Olesya Yu. Busarova, Associate Professor, Far Eastern State Technical Fisheries University (690087, Russia, Vladivostok, Lugovaya, 52b); е-mail:
Maksim V. Koval, Head of Lab., Kamchatka Branch of All-Russian Research Institute of Fishery and Oceanography (683000, Russia, Petropavlovsk-Kamchatskiy, Naberezhnaya 18); e-mail:
Evgeny V. Esin, Researcher, Kronotsky State Nature Biosphere Reserve (684000, Russia, Kamchatsky Krai, Yelizovo, Ryabikova Street 48); e-mail:
Grigorii N. Markevich, Researcher, Kronotsky State Nature Biosphere Reserve (684000, Russia, Kamchatsky Krai, Yelizovo, Ryabikova Street 48); e-mail:

Reference to article

Busarova O.Yu., Koval M.V., Esin E.V., Markevich G.N. 2019. Trophic segregation in multispecies community of salmonids in the Penzhina River lower course (Kamchatsky Krai, Russia). Nature Conservation Research 4(2): 83–94.

Section Resarch articles

Trophic relationships are presented for the juveniles of Coregonus sardinella, C. subautumnalis, C. pidschian, Prosopium cylindraceum, and Thymallus arcticus mertensii jointly inhabiting the Penzhina River lower reaches in summer. This community has no analogues in the North-Okhotsk region in terms of freshwater salmonid diversity. We analysed the stomachs content, indicative parasites infestation and stable isotopes ratio in the muscles. We demonstrated the similarity of food niches for the following pairs of species P. cylindraceumT. а. mertensii and C. sardinellaC. subautumnalis. The summer diet of the species pair P. cylindraceumT. а. mertensii mainly consisted of chironomid larvae. At the same time, mysids dominated in the diet of the species pair C. sardinellaC. subautumnalis. Coregonus pidschian mainly fed on gammarids. The following parasites have been found in juvenile fishes: Chloromyxum tuberculatum, Myxobolus spр., Proteocephalus longicollis, Triaenophorus nodulosus, Diplostomum sp., Metecercaria spp., Pronoprymna petrowi, Cystidicola farionis, Salmonema ephemeridarum, Raphidascaris acus, Pseudocapillaria salvelini, Echinorhynchus cotti, and Salmincola extensus; herewith, the intensity of invasion was low for all parasites. Only T. а. mertensii has been infested by C. tuberculatum, T. nodulosus, and C. farionis. Only C. pidschian was infested by P. longicollis. Only C. sardinella and C. subautumnalis have been infested by P. petrowi, while Salmincola extensus has infested only P. cylindraceum in the studied ecosystem. Thymallus arcticus mertensii and C. pidschian are significantly different from other fish species in term of infestation by the helminths E. сotti and P. salvelini. In the δ 13С–15N isotopes space, the fish juveniles formed three groups: 1) with high 15N level (C. sardinellaC. subautumnalis), 2) with low 13С level (C. pidschian), and 3) with low 15N – high 13С level (P. cylindraceumT. а. mertensii). The complexity of trophic relationships of juvenile salmonids in the River Penzhina and an increased feeding competition in the species pairs threaten the functioning of the unique River Penzhina salmonid community under the conditions of extreme fishing pressure in the Northern Far East.


feeding, feeding competition, grayling, parasite fauna, stable isotope ratio, trophic differentiation, whitefishes

Artice information

Received: 17.01.2019. Revised: 15.03.2019. Accepted: 19.03.2019.

The full text of the article

Amundsen P.A., Gabler H.M., Staldvik F.J. 1996. A new approach to graphical analyses of feeding strategy from stomach contents data – modification of the Costello (1990) method. Journal of Fish Biology 48(4): 607–614. DOI: 10,1111/1095-8649.1996.tb01455.x
Anikieva L.B., Malakhova R.P., Ieshko E.P. 1983. Ecological analysis of parasites of coregonid fishes. Leningrad: Nauka. 167 p. [In Russian]
Arismendi I., Soto D., Penaluna B., Jara C.G., Leal C., Leon-Munoz J. 2009. Aquaculture, non-native salmonid invasions and associated declines of native fishes in Northern Patagonian lakes. Freshwater Biology 54(5): 1135–1147. DOI: 10.1111/j.1365-2427.2008.02157.x
Baldina S.N., Gordon N.Yu., Politov D.V. 2008. Genetic differentiation of muksun Coregonus muksun (Pallas) and related species of whitefish (Coregonidae, Salmoniformes) of Siberia on mtDNA. Russian Journal of Genetics 44(7): 777–785. DOI: 10.1134/S1022795408070041
Baranova Yu.P., Biske S.F., Goncharov V.F., Kulkova I.A., Titkov A.S. 1968. Cenozoic Era in the North-East of the USSR. Novosibirsk: Nauka. 124 p. [In Russian]
Bauer O.N. (Ed.). 1987. Guide for Identification of the Parasites in the Freshwater Fishes of the USSR. Vol. 3: Parasitic Metazoans (Second Part). Leningrad: Nauka. 583 p. [In Russian]
Black G.A., Lankester M.W. 1980. Migration and development of swim-bladder nematodes, Cystidicola spp. (Habronematoidea), in their definitive hosts. Canadian Journal of Zoology 58(11): 1997–2005. DOI: 10.1139/z80-275
Blanchet S. Loot G., Grenouillet G. 2007. Competitive interactions between native and exotic salmonids: a combined field and laboratory demonstration. Ecology of Freshwater Fish 16(2): 133–143. DOI: 10.1111/j.1600-0633.2006.00205.x
Bykhovskaya-Pavlovskaya I.E. 1985. Fish Parasites: Practical Manual. Leningrad: Nauka. 121 p. [In Russian]
Chasar L.S., Chanton J.P., Glaser P.H., Siegel D.I. 2000. Methane concentration and stable isotope distribution as evidence of rhizospheric processes: Comparison of a fen and bog in the glacial lake Agassiz Peatland complex. Annals of Botany 86(3): 655‑663. DOI: 10.1006/anbo.2000.1172
Chereshnev I.A. 1996. Biological diversity of freshwater ichthyofauna in the North-East of Russia. Vladivostok: Dal'nauka. 197 p. [In Russian]
Chereshnev I.A. 1998. Biogeography of freshwater fish in the Far East of Russia. Vladivostok: Dal'nauka. 130 p. [In Russian]
Chereshnev I.A., Volobuev V.V., Shestakov A.V., Frolov S.V. 2002. Salmonid fish of the North-East of Russia. Vladivostok: Dal'nauka. 496 p. [In Russian]
Elias S.A., Brigham-Grette J. 2013. Late Pleistocene glacial events in Beringia. In: S.A. Elias, C.J. Mock (Eds.): Encyclopedia of Quaternary Science. Amsterdam: Elsevier. P. 191–201. DOI: 10.1016/B798-0-444-53643-3.00116-3
Esin E.V., Chebanova V.V., Leman V.N. 2009. Ecosystem of the small salmon river of Western Kamchatka (habitat, benthic population and fish fauna). Moscow: KMK Scientific Press Ltd. 170 p. [In Russian]
Golubtsov A.S., Cherenkov S.E., Tefera F. 2012. High morphological diversity of the genus Garra in the Sore River (the White Nile Basin, Ethiopia): one more cyprinid species flock? Journal of Ichthyology 52(11): 817–820. DOI: 10.1134/S0032945212110057
Gorin S.L., Koval M.V., Sazonov A.A., Terskiy P.N. 2015. The modern hydrological regime of the lower reaches of the River Penzhina and the first information about the hydrological processes in its estuary (according to the results of the 2014 expedition). The Researches of the Aquatic Biological Resources of Kamchatka and the North-West Part of the Pacific Ocean 37: 33–52. DOI: 10.15853/2072-8212.2015.37.33-52 [In Russian]
Gorin C.L., Romanenko F.A., Koval M.N. 2016. The first information about the winter hydrological regime and the ice cover in the hyper-tidal mouth of the River Penzhina. In: Proceedings of the Fifth All-Russian Conference «Ice and thermal processes on water bodies of Russia» (11–14 October 2016, Vladimir). Vladimir. P. 88–55. [In Russian]
Grey J., Kelly A., Jones R.I. 2004. High intraspecific variability in carbon and nitrogen stable isotope ratios of lake chironomid larvae. Limnology and Oceanography 49(1): 239–244. DOI: 10.4319/lo.2004.49.1.0239
Horn H.S. 1966. Measurement of “overlap" in comparative ecological studies. American Naturalist 100: 419–424. DOI: 10.1086/282436
Ismail G.B., Sampson D.B., Noakes L.G. 2014. The status of Lake Lanao endemic cyprinids (Puntius species) and their conservation. Environmental Biology of Fishes 97(4): 425–434. DOI: 10.1007/s10641-013-0163-1
Juncos R., Milano D., Macchi P.J., Vigliano P.H. 2014. Niche segregation facilitates coexistence between native and introduced fishes in a deep Patagonian lake. Hydrobiologia 747(1): 53‑67. DOI: 10.1007/s10750-014-2122-z
Korsu K., Huusko A., Muotka T. 2010. Invasion of north European streams by brook trout: hostile takeover or preadapted habitat niche segregation? Biological Invasions 12(5): 1363–1375. DOI: 10.107/s10530-099-9553-x
Koval M.V., Esin E.V., Bugaev A.V., Karas V.A., Gorin S.L., Shatilo I.V., Pogodaev E.G., Shubkin S.V., Zavarina L.O., Frolov O.V., Zharavin M.V., Koptev S.V. 2015a. Freshwater ichthyofauna of the Penzhina and Talovka rivers (Northwestern Kamchatka). The Researches of the Aquatic Biological Resources of Kamchatka and the North-West Part of the Pacific Ocean 37: 53–145. DOI: 10/15853/2072-8212.2015.37.53-145 [In Russian]
Koval M.V., Gorin S.L., Bugaev A.V., Frolov O.V., Zharavin M.V. 2015b. Long-term dynamics and current state of commercial fish resources of the Penzhina and Talovka rivers (Northwestern Kamchatka). The Researches of the Aquatic Biological Resources of Kamchatka and the North-West Part of the Pacific Ocean 37: 5–20. DOI: 10.15853/2072-8212.2015.37.146-163 [In Russian]
Koval M.V., Gorin S.L., Kalugin A.A. 2015c. The ecological characteristics of the community of young fish and nektobentos of the hyper-tidal estuary of the Penzhina and Talovka rivers (Northwestern Kamchatka) in August 2014. The Researches of the Aquatic Biological Resources of Kamchatka and the North-West Part of the Pacific Ocean 37: 164–191. DOI: 10.15853/2072-8212.2015.37.164-191 [In Russian]
Koval M.V., Esin E.V., Gorin S.L., Galyamov R.S., Koshel V.E. 2018. Fish Species Diversity, Distribution, and Dispersal in the Rivers of the Penzhina Bay Catchment Area. Journal of Ichthyology 58(6): 795–807. DOI: 10.1134/S0032945218050119
Krylov A.V. (Ed.). 2010. Ecology of Lake Sevan in the period of level increasing. Results of the Russian-Armenian biological expedition hydroecological investigations in Lake Sevan (Armenia) (2005–2009). Moscow: Nauka DRC. 375 p. [in Russian]
Kuperman B.I. 1973. The tapeworms of the genus Triaenophorus are fish parasites. Leningrad: Nauka. 207 p. [In Russian]
Levin B., Simonov E., Dgebuadze Y. 2018. Adaptive radiation of barbs of the genus Labeobarbus (Cyprinidae) in the East African river. BioRxiv: 478990. DOI: 10.1101/478990
Lomakin V.V., Trofimenko V.Ya. 1982. Capillariids (Nematoda: Capillariidae) of freshwater fishes of USSR fauna. Proceedings of the Helminthological Laboratory of the AS USSR 31: 60–80. [In Russian]
Maksimenkov V.V., Maksimenkova T.V. 2016. Nutrition of juveniles of three fish species from the Penzhina and Talovka rivers (Northwestern Kamchatka). In: Biodiversity Conservation of Kamchatka and the adjacent seas (Petropavlovsk-Kamchatsky, 16–17 November 2016). Petropavlovsk-Kamchatsky: Kamchatpress. P. 99–100. [In Russian]
Minagawa M., Wada E. 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between d 15N and animal age. Geochimica et Cosmochimica Acta 48(5): 1135–1140. DOI: 10.1016/0016-7037(84)90204-7
Moravec S. 1970. Studies on the development of Raphidascaris acus (Bloch, 1779) (Nematoda: Heterocheilidae). Vestnik Ceskoslovenske Spolecnosti Zoologicke 34(1): 33–49.
Nagasawa K., Egusa S. 1981. Echinorhynchus cotti Yamaguti, 1935 (Acanthocephala: Echinorhynchidae) in fish of the Kanita River, with a note on the life cycle. Japanese Journal of Parasitology 30: 45–49.
Nosil P. 2012. Ecological speciation. Oxford, UK: Oxford University Press. 304 p.
Okamura B., Gruhl A., Bartholomew J.L. 2015. Myxozoan evolution, ecology and development. Switzerland: Springer International Publisher. 441 р. DOI: 10.1007/978-3-319-14753-6
Owens N.J.P. 1988. Natural variations in δ15N in the marine environment. Advances in Marine Biology 24: 389–451. DOI: 10.1016/S0065-2881(08)60077-2
Peterson B.J., Fry B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology Systematics 18(1): 293–320. DOI: 10.1146/annurev.ecolsys.18.1.293
Piálek L., Ríčan O., Casciotta J., Almirón A., Zrzavý J. 2011. Multilocus phylogeny of Crencicichla (Teleostei: Cichlidae), with biogeography of the C. lacustris group: species flocks as a model for sympatric speciation in rivers. Molecular Phylogeny and Evolution 62(1): 46–61. DOI: 10.1016/j.ympev.2011.09.006
Pugachev O.N. 2003. Checklist of the Freshwater Fish Parasites of the Northern Asia. Trematoda. Proceedings of the Zoological Institute RAS 298: 1–224. [In Russian]
Roitman V.A., Lobanov A.L. 1985. A method for estimating parasite hemopopulation numbers in host population. Proceedings of the Helminthological Laboratory of the AS USSR 23: 102–123. [in Russian]
Schluter D. 2000. The ecology of adaptive radiation. New York: Oxford University Press. 300 p.
Shorygin A.A. 1952. Food and nutritional relationships of fish in the Caspian Sea. Moscow: Pishchepromizdat. 268 p. [In Russian]
Schulman S.S. (Ed.). 1984. Guide for Identification of Freshwater Fishes in Fauna of the Soviet Union. Vol. 1: Parasitic Protozoa. Leningrad: Nauka. 428 p. [In Russian]
Sudarikov V.E., Shigin A.A., Kurochkin Yu.V., Lomakin V.V., Stenko R.P., Yurlova N.I. 2002. Trematode Metacercariae are parasites of freshwater hydrobionts of Central Russia. Vol. 1. Moscow: Nauka. 297 p. [In Russian]
Sullivan J.P., Lavoué S., Hopkins C.D. 2002. Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei). Evolution 56(3): 597–616. DOI: 10.1554/0014-3820(2002)056[0597;DAPAOA]2.0.CO;2
Tokranov A.M. (Ed.). 2018. Red Data Book of Kamchatsky Krai. Vol. 1 Animals. Petropavlovsk-Kamchatsky: Kamchatpress Publishing House. 196 р. [In Russian]
Tronstad L.M., Hall R.O., Koel T.M. 2010. Introduced lake trout produced a four-level trophic cascade in Yellowstone Lake. Transactions of the American Fisheries Society 139(5): 1536–1550. DOI: 10.1577/T09-151.1