of pikes in December and May. Highest infestation with this parasite was observed in spring with EI equaling 68.7%.
In the intestine of the studied pikes, we observed infestation with T. nodulosus cestode over all seasons of studies. In spring, we deter-
mined high parameters of intensity and abundance. During all periods of study, AI equaled 65.7 spec. of the parasite per one examined fish. In May, we found other species of cestodes: Proteocephalus sp. in the intestine and plerocercoid larvae of D. latus in the liver and the gonads. Plerocercoid larvae were found in three specimens of pikes. 139 larval specimens ofD. latus were found in one fish.
Table 1
Extensity of the infestation (%) with protozoans and microsporidians in Esox lucius in the Lower Tobol in different seasons of the year
Species of parasite
Period of study
December, May, September, n = 16 n = 16 n = 15
Haemogregarina esoci (Nawrotzky, 1914) Trypanosoma sp. Epistylis sp.
Trichodina esocis (Lom, 1960), T. pediculus (Ehrenberg, 1838), T. rectangle (Chen et Hsien, 1964) Trichodinella epizzotica (Raabe, 1950) Apiosoma sp.
Myxidium lieberkuhni (Biitschli, 1882) Myxobolus anurus (Cohn, 1895) Chloromyxum esocinum (Dogiel, 1934) Henneguya psorospermica (Ihelohan, 1895) Myxosporidia sp._
18.7 ± 9.7 6.2 ± 6.0 -
- 12.5 ± 8.3 66.6 ± 12.2
- 6.2 ± 6.0 -
31.2 ± 11.6 93.7 ± 6.1 -
- 62.5 ± 12.1 -37.5 ± 12.1 - -
- 68.7 ± 11.6 26.7 ± 11.4 37.5 ± 12.1 37.5 ± 12.1 93.3 ± 6.5
- 68.7 ± 11.6 6.7 ± 6.5 31.2 ± 11.6 31.2 ± 11.6 86.7 ± 8.8 25.0 ± 10.8 75.0 ± 10.8 33.3 ± 12.2
Note: n - number of fish in the selection.
Over all seasons of study, pikes were observed to have one more representative of the specific parasites, A. lucii, a trematode which parasitizes the stomach. The highest parameters of II and AI were observed in winter; they gradually decreased by autumn. Over the autumn period of studies, in the intestine of 4 individuals of the fish, we found mature specimens of R. campanula.
The specific parasite R acus was found in the intestine of pikes only in spring. This nematode was found in fish at the age of 4+-8+. Also, in May, on the fins, gill operculums, and gills, glochidia - parasitic larvae of the Unionidae family of Bivalvia, were found with high intensity of infestation. In the class copepods, E. sieboldi crustaceans were found on the gills. One specimen was found in one fish in May, and in September in six fish at AI of 0.7 spec.
Analysis of parasitic component community in the studied population of pike of the lower flow of the Tobol river (Table 2) determined that the dominant species was the monogenean T. monenteron (d = 0.556), in May, its level of domination reduced at the highest uniformity of abundance of species in that period of study.
Table 2
Extent of dominance of metazoan parasites
in the community of Esox lucius in the Lower Tobol
Species Period of study, N*
in the community December May September Total number
T. monenteron 2815 1375 3379 7569
G. lucii 27 160 - 1187
T. nodulosus 862 1355 870 3087
D. latus (pl) - 139 - 139
Proteocephalus sp. - 16 - 16
R. campanula - - 42 42
A. lucii 688 516 215 1419
R.s acus - 24 - 24
Unionidae gen. sp. (l) - 1121 - 1121
E. sieboldi - - 11 11
d 0.641 0.292 0.748 0.556
1/d 1.56 3.42 1.34 1.80
Note: N* - total number of parasites in the studied selection; d - Berger-Parker index.
By analyzing the age dynamic of infestation of pike with different species of parasites (Table 4, 5), we observed the highest number of parasitic organisms (20) in the age group 4+-5+, whereas in groups 2+-3+ and 6+-8+ the number was 14, H. esoci was found only in pikes of the age group 4+-5+, and Trypanosoma sp. parasitized in specimens of all ages. The older the fish, the lower the EI. Also, with age, there was
observed a reduction of infestation with M. anurus and H. psorospermica. Increase in EI with increase in age was observed for infestation of M. lieberkuhni, representatives of Trichodina and T. epizzotica. For R. acus, Unionidae gen. sp. and G. lucii, we also observed increase in EI along with increase in age, but at the same time, these parasites were not
observed in the age group 2+-3+. We determined that only fish aged 4+-5+ were infested with Epistylis sp., D. latus and Proteocephalus sp. Obligatory parasites of pikes, such as T. monenteron, T. nodulosus and A. lucii infested fish in all age groups with the same high extensity of infestation.
Table 3
Metazoan parasites of Esox lucius in the Lower Tobol in different season of the year
Species of parasite
December, n = 16
Period of study May, n = 16
September, n = 15
EI
II
AI
EI
II
AI
EI
II
AI
Tetraonchus monenteron (Wagener, 1857) Gyrodactylus lucii (Kulakowskaja, 1951) Triaenophorus nodulosus (Pallas, 1781) Dibothriocephalus latus (Linnaeus, 1758) (pl) Proteocephalus sp.
Rhipidocotyle campanula (Dujardin, 1845) Azygia lucii (Miller, 1776) Raphidascaris acus (Bloch, 1779) Unionidae gen. sp. (l) Ergasilus sieboldi (Nordmann, 1832)
100.0 25.0 ± 10.8 100.0
100.0
9-416
4-9
7-173
175.9 ± 32.0
1.7 ± 0.8 53.9 ± 11.1
4-120 43.0 ± 10.2
87.5 ± 8.3
68.7 ± 11.6 100.0
6.2 ± 6.0
18.8 ± 9.8
93.7 ± 6.1 43.7 ± 12.4 50.0 ± 12.5 6.2 ± 6.0
2-346 2-47 13-344 139* 2-11
1-101 1-8 6-490 1*
85.9 ± 24.5 10.0 ± 3.6 84.7 ± 20.2 8.7 ± 8.7 1.0 ± 0.7
100.0
100.0
20.0 ± 10.3 100.0
94-591 225.3 ± 35.4
21-124 58.0 ± 6.9
1-37 3-33
32.2 ± 8.4
1.5 ± 0.7 -
70.1 ± 31.4 -
0.06 ± 0.06 40.0 ± 12.6 1-4
2.8 ± 2.5 14.3 ± 2.9
0.7 ± 0.3
Note: EI - extensity of infestation, %; II - intensity of infestation (min-max); AI - abundance index (spec.); n - number of fish in selection; * - in one individual of pike; pl - plerocercoid larvae; 1 - larva.
Fig. 1. Endoglobular parasite Haemogregarina esoci (a) and Trypanosoma sp. (b) in a blood smear of pike, permanent preparation
Discussion
In total, in the Ob-Irtysh basin, 82 species of parasitic organisms have been found in pike (Berendeev et al., 2006). Out of them, 20 species were protozoans, 9 - microsporidians, 8 - monogeneans, 8 - cestodes, 23 - trematodes, 5 - nematodes, 2 - acanthocephalans, 2 - leeches, 1 - mollusks, 3 - crustaceans, 4 - acari. The basis of the parasitofauna comprises 15 species of specific parasites - representatives of the boreal plain faunistic complex: C. esocinum, M. lieberkuhni, M. anurus, H. lobosa, H. psorospermica,, Н. schizura, Н. oviperda, T. monenteron, G. lucii, T. nodulosus, T. crassus, P. esocis, A. lucii, R acus, P. obturans. In most rivers and lakes specific parasites were recorded in pike, but the number of their species significantly varied in separate water bodies (Titova, 1965; Agapova, 1966). Pugachev (1984) observed a notable west to the east decrease in the species richness of both the specific and non-specific parasitofauna of E. lucius in the water bodies of the distribution range in the territory of Si-
beria and North-East of Russia. Thus, 15 specific species of parasites of E. lucius were recorded in the Ob, 10 in the Yenisei (Chugunova, 2014), 10 in Baikal (Rusinek, 2007), 7 in the Lena (Platonov et al., 2018), 7 in the Kolyma (Pugachev, 1984), and 3 in the Gizhyga (Pospekhov et al., 2010).
Fig. 2. Trichodina esoci (a), T. rectangle (b) and T. pediculus (c) from the body surface of pike, permanent preparation
a
b
r
■ IN »
from the age of two weeks (11.0-56.8%) (Polyanskij & Shul'man, 1956; Lyubarskaya 1968). We determined that pike were infested with representatives of the Trichodina genus in winter (31.2%) with increase in the extensity in spring (93.7%); in September, no trichodinids were found. T. epizzotica parasitized only over the spring period, EI was 62.5%. Endoparasitic protozoans Haemogregarina and Trypanosoma were also observed in pike of the Lower Tobol. In Staruha Lake (Ukraine), in the blood flow of pike, there was observed a low level of EI (73.0%) Trypanosoma sp. (Grybchuk-Ieremenko et al., 2014). According to Gusejnov (2008), infestation of pike with Trypanosoma carassii and T. schulmani reached a peak by the early summer (76.9% and 15.4% respectively), gradually reducing in autumn (50.0% and 28.6% respectively). In our study, infestation of pike with trepanosoms was observed in May (12.5%) and September (66.6%), but parasitism of leaches, transmitters of the parasite, was not observed in any of the study periods. An opposite result was observed for H. esoci: it was recorded in December (18.7%) and May (6.2%). These are first published data on infestation of pike with Haemogregarina in the basin of the Lower Irtysh.
Table 4
Extensity of infestation (%) of protozoans and microsporidians in Esox lucius in the Lower Tobol in different age groups
Species of parasite
Age of the pike
2+-3+, n = 15
4+-5+, n = 23
6+-8+, n = 9
b
Fig. 3. Myxobolus anurus (a) and Henneguya psorospermica (b) from the gills of pike, permanent preparation
In the Lower Tobol, the highest number of parasites in pike was observed in spring (20 species). Over that period, along with increase in water temperature, infestation of fish with ectoparasitic protozoans steeply increases. Maximum value of T. epizzotica infestation occurred in spring and early summer, and in winter the parasite was not found (Shul'man et al., 1974). Young pike become infested with this parasite
Table 5
Age dynamic of infestation of pike with parasitic organisms
H. esoci - 17.4 ± 7.9 -
Trypanosoma sp. 53.3 ± 12.9 13.0 ± 7.0 11.1 ± 10.5
Epistylis sp. - 4.3 ± 4.2 -
Trichodina esocis, T. pediculus, Т. rectangle 20.0 ± 10.3 52.2 ± 10.4 66.7 ± 15.7
T. epizzotica 6.7 ± 6.5 26.1 ± 9.2 33.3 ± 15.7
Apiosoma sp. 20.0 ± 10.3 17.4 ± 7.9 -
M lieberkuhni 26.7 ± 11.4 30.4 ± 9.6 44.4 ± 16.6
M anurus 86.7 ± 8.8 47.8 ± 10.4 33.3 ± 15.7
C. esocinum 13.3 ± 8.8 34.8 ± 9.9 22.2 ± 13.9
H. psorospermica 66.7 ± 12.2 39.1 ± 10.2 44.4 ± 16.6
Myxosporidia sp._46.7 ± 12.9 47.8 ± 10.4 33.3 ± 15.7
Note: n - number of fish in a selection.
Age group 2+-3+, n = 15 4+-5+, n = 23 6+-8+, n = 9
Species of parasite EI II AI EI II AI EI II AI
T. monenteron 93.3 ± 6.5 94-394 183.0 ± 25.0 100.0 9-591 163.9 ± 31.6 88.9 ± 10.5 2-416 117.1 ± 45.2
G. lucii - 43.5 ± 10.3 2-18 3.7 ± 1.2 55.6 ± 16.6 4-47 11.4 ± 6.1
T. nodulosus 100.0 21-115 63.7 ± 7.7 100.0 13-344 73.7 ± 15.5 100.0 7-100 48.4 ± 10.5
D. latus (pl) - 4.3 ± 4.2 139* 6.0 ± 6.0 -
Proteocephalus sp. - 13.0 ± 7.0 2-11 0.7 ± 0.5 -
R campanula 20.0 ± 10.3 1-37 2.8 ± 2.6 - -
A. lucii 93.3 ± 6.5 5-46 15.6 ± 3.3 100.0 2-120 35.7 ± 7.8 100.0 1-96 40.6 ± 13.0
R acus - 17.4 ± 7.9 1-7 0.4 ± 0.3 33.3 ± 15.7 1-8 1.6 ± 1.0
Unionidae gen. sp. (l) - 17.4 ± 7.9 6-490 28.1 ± 21.5 44.4 ± 16.6 70-186 52.7 ± 23.1
E. sieboldi 33.3 ± 12.2 1-4 0.7 ± 0.3 8.7 ± 5.9 1* 0.1 ± 0.06 -
Note: see Table 2.
High infestation of pike with spores of M. lieberkuhni and C. esocinum in spring is related to spawning. Increase in water temperature contributes to infestation of Oligochaeta, intermediate hosts in littoral parts of water body, which creates favourable conditions for infestation of young fish. Therefore, by age of three-months up to 85.0% of young pike become infested with M lieberkuhni (Lyubarskaya, 1968). Burdukovskaya et al. (2017) determined high sensitivity of this parasite to anthropogenic contamination of water bodies, which has an effect on its number. Spores of microsporidians of M anurus and H. psorospermica in pike in water bodies of Karelia occur in all seasons of the year (Malahova, 1961; Shul'man et al., 1974). In Konchezero Lake, the highest parameters of contamination with these parasites were observed in autumn (Malahova, 1961). In her studies, Gorbunova (1936) found no dependence between infestation of pike with M. anurum and the age of the fish. In the Lower Tobol, M. anurus and H. psorospermica are common species parasitizing
northern pike, but the older the fish, the lower the infestation of fish with these parasites. Many authors observed ubiquitous infestation of pike, regardless of conditions of the hydrological regime of the water body, with such obligatory parasites as T. monenteron, T. nodulosus, A. lucii, R acus. The monogenean T. monenteron infests pike with high exten-sivity and intensity of invasion, and has a dominating position in its parasitofeuna (Mitenev, 1998; Rusinek, 2007; Burdukovskaya et al., 2017; Ozturk et al., 2000). Young fish became infested with Tetraonchidae already at age of two weeks with EI up to 26.0% (Lyubarskaya, 1968). The older the pike, the higher the EI and II of T. monenteron (Gorbunova, 1936; Ozturk et al., 2000). High II of adult individuals ofE. lucius (up to 800 spec.) with monogeneans of T. monenteron, according to Gorbunova (1936), is related to increase in area of the gills with age of fish, as the place of localization of parasites. Over the year, T. monenteron produces several generations both in north and south latitudes. Ac-
cording to Malahova (1961), in Konchezer, infestation of pike with T. monenteron in the spring-summer months increases up to 97.0%, and decreases in winter to 4.5%. In a study of the seasonal dynamic of T. monenteron in pikes in Dzhapana Lake (Georgia), Chernova (1975) observed 100.0% infestation in the spring-summer period at AI of 77.2 spec., decrease in infestation in autumn to 38.5% at AI of 2.9 spec., and increase in infestation in the winter period to 86.7% at AI of 21.8 spec. According to the author, reduction in infestation of pike with this parasite in autumn is conditioned not by the temperature factor, but by some other factors. Ozturk et al. (2000) also found high infestation of the gills of pike (100.0%) in the autumn-winter and summer periods, and decrease in extensivity of infestation to 65.0% in spring. In the winter period, AI significantly decreased (25 spec.) and in spring it steeply increased (146 spec.) (Ozturk et al., 2000). Analysis of the conducted studies has revealed that intensity of infestation of pike with T. monenteron in the Lower Tobol has no clearly manifested seasonal dynamic, there was observed an insignificant decrease in EI and AI in May. A different picture was observed for infestation of pike with the specific monoge-nea G. lucii. This species occurs more rarely and with low intensity of infestation (Titova, 1965; Mitenev, 1998; Burdukovskaya et al., 2017). We recorded parasitism of Gyrodactylus with low AI in the winter and spring periods of study in fish aged from 4+-8+.
Pike is an obligatory terminal host for T. nodulosus, R. acus and A. lucii. It becomes infested with the abovementioned species by consuming fish, intermediate or reservoir hosts of the parasites. It should be mentioned that according to literature data, pike begin feeding on fish at 10-15 days after hatching at body length of 20-23 mm; at the age of 2.0-2.5 months, its diet mostly comprises fish, and also larvae of dra-gonflies, mayflies and pupae of chironomids (Ivanova & Svirskaya, 2009). High parameters of infestation with T. nodulosus have been observed throughout the distribution range of E. lucius. The cestode parasitizes pikes both in the stage of plerocercoid larva (rarer) and in their mature form. Pikes become infested with T. nodulosus early in the second year and with age, EI increases from 40.0% (1+) to 100.0% (8+-10+) (Gorbunova 1936). In the Lower Tobol, pike were infested with T. nodulosus in all periods of study in 100.0% of cases, but highest intensity and abundance of parasite was observed in spring. In many water bodies, T. nodulosus is dominant and is significant in formation of the parasitofauna of pike. Shabunov & Radchenko (2012) report that at high level of infestation with T. nodulosus in the intestine of pikes, there were no acanthocephalans, trematodes, and nematodes had low EI. A peculiarity of the relation between pike and T. nodulosus in the system parasite-host is that even at high II, pathogenity of the parasite for the host is minimum, indicating dependency of this system on long mutual evolution, and also maintenance of total homeostasis of the system (Izvekova, 2001; Vysockaya et al., 2015). At the same time, plerocercoid larvae of T. nodulosus have high pathogenity for fish and can cause mass death of young fish (Pronina & Pronin, 1988). The obligatory parasite of pike - A. lucii - infests also facultative hosts: perch, zander, burbot, trout, and ruffe. Lung flukes, in which cercaria develop, are intermediate hosts for it, and fish are terminal hosts. Plantophagous fish become para-definite host, in which the parasite undergoes the first stages of morphogenesis of adult individual, but does not reach maturity. Large predators become infested with Azygia after swallowing fish which are para-definitive and definitive hosts of lower trophic level. Infestation of pike with A. lucii occurs in the autumn-winter period, therefore in spring, large mature, as well as small immature individuals, occur. For the first time it becomes infested with Azygia in the beginning of the second year of life and extensity and intensity increase with age (Gorbunova, 1936). According to our and literature data, seasonal changes of infestation of pike with this parasite were not determined (Shul'man et al., 1974). In the data on infra-communities, there are observed clear borders of trophic relations between parasite and host, and trophic niches, between such parasitic organisms as T. nodulosus and A. lucii, expressed in differentiated selection of location, which reduces their interspecies competition.
The most commonly found species was R. acus. Adults of this ne-matode parasitize the intestine of predatory fish, mostly pike. The larval stage develops in a broad range of intermediary hosts (fish) and reser-
voir (crustaceans, Oligochaeta, larvae of chironomids and aquatic insects, mollusks) hosts (Moravec, 1970). The peak of seasonal infestation of pike with R acus occurs in the winter and spring period (Akkent & Ozturk, 2017). By the end of summer, this nematode leaves the gast-rointernal tract of fish. Infestation of young pike with R acus depends on the temperature regime of the water body and can reach 30.0% in warm years (Lyubarskaya, 1968). With age, infestation with R acus increases, maximum values were recorded in the group aged from 5+-11+ (Gorbunova, 1936). Infestation of pike in the Ob-Irtysh basin ranges from 6.2-80.0% (Titova, 1965), 6.6-38.2% in lakes of Karelia, 13.3-93.3% in water bodies of the North Kola (Mitenev, 1998), and 2.7-29.0% in the basin of the Northern Dvina River (Shabunov & Rad-chenko, 2012).
Parasitism of R campanula in pike is related to its predation. The first intermediary hosts are mollusks of Unio and Anodonta genera, the second are various fish, mostly from the Cyprinidae family. According to the literature data, in the lakes of Karelia, infestation of pike with mature stages of R campanula is significantly lower (4.8-20%) than infestation of non-predatory fish with metacercariae of this parasite (Rutilus rutilus - 20.0-80.0%, Leuciscus leuciscus - 40.0-85.7%; Shul'man et al., 1974). A similar picture of infestation of fish with R campanula was observed in our study as well. Therefore, total infestation of pike with this parasite was 6.4% at abundance index of 0.9 spec. per examined fish. We have agreed with the authors that perhaps it is related to the fact that species of fish heavily infested with metacercariae have no significant role in the diet of pike in these water bodies.
Infestation of fish with glochidia occurs in spring. In spring, in pike in the Lower Tobol, II reached 490 spec. per fish, whereas in winter and autumn, this parasite was not found. By contrast, parasitism of E. sieboldi began with increase in water temperature; in May 1 crustacean was found in 1 pike, and in September, EI equaled 40.0% with AI of 0.7 spec.
Among the parasites dangerous for humans and animals, in the lower flow of the Tobol river, we found D. latus plerocercoid larvae only in one pike, but with high intensity of infestation. Examination of different predatory fish (306 individuals) of the lower flow of the Irtysh in 2002-2009, Pel'gunov (2012) revealled no D. latus plerocercoid larvae. These data indicate improvement of sanitary-epizootic condition of water bodies of the Lower Tobol as a result of improvement of culture of the population and reduction of release of unfiltered drainage water to the water bodies.
It should be mentioned that the species composition of non-specific parasites of pike depends on the local ecological conditions. Thus, in pike, Agapova (1966) found Dactylogyrus monogeneans, which are characteristic for carp. Pike in the Gizhyga River become infested with both fresh-water and marine parasites to the same extent. They become infested with the latter presumably by consuming migratory and semi-migratory fish (Pospekhov et al., 2010). According to Ieshko & Koro-sov (2012), the main factor which determines the diversity of the parasitic community of pike is the age composition of the population. The authors have proved that the highest infestation is among fish of average age: 4+-6+ year-old fish, which play the main role in maintaining the population of parasites. This correlates with our studies.
Conclusion
Thus, for the northern pike which inhabit the Lower Tobol, the core parasitofauna is composed of M. anurus, H. psorospermica, T. mo-nenteron, T. nodulosus, and A. lucii. Seasonality has practically no effect on the extent of infestation with specific parasites. The dominant species was a monogenetic fluke T. monenteron. The age of the fish to a large extent determines the qualitative and quantitative composition of the parasitofauna. Pike are most heavily infested at the age of 4+-5+, when the food range of the predator increases. Seasonal and age change in the species composition of parasites of pike is often related not only to its selection of food objects, activity, temperature regime of water body, but to also the life cycles of the parasitic organisms.
The article has been prepared with financial support of the Ministery of Sciences and Higher Education of Russia within the scope of topic of fundamental scientific studies R&D No AAAA-A19-119011690102-1: Fish population in winter in
the wintering holes of stream beds of the Lower Irtysh, patterns of their distribution, migration and parasitic communities. Identification of monogeneans, work with literature sources, formation of publication materials was made with support of the programme of the Presidency of the Russian Academy of Sciences No 41: Biodiversity of natural systems and biological resources of Russia.
References
Agapova, A I. (1966). Parazity ryb vodoemov Kazahstana [Parasites of fishes of
reservoirs of Kazakhstan]. Nauka, Alma-Ata (in Russian). Akkent, E., & Ozturk, M. O. (2017). An investigation on intestinal helminth fauna of pike (Esox lucius Linnaeus, 1758) from Lake Karamik, Afyonkarahisar. Kocatepe Veterinary Journal, 10(3), 196-203. Álvarez, M. F., Cordeiro, J. A., Leiro, J. M., & Sanmartín, M. L. (2006). Influence of host age and sex on the helminth fauna of the yellow-legged gull (Larus michahellis) in Galicia (North-Western Spain). Journal of Parasitology, 92(3), 454-458.
Berendeev, S. F., Bogdanov, V. D., Bogdanova, E. N., Bocharova, T. M., Vizer, A. M., Vizer, L. S., Voskobojnikov, V. A., Golubcov, A. S., Goskova, O. A., Egorov, E. V. (2006). Ehkologiya ryb Ob'-Irtyshskogo bassejna [Ecology of fish of the Ob-lrtysh basin]. KMK, Moscow (in Russian). Burdukovskaya, T. G., Dugarov, Z. N., Tolochko, L. V., Batueva, M. D., Mazur, O. E., Sondueva, L. D., & Zhepholova, O. B. (2017). Mnogoletnie izmeneni-ya parazitofauny shchuki oz. Gusinoe - vodoema-ohladitelya Gusinoozers-koj GREHS [Perennial changes in the parasite fauna of pike at Goose Lake -water reservoir - cooler Gusinoozerskaya HPS]. In: Ekologiya vodoemov-ohladitelej ehnergeticheskih stancij. Pp. 23-28. Byhovskaya-Pavlovskaya, I. E. (1985). Parazity ryb. Rukovodstvo po izucheniiyu
[Fish parasites. Study Guide]. Nauka, Leningrad (in Russian). Chernova, T. N. (1975). Sezonnye izmeneniya parazitofauny shchuki i plotvy ozer Paleostomi i Dzhapana [Seasonal changes in the parasite fauna of pike and roach in Paleostomi and Dzhapan lakes]. In: Naumov, V. M. (Ed.). Trudy Vsesoyuznogo Nauchno-Issledovatel'skogo Instituta Rybnogo Hozyajstva i Okeanografii. Pp. 108-120 (in Russian). Chugunova, Y. K. (2014). Parazitofauna shchuki (Esox lucius Linnaeus, 1758) v vodoemah razlichnyh prirodno-klimaticheskih zon [Parasitic fauna of pike (Esox lucius Linnaeus, 1758) in water bodies of various climatic zones]. In: Systematics and ecology of parasites. Pp. 331-333. Qolak, H. S. (2013). Metazoan parasites of fish species from Lake Sigirci (Edirne,
Turkey). Turkish Journal of Veterinary and Animal Sciences, 37, 200-205. Crai, J. F. (Ed.). (1996). Pike. Biology and exploitation. Springer, Dordrecht. Fallah, F. J., Khara, H., Rohi, J. D., & Sayadborani, M. (2015). Hematological parameters associated with parasitism in pike, Esox lucius caught from Anza-li wetland. Journal of Parasitic Diseases, 39(2), 245-248. Fiala, I., Bartosová-Sojková, P., & Whipps, C. M. (2015). Classification and phy-logenetics of Myxozoa. In: Okamura, B., Gruhl, A., & Bartholomew, J. (eds.). Myxozoan Evolution, Ecology and Development. Springer, Cham. Pp. 85-110.
Gorbunova, M. N. (1936). Vozrastve izmeneniya parazitofauny shchuki i plotvy [The age of change of the parasite fauna of pike and roach]. Uchenye Zapiski Leningradskogo Gosudarstvennogo Universiteta, Seriya Biologicheskie nauki, 7(3), 5-30 (in Russian). Grunin, S. I. (2017). Pitanie obyknovennoj shchuki Esox lucius v srednem teche-nii r. Anadyr' [Diet of common pike Esox lucius in the middle course of the River Anadyr]. Vestnik Severo-Vostochnogo Nauchnogo Centra DVO RAN, 1, 109-110 (in Russian). Grybchuk-Ieremenko, A., Losev, A., Kostygov, A. Y., Lukes, J., & Yurchenko, V. (2014). High prevalence of trypanosome co-infections in freshwater fshes. Folia Parasitologica, 61(6), 495-504. Gusejnov, M. A. (2008). Cezonnye izmeneniya zarazhennosti shchuki (Esox lucius L.) Devechinskogo limana kroveparazitami [Seasonal changes in pike infestation (Esox lucius L.) of the Devechi estuary by blood parasites]. In: Bioraznoo-brazie i Ekologiya Parazitov Nazemnyh i Vodnyh Cenozov. Pp. 96-101. Ieshko, E. P., & Korosov, A. V. (2012). Ocenka vidovogo bogatstva parazitofauny ryb: Ehkologicheskij podhod [Assessment of the species richness of the fish parasite fauna: An ecological approach]. Principy Ehkologii, 4, 28-40 (in Russian).
Ivanova, M. N., & Svirskaya, A. N. (2009). Rost i pitanie molodi shchuki Esox lucius (Esocidae) raznyh srokov vylupleniya v techenie pervyh mesyacev zhizni [Growth and nutrition of juvenile pike Esox lucius (Esocidae) of different hatching periods during the first months of life]. Voprosy Ihtiologii, 49(4), 508-518 (in Russian). Iyaji, F., Etim, L., & Eyo, J. (2010). Parasite assemblages in fish hosts. Bio-
Research, 7(2), 561-570. Izvekova, G. I. (2001). Fiziologicheskaya specifika vzaimootnoshenij mezhdu Triaenophorus nodulosus (Cestoda) i ego hozyaevami - rybami [Physiological
specificity of the relationship between Triaenophorus nodulosus (Cestoda) and its hosts - fish]. Parazitologiya, 35(1), 60-68 (in Russian).
Kennedy, C. R (1975). Ecological animal parasitology. Blackwell Scientific Publications, Oxford.
Khidr, A.-A A., Said, A. E, Samak, O. A. A, & Sheref, S. E. A. (2012). The impacts of ecological factors on prevalence, mean intensity and seasonal changes of the monogenean gill parasite, Microcotyloides sp., infesting the Tera-pon puta fish inhabiting coastal region of Mediterranean Sea at Damietta region. The Journal of Basic and Applied Zoology, 65(2), 109-115.
Kondo, Y., Ohtsuka, S., Hirabayashi, T., Okada, S., Ogawa, N. O., Ohkouchi, N., Shimazu, T., & Nishikawa, J. (2016). Seasonal changes in infection with trematode species utilizing jellyfish as hosts: Evidence of transmission to definitive host fish via medusivory. Parasite, 23, 16.
Lamkova, K., Simkova, A., Palikova, M., Jurajda, P., & Lojek, A. (2007). Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cep-halus), a freshwater cyprinid fish. Parasitology Research, 101(3), 775-789.
Lyubarskaya, O. D. (1968). Parazitofauna molodi promyslovyh ryb Volzhskogo otroga Kujbyshevskogo vodohranilishcha [Parasitic fauna of juvenile commercial fish of the Volga spur of the Kuibyshev reservoir]. Voprosy Parazitologii, Uchenye Zapiski Kazanskogo Universiteta, 126(3), 49-99 (in Russian).
Malahova, R. P. (1961). Sezonnye izmeneniya parazitofauny nektoroyh presno-vodnyh ryb ozer Karelii (Konchezero) [Seasonal changes in the parasite fauna of some freshwater fish in the lakes of Karelia (Konchezero)]. Voprosy Parazitologii Karelli, 30, 55-78 (in Russian).
Mehgarran, E. H. (1992). Ehkologicheskoe raznoobrazie i ego izmerenie [Ecological diversity and its measurement]. Mir, Moscow (in Russian).
Mitenev, V. K. (1998). Parazitofauna shchuki Esox lucius L. vodoemov Kol'skogo Severa [Parasite fauna of pike Esox lucius L. in the Kola North water bodies]. In: Karasev, A. B. (Ed.). Parazity i bolezni morskih i presnovodnyh ryb Severnogo bassejna. Izdatel'stvo Polyarnogo Nauchno-Issledovatel'skogo Instituta Mors-kogo Rybnogo Hozyajstva i Okeanografii, Murmansk. Pp. 88-96 (in Russian).
Moravec, F. (1970). On the life history of the nematode Raphidascaris acus (Bloch, 1779) in the natural environment of the River Bystfice, Czechoslovakia. Journal of Fish Biology, 2, 313-322.
Movsesyan, S. O. (Ed.) Sistematika i ehkologiya parazitov [Systematics and ecology of parasites]. KMK, Moscow (in Russian).
Ozturk, M. O., Oguz, M. C., & Altunel, F. N. (2000). Metazoan parasites of pike (Esox lucius L.) from Lake Uluabat, Turkey. Israel Journal of Zoology, 46(2), 119-130.
Pel'gunov, A. N. (2012). Problemy opistorhoza i difillobotrioza v Nizhnem techenii Irtysha [Problems of opisthorchiasis and diphyllobothriasis in the lower reaches of the Irtysh]. Rossijskij Parazitologicheskij Zhurnal, 3, 68-73 (in Russian).
Petrushevskij, G. K., Mosevich, M. V., & Shchupakov, I. G. (1948). Fauna parazitov Obi i Irtysha [Fauna of the parasites of the Ob and the Irtysh]. Izvestiya Vsesoyuznogo Nauchno-Issledovatel'skogo Instituta Ozernogo i Rechnogo Rybnogo Hozyajstva, 27, 67-97 (in Russian).
Platonov, T. A., Kuz'mina, N. V., Nyukkanov, A. N., & Protod'yakonova, G. P. (2018). Parazitofauna ryb srednego techeniya reki Leny i ee pritokov v uslo-viyah vozrastayushchej tekhnogennoj nagruzki [Parasitic fauna of fish in the middle course of the Lena River and its tributaries under increasing man-made pressure]. Vestnik Rossijskogo Universiteta Druzhby Narodov, Seriya Ehkologiya i Bezopasnost' Zhiznedeyatel'nosti, 26(2), 185-194 (in Russian).
Polyanskij, Y. I., & Shul'man, S. S. (1956). Vozrastnye izmeneniya parazitofauny ryb [Age-related changes in the fish parasite fauna]. In: Lutta, A. S., Polyans-kij, Y. I., & Zaks, M. G. (Eds.). Trudy Karelo-Finskogo Filiala Akademii Nauk SSSR. Gosudarstvennoe Izdanie Karelo-Finskoj SSR, Petrozavodsk. Pp. 3-26 (in Russian).
Pospekhov, V. V., Atrashkevich, G. I., & Orlovskaya, O. M. (2010). Parazity ryb bassejna reki Gizhiga (Severnoe poberezh'e Ohotskogo morya) [Parasites of fish in the Gizhiga river basin (Northern coast of the Sea of Okhotsk)]. Izves-tiya Tihookeanskogo Nauchno-Issledovatel'skogo Rybohozyajstvennogo Centra, 163, 365-378 (in Russian).
Pravdin, I. F. (1966). Rukovodstvo po izucheniyu ryb (preimushchestvenno presnovodnyh) [Guidelines for the study of fish (mostly freshwater)]. Pishchevaya promyshlennost, Moscow (in Russian).
Pronina, S. V., & Pronin, N. M. (1988). Vzaimootnosheniya v sistemah gel'minty -ryby (na tkanevom, organnom i organizmennom urovnyah) [Relationships in helminths systems - fish (at the tissue, organ and organism levels)]. Nauka, Moscow (in Russian).
Pugachev, O. I. (1984). Parazity presnovodnyh ryb severo-vostoka Azii [Parasites of freshwater fish in Northeast Asia]. Izdatelstvo Zoologicheskogo Instituta Akademii Nauk SSSR, Leningrad (in Russian).
Rusinek, O. T. (2007). Parazity ryb ozera Bajkal (fauna, soobshchestva, zoogeografiya, istoriya formirovaniya) [Parasites of fish of Lake Baikal (fauna, communities, zoogeography, history offormation)]. KMK, Moscow (in Russian).
Shabunov, A. A., & Radchenko, N. M. (2012). Parazity ryb, zemnovodnyh i chaj-kovyh ptic v ehkosisitemah krupnyh vodoemov Vologodskoj oblasti [Parasites of fish, amphibians and gulls in the ecosystems of large reservoirs of the
Vologda region]. Vologodskij Gosudarstvennyj Tekhnicheskij Universitet, Vologda (in Russian). Shul'man, S. S., Malahova, R. N., & Rybak, V. F. (1974). Sravnitel'no-ehkologi-cheskij analiz parazitov ryb ozer Karelii [A comparative ecological analysis of the parasites of the fish ofthe lakes of Karelia]. Nauka Moscow (in Russian). Skarlato, O. A. (Ed.). (1984). Opredelitel' parazitov presnovodnyh ryb fauny SSSR. Paraziticheskie prostejshie [The identification guide to parasites of freshwater fish of the USSR. Parasitic Protozoa]. Nauka, Leningrad (in Russian). Skarlato, O. A. (Ed.). (1985). Opredelitel' parazitov presnovodnyh ryb fauny SSSR. Paraziticheskie mnogokletochnye [The identification guide to parasites of freshwater fish ofthe USSR. Parasitic Metazoa]. Nauka, Leningrad (in Russian). Skarlato, O. A. (Ed.). (1987). Opredelitel' parazitov presnovodnyh ryb fauny SSSR. Paraziticheskie mnogokletochnye [The identification guide to parasites of
freshwater fish fauna of the USSR. Parasitic Metazoa]. Nauka, Leningrad (in Russian).
Titova, S. D. (1965). Parazity ryb Zapadnoj Sibiri [Parasites of fishes of Western Siberia]. Tomsk (in Russian).
Vysockaya, R. U., Krupnova, M. Y., & Ieshko, E. P. (2015). Ehkologo-biohimiches-kie aspekty parazitohozyainnyh otnoshenij v transformirovannyh vodoemah (na primere cestody Triaenophorus nodulosus i ee hozyaina shchuki obyknovennoj Esox lucius) [Ecological and biochemical aspects of parasite-host interactions in transformed aquatic bodies: A case study of the cestode Triaenophorus nodulosus and its host, the northern pike Esox lucius]. Izvestiya Rossijskoj Akademii Nauk, Seriya Biologicheskaya, 42(3), 302-309 (in Russian).
Watson, R. A., & Dic, T. A (1980). Metazoan parasites of pike, Esox lucius Linnaeus, from Southern Indian Lake, Manitoba, Canada. Journal of Fish Biology, 17, 255-261.
