Abstract
Based on data from 1997–2019, morphology, growth, feeding, reproduction and early development of Arctic charr from Lake Tokko (Olekma basin, northern Transbaikalia) were studied. Three charr forms, large, small and dwarf differing in growth rate were recorded in the lake. During the last years, the large form disappeared, the small form became rare and the dwarf form became highly abundant; the proportion of old small and dwarf charr sharply decreased. The dwarf form differs in morphology from the small and large forms, which are morphologically similar. In the summer period of 1997–2001, the large form fed on fish, the small form fed mainly on amphibious insects (chironomid pupae), and the dwarf form fed on amphibious insects and benthos. Presently the small form transited to piscivorous and the dwarf form to predominantly planktivorous feeding. The dwarf form spawns from late July to mid-August at stony sites of underwater shore slope when water temperature is 5.0–6.5°С; laid eggs develop till late November–early December at water temperature decreasing to 3.0–3.5°С. According to data needing verification, the small form spawns in late autumn, but some individuals spawn in summer at the same time as the dwarf form. The results suggest substantial, though incomplete reproductive isolation between the dwarf and the small forms. It is supposed that nowadays the degree of their introgressive hybridization has increased following anthropogenic changes in population structure.
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REFERENCES
Adams, C.E., Does the underlying nature of polymorphism in the Arctic charr differ across the species? Proc. Eighth and Ninth ISACF Workshops on Arctic Char, Kircheis, F.W., Ed., ISACF Inform. Ser. no. 7, Orono: Univ. Maine Print. Off., 1999, pp. 61–69.
Adams, C.E., Fraser, D., Huntingford, F.A., et al., Trophic polymorphism amongst Arctic charr from Loch Rannoch, Scotland, J. Fish Biol., 1998, vol. 52, pp. 1259–1271. https://doi.org/10.1111/j.1095-8649.1998.tb00970.x
Alekseyev, S.S., Age and growth of sympatric and allopatric groups of Arctic charr Salvelinus alpinus complex in Transbaikalia, Tr. Kafedry Zool. Pozvonochnykh, Irkutsk. Gos. Univ., 2001, vol. 1, pp. 66–90.
Alekseyev, S.S. and Kirillov, A. F., The first finding of the Arctic charr Salvelinus alpinus complex in the basin of the Aldan River, and its significance for understanding the history of charr dispersal in Eastern Siberia, J. Ichthyol., 2001, vol. 41, no. 7, pp. 499–514.
Alekseyev, S.S. and Pichugin, M.Yu., A new form of charr Salvelinus alpinus (Salmonidae) from lake Davatchan in Transbaikalia and its morphological differences from sympatric forms, J. Ichthyol., 1998, vol. 38, no. 4, pp. 292–302.
Alekseyev, S.S., Pichugin, M.Yu., and Krysanov, E. Yu., Studies of the Transbaikalia charrs Salvelinus alpinus (Salmonidae) listed in the Red Data Book of the Russian Federation: sympatric forms from Lake Bol’shoi Namarakit (morphology, ecology, karyology), Vopr. Ikhtiol., 1997, vol. 37, no. 5, pp. 588–602.
Alekseyev, S.S., Buldygerov, V.V., Pichugin, M.Yu., and Samusenok, V.P., Distribution of Arctic charr Salvelinus alpinus (Salmonidae) in Transbaikalia, J. Ichthyol., 1999, vol. 39, no. 1, pp. 43–51.
Alekseyev, S.S., Matveev, A.N., Pichugin, M.Yu., et al., Biology of charr Salvelinus alpinus complex (Salmonidae) from lakes at the watershed of rivers Kuanda and Chara (Northern Transbaikalia) and changes in the structure of its populations in connection with anthropogenic impact (1977–1999), Byull. Mosk. O-va Ispyt. Prir., Otd. Biol., 2000a, vol. 105, no. 4, pp. 22–41.
Alekseyev, S.S., Pichugin, M.Yu., and Samusenok, V.P., Diversity of Arctic charrs in meristic characters, their position in the complex of Salvelinus alpinus and the origin of sympatric forms, J. Ichthyol. 2000b, vol. 40, no. 3, pp. 279–297.
Alekseyev, S.S., Samusenok, V.P., Matveev, A.N., et al., Diversification, sympatric speciation, and trophic polymorphism of Arctic charr (Salvelinus alpinus complex) in Transbaikalia, Environ. Biol. Fish., 2002, vol. 64, nos. 1–3, pp. 97–114. https://doi.org/10.1007/978-94-017-1352-8_8
Alekseyev, S.S., Bajno, R., Gordeeva, N.V., et al., Phylogeography and sympatric differentiation of the Arctic charr Salvelinus alpinus (L.) complex in Siberia as revealed by mtDNA sequence analysis, J. Fish Biol., 2009a, vol. 75, pp. 368–392. https://doi.org/10.1111/j.1095-8649.2009.02331.x
Alekseyev, S.S., Mina, M.V., Smirina, E.M., and Sokolov, A.A., Late ontogeny growth acceleration and size form transformations in Transbaikalian Arctic charr, Salvelinus alpinus complex: evidence from fin ray cross sections growth layers, Environ. Biol. Fish., 2009b, vol. 86, pp. 487–505. https://doi.org/10.1007/s10641-009-9548-6
Alekseyev, S.S., Gordeeva, N.V., Samusenok, V.P., et al., Extant and extinct forms of Arctic charr Salvelinus alpinus (L.) complex from the Leprindo lake system (Transbaikalia): differentiation in life history, morphology, and genetics, J. Ichthyol., 2013, vol. 53, no. 10, pp. 792–803. https://doi.org/10.1134/S0032945213100020
Alekseyev, S.S., Gordeeva, N V., Matveev, A.N., et al., Three sympatric forms of Arctic charr Salvelinus alpinus complex (Salmoniformes, Salmonidae) from Lake Kamkanda, Northern Transbaikalia, J. Ichthyol., 2014, vol. 54, no. 6, pp. 384–408. https://doi.org/10.1134/S0032945214040018
Alekseyev, S.S., Pichugin, M.Yu., Gordeeva, N.V., et al., Reproductive strategies of Arctic charr Salvelinus alpinus (L.) forms in Kiryalta lakes, Transbaikalia, Russia, Hydrobiologia, 2019a, vol. 840, pp. 113–136. https://doi.org/10.1007/s10750-019-3894-y
Alekseyev, S.S., Pichugin, M.Yu., Gordeeva, N.V., et al., Reproductive strategies and the origin of parapatric and sympatric forms of Arctic charr Salvelinus alpinus (Salmonidae) in the system of lakes Bol’shoe Leprindo and Maloe Leprindo (Northern Transbaikalia), J. Ichthyol. 2019b, vol. 59, no 4, pp. 527–544. https://doi.org/10.1134/S0032945219040015
Brenner, T., The Arctic charr, Salvelinus alpinus salvelinus, in the prealpine Attersee, Austria, in Charrs: Salmonid Fishes of the Genus Salvelinus, Perspectives in Vertebrate Science Series, Balon, E.K., Ed., Dordrecht: Springer-Verlag, 1980, pp. 765–772.
Buresch, R., Studien am Seesaibling mehrerer Alpenseen, Z. Fisch., 1925, vol. 23, pp. 99–109.
Corrigan, L.J., Winfield, I.J., Hoelzel, A.R., and Lucas, M.C., Dietary plasticity in Arctic charr (Salvelinus alpinus) in response to long-term environmental change, Ecol. Freshwater Fish., 2011, vol. 20, pp. 5–13. https://doi.org/10.1111/j.1600-0633.2010.00446.x
Doenz, C.J., Krähenbühl, A.K., Walker, J., et al., Ecological opportunity shapes a large Arctic charr species radiation, Proc. R. Soc. B, 2019, vol. 286, art. ID 20191992. https://doi.org/10.1098/rspb.2019.1992
Fraser, D., Adams, C.E., and Huntingford, F.A., Trophic polymorphism among Arctic charr Salvelinus alpinus L., from Loch Ericht, Scotland, Ecol. Freshwater Fish., 1998, vol. 7, pp. 184–191.
Gillet, C., Egg production in an Arctic charr (Salvelinus alpinus L.) brood stock: effects of temperature on the timing of spawning and the quality of eggs, Aquat. Living Resour., 1991, vol. 4, pp. 109–116. https://doi.org/10.1051/alr:1991010
Gordeeva, N.V., Alekseyev, S.S., Matveev, A.N., and Samusenok, V.P., Parallel evolutionary divergence in Arctic charr Salvelinus alpinus (L.) complex from Transbaikalia: variation in differentiation degree and segregation of genetic diversity among sympatric forms, Can. J. Fish. Aquat. Sci., 2015, vol. 72, pp. 96–115. https://doi.org/10.1139/cjfas-2014-0014
Henricson, J. and Nyman, L., The ecological and genetical segregation of two sympatric species of dwarfed char (Salvelinus alpinus (L.) species complex), Rep.–Inst. Freshwater Res., Drottningholm, 1976, no. 55, pp. 15–37.
Hesthagen, T., Hindar, K., Jonsson, B., and Ousdal, J.Ø., Effects of acidification on normal and dwarf Arctic charr Salvelinus alpinus in a Norwegian lake, Biol. Conserv., 1995, vol. 74, pp. 115–123. https://doi.org/10.1016/0006-3207(95)00020-5
Hindar, K. and Jonsson, B., Habitat and food segregation in dwarf and normal Arctic charr (Salvelinus alpinus) from Vangsvatnet Lake, western Norway, Can. J. Fish. Aquat. Sci., 1982, vol. 39, pp. 1030–1045.
Hooker, O.E., Barry, J., van Leeuwen, T.E., et al., Morphological, ecological and behavioral differentiation of sympatric profundal and pelagic Arctic charr (Salvelinus alpinus) in Loch Dughaill Scotland, Hydrobiologia, 2016, vol. 783, pp. 209–221. https://doi.org/10.1007/s10750-015-2599-0
Jacobs, A., Carruthers, M., Yurchenko, A., et al., Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish, PLoS Genet., 2020, vol. 16, no. 4, p. e1 008 658. https://doi.org/10.1371/journal.pgen.1008658
Johnson, L., Arctic charr, in Charrs: Salmonid Fishes of the Genus Salvelinus, Perspectives in Vertebrate Science Series, Balon, E.K., Ed., Dordrecht: Springer-Verlag, 1980, pp. 15–98.
Jonsson, B. and Jonsson, N., Polymorphism and speciation in Arctic charr, J. Fish Biol., 2001, vol. 58, pp. 605–638. https://doi.org/10.1111/j.1095-8649.2001.tb00518.x
Jonsson, B. and Skúlason, S., Polymorphic segregation in Arctic charr Salvelinus alpinus (L.) from Vatnshlidarvatn, a shallow Icelandic lake, Biol. J. Linn. Soc., 2000, vol. 69, pp. 55–74.
Jungwirth, M. and Winkler, H., The temperature dependence of embryonic development of grayling (Thymallus thymallus), Danube salmon (Hucho hucho), Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta fario), Aquaculture, 1984, vol. 38, pp. 315–327. https://doi.org/10.1016/0044-8486(84)90336-3
Klemetsen, A., The most variable vertebrate on Earth, J. Ichthyol., 2013, vol. 53, no. 10, pp. 781–791. https://doi.org/10.1134/S0032945213100044
Klemetsen, A., Amundsen, P.-A., Knudsen, R., and Hermansen, B., A profundal, winter-spawning morph of Arctic charr Salvelinus alpinus (L.) in lake Fjellfrøsvatn, northern Norway, Nord. J. Freshwater Res., 1997, vol. 73, pp. 13–23.
Klemetsen, A., Amundsen, P.-A., Dempson, J.B., et al., Atlantic salmon Salmo salar L., brown trout Salmo trutta L., and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories, Ecol. Freshwater Fish., 2003, vol. 12, pp. 1–59. https://doi.org/10.1034/j.1600-0633.2003.00010.x
Knudsen, R., Primicerio, R., Amundsen, P.-A., and Klemetsen, A., Temporal stability of individual feeding specialization may promote speciation, J. Anim. Ecol., 2010, vol. 79, no. 1, pp. 161–168. https://doi.org/10.1111/j.1365-2656.2009.01625.x
Knudsen, R., Eloranta, A., Siwertsson, A., et al., Introduction of Mysis relicta (Mysida) reduces niche segregation between deep-water Arctic charr morphs, Hydrobiologia, 2019, vol. 840, no. 1, pp. 245–260. https://doi.org/10.1007/s10750-019-3953-4
Malmquist, H.J., Snorrason, S.S., Jonsson, B., et al., Diet differentiation in polymorphic Arctic charr, Salvelinus alpinus (L.), in Thingvallavatn, Iceland: ecological correlates of morphological specialization, J. Anim. Ecol., 1992, vol. 61, pp. 21–35.
Markevich, G.N. and Esin, E.V., Evolution of the charrs, genus Salvelinus (Salmonidae). 2. Sympatric inner-lake diversification (ecological peculiarities and evolutionary mechanisms illustrated by different groups of fish), J. Ichthyol., 2018, vol. 58, no. 3, pp. 333–352. https://doi.org/10.1134/S0032945218030074
Mayr, E., Animal Species and Evolution, Cambridge: Harvard Univ. Press, 1963.
Metodicheskoe posobie po izucheniyu pitaniya i pishchevykh otnoshenii ryb v estestvennykh usloviyakh (Manual for Analysis of Feeding and Food Relationships of Fishes in Natural Сonditions), Moscow: Nauka, 1974.
Mina, M.V., Mironovsky, A.N., and Dgebuadze, Yu.Yu., Morphometry of barbel of Lake Tana, Ethiopia: multivariate ontogenetic channels, Folia Zool., 1996, vol. 45, suppl. 1, pp. 109–116.
Moccetti, P., Siwertsson, A., Kjaer, R., et al., Contrasting patterns in trophic niche evolution of polymorphic Arctic charr populations in two subarctic Norwegian lakes, Hydrobiologia, 2019, vol. 840, no. 1, pp. 281–299. https://doi.org/10.1007/s10750-019-3969-9
Nilsson, N.-A., Studies on the feeding habits of trout and char in north Swedish lakes, Rep.–Inst. Freshwater Res., Drottningholm, 1955, vol. 36, pp. 162–225.
Nilsson, N.-A. and Filipsson, O., Characteristics of two discrete populations of Arctic charr (Salvelinus alpinus L.) in a north Swedish lake, Rep.–Inst. Freshwater Res., Drottningholm, 1971, vol. 51, pp. 90–108.
Noakes, D.L.G., Charr truth: sympatric differentiation in Salvelinus species, Environ. Biol. Fish., 2008, vol. 83, pp. 7–15. https://doi.org/10.1007/s10641-008-9379-x
Pavlov, D.A. and Osinov, A.G., Reproduction and development in the dwarf form of Arctic charr Salvelinus alpinus from Lake Davatchan, Transbaikalia, J. Ichthyol., 2008, vol. 48, pp. 96–113.
Pichugin, M.Yu., Development of skeleton elements in juvenile dwarf and small sympatric forms of Salvelinus alpinus complex from Lake Davatchan (Transbaikalia), J. Ichthyol., 2009, vol. 49, no. 9, pp. 741–758.
Pravdin, I.F., Rukovodstvo po izucheniyu ryb (Manual for Analysis of Fishes), Moscow: Pishchevaya Prom-st’, 1966.
Reist, J.D., An empirical evaluation of several univariate methods that adjust for size variation in morphometic data, Can. J. Zool., 1985, vol. 63, pp. 1429–1439.
Samusenok, V.P., Ecology of Arctic charr Salvelinus alpinus (L.) in high-altitude reservoirs of northern Transbaikalia, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Irkutsk: Irkutsk State Univ., 2000.
Samusenok, V.P., Alekseyev, S.S., Matveev, A.N., et al., The second population of Arctic charr Salvelinus alpinus complex (Salmoniformes, Salmonidae) in the Lake Baikal basin, the highest mountain charr population in Russia, J. Ichthyol., 2006, vol. 46, no. 8, pp. 587–599.
Sandlund, O.T., Gunnarson, K., Jonasson, P.M., et al., The Arctic charr Salvelinus alpinus in Thingvallavatn, Oikos, 1992, vol. 64, pp. 305–351. https://doi.org/10.2307/3545056
Savvaitova, K.A., Arkticheskie gol’tsy (struktura populyatsionnykh sistem, perspektivy khozyaistvennogo ispol’zovaniya) (Arctic Charrs: Population Structure and Prospective Economic Use), Moscow: Agropromizdat, 1989.
Savvaitova, K.A., Sympatric forms of charrs of genus Salvelinus (Salmonidae) from Far Eastern water bodies, in Biologicheskie problemy Severa. Biologiya gol’tsov Dal’nego Vostoka (Biological Problems of the North. Biology of Far Eastern Charrs), Vladivostok: Dal’nevost. Otd., Akad. Nauk SSSR, 1991, pp. 5–20.
Savvaitova, K.A., Maksimov, V.A., and Merezhin, V.K., Charrs of genus Salvelinus (Salmonidae, Salmoniformes) from Kuando-Chara mountain lakes of Transbaikalia, in Ekologo-faunisticheskie issledovaniya. Biologicheskie resursy territorii v zone stroitel’stva BAM (Ecological and Faunistic Studies: Biological Resources of the Baikal-Amur Mainline Area), Moscow: Mosk. Gos. Univ., 1981, pp. 119–166.
Skoglund, S., Siwertsson, A., Amundsen, P.-A., and Knudsen, R., Morphological divergence between three Arctic charr morphs—the significance of the deep-water environment, Ecol. Evol., 2015, vol. 5, no. 15, pp. 3114–3129. https://doi.org/10.1002/ece3.1573
Smalås, A., Amundsen, P.-A., and Knudsen, R., Contrasting life history strategies of sympatric Arctic charr morphs, Salvelinus alpinus, J. Ichthyol., 2013, vol. 53, no. 10, pp. 856–866. https://doi.org/10.1134/S0032945213100111
Snorrason, S.S. and Skúlason, S., Adaptive speciation in northern freshwater fishes, in Adaptive Speciation, Dieckmann, U., Eds., Cambridge: Cambridge Univ. Press, 2004, pp. 210–228.
Swift, D.R., Effect of temperature on mortality and rate of development of the eggs of the Windermere char (Salvelinus alpinus), J. Fish. Res. Board Can., 1965, vol. 22, no. 4, pp. 913–917.
Wilson, A.J., Gislason, D., Skúlason, S., et al., Population genetic structure of Arctic charr, Salvelinus alpinus from northwest Europe on large and small spatial scales, Mol. Ecol., 2004, vol. 13, pp. 1129–1142. https://doi.org/10.1111/j.1365-294X.2004.02149.x
Woods, P.J., Skúlason, S., Snorrason, S.S., et al., Intraspecific diversity in Arctic charr, Salvelinus alpinus, in Iceland: I. Detection using mixture models, Evol. Ecol. Res., 2012, vol. 14, pp. 973–992.
Woods, P.J., Young, D., Skúlason, S., et al., Resource polymorphism and diversity of Arctic charr Salvelinus alpinus in a series of isolated lakes, J. Fish Biol., 2013, vol. 82, pp. 569–587. https://doi.org/10.1111/jfb.12011
Zhivotovskii, L.A., Index of similarity of populations in polymorphic characters, Zh. Obshch. Biol., 1979, vol. 40, no. 4, pp. 587–602.
ACKNOWLEDGMENTS
The authors thank S.G. Afanas’ev (Vostsibrybtsentr), B.E. Bogdanov (Limnological Institute SB RAS) V.V. Buldygerov (VOSTSIBNIIGIMS), R.S. Andreev, A.V. Isaev, I.B. Knizhin, V.K. Pomazkin, D.B. Salmanov, D.V. Cherkashin, I.G. Khoroshev (Irkutsk State University), N.V. and A.S. Alekseyev, V.V., M.M. and E.M. Pichugin (Moscow State University), F.N. Shkil’ (Kolzov Institute of Developmental Biology, RAS) for field assistance; I.V. Samusenok (ISU) for help with the illustrations; M.V. Mina (IDB RAS) and anonymous reviewer for valuable comments on the manuscript.
Funding
The study was funded by Russian Foundation for Basic Research (project no. 18-04-00092) and conducted under Government basic research programs of Institute of Developmental Biology, Russian Academy of Sciences, no. 0108-2019-0007 and Institute of Ecology and Evolution, Russian Academy of Sciences, no. 0109-2019-0005.
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Alekseyev, S.S., Samusenok, V.P., Yur’ev, A.L. et al. Morphological and Ecological Differentiation of Sympatric Forms of Arcrtic Charr Salvelinus alpinus (Salmonidae) in Lake Tokko (Northern Transbaikalia). J. Ichthyol. 61, 109–129 (2021). https://doi.org/10.1134/S0032945221010021
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DOI: https://doi.org/10.1134/S0032945221010021