Infestation of Black Sea-Caspian Sprat (Clupeonella Cultriventris) with Cestodes of the Genus Proteocephalus in the Kama Reservoir and Histological Examination of Fish Intestines Infested with These Parasites

Introduction. The Black Sea-Caspian sprat (Clupeonella cultriventris) is an alien species adapted to the Kama Reservoir conditions, capable of affecting the trophic relationships in this ecosystem. However, the composition of helminth fauna in this ecosystem and the pathological changes induced by the certain pathogens, such as cestodes of the genus Proteocephalus, are currently poorly investigated. The aim of the study is to investigate the infestation of C. cultriventris with cestodes of the genus Proteocephalus in the Kama Reservoir and to describe the histological changes in the fish intestines caused by this infestation.
Materials and Methods. In the autumn-winter period of 2024, the C. cultriventris (n=83) were taken from the several parts of the Kama Reservoir. A partial biological analysis, partial helminthological dissection and histological examination of the intestines infested with cestodes were carried out. Parasitological examination was performed at the Department of Infectious Diseases of Perm State Agro-Technological University. Preparation of histological specimens was performed in the histopathology laboratory of Perm Regional Children’s Clinical Hospital. The prepared histological sections were scanned using the Vision Assist automated system and Vision microscopy automation software. Mathematical processing of the obtained data was performed in Microsoft Excel.
Results. The highest infestation extensity (IE 50%) of Proteocephalus sp. (juv) corresponding to infestation intensity (II) range 1–2 was observed in sprat form the middle part of the Kama Reservoir; in sprat from the upper part, it was several times less (IE 13% corresponding to II range 1–3); sprat from the lower part was not infested at all. The size and weight parameters in sprat from the upper and lower parts of the Reservoir were significantly higher than that in the fish from the middle part — approximately 2 times exceedance in weight and 1.2 times — in length. Histological examination of sprat intestines revealed changes in mucosa and submucosa layers; the epithelium was in a state of desquamation, the stromal state of the villi was loose and edematous.
Discussion and Conclusions. Data on infestation of C. cultriventris with the cestodes of the genus Proteocephalus sp. in the Kama Reservoir are presented for the first time. It has been revealed that cestode infestation affects the biological parameters of fish and causes minor inflammatory pathological changes in the intestines. Detection of the pre-mature cestodes in the non-specific hosts is not enough factor for their identification, therefore, further research is needed to clarify the host-parasite relationships of C. cultriventris and Proteocephalus sp.

1. Karabanov DP, Pavlov DD, Dgebuadze YuYu, Bazarov MI, Borovikova EA, Gerasimov YV, et al. Dataset of Non-Indigenous and Native Fish of the Volga and Kama Rivers (European Russia). Data. 2023;8(10):154. https://doi.org/10.3390/data8100154

2. Osipov VV, Dgebuadze YY. Variability of Black and Caspian Sea Sprat Clupeonella Cultriventris (Clupeidae) Growth in the Contemporary Range. Journal of Ichthyology. 2016;56(5):767–774. https://doi.org/10.1134/S003294521605009Х

3. Shakirova FM, Govorkova LK, Anokhina OK. Modern State of Niznekamsky Reservoir and Possibility Rational Development of It’s Fishery Resources. Izvestia of Samara Scientific Center of the Russian Academy of Sciences. 2013;15(3–1):518–527. (In Russ.)

4. Kazarinov SN, Merzlyakov IN, Ponosov SV, Komarova LV. Species Composition and Distribution Features of the Ichthyofauna of the Kama Reservoir. Vestnik Permskogo universiteta. Biologija. 2021;(1):39–52. (In Russ.) https://doi.org/10.17072/1994-9952-2021-1-39-52

5. Tyutin AV, Medyantseva EN, Bazarov MI, Tyutin VA. Distribution Patterns of Metacercariae of the Trematoda Apophallus Muehlingi (Jagerskiold, 1899) in Underyearlings in an Invasive Population of Clupeonella Cultriventris (Nordmann, 1840) from the Gorky Reservoir (Upper Volga Basin). Russian Journal of Biological Invasions. 2022;15(4):80–96. (In Russ.) https://doi.org/10.35885/1996-1499-15-4-80-96

6. Zhokhov AE, Pugacheva MN, Molodozhnikova NM, Berechikidze IA. Alien Parasite Species of the Fish in the Volga River Basin: A Review of Data on the Species Number and Distribution. Russian Journal of Biological Invasions. 2019;10(2):136–152. https://doi.org/10.1134/S2075111719020140

7. Rubanova MV, Mukhortova OV. Ecological Aspects of Changes in the Fauna of Multicellular Parasites of Perch (Perca Fluviatilis Linnaeus, 1758) in a Tributary of the Kuibyshev Reservoir. Biosphere. 2024;16(2):223–234. (In Russ.) http://doi.org/10.24855/biosfera.v16i2.922

8. Voronina EA. Monitoring of Infections and Invasions of Caspian Kilka. Trudy VNIRO. 2016;162:28–35 (In Russ.)

9. Voykina AV, Bugayov LA, Bortnikov ES, Ruzhinskaya LP, Tsyibulskaya MA, Sergeeva SG, et al. Physiological and parasitological status of the tyulka sprat (Clupeonella Cultriventris) of the Sea of Azov in 2018. Ecology Economy Informatics. Geoinformation Technologies and Space Monitoring. 2019;4:202–207. (In Russ.) https://doi.org/10.23885/2500-123X-2019-2-4-202-207

10. Plaksina MP. Fauna and Ecology of Helminth Communities of Pelagic and Bottom-Pelagic Fish of The Crimean Coast (Black and Azov Seas). Diss. Cand. Sci. (Biology). St. Petersburg; 2022. 314 p. (In Russ.)

11. Abdybekova AM, Abdibayeva AA, Popov NN, Zhaksylykova AA, Barbol BI, Bozhbanov BZh, et al. Helminth Parasites of Fish of the Kazakhstan Sector of the Caspian Sea and Associated Drainage Basin. Helminthologia. 2020;57(3):241–251. https://doi.org/10.2478/helm-2020-0030

12. Hajipour N, Valizadeh H, Ketzis J. A Review on Fish-Borne Zoonotic Parasites in Iran. Veterinary Medicinand Science. 2023;9(2):748–777. https://doi.org/10.1002/vms3.981

13. Tyutin AV, Verbitsky VB, Verbitskaya TI, Medyantseva EN. Parasites of Alien Aquatic Animals in the Upper Volga Basin. Russian Journal of Biological Invasions. 2013;4(1):54–59. https://doi.org/10.1134/S2075111713010098

14. Trofimov DYu, Zabotkina EA. Effect of Trypanosome Infection on Hematological Parameters of the Black Sea Sprat (Clupeonella Cultriventris) from the Ivankovo Reservoir. Inland Water Biology. 2024;17(2):354–357. (In Russ.) https://doi.org/10.31857/S0320965224020147

15. Fedorova NN, Voronina EA, Dubovskaya AV, Altufyeva NS. Morphological Changes in Internal Organs of Caspian Sardelle (Clupeonella Cultriventris Caspia). Vestnik of Astrakhan State Technical University. Series: Fishing Industry. 2014;(1):84–88. (In Russ.)

16. Pravdin IF. A Guide to the Study of Fish (Mainly Freshwater). Moscow: Pishchevaya promyshlennost; 1966. 376 p. (In Russ.)

17. Bykhovskaya-Pavlovskaya IE. Fish Parasites: A Study Guide. Leningrad: Nauka: Leningrad Branch; 1985. 123 p. (In Russ.)

18. Identifier of Parasites of Freshwater Fish of the USSR Fauna. Vol. 3. Parasitic Multicellular, Part 2. Leningrad: Nauka: Leningrad Branch; 1987. 583 p. (In Russ.)

19. Kurovskaya LY. Influence of the Cestode Bothriocephalus Acheilognathi on Morphological and Physiological Characteristics of Carps Reared in Warm Water. Parazitologiya (Parasitology). 2001;35(3):249–256. (In Russ.)

20. Frolova TV, Izvekova GI. A Comparative Analysis of the Effect of Intestinal Cestodes in Different Fish Species on Activity of Proteolytic Enzymes. Journal of Evolutionary Biochemistry and Physiology. 2022;58(3):188–195. (In Russ.) https://doi.org/10.31857/S0044452922030032

21. Scholz T. Life Cycles of Species of Proteocephalus, Parasites of Fishes in the Palearctic Region: A Review. Journal of Helminthology. 1999;73(1):1–19. https://doi.org/10.1017/S0022149X99000013

22. Scholz T, Kuchta R, Oros M. Tapeworms as Pathogens of Fish: A review. Journal of Fish Diseases. 2021;44(12):1883–1900. https://doi.org/10.1111/jfd.13526

23. Hamoudа AH, Younis AE. Two Proteocephalid Cestodes in the Fish Malapterurus Electricus and Heterobranchus Bidorsalis from Lake Nasser, Egypt: A Morphological, Molecular, And Histopathological Study. BMC Veterinary Research. 2024;20(1):213. https://doi.org/10.1186/s12917-024-04048-1

24. Kosareva NA. On the Parasite Fauna of Fishes of the Volga-Don Canal Named after Lenin. In: Proceedings of the All-Union Conference on the Biological Foundations of Fisheries Development of Reservoirs (Leningrad, November 24–29, 1958). Moscow; Leningrad: Publishing House of the USSR Academy of Sciences [Leningrad Branch]; 1961. P. 178–181. (In Russ.)

25. Tyutin АV. Comparative Analysis of Parasite Fauna for Two Pelagic Fish Invaders in the Rybinsk Reservoir. Inland Water Biology. 2003;(2):86–91. (In Russ.)

26. Tyutin AV. New Examples of Parasites Exchanges Between Alien and Aboriginal Fish Species in the Ecosystem of Upper Volga (Russia). Invasion of Alien Species in Holarctic. In: Proceedings of U.S. – Russia Invasive Species Workshop (August 27–31, Institute for Biology of Inland Waters RAS). Borok: Russian Academy of Sciences; 2003. P. 561–565. https://doi.org/10.13140/2.1.2726.8165

27. Anikieva LV. Population Aspect in Study of Morphological Variability of the Cestode Proteocephalus Percae (Cestoda: Proteocephalidea) through the Ontogeny. Trudy Karelskogo nauchnogo tsentra Rossiiskoi akademii nauk (Proceedings of the Karelian Scientific Center of the Russian Academy of Sciences). 2007;(11):3–9. (In Russ.)

28. Anikieva LV. Cestodes of the Genus Proteocephalus (Cestoda: Proteocephalidea) from the European Smelt Osmerus Eperlanus. Parazitologiya (Parasitology). 1998;32(2):134–140. (In Russ.)

29. Anikieva LV, Ieshko EP. Phenotypic Diversity of Population Groupings of Proteocephalus Longicollis (Zeder 1800) (Cestoda: Proteocephalidae), a Parasite of the Whitefish Coregonus Lavaretus (L.). Parazitologia (Parasitology). 2022;56(2):91–107. (In Russ.)

30. Vlasenko PG, Izotova GV, Kashinskaya EN, Shokurova AV, Markevich GN, Soloviev MM. Species Diversity of Cestodes of the Genus Proteocephalus Weinland, 1858 – Parasites of Salmon Fishes of Siberia and the Far East. In: Proceedings of the Russian National Scientific Conference “Salmonoids: Biology, Reproduction, Fisheries” (Murmansk, March 23–24, 2023). Murmansk: PINRO Named after NM Knipovich; 2023. Р. 85–89. (In Russ.)

31. Scholz T, Hanzelova V, Skerıkova A, Shimazu T, Rolbiecki L. An Annotated List of Species of the Proteocephalus Weinland, 1858 Aggregate Sensu De Chambrier Et Al. (2004) (Cestoda: Proteocephalidae), Parasites of Fishes in the Palaearctic Region, Their Phylogenetic Relationships and a Key to Their Identification. Systematic Parasitology. 2007;67(2):139–156. https://doi.org/10.1007/s11230-006-9089-8

32. Mikheeva OI, Mikheev PB. Preliminary Data on Fish Parasite Basin Kama Reservoir. Part 2. Discussion. Izvestia of Samara Scientific Center of the Russian Academy of Sciences. 2014;16(5–1):582–587. (In Russ.)

33. Kostarev GF. Parasites and Diseases of Fish in the Middle Kama Basin (Under Pollution Conditions). Perm: Perm University Publishing House; 2003. 194 p. (In Russ.)

34. Anikieva LV. Variability and Phenotypic Structure of Proteocephalus Torulosus (Cestoda: Proteocephalidea) — A Parasite of Cyprinid Fishes. Parazitologiya (Parasitology). 2004;38(2):171–179. (In Russ.)

35. Anikieva LV, Lebedeva DI. Phenotypic Diversity and Hostal Variability of Proteocephalus Longicollis (Zeder 1800) (Cestoda, Proteocephalidae), a Parasite of Salmoniformes Fishes of Siberia. Zoologicheskii zhurnal (Zoological Journal). 2023;102(8):843–851. (In Russ.) https://doi.org/10.31857/S0044513423070036

36. Azadikhah D, Nekuie Fard A, Seidgar M, Amin H. The Infection Rate and Pathologic Lesions Induced by Proteocephalus Osculates (Goeze, 1782) in European Catfish (Silurus Glanis) from North-West of Iran. Bulletin of Environment, Pharmacology and Life Sciences. 2014;(3):63–68.