Sexual and age characteristics of the parasitofauna of Abramis brama (Cypriniformes, Cyprinidae) of the Lower Irtysh (Russia)
AbstractIn the present study, an evaluation was made of the dependence between infections by various types of parasites and the sex and age of the host. The parasitic community of Abramis brama includes 24 species of parasites. We assessed the degree of infestation by parasites in groups of male, female and juvenile specimens. It was established that only male bream were infested with Zschokkella nova (Klokacewa, 1914), Hysteromorpha triloba (Rudolphi, 1819), Allocreadium isoporum (Looss, 1894), Ichthyocotylurus platycephalus (Сrерlin, 1852). The ciliates of Trichodina nigra (Lom, 1960) were noted on the gills and fins of all the examined fish, the extensiveness of infection in the group of juveniles exceeded that of the groups of females and males. Specimens of Myxobolus rotundus (Nemeczek, 1911) were found on the gills and in the kidneys, and M. parviformis only on the gills of the fish. The level of infection in males was three times the EI in females and juvenile fish. The infestation on the fins by the metacercaria of Rhipidocotyle campanula (Dujardin, 1845) in male bream was more than 6 times higher than infection in females and juveniles. An increase in the extensiveness of infection in males by the nematode Philometra ovata (Zeder, 1803) was also noted in comparison with groups of females and juvenile fish. Species-specific monogeneans: Dactylogyrus falcatus (Wedl, 1857), D. wunderi (Bychowsky, 1931), D. zandti (Bychowsky, 1933), Gyrodactylus elegans (Nordmann, 1832); the trematodes Sphaerostomа bramae (Müller, 1776) and Diplostomum chromatophorum (Brown, 1931) infested all individuals of bream in approximately the same proportion, whereas an increase in the EI of the Caryophyllaeus laticeps (Pallas, 1781) cestode in males was observed. Infection with metacercariae Metorchis sp. in males exceeded that in females and juvenile fish. At the same time, only females and juvenile bream were infected by Chilodonella sp., metacercariae Opisthorchis felineus (Rivolta, 1884) and glochidia Unionidae gen. sp. During the studies in females, the following species of parasite were observed singly : Proteocephalus sp., Azygia lucii (Miiller, 1776), Ergasilus sieboldi (Nordmann, 1832). Parasitization by Raphidascaris acus (Bloch, 1779) was recorded only in males and juveniles, whereas in females this parasite was not observed. The dominant parasite in males was G. elegans, in females – the representatives of the genus Dactylogyrus, in the juvenile individuals the trematode S. bramae dominated. Analysis of the parasite fauna in various age groups allowed us to establish that at the age of 5+–6+ bream were infected by 20 species of parasites, in age group 3+–4+ there were 15 species, at the age of 7+–8+ the fish were infected only with 11 parasitic species. The fish in all three groups were infected by T. nigra, Dactylogyrus spp., G. elegans, D. chromatophorum, S. bramae, R. acus almost at the same level and had no sharp differences in extensiveness and abundance of infection. Unionidae gen. sp. were observed only in group 3+–4+. Parasitization by Proteocephalus sp., metacercariae H. triloba and I. platycephalus, A. isoporum, and A. lucii was found in bream of age group 5+–6+, the species did not occur in bream at other ages. Nematode P. ovata and crustacean E. sieboldi infested the fish in age groups 3+–4+ and 5+–6+ with a slight increase in the extensiveness of infection at low abundance rates. The same age groups were observed to have decrease in the extensiveness of infection with Chilodonella sp. and metacercariae O. felineus. Myxozoan Z. nova parasitized in age group 5+–6+ and had an increase in extensiveness in age group 7+–8+. In all groups, infection was noted by representatives of the genus Myxobolus, R. campanula and Metorchis sp. with EI increasing with age. The obligate parasite of bream – C. laticeps infested fish the most in age group 3+–4+ in comparison with age groups 5+–6+ and 7+–8+. In the younger age group, the dactylogyruses were dominant parasites, in the age group 5+–6+ Gyrodactylus dominated, in the older age group – Metorchis sp.
Agapova, A. I. (1958). Osobennosti parazitofauny ryb, akklimatizirovannyh v vodoemah Kazahstana [Features of the parasite fauna of fish acclimatized in the water bodies of Kazakhstan]. Trudy Instituta Zoologii, Akademii Nauk Kazahskoj SSR, 9, 25–31 (in Russian).
Agapova, A. I. (1966). Parazity ryb vodoemov Kazahstana [Parasites of fishes of reservoirs of Kazakhstan]. Nauka, Alma-Ata (in Russian).
Byhovskaya-Pavlovskaya, I. E. (1985). Parazity ryb. Rukovodstvo po izucheniiyu [Fish parasites. Study Guide]. Nauka, Leningrad (in Russian).
Chunchukova, M., Kirin, D., Kuzmanova, D., & Shukerova, S. (2017). Accumulation of lead in Abramis brama and its parasite pomphorhynchus tereticollis from Danube river (Vetren area), Bulgaria. Scientific Papers-Series D-Animal Science, 60, 327–332.
Diamont, A. (1997). Fish-to-fish transmission of marine myxosporidians. Diseases of Aquatic Organisms, 30, 99–105.
Folstad, I., & Karter, A. J. (1992). Parasites, bright males and the immuno competence handicap. The American Naturalist, 139, 603–622.
Hayatbakhsh, M. R., Khara, H., Movahed, R., Sayadborani, M., Rohi, J. D., Ahmadnezhad, M., Rahbar, M., & Rad, A. S. (2014). Haematological characteristics associated with parasitism in bream, Abramis brama orientalis. Journal of Parasitic Diseases, 38(4), 383–388.
Hayatbakhsh, M., Khara, H., Rahabar, M., & Ahmadnezhad, M. (2011). Parasite infection of bream (Abramis brama orientalis) in the Caspian Sea (Bandar Anzali Coast). International conference on chemical, environmental and biological sciences, Pattaya. Pp. 320–323.
Karasev, S. G. (2008). Ekologiya ryb nizhnego Tobola i nizhnego Irtysha [Ecology of fishes of lower Tobol and lower Irtysh]. Poligrafist, Tobol'sk (in Russian).
Kashkovskij, V. V., Razmashkin, D. A., & Skripchenko, E. G. (1974). Bolezni i parazity ryb rybovodnyh hozyajstv Sibiri i Urala [Diseases and parasites of fish from fish farms in Siberia and the Urals]. Sredneural'skoe Knizhnoe Izdatel'stvo, Sverdlovsk (in Russian).
Kostarev, G. F. (2003). Parazity i bolezni ryb bassejna Srednej Kamy (v usloviyah zagryazneniya) [Parasites and fish diseases in the basin of the Middle Kama (in terms of pollution)]. Izdatel'stvo Permskogo Universiteta, Perm' (in Russian).
Kuderskij, L. A. (2001). Akklimatizaciya ryb v vodoеmah Rossii: Sostoyaniе i puti razvitiya [Acclimatization of fish in the waters of Russia: Condition and ways of development]. Voprosy Rybolovstva, 2(5), 6–85 (in Russian).
Lebedeva, D. I. (2005). Trematody ryb Ladozhskogo ozera. Biogeografiya Karelii [Trematodes of fishes of the Ladoga Lake. Biogeography of Karelia]. Vol. 7. Ieshko, Е. P. (Ed.). Trudy Karel'skogo Nauchnogo Centra RAN. Petrozavodsk (in Russian).
Liberman, E. L., & Voropaeva, E. L. (2018). New data on parasitic fauna of bream Abramis brama (Linnaeus, 1758) of the Lower Irtysh (acquired part of the range). Russian Journal of Biological Invasions, 9(3), 232–236.
Lizama, M., De Los, A. P., Takemoto, R. M., & Pavanelli, G. C. (2006). Influence of host sex and age on infracommunities of metazoan parasites of Prochilodus lineatus (Valenciennes, 1836) (Prochilodontidae) of the Upper Paraná River floodplain, Brazil. Parasite, 12(4), 299–304.
Lymbery, A. J., Morine, M., Kanani, H. G., Beatty, S. J., & Morgan, D. L. (2014). Co-invaders: The effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife, 3(2), 171–177.
Machado, M. H., Pavanelli, G. C., & Takemoto, R. M. (1994). Inﬂuence of hosts sex and size on endoparasitic infra populations of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Parana river, Brazil. Revista Brasileira Parasitologia Veterinaria, 3, 143–148.
Mehgarran, E. H. (1992). Ehkologicheskoe raznoobrazie i ego izmerenie [Ecological diversity and its measurement]. Mir, Moscow (in Russian).
Ottová, E., Simková, A., Jurajda, P., Dávidová, M., Ondračková, M., Pečínková, M., & Gelnar, M. (2005). Sexual ornamentation and parasite infection in males of common bream (Abramis brama): A reflection of immunocompetence status or simple cost of reproduction? Evolutionary Ecology Research, 7, 581–593.
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 usloviyah vozrastayushchej tekhnogennoj nagruzki [Parazitofauna of fish in the middle course of the Lena River and its tributaries under increasing man-made pressure]. Vеstnik Rossijskogo Univеrsitеta Druzhby Narodov, Seriya Ekologiya i Bezopasnost' Zhiznedeyatel'nosti, 26(2), 185–194 (in Russian).
Popov, P. A. (2010). Formirovanie ihtiocenozov i ekologiya promyslovyh ryb vodohranilishch Sibiri [Formation of ichthyocenoses and ecology of commercial fish of Siberian reservoirs]. Geo, Novosibirsk (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).
Rahman, W. A., & Saidin, H. (2011). Relationship between sex and parasite intensity in four freshwater fish species from Tasik Merah, Perak, Peninsular Malaysia. World Journal of Zoology, 6(4), 370–374.
Ranzani-Paiva, M. J. T., Ishikawa, C. M., Campos, B. E. S., & Eiras, A. C. (1997). Haematological characteristics associated with parasitism in Mugil platanus Gunther, from the estuarine region of Cananela, Sao Paulo, Brazil. Revista Brasileira de Zoologia, 14(2), 329–339.
Reshetnikov, Y. S. (Ed.). (2003). Atlas presnovodnyh ryb Rossii [Atlas of freshwater fish of Russia]. Nauka, Moscow (in Russian).
Rueckert, S., Klimpel, S., & Palm, H. W. (2007). Parasite fauna of bream Abramis brama and roach Rutilus rutilus from a man-made waterway and a freshwater habitat in Northern Germany. Diseases of Aquatic Organisms, 74(3), 225–233.
Rumyancev, Е. A. (1975). Vliyanie nekotoryh faktorov na parazitofaunu ryb pri introdukcii v ozera Karelii [The influence of some factors on the parasitic fauna of fish introduced into lakes of Karelia]. Parazitologiya, 9(4), 305–311 (in Russian).
Rusinek, O. T., & Kondratistov, Y. L. (2010). Izuchenie zarazhennosti karpovyh ryb metacerkariyami trematod v ochage opistorxoza (Tajshetskij rajon, Irkutskaya oblast`, Rossiya) [The study of the infection of carp swarms by trematode metacercariae in the focus of opisthorchiasis (Taishet District, Irkutsk Region, Russia)]. Izvestiya Irkutskogo Gosudarstvennogo Universiteta, Seriya Nauki o Zemle, 3(1), 132–142 (in Russian).
Shatunovskij, M. I., Dgebuadze, Y. Y., Bobyrev, A. Е., Sokolova, Е. L., Usatyj, M. A., Krepis, O. I., Usatyj, A. M., & Chebanu, A. S. (2009). Nekotorye zakonomernosti izmenchivosti struktury i dinamiki populyacij leshcha Abramis brama vodoyomov Vostochnoj Еvropy [Some regularities of the variability of the structure and dynamics of the population of bream Abramis brama in water bodies of Eastern Europe]. Voprosy Ihtiologii, 49(4), 495–507 (in Russian).
Sheath, D. J., Williams, C. F., Reading, A. J., & Britton, J. R. (2015). Parasites of non-native freshwater fishes introduced into England and Wales suggest enemy release and parasite acquisition. Biological Invasions, 17(8), 2235–2246.
Skarlato, O. A. (Ed.). (1984). Opredelitel' parazitov presnovodnyh ryb fauny SSSR. Paraziticheskie prostejshie [The determinant of 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 determinant of parasites of freshwater fish of the USSR. Parasitic Metazoa]. Nauka, Leningrad (in Russian).
Skarlato, O. A. (Ed.). (1987). Opredelitel' parazitov presnovodnyh ryb fauny SSSR. Paraziticheskie mnogokletochnye [The determinant of parasites of freshwater fish fauna of the USSR. Parasitic Metazoa]. Nauka, Leningrad (in Russian).
Sokolov, S. G., Reshetnikov, A. N., Protasova, E. N., & Voropaeva, E. L. (2017). New data on alien species of parasites and hosts in the ecosystem of lake Glubokoe (Moscow oblast, Russia). Russian Journal of Biological Invasions, 8(1), 108–114.
Sous', S. M. (1975). Fauna parazitov ryb ozer i prudov yuga Zapadnoj Sibiri [The fauna of parasites of fishes of lakes and ponds of the south of Western Siberia]. In: Ryzhikov, K. M. (Ed.). Parazity v prirodnyh kompleksah Severnoj Kulundy [Parasites in the natural complexes of North Kulunda]. Nauka, Novosibirsk. Pp. 183–196 (in Russian).
Sous', S. M., & Rostovcev, A. A. (2006). Parazity ryb Novosibirskoj oblasti [Parasites of fishes of the Novosibirsk region]. Gosrybcentr, Tyumen' (in Russian).
Sudarikov, V. Е., & Shigin, A. A., Kurochkin, Y. V., Lomakin, V. V., Sten'ko, R. P., & Yurlova, N. I. (2002). Metacerkarii trematod – parazity presnovodnyh gidrobiontov Central'noj Rossii [Trematode metacercariae – parasites of freshwater hydrobionts of Central Russia]. Nauka, Moscow (in Russian).
Supryaga, V. G., & Mozgovoj, A. A. (1974). Biologicheskie osobennosti Raphidascaris acus (Anisakidae: Ascaridata) – parazita presnovodnyh ryb [Biological features of Rafidaskaris asus (Anisakidae: Ascarridat) – freshwater swarm parasite]. Parazitologiya, 8(6), 494–503 (in Russian).
Taskinen, J., Valtonen, E. T., & Mäkelä, T. (1994). Quantity of sporocysts and seasonality of two Rhipidocotyle species (Digenea: Bucephalidae) in Anodonta piscinalis (Mollusca: Bivalvia). International Journal for Parasitology, 24(6), 877–886.
Tkachev, V. A. (1998). K izucheniyu parazitofauny ryb ozera Turgoyak [To study the parazitofauna of the fish of the lake Turgoyak]. Izvestiya Chelyabinskogo Nauchnogo Centra UrO RAN, 1, 161–170 (in Russian).
Tyutyaev, P. Y. (2008). Neorganicheskij sostav obolochki miksosporidij Henneguya oviperda (Cohn, 1895) i Myxobolus pseudodispar (Gorbunova, 1936) (Myxozoa) [The inorganic composition of the shell of myxospores Henneguya oviperda (Cohn, 1895) and Myxobolus pseudodispar (Gorbunova, 1936) (Myxozoa)]. Citologiya, 50(1), 83–87 (in Russian).