ISSN 1063-0740, Russian Journal of Marine Biology, 2017, Vol. 43, No. 3, pp. 216–223. © Pleiades Publishing, Ltd., 2017. Original Russian Text © G.N. Markevich, E.V. Esin, E.A. Saltykova, O.Yu. Busarova, L.A. Anisimova, K.V. Kuzishchin, 2017, published in Biologiya Morya.

ORIGINAL PAPERS Ichthyology

New Endemic Deepwater Charr Morphs of the Genus Salvelinus (Salmoniformes: Salmonidae) from Lake Kronotskoe, Kamchatka G. N. Markevicha, *, E. V. Esina, b, E. A. Saltykovac, O. Yu. Busarovad, L. A. Anisimovab, and K. V. Kuzishchine aKronotsky State Natural Biosphere Reserve, Yelizovo, 684000 Russia bAll-Russian Research Institute of Fisheries and Oceanography, Moscow, 107140 Russia cSevertsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russia dFar Eastern State Technical Fisheries University, Vladivostok, 690087 Russia eDepartment of Biology, Moscow State University, Moscow, 119234 Russia *e-mail: [email protected] Received December 1, 2016

Abstract⎯Two previously unknown profundal dwelling charr morphs of the genus Salvelinus from Lake Kro- notskoe are described in this article. According to their lifestyle peculiarities, these morphs were named the “bigmouth charr” and “smallmouth charr.” The former group is near-bottom benthivorous, while the latter one inhabits the water column and occupies the omnivorous niche. Bigmouth and smallmouth charrs are dis- tinguished from the rest of the sympatric charr morphs by their smaller size, shorter snout, larger eyes, as well as by several craniological traits and lower parasite abundance. Spawning of both morphs takes place directly in the profundal zone and lasts from late October to February. Additional studies are required to determine the systematic status of the new morphs.

Keywords: microevolution, sympatric speciation, trophic-based specialization, profundal zone DOI: 10.1134/S1063074017030087

INTRODUCTION niches of the littoral zone and epilimnion were previ- Charrs of the genus Salvelinus are an extremely ously described in this water body [3, 11]. Subse- flexible group of salmonids. Their diversification is quently, a dwarf charr was described from the source of determined by resource utilization in distinct food the Kronotskaya River [8, 22]. It was also proposed to niches, which is connected with the evolution of spe- consider Dolly Varden from the lower reaches of the cific morphological traits and results in the origin of lake tributaries as an independent morph [7, 22]. similar morphs in numerous lacustrine–riverine sys- No catches were conducted previously in the pro- tems of the Holarctic [17]. The most widespread diver- sification pathway is specialization along the pelagic– fundal zone of Lake Kronotskoe for various reasons. benthic resource axes [15], which basically results in This lake is one of the deepest water bodies in the the benthivorous and planktivorous, or predatory, region (with its maximum depth of 136 m and the morphs [19]. Apart from relatively simple examples of average depth of 58 m). The majority of sediments in intralacustrine diversification, the genus Salvelinus the profundal zone of the lake basin are composed of charrs exhibit from three to five morphs in rare cases silt reaching a thickness up to 12 m, while the extensive [20, 23]. In particular, in addition to the shallow-water coastal slopes are composed of unsilted lava boulders. morphs, large and deep lakes are also inhabited by During the profundal zone surveys in 2012–2014, it charrs in the profundal zone. Such specific morphs was originally established that the deepwater part of have been described for S. namaycush (Walbaum, the lake is inhabited by two previously unknown charr 1792) from the Great Lakes of North America [18, 24], morphs. These new morphs were named the “big- for S. alpinus (Linnaeus, 1758) from lakes of Scandina- mouth” and “smallmouth” charrs. The skull mor- via [19], Transbaikalia [16], and the Taimyr Peninsula phology, ecology, and parasite fauna of these morphs [6]. A high variability in trophic and ecological char- were briefly described as a result of the first catches [1, acteristics was found for charrs in Lake Kronotskoe on 5, 12–14]. The objective of this study is to provide a the . Three charr morphs that detailed description of the morphology, feeding pecu- occupy the benthivorous (nosed charr), predatory liarities, and lifestyle of the recently discovered pro- (longhead charr), and omnivorous (white charr) fundal charr morphs in Lake Kronotskoe.

216 NEW ENDEMIC DEEPWATER CHARR MORPHS OF THE GENUS SALVELINUS 217

Table 1. The morphometric characteristics (mean ± error of on lines of an estimated length were applied to catch the mean/lim) of deepwater charrs of the genus Salvelinus fish in the water column. A total of 516 bigmouth and from Lake Kronotskoe 403 smallmouth charrs were sampled. The length and Traits Bigmouth charr Smallmouth charr weight of all individuals were measured and the sex was determined. In 30 fish of each morph the age was FL*, mm established using polished otoliths (the opaque zone 274± 1.7 204± 1.4 edge was considered as annual ring). In 50 fish of each 240–358 168–330 morph, morphometric measurements were conducted by the standard scheme [9]. Variations in skull mor- FL, % phology (chondrocranium and 11 bones) were quanti- ± ± fied in 20 fish of each morph. The cranial traits were c* 19.7 0.17 18.9 0.17 18–23 17–21 evaluated based on the principle that was applied ear- ± ± lier to the epilimnic morphs of Lake Kronotskoe aD 42.1 0.14 41.7 0.16 charrs [3]. In 30 fish of each morph, the food compo- 40–45 39–45 sition was determined as the proportions in stomach of ± ± pD 40.5 0.16 41.4 0.19 different prey groups [10]. In the same fish, parasite 38–43 39–44 species composition and abundance [1], as well as ± ± infection intensity, were assessed by complete parasi- aV 48.5 0.18 48.4 0.22 46–52 45–51 tological dissection [2]. 67.4± 0.13 67.6± 0.14 To assess the statistical significance of morpho- aA metric and size–weight differences between the fish 66–68 66–69 groups, the Student’s t-test was used after checking the ± ± P–V* 29.4 0.20 30.5 0.25 normality of the characteristics by the Kolmogorov– 27–32 28–34 Smirnov test. The differences in diet and parasite ± ± infection were validated by the Mann–Whitney U-test V–A 20.5 0.16 20.5 0.18 19–23 18–23 [4]. Mathematical processing of the data was carried out in the Statsoft Statistica 13.0 software package. ± ± lP* 16.6 0.16 14.5 0.11 15–18 12–17 ± ± RESULTS AND DISCUSSION lV* 12.0 0.12 10.6 0.09 10–14 8–12 External View B“c”, % The bigmouth charr is characterized by a massive ± ± ao* 17.0 0.34 15.7 0.29 head with protruding supraorbital arcs; eyes are shifted 13–22 12–20 towards the nape, their average diameter is 27% of 26.8± 0.33 31.5± 0.30 head length. Upper jaw extends far behind the poste- o* rior eye edge, reaching 50% of head length on average; 22–31 29–35 lower jaw is long, curved, protruding forward and ± ± lmx* 49.9 0.55 44.5 0.43 reaching 70% of head length on average that provides 44–57 40–50 the upper mouth position. Body is cylindrical; caudal ± ± peduncle is long and low. Pectoral and ventral fins are lmd* 69.9 0.51 62.7 0.63 62–79 54–70 long and wide; pectoral fins length is greater than 0.5 of the P–V distance (Table 1). Caudal fin is slightly ± ± cH* 70.5 0.71 73.3 0.75 forked or truncated (Fig. 1a). Meristic characters are 50–79 65–84 as follows: D 8–10 (9), A 7–9 (8), P 12–14 (13), V 8– * The differences between the morphs are significant (t-test, p < 9 (8) branched rays; ll 123–132 (127); pc 27–42 (33); 0.05). rb 10–12 (11); sp. br. 15–18 (16); vert 61–68. FL, body length; c, head length. Distances are as follows: aD and pD, ante- and postdorsal; aV, anteventral; aA, anteanal; P–V, pecto- Mature individuals are characterized by dark flanks ventral; V–A, ventro-anal; lP and lV, length of pectoral and ven- and a reddish belly; parr spots are absent. Spots tral fins. Head measurements are as follows: ao, snout length; o, (always smaller than the pupil diameter) below the lat- eye diameter; lmx and lmd, length of upper and lower jaws; eral line are red or pink; above the lateral line, pink or cH,head height. white; no spots are found on fins. Jaws are usually uncolored, sometimes with red bordering along the MATERIALS AND METHODS edge. Gill rays have a deep black pigmentation. All fins are red; the first ray of pectoral and ventral fins, as well Catches were carried out from May to November as the lower rays of caudal fin are white. Bigmouth 2012–2014 in the profundal, limnetic, and littoral charr acquire the characteristic traits at an early age zones of the lake using a set of gill nets with a mesh size and are well identified by the curved lower jaw begin- from 18 to 35 mm. Floating gill nets with weights fixed ning from a body length (FL) of 7–10 cm.

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(a)

(b)

Fig. 1. The external form of bigmouth (a) and smallmouth (b) charrs from the profundal zone of Lake Kronotskoe. Scale bar, 5 cm.

The smallmouth charr head is mostly conic, wedge-shaped protrusion anteriorly to ventral fins. rounded, but the head shape is characterized by high Pectoral fins are moderate in length, not exceeding 0.5 variability. Eyes are large and prominent, with an aver- of the P–V distance (Table 1). Caudal fin has a deep age diameter of 32 to 35% of head length. Upper jaw is fork (Fig. 1b). Meristic characters are as follows: D 9– straight and thin, never extending behind the posterior 11 (10), A 8–10 (9), P 12–13 (13), V 7–9 (8) branched eye edge, and reaching 45% of head length on average; rays; ll 121–136 (126); pc 24–43 (32); rb 10–13 (12); lower jaw is not prolonged forward beyond the upper sp. br. 15–22 (19); vert 61–67. jaw, reaching 63% of head length on average. Mouth is small and terminal. Body is laterally flattened; caudal The flank color is light; back is dark; fins are pale peduncle is long and low. Belly has a distinctive red with barely perceptible white edging. Spots on the

RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 43 No. 3 2017 NEW ENDEMIC DEEPWATER CHARR MORPHS OF THE GENUS SALVELINUS 219

(b) (e)

(a) (c)

(d)

(f) (j) (h) (i)

(g)

Fig. 2. The skull elements of bigmouth (left) and smallmouth (right) charrs. (a) Chondrocranium of the most typical shape; (b) maxillare; (c) articulare; (d) dentale; (e) hyomandibulare; (f) praemaxillare; (g) vomer; (h) glossohyale; (i) supraetmoideum; (j) parasphenoideum. Scale bar, 1 cm. body are pale pink, almost inconspicuous in some than the anterior one. Half of the fish have an addi- cases. No spots are found on fins. The juvenile traits tional middle row of teeth on the glossohyale. are retained in the appearance of mature fish; particu- larly, parr spots occur on the flanks of spawning fish. The chondrocranium in bigmouth charr has a well- defined rostral fossa, as well as orbital processes of the Thus, the described morphs are markedly different ethmoid region. Half of the fish lack fontanelles on the from each other in a number of morphometric charac- epiphyseal bridge and the characteristic lateral crests ters, particularly in the head proportions. Moreover, on the pteroticum (Fig. 2). The praemaxillare is charac- the exterior differences between the deepwater and the terized by a thin ascending process; the maxillare epilimnic morphs (nosed, longhead, and white charrs) shape in senescent fish is either straight and narrow are most evident in the snout length (an average of 16– (80%) or slightly curved and narrow. The dentale pro- 17% of head length versus 18–25%, respectively), as file is curved; the parasphenoideum is without a pro- well as in the eye diameter (27–32% vs. 20–24%). nounced neck and with a short and wide anterior part. Deepwater charr are also distinguished from epilimnic The vomer head is massive and rounded; the arrange- ones by anal fins slightly shifted towards the head ment of the teeth is predominantly V-shaped. The (anteanal distance 67–68% vs. 68–69% of body length). vomer arm is mostly (in 65% of fish) wider than the vomer head. The hyomandibulare is defined both by a well-developed posterior crest and by the absence of a Skull Structure lateral crest; in 70% of the fish it has ventral blade of anterior edge (Fig. 2). The chondrocranium in the deepwater morph is defined by a short and non-bifurcate rostrum. Eth- In the smallmouth charr, the ethmoid region gradu- moid fontanelles are small and sheeted with cartilagi- ally turns into a bridge in the chondrocranium (Fig. 2). nous membrane in 80% of the fish, while 20% of the The praemaxillare is defined by the relatively broad individuals have only one fontanelle. The supraoccipi- ascending process. The maxillare shape is straight and tale reaches the edges of dorsal fontanelles in 60% of wide in 75% of the fish; it is also much wider than that bigmouth and almost all smallmouth charrs. The in the bigmouth charr. The profile of the dentale is pteroticum, with a moderate length of posterior out- straight, with a deep articulary groove; the parasphe- growths, always overlies the sphenoticum. All dermal noideum, having the well-defined neck, is longer and bones are sculptured, with well-pronounced crests. narrower in the anterior part than that in the bigmouth The articulare is characterized by a low posterior edge charr. The vomer head is elongated, without crests; and much shortened ascending process in both teeth are arranged into a straight transverse row in 70% morphs. The supraethmoideum is defined by a narrow of fish. The hyomandibulare has a narrowed profile; posterior part, which is comparable in width to the the posterior crest is well developed in 70% of the anterior part in the bigmouth charr; in 75% of the specimens; the lateral crest is lacking; the ventral blade smallmouth charr the posterior part it is even narrower is developed in 75% of fish.

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Table 2. Size parameters (mean ± error of the mean/lim) of deepwater charrs of the genus Salvelinus from Lake Kronotskoe Bigmouth charr Smallmouth charr Parameter juveniles (n = 68) adults (n = 448) juveniles (n = 98) adults (n = 305) ± ± ± ± Body length, mm 128.8 2.04 273.9 1.70 110.8 1.93 203.8 1.44 79–198 210–358 65–170 161–330 ± ± ± ± Body weight, g 20.9 1.64 175.2 0.94 14.1 0.88 74.3 0.65 4.3–109 82–360 2.3–40 38–143 * The differences between the morphs in both parameters are significant (t-test, p < 0.01). Juveniles include samples of fish of ages 1+…5+ at the gonad maturity stage II.

The qualitative cranial differences between the charr. The smallmouth charr had a wider food range: deepwater charr morphs also become evident as signif- in addition to the aforementioned items, chironomid icant differences in the metrics of their dermal, vis- pupae and insect imagoes were important components ceral, and jaw bones [13, 14]. of their diet. Moreover, single gammarids and plank- tonic crustaceans were also found in fish stomachs. Size and Age Structure The number of prey in the stomach, excluding chiron- omid larvae, differed significantly between the charr Bigmouth and smallmouth charrs become mature morphs (Table 3). Mayfly, stonefly, and caddisfly lar- by the fifth or sixth year of life at a body length of 20 and 15 cm and a body weight of 80 and 30 g, respec- vae, as well as fish fragments, were never found in tively. The maximum lifespan of both morphs is 12 charr stomachs . Based on these data, it can be con- years. The spawning group of bigmouth charr con- cluded that bigmouth charr are benthivorous, special- sisted predominantly of fish at 5+…9+ years with a ized in feeding on invertebrates dwelling in the depth body length of 27–30 cm; smallmouth charr, at of silt sediments. Smallmouth charr feed in the water 5+…8+ years and a body length of 20–22 cm. The column and can be regarded as euryphages. sizes of males and females were similar, whereas the size–weight differences between bigmouth and small- Both deepwater charr morphs, in comparison with mouth charrs were significant (Table 2). the epilimnic one, were characterized by a relatively low parasite infection intensity [1]. Almost no direct- development and benthos-transmitted parasites were Lifestyle found in bigmouth and smallmouth charrs. The hel- Adult charrs of both morphs occurred all over the minths Eubothrium salvelini (Schrank, 1790), Proteo- lake area, starting from a depth of 20–30 m. This lake cephalus longicollis (Zeder, 1800), and Philonema zone is considered as profundal due to its location oncorhynchi Kuitunen-Ekbaum, 1933, the intermedi- below the thermocline and the photic layer border ate hosts of which are Cyclops, were most common in (defined as a triple Secchi disk depth transparency). profundal charrs. These fish were also characterized According to the catch composition, the largest big- mouth charr aggregations in the summer season by a high abundance of Diplostomum gasterostei Wil- formed in the near-bottom layer at a depth of 30–60 m, liams, 1966, which infect fish during their direct con- in the bottom parts covered with silt sediments. Juve- tact with snails. The infection intensity of the small- nile bigmouth charr were found there as well. Adult mouth charr by the cestode P. longicollis was 4 times as smallmouth charr were mainly caught in the water col- high as that of bigmouth charr; by the trematode umn at depths of 20–50 m; juvenile smallmouth charr D. gasterostei it was 10 times as high (Table 4). The rel- concentrated in the littoral zone at the Kronotskaya atively high smallmouth charr’s infection intensity by River source during August and September. Single plankton-transmitted helminths indicates the back- smallmouth and bigmouth charrs occurred at depths ground role of pelagic zooplankton in the diet of this of up to 100 m. These charrs were never found in the lake tributaries and in the Kronotskaya River source. fish. The trematode D. gasterostei infects smallmouth charr in the lake littoral zone as early as in the juvenile Deepwater charrs were actively feeding in July and period and is kept throughout the fish’s lifespan. A August (Table 3): the stomach fullness was more than 50%, on average. Oligochaetes, chironomid larvae, characteristic feature of bigmouth charr is the highest and bivalves (genus Pisidium) dominated in the diet of species diversity of myxosporidian fauna. This is bigmouth charr by number. Oligochaetes constituted explained by the continuous contact of the fish with more than 40% of the food bolus by weight. Detritus oligochaetes, which are the main hosts of myxosporid- was found in 74% of the stomachs of the bigmouth ian parasites [1].

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Table 3. The occurrence of food items in stomachs of deepwater charrs of the genus Salvelinus from Lake Kronotskoe Bigmouth charr Smallmouth charr Food components Freq, % spec. number Freq, % spec. number

Sphaeriidae clams* 100 7.7 (20) 47 2.5 (10) Gammarids* 0 0 3 0.7 (20) Plankton crustaceans* 0 0 7 0.7 (20) Chironomid larvae 100 19.1 (60) 80 20.8 (82) Chironomid pupae* 27 2.6 (15) 43 4.0 (35) Insect imagoes* 7 0.4 (5) 30 2.9 (80) Oligochaetes* 100 28.6 (65) 86 20.4 (84) * The differences between the morphs are significant (U-test, p < 0.05). Freq, percentage of fish with this type of food in stomach; Spec. number, mean (maximum) number of food items of each group per fish.

Table 4. The main indicator parasites in deepwater charrs of the genus Salvelinus from Lake Kronotskoe Bigmouth charr Smallmouth charr Species Freq/d AI Freq/d AI

Diplostomum gasterostei 80.0/65.0–91.6 7.2 100.0/90.5–100.0 64.2

Eubothrium salvelini 97.1/88.9–100.0 11.0 56.7/38.5–73.9 1.1

Proteocephalus longicollis 94.3/84.1–99.5 17.0 96.7/87.2–100.0 67.0

Philonema oncorhynchi 97.1/88.9–100.0 10.0 93.3/81.6–99.4 6.3

* The differences between the morphs in AI of all the species are significant (U-test, p < 0.05). Freq, percentage of fish with this parasite species, %; d, confidence interval of occurrence; AI, abundance index.

Spawning 30–40 m and lasts from late October to the middle of December. The fecundity of smallmouth charr varies Breeding of bigmouth and smallmouth charrs takes from 150 to 500 (average 280) eggs. place directly in the lake. Maturing bigmouth charr are concentrated in the southwestern part at depths of approximately 50–60 m, along the coasts composed CONCLUSIONS by the ancient lava flow of the Uzon volcano. We could not conduct direct observations of the spawning These data demonstrate that the profundal zone of of this morph. However, based on the physiological Lake Kronotskoe is not a low-production “uninhab- state of the fish by late November (males were at ited desert,” as was previously believed [3]. This part of maturity stage V; females were at late stage IV), we can the lake is inhabited by specialized fish with a specific assume that spawning takes place in January and Feb- lifecycle that is completely associated with the deep- ruary. The fecundity of bigmouth charr varied from water zone of the basin. The external morphology and 300 to 850 (average 550) eggs. the bigmouth charr skull structure are evidence of According to the catches of fish with gonads at the their long-term specialization in feeding on benthic late IV and V–VI maturity stages, the smallmouth invertebrates in silt sediments of the profundal zone. charr spawning grounds are located in the southeast- The long and curved lower jaw can be considered as an ern part of the lake and distributed along the large- adaption for excavating prey organisms from the silt. boulder lava flows of the Krasheninnikov and Kro- In contrast to bigmouth charr, smallmouth charr are notsky volcanoes. Spawning takes place at depths of characterized by a more generalized morphology and

RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 43 No. 3 2017 222 MARKEVICH et al. wide food niche: they feed both at the bottom and in Statistical Tests in Biomedical Research), Leningrad: the water column. In their exterior, smallmouth charr Meditsina, 1973, 2nd ed. are close to the previously described dwarf charr [7, 8], 5. Markevich, G.N., Anisimova, L.A., Saltykova, E.A., but, unlike the latter, they are abundant in the ecosys- et al., Diversity and the life cycle of the endemic tem, show a different age structure, have never been morphs of Dolly Varden Salvelinus malma from the observed in streams, including the mouth of the Kro- Kronotskoe Lake watershed (eastern Kamchatka), XV Mezhdunarodnaya nauchnaya konferentsiya “Sokhrane- notskaya River, and spawn at great depth starting from nie bioraznoobraziya Kamchatki i prilegayushchikh late October but not from early September. In their morei,” Tezisy dokladov (XV Int. Sci. Conf. “Conserva- appearance and lifestyle, bigmouth and smallmouth tion of Biodiversity of Kamchatka and Coastal Waters,” charrs are substantially different from the known Abstracts of Papers), Petropavlovsk-Kamchatsky: deepwater charrs S. alpinus and S. namaycush. The Kamchatpress, 2014, pp. 325–329. former, as a rule, specializes into a single slow-growing 6. Pavlov, D.S., Savvaitova, K.A., Gruzdeva, M.A., et al., profundal morph [6, 16, 19], while S. namaycush Raznoobraziye ryb Taimyra (Diversity of Fishes in forms two morphs in some lakes: “humper”, which Taimyr), Moscow: Nauka, 1999. feeds on crustaceans, and “siscowet”, which is a pred- 7. Pavlov, S.D., Kuzishchin, K.V., Gruzdeva, M.A., Sen- ator that feeds on deepwater whitefish [18, 21]. chukova, A.L., and Pivovarov, E.A., Phenetic diversity and spatial structure of chars (Salvelinus) of the Kro- Bigmouth and smallmouth charrs, like other sym- notskaya riverine-lacustrine system (Eastern Kam- patric charr morphs of Lake Kronotskoe, are progeny chatka), J. Ichthyol., 2013, vol. 53, no. 9, pp. 662–686. of the Dolly Varden trout, S. malma [7, 22]. At the 8. Pavlov, S.D., Pivovarov, E.A., and Ostberg, C.O., same time, the status of isolated lacustrine morphs Dwarf char, a new form of chars (the genus Salvelinus) and their phylogenetic relationships are not com- in Lake Kronotskoe, Dokl. Biol. Sci., 2012, vol. 442, pletely clear; therefore, additional studies are required. no. 1, pp. 20–23. The discovery of the new charr morphs that inhabit 9. Pravdin, I.F., Rukovodstvo po izucheniyu ryb (Guide to the profundal zone of Lake Kronotskoe significantly the Study of Fish), Moscow: Pishchepromizdat, 1966. expands our understanding of the diversity in this 10. Rukovodstvo po izucheniyu pitaniya ryb (Guide to the “flock”. It can be stated that the complex of sympatric Study of Diet of Fish), Vladivostok: Tikhookean. charr morphs in Lake Kronotskoe is one of the most Nauchno–Issled. Inst. Rybn. Khoz. Okeanogr., 1986. diverse in the genus Salvelinus. 11. Savvaitova, K.A., Arkticheskiye gol’tsy (Arctic Charrs), Moscow: Agropromizdat, 1989. 12. Saltykova, E.A., Phenetic diversity of the benthivorous ACKNOWLEDGMENTS charrs Salvelinus from the Lake Kronotskoe, eastern The authors are grateful to A.A. Krzhevitskaya for Kamchatka, Tez. dokl. XV mezhdunar. nauchn. konf. her contribution to determination of fish age, as well as “Sokhraneniye bioraznoobraziya Kamchatki i prilegay- to the administration of the State Natural ushchikh morei” (Abstr. XV Int. Sci. Conf. “Conserva- tion of Biodiversity of Kamchatka and Coastal Biosphere Reserve for assistance in organizing and Waters”), Petropavlovsk-Kamchatsky: Kamchatpress, conducting the works. The study was financially sup- 2014, pp. 358–361. ported by the Wild Salmon Center, the Association of 13. Saltykova, E.A., Morphological diversity and diver- Kamchatka’s Specially Protected Natural Territories, gence of charrs of the genus Salvelinus in Lake Kro- and the Russian Science Foundation, project no. 14- notskoe (Eastern Kamchatka), Extended Abstract of 50-00029 (Moscow State University Depository). Cand. Sci. (Biol.) Dissertation, Moscow: Moscow State Univ., 2015. 14. Saltykova, E.A., Markevich, G.N., Esin, E.V., and REFERENCES Kuzishchin, K.V., Structure of “species flocks” in 1. Busarova, O.Yu., Knudsen, R., and Markevich, G.N., fishes: Channels of the splanchnocranium divergence Parasite fauna of charrs (Salvelinus) of Lake Kro- in endemic lacustrine benthivorous charrs (Salvelinus, notskoe, Kamchatka, Parazitologiya, 2016, vol. 50, Salmonidae, Teleostei) in Lake Kronotskoye, Kam- no. 6, pp. 409–425. chatka, Dokl. Biol. Sci., 2015, vol. 464, no. 1, pp. 226– 2. Bykhovskaya-Pavlovskaya, I.E., Parazity ryb. Rukovod- 229. stvo po izucheniyu (Fish Parasites: Handbook), Lenin- 15. Adams, C.E., Fraser, D., Huntingford, F.A., et al., grad: Nauka, 1985. Trophic polymorphism amongst Arctic charr from 3. Viktorovskii, R.M., Mekhanizmy vidoobrazovaniya u Loch Rannoch, Scotland, J. Fish Biol., 1998, vol. 52, gol’tsov Kronotskogo ozera (Mechanisms of Speciation no. 6, pp. 1259–1271. in Charrs of Lake Kronotskoye), Moscow: Nauka, 16. Alekseyev, S.S., Samusenok, V.P., Matveev, A.N., and 1978. Pichugin, M.Yu., Diversification, sympatric specia- 4. Gubler, E.V. and Genkin, A.A., Primeneniye nepara- tion, and trophic polymorphism of Arctic charr, Salve- metricheskikh kriteriev statistiki v mediko-biologich- linus alpinus, complex in Transbaikalia, Environ. Biol. eskikh issledovaniyakh (Application of Nonparametric Fishes, 2002, vol. 64, no. 1, pp. 97–114.

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17. Bolnick, D.I. and Fitzpatrick, B.M., Sympatric specia- 22. Ostberg, C.O., Pavlov, S.D., and Hauser, L., Evolu- tion: models and empirical evidence, Annu. Rev. Ecol. tionary relationships among sympatric life history Evol. Syst., 2007, vol. 38, pp. 459–487. forms of Dolly Varden inhabiting the landlocked Kro- 18. Eshenroder, R.L., Differentiation of deep-water lake notsky Lake, Kamchatka, and a neighboring anadro- charr Salvelinus namaycush in North American lakes, mous population, Trans. Am. Fish. Soc., 2009, vol. 138, Environ. Biol. Fishes, 2008, vol. 83, no. 1, pp. 77–90. no. 1, pp. 1–14. 19. Hindar, K. and Jonsson, B., Habitat and food segrega- 23. Sandlund, O.T., Gunnarson, K., Jánasson, P.M., et al., tion of dwarf and normal arctic charr (Salvelinus alpi- The arctic charr Salvelinus alpinus in Thingvallavatn, nus) from Vangsvatnet Lake, western Norway, Can. J. Oikos, 1992, vol. 64, pp. 305–351. Fish. Aquat. Sci., 1982, vol. 39, no. 7, pp. 1030–1045. 20. Jonsson, B. and Jonsson, N., Polymorphism and spe- 24. Zimmerman, M.S., Krueger, C.C., and Eshenroder, R.L., ciation in Arctic charr, J. Fish Biol., 2001, vol. 58, no. 3, Phenotypic diversity of lake trout in Great Slave Lake: pp. 605–638. Differences in morphology, buoyancy, and habitat depth, Trans. Am. Fish. Soc., 2006, vol. 135, pp. 1056– 21. Muir, A.M., Bronte, C.R., Zimmerman, M.S., et al., 1067. Ecomorphological diversity of lake charr Salvelinus namaycush at Isle Royale, Lake Superior, Trans. Am. Fish. Soc., 2014, vol. 143, pp. 972–987. Translated by E. Shvetsov

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