Phenetic Diversity and Spatial Structure of Chars ...€¦ · A. L. Senchukova, and E. A. Pivovarov Biological Faculty, Moscow State University, Moscow, 119992 Russia email:[email protected]

ISSN 0032�9452, Journal of Ichthyology, 2013, Vol. 53, No. 9, pp. 662–686. © Pleiades Publishing, Ltd., 2013.Original Russian Text © S.D. Pavlov, K.V. Kuzishchin, M.A. Gruzdeva, A.L. Senchukova, E.A. Pivovarov, 2013, published in Voprosy Ikhtiologii, 2013, Vol. 53, No. 6, pp. 645–670.

662

Chars of the genus Salvelinus (Salmonidae) inhab�iting the northern latitudes are represented by a num�ber of species often forming a complex populationstructure within the range and sympatric species flocsin individual water bodies. The origin, taxonomic sta�tus, and relationships between many forms still remaincontroversial and are the subject of long�term discus�sion (Nordeng, 1983; Behnke, 1984; Savvaitova, 1989;Glubokovskii, 1995; Hammar, 1998; Chereshnevet al., 2002).

The strongest divergence in chars is observed in iso�lated water bodies, especially in the lakes where vari�ous forms (benthophages, carnivorous, plankto�phages, deep�water forms, dwarf forms, etc.) aredescribed (Vasil’ieva, 1980; Nyman et al., 1981; Sav�vaitova, 1989, Pavlov, 1995, 1997; Alekseev et al.,1999, 2006). One of the most illustrative examples ofthis diversity in isolation are the chars of the Kro�notskaya riverine�lacustrine system in Kamchatka.Lake Kronotskoe has numerous tributaries; the Kro�notskaya River is the only outlet from the lake, it flowsinto the Pacific Ocean. The lake basin is isolated fromthe penetration of anadromous fish by insurmountablerapids and waterfalls. The formation of a volcanic lavadam as a result of the Kronotskaya volcano eruptionled to the formation of an endemic ichthyofauna in the

lake, represented by several forms of chars and at leasttwo forms of the lacustrine sockeye, kokanee Onco�rhynchus nerka kennerley.

The first detailed studies on chars of Lake Kro�notskoe were performed by Viktorovskii (1978),Kurenkov (1979), and Vvedenskaya (1980). Theyincluded primarily the analysis of morphological andkaryological characters. Having studied the variety ofchars from Lake Kronotskoe by these characters, theauthors of those studies have identified three well�dif�ferentiated forms—“white,” “nosed,” and “long�headed” chars—that they regarded as separate speciesS. albus, S. shmidti, and S. cronocius. Since then, theattention of researchers to chars of Lake Kronotskoesteadily increased, and different systems of characters,including genetic data were studied (Salmenkovaet al., 2005; Radchenko et al., 2006; Ostberg et al.,2009; Pavlov et al., 2012; Senchukova et al., 2012).Currently, the majority of researchers believe that allchars of Lake Kronotskoe originated from one or moreinvasions of an ancestral form, anadromous malmaS. malma (Salmenkova et al., 2005; Ostberg et al.,2009; Pavlov et al., 2012; Senchukova et al., 2012).The pathways of occurrence of the polymorphism ofchars of Lake Kronotskoe are not completely clear.Different researchers propose both allopatric and

Phenetic Diversity and Spatial Structure of Chars (Salvelinus) of the Kronotskaya Riverine�Lacustrine System

(Eastern Kamchatka)S. D. Pavlov, K. V. Kuzishchin, M. A. Gruzdeva,

A. L. Senchukova, and E. A. PivovarovBiological Faculty, Moscow State University, Moscow, 119992 Russia

e�mail:[email protected] December 13, 2012

Abstract—Chars of the genus Salvelinus inhabiting the Kronotskaya riverine�lacustrine system (EasternKamchatka) were studied. It was found that the morphological and genetic polymorphism in chars of LakeKronotskoe is higher than was believed earlier: to date, five forms of chars have been identified in the LakeKronotskoe basin. The description, external morphology and biological attributes of chars inhabiting thebasin of the lake and the anadromous malma (S. malma) from the Kronotskaya River below the rapids aregiven. The differences between the forms of chars are continual, and the outermost forms are often connectedby a continuous series of transitional forms. According to the morphological and genetic characteristics, theanadromous malma from the lower reaches of the Kronotskaya River is not isolated from the lake chars: bythe whole set of characters its position is intermediate between all lacustrine forms. Chars from the Kro�notskaya riverine�lacustrine system are represented by the anadromous malma from the lower reaches of theKronotskaya River and by a metapopulation of lacustrinechars whose forms are not completely isolatedgenetically. Currently, the chars of the Kronotskaya system are in a quasi�stationary state, when an evolution�ary stasis of the lacustrine forms is ensured.

DOI: 10.1134/S003294521306009X

Keywords: biodiversity, chars of the genus Salvelinus, species structure, speciation , microevolution

JOURNAL OF ICHTHYOLOGY Vol. 53 No. 9 2013

PHENETIC DIVERSITY AND SPATIAL STRUCTURE OF CHARS 663

sympatric pattern of speciation. The status of charsremains controversial: some authors recognize that allthree forms of chars already reached the specie’s levelof divergence and, therefore, should be distinguishedas separate species (Viktorovskii, 1978; Glubokovskii,1995; Chereshnev et al., 2001, 2002), while othersbelieve that they are still forms that have not reachedthe level of species isolation (Savvaitova, 1989; Pavlovet al., 2012; Senchukova et al., 2012).

As a result of studying the chars of the Kronotskayariverine�lacustrine system for a number of years(2003–2012), ample and versatile material has beenaccumulated, which extends the existing ideas aboutthe diversity of chars in this water body. In part, thishas been done before when studying various parame�ters (Ostberg et al., 2009; Senchukova et al., 2012) anddescribing individual forms (Pavlov et al., 2012).

The goal of this study was to combine the versatiledata accumulated to date and obtain a complete pic�ture of the relationships and the spatial structure ofchars of the Kronotskaya riverine�lacustrine system.The objectives of this study were to give a morpholog�ical and ecological description of different forms ofchars using an extended material, revisit the existingphenetic diversity, and perform a comparative analysisof the morphological and genetic diversity of charsfrom the Kronotskaya riverine�lacustrine system.

MATERIALS AND METHODS

This study was performed on a samples of chars,obtained in 2003–2010 in different parts of the lakeand its bays and in the source of the KronotskayaRiver, as well as during float trips by the major tributar�ies of the lake (rivers Listvenichnaya, Uzon, andUnana). For a comparative analysis by the morpho�

logical characters, we used a sample of anadromousmalma from the Kronotskaya River that was collectedbelow the rapids in 2010. Fish were caught by hook�and�line technique and a set of fixed gill nets with amesh size of 20 to 60 mm. In total, by different typesof analysis, we examined 408 individuals of differentforms of chars (Table 1, Fig. 1).

Fish collected for morphological description werephotographed and subjected to a complete biologicalanalysis and morphometry according to Pravdin’smodified scheme (Pavlov et al., 2001). In the text, thefollowing designations of characters are used: AC—body length according to Smith; c—head length;cH—height at back of head; D, A, P, V—number ofrays in dorsal, anal, pectoral, and pelvic fins, respec�tively; aD, P–V, V–A—antedorsal, pectoventral, andventroanal distance, respectively; ll—number of per�forated scales in lateral line; sp.br.—number of gillrakers on first gill arch; rb.1, rb.2—number of gill rayson left and right, respectively; pc—number of pyloriccaeca and vert.—number of vertebrae. The originaldrawings presented in this paper were made using fixedspecimens and photographs. The foraging patternswere determined visually after dissection. Some stom�achs were fixed in 4% formaldehyde solution; thecomposition of the bolus in this case was determinedin the laboratory in accordance with the conventionaltechniques (Metodicheskoe posobie …, 1974).

For genetic studies, we selected lacustrine chars offive different forms (nosed, long�headed, white, anddwarf chars and riverine malma) as well as the anadro�mous malma from the Kronotskaya River (Table 1). Toperform generic analysis, tissue samples, which werefixed in 96% ethanol, were taken from each fish(approximately 1�cm2 piece of the pelvic fin). Data oncertain types of genetic analysis and a detailed meth�

Table 1. Material examined in samples of lacustrine chars of the genus Salvelinus and anadromous malma S. malma, col�lected in different years, by the type of analysis (ind.)

Sam�ple no. Form (year of collection) Place

of collectionSample

size, ind.

Type of analysis

bio�analysis

mor�phometry

genetic (published data)

Ostberg et al., 2009

Pavlov et al., 2012

Senchukova et al., 2012

1 Nosed char (2003) Lake Kronotskoe 37 37 25 24 5 28

2 Nosed char (2010) Same 22 – – – – 22

3 White char (2003) '' 62 62 38 52 5 57

4 Dwarf char (2003) '' 4 4 4 4 4 4

5 Riverine malma (2003) '' 37 33 33 28 5 37

6 Long�headed char (2003) '' 14 13 12 14 5 14

7 Long�headed char (2010) '' 9 – – – – 9

8 Anadromous malma (2010) Kronotskaya River 194 194 72 – – 39

9 Anadromous malma (2004) Same 29 – – 13 5 29

Total 408 343 184 135 29 239

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PAVLOV et al.

odology of genetic studies were described in our previ�ous studies (Ostberg et al., 2009; Pavlov et al., 2012;Senchukova et al., 2012). In 135 chars of differentforms, we studied the restriction polymorphism of fourmitochondrial genome regions amplified by poly�merase chain reaction (D�loop, ND2, ND3/ND4, andND5/ND6). Restriction of each site was performedusing 16 endonucleases: CfoI, HaeIII, Hsp92II, MspI,AvaII, DdeI, TaqI, AluI, Bsp143I, Csp61, HinfI,NmuCI, SatI, TaaI, TasI, and TruII (Ostberg et al.,2009). In 29 chars of different forms, we studied therestriction polymorphism of the mitochondrialgenome region comprising the D�loop and the Cyt bgene (approximately 2400 bp total length), which wasamplified by polymerase chain reaction. Restrictionwas performed using four endonucleases: HhaI, TaqI,HaeIII, and MvaI (Pavlov et al., 2012). In 196 of239 chars used for genetic analysis, the controlmtDNA region (D�loop) 558�bp long and the Cyt bgene 1015 bp long (Senchukova et al., 2012) weresequenced and analyzed for variation.

All morphological data was processed by the stan�dard methods of univariate statistics (Lakin, 1990). Inaddition, multivariate statistical methods (James andMcCullach, 1990), in particular the method of princi�pal components, were used. When grouping using themethod of principal components, we calculated vari�ance–covariance matrix; the length of the eigenvectorwas equated to the square root of the eigenvalue(Rholf, 1993). Calculations were performed and chartsand graphs were constructed using the Statistica 7.0 soft�ware.

RESULTS

In modern literature, the status of chars from theKronotskaya riverine�lacustrine system remainsdebatable. In this paper, the groupings of lake charsdistinguished by some authors as S. albus, S. shmidti,and S. cronocius are designated by the term “form”with the corresponding names—the white, nosed, andlong�headed chars. For other chars inhabiting this sys�tem that have not been described in the literature as a

1, 5, 6

3, 6

7

1–78, 9

3

3

5

Lake Kronotskoe

Kronotskaya River

Kronotskaya Riverlower reach

Fig. 1. Schematic map of the Kronotskaya riverine�lacustrine system and sample collection sites. Designations: 1–9, samplenumbers (see Table 1).



species, the names of forms that are commonly used inthe studies of char—the dwarf char, riverine malma,and anadromous malma—were used. This studyrevealed a high plasticity of chars of the Kronotskayasystem and the presence of individuals with transi�tional characters between the previously describedforms. However, the majority of caught fish had thecharacters of one of the five well�differentiated, wide�spread morphotypes that can be differentiated by thelifestyle, foraging patterns, morphology, and geneticcharacteristics.

White Char

D i a g n o s i s. ll 133.9 ± 0.63 (128–143), D 10.2 ±0.10 (9–11), A 9.1 ± 0.10 (8–10), P 12.8 ± 0.10 (12–14), rb.1 12.6 ± 0.09 (12–14), rb.2 12.1 ± 0.08 (11–14), sp.br. 22.3 ± 0.26 (19–26), pc 28.1 ± 0.72 (22–38), and vert. 65.1 ± 0.17 (63–67).

D e s c r i p t i o n. Appearance of mature whitechars varies significantly (Figs. 2a–2d). Sexuallymature fish (AC > 450 mm) with cone�shaped, mas�sive, high head (c about 22% of AC, cH about 14% ofAC), rounded on top, short snout, and jaws of equallength (Table 2). Large males (AC > 650 mm) have apronounces kype on a lower jaw and recess in maxilla.Mouth large, terminal; maxillary bone straight, some�times curved downward, and goes far beyond rear edgeof eye. Both jaws, palatine bones, and tongue coveredwith strong sharp canine teeth. Postorbital distancemore than twice greater than preorbital distance. Bodymassive and terete before dorsal fin and laterally com�pressed, high, and thin behind it. Maximum height ofbody situated at approximately 1/2 of aD. Base of cau�dal fin rounded or trapezoidal; caudal fin often trun�cated, more rarely slightly forked or convex. Pectoralfins usually acuminate, more rarely rounded, and long(their length varies from 1/2 to 3/4 of the P–V dis�tance). Pelvic fins usually acuminate and long (morethan 1/2 of the V–A distance). Immature fish(AC 250–450 mm) with tapered head, mandibles ofequal length, and straight maxillary bone that goesbeyond rear edge of eye. Body is terete, its maximumheight observed at beginning of dorsal fin (Fig. 2e).Pectoral and pelvic fins long and acuminate, and cau�dal fin is forked.

M o r p h o l o g i c a l c h a r a c t e r s of whitechar are summarized in Table 2.

C o l o r of white chars varies significantly depend�ing on stage of maturity of gonads. In individuals withgonads of stages III and III–IV of maturity, head andtorso along back are light green, gray, or olive. Sides ofbody silver, light green, or light olive; belly white, morerarely yellowish. On back, multiple (at least 5–6 per1 cm2) bright spots less than one third diameter ofpupil. On sides of body, these spots are less numerous(2–3 per 1 cm2) and larger (up to 1/2 diameter ofpupil), of bright, pinkish, yellowish, or light�purplecolor. Lower jaws gray or dirty�yellow with dark bor�

der. Dorsal and caudal fins dark gray, without spots;sometimes individuals with light border around edgeof caudal fin. Pectoral and pelvic fins gray with brownor reddish outer edge; unbranched rays with lightercolor. Anal fin light gray with reddish tinge; its frontedge light, almost white.

Individuals with gonads of stages IV, IV–V, and Vof maturity with well�expressed breeding color. Theirhead dark, almost black; mandibles bright orange; pal�ate black. Back olive or light brown; sides green; bellyred, bright orange, yellow, or pink. Spots on sides ofbody become bright pink or red. Dorsal and caudalfins dark or brownish red, and pectoral, pelvic, andanal fins red with milky white front edge.

White chars had numerous parasites in body cavityon internal organs, and gut tightly adhered to abdom�inal cavity lining.

In summer and autumn period, individuals withhigh and thin (lorate) body sometimes encounteredamong large white chars (Fig. 2d). They have dispro�portionately massive head and long, low, strongly lat�erally compressed body with long caudal peduncle.Greatest height of body in such fish observed immedi�ately behind head or a distance of approximately onethird between back of the head and beginning of dorsalfin. Such fish have gonads of VI–II stages. Femalescontain a significant amount of unspawned eggs inbody cavity; gonads of males deflated, dark red or pur�ple. Apparently, these individuals experienced spawn�ing in the previous year and continue to recover fromit; judging by state of gonads, such fish will spawn nexttime at least in one year.

S i z e , a g e , a n d s e x c o m p o s i t i o n. Inour samples, AC of white chars varied from 385 to900 mm (on average, 537); weight varied from 500 to5500 g (1526 g). Maximum age 18 years; majority ofmature were 6–10 years old. Maturation occurs start�ing from age 6+, at AC of approximately 300 mm.After onset of puberty, chars usually breed once every2–3 years. Sizes of the white chars in different parts oflake generally similar. Typically, large individuals areextremely rare in the outlet region of the KronotskayaRiver, whereas small individuals are not encounteredalong the northeast shore of the lake (“La Manche”area). Growth in the course of development is charac�terized by a considerable unevenness. In first 4 years oflife, growth rate is relatively low, then increases, andafter age of 7+ increases dramatically due to the tran�sition of the fish diet. Relationship between length(AC, mm) and weight (W, g) of the body is describedby the equation W = 285.24 – 33.27AC + 1.08AC2. Sexratio in juvenile and adult fish is approximately 1 : 1;among the largest older chars, proportion of malesslightly greater (56%).

D i e t. During the life span of individual white char,substantial dietary changes are observed (Table 3).Immature and mature individuals (AC < 460 mm) feedprimarily on benthic invertebrates; after reaching this

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PAVLOV et al.

(а)

(b)

(c)

(d)

(e)

0 5 cm

0 10 cm

Fig. 2. Appearance of chars of the genus Salvelinus of the Kronotskaya riverine�lacustrine system. (a–e) White chars ((a, b)mature females with gonads of maturity stages IV and IV–V, respectively; (c) male with gonads of maturity stage IV–V; (d) femaleskipping spawning; and (e) immature fish); (f–k) mature nosed chars; (l, m) long�headed chars; (n) dwarf char; (o) riverinemalma; (p, q) anadromous malma of the Kronotskaya River (p—female, stage IV; q—male, stage IV–V).



(f)

(g)

(h)

(j)

(k)

0 5 cm

(i)

Fig. 2. (Contd.).

length, white chars start feeding fish. Their main fooditem is kokanee.

L i f e s t y l e , d i s t r i b u t i o n , a n d a b u n �d a n c e. White char is a lacustrine form and spends alarge part of its life cycle in Lake Kronotskoe. It forms

a schools, more rarely can be found alone, andmigrates along the shoreline. White chars spawn in thelake; however, some fish breed in large rivers flowinginto the lake (Listvennichnaya, Unana, and Uzon),where we encountered ripe spawners. The white char

668


PAVLOV et al.

(l)

(m)

(n)

(p)

(q)

0 8 cm

(o)

0 5 cm

0 4 cm

0 10 cm

Fig. 2. (Contd.).



Table 2. Morphometric characteristics of different forms of chars of the genus Salvelinus from the Kronotskaya riverine�lacustrine system

Char�acters

Form (number of fish, ind.)

white char (38) nosed char (25) long�headed

char (12)riverine

malma (33)dwarf

char (4)anadromous malma (72)

in % AC

c

ao

o

op

io

cH

lmx

hmx

lmd

H

h

lpc

lD

hD

lA

hA

lP

lV

aD

22.31 0.18 1.13( )±

20.2–25.2�� 20.15 0.28 1.42( )±

17.9–23.7�� 24.38 0.25 0.83( )±

23.2–25.6�� 21.80 0.25 1.46( )±

19.4–25.3�� 21.30 0.35 0.71( )±

20.6–22.0�� 20.44 0.17 1.43( )±

17.9–24.8��

6.40 0.14 0.87( )±

4.6–8.6�� 5.40 0.16 0.79( )±

4.2–7.3�� 7.87 0.23 0.79( )±

6.9–9.6�� 6.16 0.16 0.94( )±

4.6–8.4�� 5.96 0.19 0.38( )±

5.4–6.3�� 5.79 0.12 1.05( )±

4.2–9.7��

2.58 0.05 0.32( )±

2.0–3.4�� 2.86 0.09 0.45( )±

2.2–3.9�� 2.55 0.07 0.23( )±

2.2–3.0�� 2.64 0.08 0.46( )±

1.9–4.0�� 3.93 0.18 0.37( )±

3.5–4.3�� 2.98 0.03 0.26( )±

2.4–3.8��

12.20 0.12 0.72( )±

10.1–13.8�� 11.08 0.14 0.73( )±

9.9–13.3�� 12.50 0.15 0.48( )±

11.7–13.0�� 11.94 0.11 0.64( )±

10.7–13.2�� 11.80 0.27 0.54( )±

11.1–12.3�� 11.57 0.06 0.51( )±

10.3–12.7��

7.65 0.08 0.51( )±

6.7–9.1�� 7.34 0.13 0.68( )±

6.3–8.7�� 7.85 0.17 0.59( )±

6.6–8.8�� 7.84 0.16 0.95( )±

6.3–9.7�� 7.58 0.62 1.25( )±

6.5–9.2�� 7.25 0.05 0.43( )±

6.4–8.1��

14.46 0.16 0.93( )±

12.8–16.5�� 13.60 0.17 0.85( )±

11.8–15.1�� 13.43 0.24 0.82( )±

11.8–14.6�� 14.41 0.17 0.98( )±

12.5–16.6�� 14.80 0.26 0.52( )±

14.4–15.5�� 12.86 0.08 0.66( )±

11.4–14.4��

9.01 0.12 0.76( )±

7.4–10.4�� 7.68 0.15 0.75( )±

6.4–9.4�� 9.94 0.21 0.75( )±

8.6–11.8�� 8.60 0.14 0.80( )±

7.4–10.3�� 8.69 0.50 1.00( )±

8.1–10.2�� 8.55 0.13 1.12( )±

7.1–11.5��

1.62 0.05 0.29( )±

1.13–2.25�� 1.65 0.03 0.18( )±

1.21–1.92�� 1.55 0.07 0.25( )±

1.23–1.91�� 1.73 0.03 0.21( )±

1.26–2.06�� 1.98 0.14 0.28( )±

1.69–2.30�� 1.45 0.02 0.15( )±

1.2–1.8��

14.09 0.19 1.19( )±

12.0–17.0�� 11.30 0.26 1.29( )±

9.2–13.8�� 15.55 0.27 0.94( )±

14.2–17.9�� 13.25 0.24 1.39( )±

11.1–17.3�� 12.85 0.33 0.67( )±

12.5–13.8�� 13.44 0.22 1.91( )±

10.4–19.6��

19.25 0.37 2.29( )±

15.7–23.6�� 20.67 0.47 2.36( )±

17.2–24.3�� 17.08 0.27 0.95( )±

15.8–19.5�� 20.51 0.38 2.21( )±

17.0–25.5�� 20.87 0.36 0.72( )±

20.0–21.8�� 20.12 0.18 1.55( )±

16.3–23.1��

7.09 0.08 0.49( )±

6.2–8.3�� 7.57 0.08 0.38( )±

6.8–8.4�� 6.73 0.11 0.37( )±

6.0–7.3�� 7.37 0.08 0.47( )±

6.5–8.4�� 7.88 0.60 1.19( )±

6.6–9.3�� 7.48 0.04 0.35( )±

6.7–8.4��

17.90 0.14 0.89( )±

16.0–20.9�� 17.99 0.21 1.04( )±

15.1–20.5�� 17.53 0.24 0.81( )±

16.6–19.0�� 18.05 0.15 0.86( )±

16.5–20.1�� 18.18 0.51 1.01( )±

16.8–19.0�� 18.82 0.10 0.82( )±

17.0–20.6��

11.9 0.12 0.77( )±

10.0–13.6�� 11.79 0.15 0.77( )±

10.0–13.2�� 10.10 0.24 0.83( )±

9.2–12.2�� 11.41 0.13 0.77( )±

9.9–12.9�� 13.10 0.36 0.72( )±

12.2–13.9�� 11.77 0.08 0.65( )±

10.0–13.5��

12.00 0.15 0.92( )±

10.4–14.8�� 12.73 0.31 1.55( )±

11.2–17.8�� 10.12 0.24 0.83( )±

9.0–11.7�� 11.73 0.22 1.28( )±

8.1–14.4�� 15.13 1.18 2.36( )±

11.8–17.3�� 13.52 0.14 1.17( )±

10.4–15.7��

7.74 0.08 0.50( )±

6.8–9.2�� 8.26 0.10 0.51( )±

7.1–9.2�� 7.29 0.23 0.78( )±

5.7–8.8�� 8.10 0.14 0.78( )±

6.7–10.2�� 9.57 0.52 1.05( )±

8.2–10.8�� 9.07 0.08 0.66( )±

7.8–12.6��

13.25 0.16 1.02( )±

11.4–16.5�� 13.94 0.24 1.21( )±

12.0–16.5�� 11.37 0.16 0.55( )±

10.5–12.1�� 13.22 0.19 1.09( )±

11.7–15.8�� 14.62 0.98 1.96( )±

12.5–17.2�� 13.32 0.13 1.14( )±

8.3–15.9��

14.34 0.18 1.12( )±

11.9–16.8�� 15.58 0.41 2.08( )±

13.8–22.1�� 12.29 0.30 1.04( )±

10.6–14.6�� 14.38 0.24 1.38( )±

11.6–17.0�� 16.39 0.18 0.35( )±

16.1–16.9�� 14.12 0.15 1.26( )±

12.0–17.1��

11.95 0.17 1.08( )±

10.8–15.3�� 12.69 0.38 1.89( )±

10.2–18.1�� 9.99 0.27 0.94( )±

8.3–11.5�� 11.84 0.21 1.24( )±

9.9–14.6�� 13.88 0.56 1.13( )±

12.9–15.5�� 12.43 0.17 1.47( )±

10.0–16.5��

42.82 0.17 1.07( )±

40.5–44.5�� 41.87 0.31 1.54( )±

38.3–45.4�� 45.01 0.33 1.15( )±

43.2–46.7�� 42.69 0.26 1.49( )±

39.3–46.7�� 42.21 0.40 0.80( )±

41.2–43.1�� 41.37 0.16 1.32( )±

37.4–45.4��

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PAVLOV et al.

is a common form of chars in Lake Kronotskoe thatdominates in all catches. In the lake, this is ubiquitousand frequently occurs along the shore and near theislands but is less common in the open area. Whitechars form feeding and spawning aggregations in theoutlet area of the Kronotskaya River and near themouths of Listvennichnaya, Unana, and Uzon rivers.

Nosed Char

D i a g n o s i s. ll 132.1 ± 0.74 (122–139), D 10.2 ±0.09 (9–11), A 9.0 ± 0.13 (8–10), P 12.8 ± 0.10 (12–14),rb.1 12.5 ± 0.15 (10–13), rb.2 11.9 ± 0.11 (11–13),

sp.br. 21.3 ± 0.29 (18–24), pc 27.7 ± 0.76 (22–37), andvert. 65.3 ± 0.22 (63–67).

D e s c r i p t i o n. By shape of head, snout, andmaxillary bones and shape and size of fins, nosed charsshowed a high level of morphological diversity (Figs. 2f–2k). Head, on average, small (с approximately 20% ofAC); the upper jaw always longer than lower jaw andhangs over it. Some individuals with broad, roundedsnout (Figs. 2f, 2g, 2j, 2k); more elongated and acumi�nate in others (Figs. 2h, 2i). Maxilla of nosed char cov�ered by thick skin and connective tissue; front edge ofupper jaw also covered with thick skin. Maxilla straight

Table 2. (Contd.)

Char�acters

Form (number of fish, ind.)

white char (38) nosed char (25) long�headed

char (12)riverine

malma (33)dwarf

char (4)anadromous malma (72)

pD

aV

aA

P–V

V–A

Above the line are the mean value and its error (the standard deviation is shown in parentheses); below the line are the limits of variationof the index. Designation of characters: c—length of head; ao—length of snout; o—horizontal diameter of eye; op—postorbital dis�tance; io—interorbital distance; cH—head height at back of head; lmx—length of maxilla; hmx—height of maxilla; lmd—length ofmandible; H—maximum height of body; h—height of caudal peduncle; lpc—length of caudal peduncle; lD, lA—length of base of dor�sal and anal fins, respectively; hD, hA—height of dorsal and anal fins, respectively; lP, lV—length of pectoral and ventral fins, respec�tively; aD, pD, aV, aA, P–V, V–A—antedorsal, postdorsal, anteventral, anteanal, postventral, and ventroanal distance, respectively.

40.86 0.22 1.35( )±

38.6–43.9�� 40.79 0.42 2.10( )±

37.5–48.7�� 39.21 0.10 1.39( )±

36.8–41.6�� 40.52 0.21 1.20( )±

37.9–42.3�� 40.70 1.23 2.47( )±

37.5–43.5�� 41.49 0.14 1.23( )±

38.3–44.4��

49.92 0.17 1.08( )±

47.9–53.4�� 47.89 0.34 1.70( )±

44.8–51.7�� 50.94 0.34 1.18( )±

47.9–52.3�� 49.27 0.25 1.42( )±

46.4–52.3�� 48.04 0.47 0.93( )±

46.7–48.6�� 47.27 0.18 1.49( )±

44.0–52.1��

68.82 0.20 1.26( )±

67.2–72.2�� 67.97 0.33 1.64( )±

64.8–71.1�� 70.24 0.31 1.06( )±

68.3–71.7�� 68.93 0.20 1.17( )±

66.9–70.8�� 67.24 1.05 2.11( )±

64.1–68.6�� 66.88 0.17 1.41( )±

64.5–70.9��

27.02 0.27 1.66( )±

23.8–31.6�� 28.10 0.37 1.85( )±

24.4–31.8�� 26.86 0.52 1.72( )±

24.5–29.7�� 27.26 0.22 1.24( )±

25.4–30.7�� 26.88 0.23 0.46( )±

26.4–27.4�� 26.38 0.17 1.41( )±

22.4–29.6��

20.37 0.23 1.39( )±

18.1–24.5�� 21.78 0.36 1.79( )±

17.9–24.3�� 20.66 0.44 1.52( )±

17.8–23.1�� 21.05 0.22 1.29( )±

18.9–24.3�� 20.64 0.22 0.43( )±

20.0–20.9�� 21.04 0.15 1.32( )±

18.0–24.6��

Table 3. Bolus composition in white char (genus Salvelinus) individuals of different size in Lake Kronotskoe, %

Food itemsSize groups, mm (number of fish, ind.)

180–260 (15) 261–360 (12) 361–460 (15) >460 (17)

Fish – – 13.4 81.3

Chironomidae larvae 45.4 39.3 10.1 –

Chironomidae pupae 20.2 21.2 13.1 3.1

Trichoptera larvae 18.9 20.7 25.0 3.2

Stoneflies (Plecoptera) – – 1.2 1.3

Insecta imagoes – 6.5 5.8 6.2

Amphipoda (Gammaridae) 3.2 2.6 6.7 –

Mollusca 4.6 5.4 13.0 4.4

Kokanee eggs – – 4.9 –

Plant residues – – – 0.5

Unidentifiable remains 7.7 4.3 6.8 –



or curved concave downwards; does not reach orreaches rear edge of eye but does not protrude beyondit. Small weak teeth on upper jaw, palatine bones, andtongue; they are almost hidden under skin on maxil�lary bone. Body elongated and laterally compressed;most high at beginning of dorsal fin. Caudal pedunclelong and low and strongly compressed laterally. Baseof caudal fin usually rounded, less frequently trapezoi�dal; caudal fin forked. The length of pectoral and pel�vic fins varies significantly. In some fish, pectoral andpelvic fins are very long: pectoral fins almost reachbase of ventral ones, and latter reach base of anal fin,with their apices being sharpened (Figs. 2g, 2j, 2k). Inother fish, fins are less long: length of pectoral fins var�ies from 1/2 to 3/4 f P–V; abdominal fins, from 1/3 to2/3 of V–A. In some fish, pectoral and ventral finsshort—less than 1/3 of P–V and less than 1/3 of V–A,respectively (Figs. 2f, 2h, 2i).

M o r p h o l o g i c a l c h a r a c t e r s. A number ofmorphometric characters of nosed chars are charac�terized by wide variation limits and a considerable dis�persion. This primarily applies to length of pectoraland pelvic fins (Table 2).

C o l o r. Similar color of mature and immaturenosed chars. Back brown or dark olive; sides lightbrown, green, or dark green, never light or silver; bellybright, pink, orange, or red. Numerous pink, orange,or red spots approximately half the diameter of pupilon sides of body. Jaws orange, dirty yellow with blackor dark border. Pectoral, pelvic, and anal fins brightred; front edge of them milk�white. Dorsal and caudalfins reddish brown or reddish with distinct borderaround edge. Spawning males and females of nosedchar (IV–V and V maturity stages of gonads) withsomewhat brighter and more contrasting color com�pared to fish that skip spawning.

S i z e, a g e, a n d s e x c o m p o s i t i o n. In oursamples, nosed chars 190–500 mm (on average,368 mm) in length and with weight of 160–1200 g(on average, 526 g). Maximum age 10 years; majorityof mature individuals 4–8 years of age; seven�year�old(6+) individuals occurred most commonly. In general,size and weight of nosed chars in the lake vary insignif�icantly. In the outlet area of the Kronotskaya River,small younger chars are more common; in Krashenin�nikov Bay and in the near�estuary area of the Listven�nichnaya River, larger and older individuals occurmore frequently. Nosed chars become mature at anage of 4+ at AC 260–280 mm. Reproduction occursannually in approximately 60% of mature fish, andother fish breed once in two years. The growth ofnosed char is even throughout life, which is probablyassociated with a similar type of feeding at differentages and different body length. The relationshipbetween length and weight of body is described by theequation: W = 625.27 – 54.84AC + 1.30AC2. The ratioof males and females is equal.

D i e t. According to foraging typenosed chars aretypical benthophages; major part of their diet is com�

posed of invertebrates. In contrast to the diet of smallindividuals, a key component of the diet of large indi�viduals is scuds (Gammaridae), whereas chironomidlarvae are less important (Table 4).

L i f e s t y l e , d i s t r i b u t i o n , a n d a b u n �d a n c e. The nosed chars inhabit coastal areas of thelake at relatively shallow depths (8–10 m). Catches inthe open part of the lake were not registered reliably. Itleads a gregarious life and is found near the shorelineof the lake, including the vicinities of islands. Cases ofcatches of single nosed chars in the lower reaches ofthe Listvenichnaya River were reported. Breedingtakes place in the lake. The nosed char is an abundantform of chars in Kronotskoe Lake, comparable inabundance with white char.

Long�Headed Char


D e s c r i p t i o n. Head long (с > 23.2% of AC),cone�shaped, low (cH approximately 13% of AC), flaton top, with large postorbital distance. Snout long,jaws of equal length. Mouth large and terminal; max�illa straight or slightly curved concave upwards andgoes far beyond rear edge of eye. Jaws, palatine bones,and tongue covered with large canine teeth. Bodyelongated and terete; caudal peduncle long and low,rounded in cross�section. Greatest height of bodyobserved at beginning of dorsal fin. Base of caudal finbroad and rounded; caudal fin wide, its shape variesfrom forked to truncated. Pectoral and pelvic finsshort: less than 1/3 of P–V and less than 1/2 of V–A,respectively (Figs. 2l, 2m).

M o r p h o l o g i c a l c h a r a c t e r s are summa�rized in Table 2.

Table 4. Composition of the bolus in nosed char (genusSalvelinus) individuals of different size in Lake Kronotskoe, %

Food itemsSize groups, mm

175–260 261–360 361–460

Chironomidae larvae 47.5 41.6 27.4

Chironomidae pupae 21.2 19.3 26.8

Trichoptera larvae 19.9 18.2 21.5

Plecoptera larvae 3.3 4.4 3.4

Coleoptera larvae 0.1 1.0 0.5

Musca larvae – 0.1 –

Amphipoda (Gammaridae) 3.7 8.9 16.0

Mollusca 3.4 5.2 4.4

Unidentifiable remains 0.9 1.3 –

672


PAVLOV et al.

C o l o r. Color of back of fish with gonads of matu�rity stages III–IV and IV gray, dark gray, or gray with abluish tinge; sides silvery or gray�silver; belly milkywhite. Head dark on top, with silvery sides; mandiblewhite. Some individuals have scarce (less than one per1 cm2) large contrasting light spots on sides of body,which reach three fourth or one diameter of pupil.Others have small (less than one third of diameter ofpupil) numerous light spots on sides of body. Spot oncaudal peduncle more rare and larger than in frontpart of body. Pectoral fins gray or dark; ventral and analfins light, their first rays do not differ in color fromother fins. Caudal fin gray or dark, its rays are silver atbase. Spawning color of long�headed chars (withgonads of stages IV–V and V of maturity) differs fromthat of immature fish by darker background of body:back dark, almost black; sides of body dark gray; bellydirty�gray with yellowish tint; whole head, includingmaxilla and mandible, black. Spots on sides of bodylight with pink tint and blurred edge.

S i z e , a g e , a n d s e x c o m p o s i t i o n.In our samples, body length of chars varies in the range321–750 mm (on average, 570 mm); weight varied inthe range 1000–2500 g (on average, 1721 g); maxi�mum age was 18 years, majority of mature fish were 6–11 (usually 8) years of age. Maturation occurs at an ageof 6+ at AC approximately 400 mm. After reachingsexual maturity, long�headed chars breed usually oncein 2–3 years. The sex ratio is approximately equal.

D i e t. By foraging type, long�headed chars aretypical predators: only fish was found in stomachs ofanimals with AC > 300 mm. The main food item ofthese chars is adult sockeye kokanee and its young;occasionally, they can feed on juvenile chars.

L i f e s t y l e , d i s t r i b u t i o n , a n d a b u n �d a n c e. By lifestyle, long�headed char is a singlepredator, which is found throughout the lake both nearthe shoreline and in the open part of the lake, at greatdepths. It does not form schools. The abundance oflong�headed chars is low; this is a fairly rare form inLake Kronotskoe.

Riverine Malma

This form in Lake Kronotskoe was mentioned ear�lier by Pavlov et al. (2003). It was used in the compar�ative analysis by Ostberg et al. (2009); however, itsdescription is given here for the first time.


D e s c r i p t i o n. Shape of head conical, snoutrounded, maxillary bone slightly extends beyond rearedge of eye. Head large (с 21.8% AC) and high(ch 14.4% AC). In small fish, lower jaw slightly shorterthan upper jaw (in this case, mouth occupies a distinctsemi�inferior position); in larger mature fish, jaws of

equal length. Maxillary, palatine, and lingual bonecovered with numerous small weak teeth. Body trout�like, slightly laterally compressed; maximum heightobserved at beginning of dorsal fin. Caudal pedunclelong (on average, 18.05% of AC), round in cross�sec�tion. Base of caudal fin trapezoidal or rounded, caudalfin forked or slightly forked. Pectoral fins small, rounded,or slightly acuminate, usually less than half of P–V, morerarely equal to one half of P–V (Fig. 2o).


C o l o r. Back dark green, dark, or almost black;sides of body greenish or green; belly yellow or pink.Upper part of head dark; sides of head dark green; bot�tom of head light. Some fish (AC > 450 mm) with 9–11 round spots (parr marks) on sides of body arrangedin a single row; however, these spots missing on bigfish. On sides of body, numerous spherical or irregu�larly shaped pink or bright red spots. Below lateralline, size of spots reaches 1/2–3/4 of pupil diameter;somewhat smaller above lateral line. Fins dark red orred, their front edge milky white. Caudal fin dark redwith red, orange, or dirty�yellow border.

S i z e , a g e , a n d s e x c o m p o s i t i o n. Inour samples, body length of riverine malma varied inthe range 284–600 mm (on average, 448 mm); weightvaried in the range 210–2200 g (on average, 884 g).Maximum age was 8 years; mature fish mostly repre�sented by individuals of age 6+. Onset of maturation isat an age of 5+. Breeding occurs apparently annually.Sex ratio is approximately equal. Samples from theoutlet area of the Kronotskaya River and from theUnana River were similar in the age structure but dif�fered slightly in the size–weight characteristics: in thesame age groups, individuals from the Unana Riverwere smaller.

D i e t. By foraging type, riverine malma is a ben�thophage; basis of its diet is formed by amphibiotic lar�vae of insects (stoneflies, mayflies, caddis flies, chi�ronomids). The composition of bolus varies greatly indifferent seasons of the year; as a rule, riverine malmafeeds on the most abundant and readily available fooditems.

L i f e s t y l e , d i s t r i b u t i o n , a n d a b u n �d a n c e. Riverine malma inhabits all rivers flowinginto Lake Kronotskoe (Unana, Uzon, Listvennich�naya) and the Kronotskaya River flowing out of thelake (from the source of the river to the rapids). Leadsa riverine life; however, at low water in summer, it canleave the rivers and come out to the surrounding areasof the lake for feeding; usually, the largest specimensenter the lake. In rivers, riverine malma is usuallyencountered on stretches and in pits under rapids. Incomparison to the white and nosed chars, its abun�dance is low.



Dwarf Char

The first description of this form of Lake Kro�notskoe was made by Pavlov et al. (2012). Advanceddata on the dwarf char are presented below.

D i a g n o s i s. ll 130.0 ± 1.08 (128–133),D 10.5 ± 0.29 (10–11), A 9.0 ± 0.41 (8–10), P 13.0 (–),rb.1 12.0 ± 0.41 (11–13), rb.2 12.0 ± 0.41 (11–13),sp.br. 22.0 ± 1.08 (20–25), pc 28.0 ± 1.47 (25–32),vert. 66.0 ± 0.41 (65–67).

D e s c r i p t i o n. Head rounded, large (c > 20.6%of AC), moderately high (cH 14.8% of AC). Snoutslightly acuminate, jaws of equal length, mouth alwaysterminal. Size of mouth different: maxillary bone cango beyond rear edge of eye, reach rear edge of eye, ornot reach it. Jaws, palatal and lingual bones, andvomer head covered with well�defined, multiple, tightlyfitting teeth. Eyes large (3.93% of AC). Body trout�like,terete, greatest body depth measured at dorsal fin (onaverage, 21% of AC); caudal peduncle moderately long(18% of AC). Pectoral fins wide, rounded, and short(less than 1/2 P–V in length) (Fig. 2n).

M o r p h o l o g i c a l c h a r a c t e r s are summa�rized in Table 2. In general, dwarf char of Lake Kro�notskoe is characterized by the presence of juvenilefeatures in appearance, which is characteristic ofmature individuals of other forms of dwarf chars of thegenus Salvelinus (Savvaitova, 1989); however, it is welldistinguished from them by terminal position ofmouth.

C o l o r. Back dark green, sides olive, fins brightorange. Oval parr marks on sides of body. Body coveredwith small bright orange spots reaching 1/3–1/2 eyediameter. Spots on fins absent. Fins dark; edges of pec�toral, pelvic and anal fins reddish. Unbranched rays Vand A milky white.

S i z e , a g e , a n d s e x c o m p o s i t i o n. Inour sample, body length of dwarf chars varied in therange 195–296 mm (on average, 240 mm), and weightvaried in the range 72–250 g (on average, 151 g). Max�imum age was 4+; mature males and females aged 3+and 4+. Sex ratio was approximately 1 : 1.

D i e t. In stomachs of caught specimens, we foundalgae and planktonic crustaceans.

L i f e s t y l e , d i s t r i b u t i o n , a n d a b u n �d a n c e. Dwarf char is a scarce, rarely occurring formfound in Lake Kronotskoe only at the outlate area ofthe Kronotskaya River. The first single dwarf maleswere caught by Viktorovskii (1978).

Anadromous Malma

For anadromous malma in lower reaches of theKronotskaya River, a high level of polymorphism incolor and shape of body and size of fins was detected(Gruzdeva et al., 2011). This heterogeneity wasobserved only in anadromous malma in the Kro�notskaya River basin; in the neighboring BogachevkaRiver, malma had exclusively typical coloration. It is

possible that there is the zone of the secondary contactof anadromous malma with its derivatives (lacustrinechars) in the Kronotskaya River below the rapids. Dif�ferent forms may undergo hybridization, which isreflected in their high polymorphism in the bodyshape (Gruzdeva et al., 2012). For comparison withthe lacustrine chars , we used only the typical speci�mens of anadromous malma.


D e s c r i p t i o n. Head of males conical (females,rounded), small (c ~ 20% of AC), and low (cH 2.9% ofAC). Mouth terminal, jaws of equal length. Largemales (AC > 400 mm) have a kype on a lower jaw andnotch on a snout. Maxillary bone either straight(approximately in half of fish) or slightly curved con�cave upwards and always extends beyond rear edge ofeye. Postorbital distance exceeds preorbital distanceno more than 1.5 times. Fish that just have come fromthe sea with small, slightly curved teeth on mandiblesand palatine bones; on tongue, teeth small and almostcompletely hidden under skin. Body streamlined,cigar�like, and terete; caudal peduncle rounded incross�section. Base of caudal fin usually rounded,more rarely trapezoidal. Caudal fin slightly forked,with pointed tops of blades. Pectoral and pelvic finsshort (length of pectoral and ventral fins <1/2 of P–Vand <1/2 of V–A); edges acuminate (Figs. 2p, 2q).


C o l o r. Color of anadromous malma depends ontime spent in the river after arrival from the sea and onmaturity stage of gonads. Individuals with gonadsmaturity stage III that recently arrived from the sea(no more than 2 weeks ago), with gray or gray withsteel, turquoise, or purple shades of back and top ofhead, bright silvery sides of body and gill covers, andmilky white belly and mandible. On sides of body, lightspots with a blurred edge. Pectoral, pelvic, and analfins light and transparent; dorsal and caudal fins gray;base of caudal fin rays silvery or pearlescent. Beforespawning (first half of September), individuals withgonads of maturity stages IV–V and V acquire spawn�ing color.

The spawning color of anadromous malma fromthe Kronotskaya River is characterized by polymor�phism, which fits into two color forms. Color of form 1:back and sides of body olive, green, or purple; belly pinkor reddish; pink or bright pink contrasting spots on sidesof body, which are small (approximately 1/2 diameter ofpupil) and multiple (up to 3–4 per 1 cm2) on back. Onsides of body, spots are rarer and more comparablewith the diameter of pupil. Pectoral, pelvic, and analfins red; their front edge milky white. Caudal fin darkwith reddish rim along outer edge. Head dark, almostblack; jaws dirty orange; oral cavity, including palate

674


PAVLOV et al.

and tongue, black. Color of form 2: back and sidespurple or dark purple; belly orange, yellow, or yellow�ish; jaws yellow or dirty�yellow. Spots on sides of bodysmall (less than 1/2 diameter of pupil), yellowish, yel�low, orange, or red, with blurred edge. Paired and analfins dark red or dirty pink; their front edge milkywhite. Both color forms occur together, both in malesand females; no differences in length and weight andmorphometric characters between them have beenfound.

S i z e , a g e , a n d s e x c o m p o s i t i o n.In our samples, anadromous malma was represented byindividuals 312–585 mm long (on average, 409 mm)weighing 354–1760 g (on average, 661 g). The maxi�mum age was 8 years; the modal age class was formedby five�year�old (4+) individuals. The sex ratio isapproximately equal. Maturation occurs at age of 3+at AC 320–400 mm. After reaching sexual maturity,anadromous malma spawns annually.

D i e t. After coming from the sea to the river,anadromous malma does not feed for 1–2 weeks.Later, it begins to feed on larvae and adults of amphib�iotic insects (mainly mayflies and stoneflies). Duringmass spawning of pink salmon Oncorhynchus gorbu�scha, anadromous malma switches to feeding on itseggs. Occasionally, remains of small terrestrial mam�mals (shrews of genus Sorex) are found in the stomachof malma.

L i f e s t y l e , d i s t r i b u t i o n , a n d a b u n �d a n c e. In anadromous malma stock, several life his�tory patterns can be distinguished. Anadroms (typi�cally anadromous) individuals—juveniles live in theriver for several years, then they undergo smoltifica�tion and migrate to the sea. After migration, they fat�ten for several years in the sea before the onset of mat�uration. Mature individuals perform spawning migra�tion back into the river. Thousanders (term givenaccording to Savvaitova (1989))—juveniles first live inthe river, then undergo smoltification and migrate tothe sea. After several months of fattening they returnback to the river for autumn fattening and wintering.The following spring, they again perform seawardmigration and continue fattening before the onset ofmaturation or until the next wintering in the river. Res�ident (nonanadromous) individuals—the entire life�cycle of these fish proceeds in fresh water, withoutmigration to the sea. Within a river system, such indi�viduals can perform catadromous and anadromousmigrations, enter the major tributaries and go back tothe mainstream. Resident individuals have a darkcolor throughout the year, a bright orange belly, andcontrasting pink and red spots on the sides of the body.Dwarf males—individuals that retained the juvenileappearance (body proportions and color), whichreached the maturation in the river and spawn togetherwith the anadromous and resident fish.

Anadromous fish migrate from the sea to the riverin July and early August. After the migration from thesea, the anadromous malma are widely distributed

over the Kronotskaya River. In July, they reach thepiedmont area and enter the major tributaries(Khryukina and Lebyazh’ya rivers). In July and earlyAugust, the catches in the lower reaches of the Kro�notskaya River contain mainly silver specimens; start�ing from the second half of August, the mature fishacquire the spawning color of varying degrees ofexpression. In the piedmont area, especially in itsupper part, all anadromous individuals have more orless pronounced spawning color. In the second half ofAugust and September, anadromous migration ofsmall thousanders is observed. The anadromousmalma and its juveniles are found in the KronotskayaRiver until the rapids (at a distance of 30 km from thesea). The abundance of the anadromous malma ishigh; this is a common species in the KronotskayaRiver below the rapids.

Individuals with an Intermediate State of Characters

Despite the fact that the majority of caught fishcorrespond sufficiently well to the described morpho�types, some specimens occurring in the Kronotskayariverine�lacustrine system basin cannot be classified byappearance with any of the forms described above.They occupy an intermediate position between thewidespread forms. This group includes the individualswith a rounded head and a big semi�inferior mouth(the maxillary bone extends beyond the rear edge ofthe eye); the sides of the body of such fish are lightgreen or gray with a greenish tinge, and the greatestheight of the body is observed in front of the dorsal fin.These fish have similarities with both the white andnosed chars. In addition, there are fish with a big head,big mouth, and maxillary bone curved upward. How�ever, the body of these fish is high (the greatest heightis in front of the dorsal fin), and the sides of the bodyare gray or light green; these fish are intermediatebetween the white and long�headed chars. Catchesalso contained medium�sized (AC ≈ 300 mm) maturefish whose lower jaw was somewhat shorter than theupper jaw, but the position of their mouth could not becharacterized as semi�inferior. In a strict sense, thesefish cannot be attributed by appearance to the nosedchar; they are more similar to the dwarf char butexceed it in size.

In the lower reaches of the Kronotskaya River,along with the anadromous malma, which stronglydominated the catches, we found three forms of lacus�trine chars (white, nosed, long�headed). In addition,we encountered the chars that could hardly be classi�fied with any particular form based on the proportionsof the body and the color. They had a high massivehead, a large mouth (the maxilla extends far beyondthe rear edge of the eye), a high body (especially in thesection between the rear edge of the head and thebeginning of the dorsal fin), a relatively short caudalpeduncle, a truncated caudal fin, and very long fan�shaped pectoral and pelvic fins. The color of head and



body was brownish�purple, the jaws were dirty yellow,the belly was orange, the spots on the sides of the bodywere rose�red, and the fins were dark gray with a red�dish border on the outer edge. In some proportions ofthe body, these chars are similar to the lake forms ofchars—the white char (the structure of the head andbody shape) and the nosed char (the size and shape ofpectoral and ventral fins).

Unfortunately, it is difficult to give a quantitativeassessment of the individuals with an intermediatestate of characters in the Kronotskaya system. Theproportion of these fish was small relative to the fish ofthe major morphotypes; however, they were encoun�tered in different parts of the riverine�lacustrine sys�tem in all years of field research.

Comparative Notes

Meristic characters are conventionally used in thetaxonomy of chars, because they are often diagnosticcharacters for distinguishing species or forms. By anumber of meristic characters, significant differencesbetween different forms of chars of Lake Kronotskoewere found; however, in different pairwise compari�sons, the sets of such characters were not the same(Table 5). The magnitude of these differences wassmall: Mayr’s test values never exceeded the thresholdlevel (1.28).

At the same time, the variation curves for the mer�istic characters that are most often used in the taxon�omy of chars were similar (Fig. 3). The shift of thecurves towards the larger values relative to other formswas observed in only two cases: for the long�headedchars (the number of scales in the lateral line, Fig. 3a)and for the riverine malma (the number of pyloriccaeca Fig. 3c). However, the limits of variation ofcharacters in all forms were similar or coincided.Thus, the divergence of the lake forms of chars of theKronotskaya riverine�lacustrine system did not affectthe main diagnostic characters of the Northernmalma. The same conclusion was made earlier by Sav�vaitova (1989).

The greatest differences between the forms of charsof the Kronotskaya riverine�lacustrine system werefound for the body proportions: the proportions of thebody, the elements of the structure of the head, and thesize and shape of paired and unpaired fins (Table 6,Fig. 4). The forms of chars differ most strongly by thestructural characters of the head; for most of them,differences were significant. By a number of charac�ters, there were substantial differences between someforms (Mayr’s test values were greater than the thresh�old level 1.28). The largest number of significantly dif�ferent characters of chars was found among the formsspecialized by the type of feeding: the pelagic predatorlong�headed char and bottom benthophage nosed

1240

126 128 130 132 134 136 138 140 142 144 146

5

15

10

20

25(а) (b)

180

19 20 21 22 23 24 25 26 27

5

15

10

30

35

20

25

210

22 24 25 26 27 28 29 30

5

15

10

20

25 (c)

23 31 32 33 34 35 36 37 38 620

64 65 66

5

25

15

35

45(d)

63 67 68

40

30

20

10

Pro

po

rtio

n o

f fi

sh,

%

pc vert.

sp.br.ll

Fig. 3. Distribution curves of some meristic characters of chars of the genus Salvelinus of the Kronotskaya riverine�lacustrine sys�tem: (a) number of perforated scales in the lateral line (ll); (b) number of gill rakers on the first gill arch (sp.br.); (c) number ofpyloric appendages (pc); (d) number of vertebrae (vert.); ( ) white char, ( ) nosed char, ( ) long�headed char,( ) riverine malma, and ( ) anadromous malma.

676


PAVLOV et al.

Tabl

e 5.

Ass

essm

ent

of d

iffe

ren

ces

betw

een

form

s of

ch

ars

(gen

us S

alve

linus

) of

th

e K

ron

otsk

aya

rive

rin

e�la

cust

rin

e sy

stem

by

mer

isti

c ch

arac

ters

Ch

arac

�te

rs

Com

pare

d fo

rms

WC

–L

NC

WC

–L

HC

WC

–R

MW

C–

DC

WC

–A

ML

NC

–L

HC

LN

C–

RM

LN

C–

DC

t st

(df =

63)

CD

t st(d

f = 5

0)C

Dt st

(df =

71)

CD

t st(d

f = 4

2)C

Dt st

(df =

110

)C

Dt st

(df =

37)

CD

t st(d

f = 5

8)C

Dt st

(df =

29)

CD

ll–

––

–2.

65**

0.31

3.11

**0.

64–

–2.

82**

0.52

––

––

D–

–2.

79**

0.47

––

––

3.03

**0.

302.

76**

0.51

––

––

A–

–2.

86**

0.50

––

––

4.26

***

0.43

2.31

*0.

41–

––

–

P–

––

––

–2.

40*

0.41

––

––

––

2.40

*0.

46

rb.1

––

––

––

––

4.12

***

0.39

––

––

––

rb.2

––

––

––

––

5.55

***

0.53

––

––

––

sp.b

r.2.

77**

0.33

––

––

––

––

2.97

**0.

502.

54*

0.33

––

pc–

––

–2.

70**

0.32

––

2.34

*0.

25–

–3.

07**

0.41

––

vert

.–

––

–4.

24**

*0.

512.

03*

0.49

3.81

**0.

38–

–3.

10**

0.41

––

Ch

arac

�te

rs

Com

pare

d fo

rms

LN

C–

AM

LH

C–

RM

LH

C–

DC

LH

C–

AM

RM

–D

CR

M–

AM

DC

–A

M

t st

( df =

97)

CD

t st

( df =

55)

CD

t st

( df =

16)

CD

t st

( df =

84)

CD

t st

( df =

37)

CD

t st

( df =

105

)C

Dt st

( d

f = 7

6)C

D

ll2.

81**

0.36

3.25

**0.

633.

73**

0.94

––

––

4.54

***

0.48

3.89

***

0.93

D3.

07**

0.32

2.37

**0.

412.

65*

0.74

––

––

2.22

*0.

232.

31*

0.57

A2.

84**

0.34

3.80

***

0.71

––

––

––

6.77

***

0.67

––

P–

–2.

05*

0.39

––

––

4.30

***

0.77

3.52

***

0.37

––

rb.1

2.11

*0.

25–

––

–2.

72**

0.39

––

2.45

*0.

24–

–

rb.2

3.14

**0.

35–

––

––

––

–5.

35**

*0.

54–

–

sp.b

r.3.

43**

*0.

38–

––

––

––

––

––

–

pc–

–2.

49*

0.38

––

3.42

***

0.46

––

6.08

***

0.67

––

vert

.2.

53*

0.29

––

––

––

––

––

––

Her

e an

d in

Tab

le 6

, S

tude

nt’

s t t

est

(tst)

and

May

r’s

test

(C

D)

valu

es a

re in

dica

ted

only

for

sig

nif

ican

t di

ffer

ence

s (p

> 0

.95)

; df

is t

he

num

ber

of d

egre

es o

f fr

eedo

m.

Des

ign

atio

ns

of fo

rms:

WC

—w

hit

e ch

ar; L

NC

—n

osed

ch

ar; L

HC

—lo

ng�

hea

ded

char

; RM

—ri

veri

ne

mal

ma;

DC

—dw

arf c

har

; AM

—an

adro

mou

s m

alm

a. D

es�

ign

atio

ns

of c

har

acte

rs: l

l—n

umbe

r of

per

fora

ted

scal

es in

late

ral l

ine;

D,

A,

R—

num

ber

of r

ays

in d

orsa

l, a

nal

, an

d pe

ctor

al f

ins,

res

pect

ivel

y; r

b.1,

rb.

2—n

umbe

rof

gil

l ray

s of

left

an

d ri

ght,

res

pect

ivel

y; s

p.br

.—n

umbe

r of

gil

l rak

ers

on fi

rst

gill

arc

h;

pc—

num

ber

of p

ylor

ic a

ppen

dage

s; v

ert.

—n

umbe

r of

ver

tebr

ae. D

iffe

ren

ces

wer

e si

gnif

ican

t at

* P

> 0

.95,

**

P >

0.9

9, a

nd

***

P >

0.9

99.



char. However, clear distinctions between the forms ofchars have been found for none of the plastic charac�ters studied: all the differences were continual. At thesame time, the identified differences in the habituscannot serve as a reliable criterion for distinguishingdifferent forms, because no discreteness was observedwhen comparing all forms of chars by the plastic charac�ters: their factor areas more or less overlapped (Fig. 5a,Table 7). In the analysis of the five forms of the lacus�trine chars, except for the anadromous malma (as themost generalized form), discreteness was not detectedeither (Fig. 5b). The comparison of the three abundantforms of chars (white, nosed, long�headed) showedthat the scatterplots in the space of the first and secondprincipal components were almost separated (Fig. 5c).Similar results on the differences between the chars ofthe Kronotskaya riverine�lacustrine system by theexternal morphological characters were obtained pre�viously by Ostberg et al. (2009).

Genetic Diversity of Chars of Lake Kronotskoe

The genetic diversity of the majority of samples ofchars of the Kronotskaya riverine�lacustrine system,which served as a basis for the morphological and eco�logical description and research, was estimated in ourprevious studies (Table 1).

For the genetic identification of the dwarf char bymtDNA, Pavlov et al. (2012) used four restrictionendonucleases. For three restriction enzymes, nodivergence among the five forms of the lacustrinechars was revealed. For one restriction enzyme, one

haplotype in the dwarf char was found (MvaI (410 bp ×3 + 320 bp × 3)), which was taken as unique. However,Senchukova et al. (2012) later also identified this hap�lotype as rare in other chars of the Kronotskaya river�ine�lacustrine system, which does not allow an unam�biguous conclusion to be made about the genetic iso�lation of the dwarf form.

Ostberg et al. (2009) used 16 restriction enzymesfor the restriction analysis of mtDNA of the chars ofthe Kronotskaya riverine�lacustrine system. Theyidentified 15 haplotypes in four studied regions of themitochondrial genome (D�loop and ND2, ND3/ND4,and ND5/ND6 genes). The level of intersample pair�wise differentiation in that study varied by the FSTvalue from 0.002 to 0.691, and the overall FST level wasfound to be 0.106. In general, this is close to the levelof the genetic divergence in the populations of thenorthern malma S. malma malma (FST = 0.089; Osi�nov, 2002). A significant difference of the long�headedchars from the other forms was found, which was iden�tified primarily by the low proportion of diversity bythe mitochondrial genome. In general, the level ofdivergence of the forms of chars was fairly low. Such aconsiderable difference in the genetic divergencewithin the forms has led to the speculation about theexistence of two phylogenetic lines of chars of the Kro�notskaya riverine�lacustrine system. One of themcould yield the riverine malma and the nosed, white,and dwarf chars; the other could yield the long�headedchar. Later, as the sample of the long�headed charsincreased and a more thorough study of mtDNA bysequencing of individual genes and regions was per�

15

17

19

21

23

25

27

15

789

111213

(а)

3

56789

11 (b)

4

10

9

10

11

12

13

14

15 (c)

(d)

10

6

2 3 4 5 6 17

9

11

13

17

19

21 (e)

15

2 3 4 5 6 142

44

46

48

52

54 (f)

50

2 3 4 5 6

clm

x

aolm

d

opaV

Fig. 4. (�) Average values and (|) limits of variation of plastic characters of chars of the genus Salvelinus of the Kronotskaya river�ine�lacustrine system: (a) head length (c); (b) snout length (ao), (c) postorbital distance (op); (d) maxilla length (lmx); (e) man�dible length (lmd); and (f) anteventral distance (aV). Designations: 1—white char; 2—nosed char; 3—long�headed char; 4—riverine malma; 5—dwarf char; 6—anadromous malma; ( )—limits of variation of the character of the anadromous malma.

678


PAVLOV et al.

6

–6–4

–2

–3

–1

1

0

2

4

3

5

–4 –2 2 4 6 80

(а)

5

–4–6

–1

1

–3 –2 1 43 50

(b)

0

–2

–4–3

–5

4

3

2

–1 2

–8–4

1

3

–6 –4 6 80

(c)

2

0

–2

–1

–3

6

5

4

–2 2 4

Principal component 1

Pri

nci

pal c

ompo

nen

t 2

Fig. 5. Phenetic relationships between chars of the genus Salvelinus of the Kronotskaya riverine�lacustrine system, estimated bythe method of principal component of the total by the aggregate of 24 plastic characters: (a) all forms, (b) forms that live in thelake and inflowing tributaries, (c) three abundant lacustrine forms. Designations: (�)—anadromous malma; (�)—white char;(�)—nosed char; (�)—long�headed char; (�)—riverine malma; ( )—dwarf char.

formed (Senchukova et al., 2012), a high genetic vari�ation in this form was identified. As a result, thehypothesis of several historical invasions of chars toLake Kronotskoe was rejected, although such a lowvariation of the mitochondrial genome in the long�headed char still allows for this form to be regarded asthe most isolated among the chars of the Kronotskayariverine�lacustrine system.

After sequencing a large part of the mitochondrialgenome (D�loop region, 558 bp; Cyt b gene, 1015 bp)in specimens of all forms of chars of the Kronotskayariverine�lacustrine system, as many as 39 variable sitesand 43 mtDNA haplotypes were identified (Fig. 6)(Senchukova et al., 2012). The anadromous malma ofthe Kronotskaya River was also included in the analy�sis, which allowed a more detailed assessment of the



Tabl

e 6.

Ass

essm

ent

of d

iffe

ren

ces

betw

een

form

s of

ch

ars

(gen

us S

alve

linus

) of

th

e K

ron

otsk

aya

rive

rin

e�la

cust

rin

e sy

stem

by

plas

tic

char

acte

rs

Ch

arac

�te

rs

Com

pare

d fo

rms

WC

–L

NC

WC

–L

HC

WC

–R

MW

C–

DC

WC

–A

ML

NC

–L

HC

LN

C–

RM

LN

C–

DC

t st(d

f = 6

3)C

Dt st

(df =

50)

CD

t st(d

f = 7

1)C

Dt st

(df =

42)

CD

t st(d

f = 1

10)

CD

t st(d

f = 3

7)C

Dt st

(df =

58)

CD

t st(d

f = 2

9)C

D

c8.

48**

*0.

846.

72**

*1.

06–

–2.

57*

0.54

7.55

***

0.73

11.2

7***

1.88

4.39

***

0.57

2.57

*0.

54

ao5.

05**

*0.

605.

46**

*0.

88–

––

–3.

30**

0.32

8.81

***

1.56

3.35

**0.

432.

25*

0.48

o3.

95**

*0.

36–

––

–7.

22**

*1.

966.

86**

*0.

692.

71*

0.45

––

5.32

***

1.30

op6.

59**

*0.

77–

––

––

–4.

69**

*0.

516.

92**

*1.

174.

83**

*0.

622.

37*

0.57

io2.

74**

0.26

––

––

––

4.24

***

0.42

2.38

*0.

402.

42*

0.30

––

cH3.

80**

*0.

483.

57**

*0.

59–

––

–8.

94**

*1.

010.

570.

103.

36**

0.44

3.86

***

0.88

lmx

7.83

***

0.88

3.84

***

0.61

2.22

*0.

27–

–2.

60*

0.24

8.75

***

1.51

4.48

***

0.59

––

hmx

––

––

–2.

42*

0.63

3.15

**0.

38–

––

–2.

30*

0.72

lmd

10.3

8***

1.12

4.42

***

0.68

2.74

**0.

323.

25**

0.67

2.24

*0.

2111

.33*

**1.

905.

51**

*0.

723.

69**

*0.

79

H2.

71**

0.30

4.73

***

0.67

2.37

*0.

283.

13**

0.54

2.11

*0.

236.

62**

*1.

08–

––

–

h4.

24**

*0.

552.

65*

0.42

2.47

*0.

29–

–4.

36**

*0.

466.

17**

*1.

12–

––

–

lpc

––

––

––

––

5.34

***

0.54

1.44

0.24

––

––

lD3.

53**

*0.

394.

06**

*0.

68–

–5.

03**

*1.

284.

02**

*0.

415.

97**

*1.

05–

–3.

36**

0.88

hD3.

44**

0.29

6.64

***

1.07

––

2.63

*0.

957.

41**

*0.

726.

65**

*1.

092.

63*

0.35

––

lA4.

59**

*0.

51–

–2.

23*

0.28

3.47

**1.

1811

.75*

**1.

143.

86**

*0.

75–

–2.

47*

0.84

hA3.

05**

0.31

8.30

***

1.20

––

––

––

8.90

***

1.46

2.35

*0.

31–

–

lP4.

87**

*0.

385.

86**

*0.

95–

–8.

05**

*1.

39–

–6.

47**

*1.

052.

52*

0.34

––

lV3.

08**

0.25

6.14

***

0.97

––

3.29

**0.

872.

00*

0.19

5.79

***

0.95

––

––

aD3.

95**

*0.

365.

90**

*0.

98–

––

–6.

21**

*0.

616.

93**

*1.

172.

03*

0.27

––

pD–

–3.

61**

*0.

60–

––

–2.

41*

0.24

2.72

*0.

45–

––

–

aV8.

44**

*0.

732.

68**

0.45

2.15

*0.

263.

76**

*0.

9310

.70*

**1.

036.

34**

*1.

053.

27**

0.44

––

aA3.

00**

0.29

3.85

***

0.61

––

––

7.39

***

0.73

5.01

***

0.84

2.49

*0.

34–

–

P–

V2.

83**

0.31

––

––

––

2.00

*0.

211.

940.

35–

–2.

80**

0.53

V–

A4.

33**

*0.

44–

–2.

13*

0.25

––

2.43

*0.

251.

970.

33–

–2.

70*

0.51

680


PAVLOV et al.

Tabl

e 6.

(Co

ntd

.)

Ch

arac

�te

rs

Com

pare

d fo

rms

LN

C–

AM

LH

C–

RM

LH

C–

DC

LH

C–

AM

RM

–D

CR

M–

AM

DC

–A

M

t st(d

f = 9

7)C

Dt st

(df =

55)

CD

t st(d

f = 1

6)C

Dt st

(df =

84)

CD

t st(d

f = 3

7)C

Dt st

(df =

105

)C

Dt st

(df =

76)

CD

c–

–7.

30**

*1.

137.

16**

*2.

0013

.03*

**1.

74–

–4.

50**

*0.

472.

21*

0.40

ao–

–6.

10**

*0.

996.

40**

*1.

638.

02**

*1.

13–

––

––

–

o–

––

–7.

15**

*2.

305.

65**

*0.

886.

55**

*1.

553.

98**

*0.

475.

21**

*1.

51

op3.

22**

0.40

3.01

**0.

502.

27*

0.69

5.76

***

0.94

––

2.95

**0.

32–

–

io–

––

––

–3.

39**

0.59

––

3.52

***

0.43

––

cH3.

94**

*0.

493.

33**

0.54

3.87

**1.

022.

25*

0.39

––

8.25

***

0.95

7.13

***

1.64

lmx

4.38

***

0.47

5.31

***

0.86

2.30

*0.

715.

63**

*0.

74–

––

––

–

hmx

5.55

***

0.61

2.36

*0.

392.

75*

0.81

––

––

7.77

***

0.78

3.75

***

1.23

lmd

6.28

***

0.67

6.37

***

0.99

6.33

***

1.68

6.06

***

0.74

––

––

––

H–

–7.

36**

*1.

098.

42**

*2.

279.

37**

*1.

22–

––

––

–

h–

–4.

71**

*0.

76–

–6.

41**

*1.

04–

––

––

–

lpc

3.57

***

0.45

––

––

4.96

***

0.79

––

4.27

***

0.46

––

lD–

–4.

80**

*0.

826.

93**

*1.

946.

60**

*1.

134.

42**

*1.

132.

36*

0.25

3.61

***

0.97

hD2.

32*

0.29

4.95

***

0.76

4.16

***

1.57

12.2

4***

1.70

2.83

**0.

936.

86**

*0.

73–

–

lA6.

33**

*0.

693.

01**

0.52

4.01

**1.

257.

31**

*1.

242.

73**

0.80

6.02

***

0.67

––

hA2.

27*

0.26

7.45

***

1.13

3.27

**1.

299.

46**

*1.

15–

––

––

–

lP3.

34**

0.44

5.44

***

0.86

11.7

2***

2.95

5.46

***

0.80

6.70

***

1.16

––

9.69

***

1.41

lV–

–5.

41**

*0.

856.

26**

*1.

887.

65**

*1.

013.

41**

0.86

2.18

*0.

222.

48*

0.56

aD–

–5.

52**

*0.

885.

40**

*1.

449.

93**

*1.

47–

–4.

32**

*0.

47–

–

pD–

–2.

90**

0.51

––

5.38

***

0.87

––

3.84

***

0.40

––

aV–

–3.

96**

*0.

645.

00**

*1.

379.

54**

*1.

372.

31*

0.52

6.49

***

0.69

––

aA2.

94**

0.36

3.55

***

0.59

2.74

*0.

959.

50**

*1.

36–

–7.

81**

*0.

79–

–

P–

V4.

22**

*0.

53–

––

––

––

–3.

17**

0.33

––

V–

A–

––

––

––

––

––

––

–

See

Tab

le 5

for

not

es;

see

Tab

le 2

for

desi

gnat

ion

s of

ch

arac

ters

.



relationships between the chars of the entire Kro�notskaya riverine�lacustrine system.

When comparing the samples of the same form ofchars collected in different years, a certain heteroge�neity by the FST test was found. Small but significantdifferences were found between the samples of thenosed char (0.18807, p < 0.01) and the anadromousmalma (0.08516, p < 0.01) collected in different years.For the anadromous malma, these differences may bedue to the interannual variations in the genetic struc�ture of the spawning stock, which are typical of theanadromous fish with a strong homing. In the case ofthe nosed char, these differences are mainly due to thepresence of haplotype H2 (9 copies) in the sample in2003 and its absence in the sample in 2010. It shouldbe noted that, in 2003, this haplotype was identified inthe majority of fish in the Listvenichnaya River (7 of9 specimens); in 2010, catches in this area were absent.Thus, the differences between the samples for haplo�type H2 are apparently determined by the nonuniformdistribution of haplotypes in the lake. At the same time,the high frequency of occurrence of haplotypes H11 andH39 in both samples is indicative of the genetic simi�larity of the nosed chars caught in different years.

In the samples representing all forms analyzed, thelevel of pairwise intersample differentiation FST rangedfrom 0.00425 to 0.46268 (Senchukova et al., 2012).The greatest difference (0.46268) was detectedbetween the long�headed and dwarf chars; the lowest(0.00425) was detected between the riverine malmaand the nosed char. The differences in FST between thewhite and nosed chars, as well as the differences of thelong�headed char and anadromous malma from theother forms of chars, were highly significant (p < 0.01).The overall level of differentiation of all samples was(0.134) and the molecular variance (AMOVA) valueswere 13.44% between populations and 86.56% withinpopulations. Genetic distances (Tamura and Nei,1993) indicated a very low level of differences betweenthe forms (0.00225–0.00339). The lowest level of dif�ferences (0.00225) was observed between the long�headed char and anadromous malma; the highest(0.00339) was observed between the nosed and dwarfchars.

The phylogenetic relationships between the studiedforms of chars of the Kronotskaya riverine�lacustrinesystem are shown in Fig. 6. It can be seen that thechars from Lake Kronotskoe carry four abundant hap�lotypes (H1, H11, H19, and H39), which are alsopresent in the anadromous malma from the Kro�notskaya River. Other haplotypes found in the lakemorphs are derived from one of the abundant haplo�types by one or two substitutions. Some specimens ofthe anadromous malma have abundant haplotypes ofchars from Lake Kronotskoe, and the remaining spec�imens form a separate network of haplotypes that doesnot overlap with the lacustrine forms.

DISCUSSION

The morphological and genetic polymorphism ofchars in Lake Kronotskoe was found to be higher thanwas previously thought. Today, the existence of at leastfive forms of chars has been reliably established; how�ever, the boundaries between these forms are blurred.

Researchers experience difficulties in distinguish�ing virtually all forms of chars when sufficiently largesamples of each of them are examined. Data of differ�ent authors are also contradictory. In particular, Vik�torovskii (1978) pointed out that the long�headed andwhite chars well (with hiatus) differ from each other inthe height of the head. However, the sample studied bySavvaitova (1989) and ower samples did not differ bythis character. The differences between the white andlong�headed chars in the length of the snout, whichare used as discriminatory characters (Viktorovskii,1978), according to Savvaitova (1989), are associated

Table 7. Loads of eigenvectors of meristic characters ofchars of the genus Salvelinus of the Kronotskaya riverine�lacustrine system

Character Principalcomponent 1

Principal component 2

c 0.9204 0.2327

ao 0.8333 0.3584

o –0.4363 0.3888

op 0.7226 0.2345

io 0.6210 –0.0190

cH 0.6005 0.0557

lmx 0.7442 0.4775

hmx 0.2257 –0.0423

lmd 0.7528 0.4566

H –0.2075 –0.1125

h –0.3232 0.3321

lpc –0.4919 0.0746

lD –0.4226 0.4434

hD –0.3867 0.7373

lA –0.4633 0.4957

hA –0.2228 0.5743

lP 0.0595 0.7287

lV –0.0187 0.8710

aD 0.6675 –0.1371

pD –0.5621 –0.1482

aV 0.7927 –0.2410

aA 0.5555 –0.5195

P–V –0.0506 –0.5780

V–A –0.3584 –0.4424

The values of the characters that made a significant contribution todiscrimination are indicated in bold; see Table 2 for designations ofcharacters.

682


PAVLOV et al.

with the acquisition of the breeding dress by the long�headed chars. In addition, it is known that a pro�nounced ontogenetic variation associated with achange in the diet can be observed in isolates of chars.Such situation was described in detail for the charsfrom the lakes of Transbaikalia, when a significantchange in the growth rate and the external appearanceof fish can be observed during the life of one individual(Alekseev et al., 2006). A similar situation wasdescribed in Lake Chernoe (island Onekotan, KurilIslands), where small benthophagous chars and largecannibal chars were distinguished (Savvaitova et al.,2000a, 2000b, 2001). Chars of these two groups can beeasily distinguished from one another, especially bythe structure of the head; however, by the genetic char�acteristics, they represent a single population. Thelarge predator phenotype is formed in those small ben�thophages that, after three or four reproduction cycles

at a younger age, suspend the maturation of gonads,grow, and switch to feeding on fish. A similar patterncan also be seen in the chars in large riverine�lacus�trine systems of the Taimyr Peninsula (Pavlov, 1995,1997; Pavlov et al., 1999), where adaptive radiationfrom an ancestral anadromous char led to the emer�gence of a number of forms that populated differentecological niches in lakes. The lack of well�expressedgenetic differences and the low levels of genetic differ�entiation among the Taimyr chars drastically contrastto the numerous morphological and ecological char�acteristics of the local forms that evolved primarily asa result of sympatric divergence.

It cannot be ruled out that the morphological char�acters of chars of the Kronotskaya riverine�lacustrinesystem are subject to variation in time under the influ�ence of climatic fluctuations and changes in the exter�

H38

H22

H23

H43H42

H41

H40

H39

H36

H37

H28

H35

H27

H25 H26

H19

H21

H9

H8H6

H24

H30H20

H10

H34

H31

H29

H33

H7

H5

H4

H3

H1H13

H14

H2H12

H11

H17

H32

H16

H15

H18

Fig. 6. Phylogenetic network of haplotypes of the D�loop region of mtDNA and the cytochrome b gene of chars of the genusSalvelinus of the Kronotskaya riverine�lacustrine system built using the TCS algorithm (according to Senchukova et al., 2012,with some modifications). The size of circles and sectors is proportional to the frequency of occurrence of haplotypes H1–H43.Designations: ( ) nosed char, ( ) white char, ( ) long�headed char, ( ) dwarf char, ( ) riverine malma, and ( )anadromous malma.



nal environment, as described for the Kamchatkamykizha (Parasalmo (O.) mykiss) (Savvaitova et al.,1988; Savvaitova and Kuzishchin, 1998). Judging bythe description and illustrations presented by Viktor�ovskii (1978), the nosed chars had short pectoral andpelvic fins with rounded tops. In our sample, thesecharacters varied: there were both individuals with finscorresponding to the description by Viktorovskii(1978) and individuals with very long acuminate, pec�toral, and ventral fins. The high variability of the shapeof the snout of the nosed chars was mentioned by Sav�vaitova (1989); in her opinion, the “nose” may be theresult of mutations that occurred in isolation. It shouldbe noted that the “nosed” chars are commonly foundin small water bodies separated from the sea in theKuril Islands (Savvaitova et al., 2000a, 2000b, 2004).Therefore, the overhanging snout of the nosed char inLake Kronotskoe can hardly be regarded as its uniquecharacter.

According to some authors, the wide diversity ofchars at the form level reflects the diversity of ecologi�cal niches in the water body (Hammar, 1984; Hindarand Jonsson, 1984). However, in the Lake Kronotskoebasin, which experiences a year�on�year impact oflarge�scale climate changes, volcanic activity, andother factors, the existence of isolated niches isunlikely, because the boundaries between them areblurred and they largely overlap with one another, as inthe majority of typical water bodies of the boreal zone(Hammar, 1989). Therefore, the existence of a largenumber of intermediate forms of chars in the waterbody reflects their ability for a wide adaptation.

In the papers devoted to the chars of Lake Kro�notskoe, little attention is paid to the analysis of formswith an intermediate state of morphological charac�ters. Only Savvaitova (1989) emphasizes that the pres�ence of transgression by morphological traits does notcontradict the hypothesis of the reproductive isolationof forms. The available data on the specific popula�tion�genetic features of chars from Lake Kronotskoeare indicative of a greater or smaller gene flow betweenthe forms. Thus, various forms of char currently exist�ing in Lake Kronotskoe have not reached the specieslevel of divergence and can only be considered as sub�populations within a single metapopulation.

The white char was first described by Glubokovskii(1977) in the Kamchatka River basin. By the combi�nation of morphological and craniological characters,its isolation from the anadromous malma at the spe�cies level was shown. However, according to our data,by the morphological and genetic characters, thewhite char from Lake Kronotskoe has not reached thespecies level of divergence with respect to the anadro�mous malma from the Kronotskaya River. To deter�mine the allied relationships between the white charfrom the Kamchatka River basin and the white charfrom Lake Kronotskoe, a detailed study using all sys�tems of characters, including the population�geneticmarkers, in ample material is required.

The differences between the forms of chars arecontinual in nature, with the extreme variants beingconnected by a continuous series of transitional forms.Individuals with the intermediate phenotypes are dif�ficult to attribute to one or another form. A similar sit�uation was described earlier for another species, theKamchatkan mykizha , which is represented by indi�viduals or separate local groups that have structuralelements of the North American lines—the redbandtrout (P. mykiss gairdneri) and the coastal cutthroattrout (P. clarkii clarkii). To describe this phenomenon,the term “series of forms” (by: Behnke, 1992) was used(Savvaitova et al., 1998). Since there are several formsof chars in Lake Kronotskoe and transitions areobserved between almost all of them, in our view, it ismore appropriate to use another term, the “network offorms,” when the extreme variants of several rows ofvariability are located in the peripheral nodes of thenetwork. In this case, the genetic data confirm well theoverlap of distributions by the morphological charac�ters. It can be postulated that the chars from LakeKronotskoe are representative of a sophisticated sys�tem of partially isolated and constantly interactinggroups of a populational but not species level.

The coexistence of various groups of chars in iso�lated lakes throughout the Arctic region has beendescribed in detail in the literature (Behnke, 1984;Savvaitova, 1989; Glubokovskii, 1995; Hammar,1998; Pavlov et al., 1999; Chereshnev et al., 2002).The interpretation of the existing diversity of chars bydifferent authors widely varies. The supporters of theallopatric speciation believe that the sympatrically liv�ing groups originated from different ancestral forms orseveral waves of introduction of a certain one form(Viktorovskii, 1978; Glubokovskii, 1995; Chereshnevet al., 2002). However, in this case, the level of diversityis often not taken into account, and the forms with anintermediate phenotype are not considered at all. Thesupporters of the sympatric speciation consider theexisting diversity of chars as a result of disruptive selec�tion associated with the development of changeableand very limited resources of boreal water bodies (Sav�vaitova, 1989).

The studies of the mtDNA variation performed bySalmenkova et al. (2005) and Radchenko et al. (2006)showed genetic heterogeneity of chars from Lake Kro�notskoe for the Cyt b gen, which was expressed in thepresence of two mtDNA lines (two groups of haplo�types) specific for the populations of the Northernmalma inhabiting the Chukchi and Bering Sea coasts.Insufficient data did not allow these authors to inferthe sequence of invasions of these groups of haplotypesin Lake Kronotskoe. In our studies (Senchukova et al.,2012) performed with much more ample data, we alsodistinguished two mtDNA lines for the Cyt b gene.Similarly to the previous researchers, we found no dif�ferences in the forms of chars from Lake Kronotskoein terms of affiliation to these lines. Therefore, takinginto account the published data (Salmenkova et al.,

684


PAVLOV et al.

2005; Radchenko et al., 2006) and our own results, wecannot consider several lines of the mitochondrialgenome of the modern forms of chars from Lake Kro�notskoe as a fact that points to their allopatric origin.

After the analysis of obtained network of mtDNAhaplotypes, Senchukova et al. (2012) showed that theanadromous malma from the Kronotskaya River isancestral in relation to the other lacustrine forms,because it has all widespread haplotypes in the lacus�trine forms. It is most likely that the lacustrine forms,which received the original haplotypes from theanadromous malma, formed new haplotypes underthe conditions of isolation, differing from the originalhaplotypes in one or two mutations. It can be assumedthat the chars with the four widespread haplotypeswere present in the Paleokronotskaya River basin atthe time of formation of the lake. This testifies to thefounder effect under the conditions of isolation of theancestral population of chars in Lake Kronotskoe andits initially small size.

The existing diversity of the forms of chars in LakeKronotskoe is the result of microevolution aimed atdeveloping adaptations to unstable, fluctuating envi�ronmental conditions. This leads to the formation of astructure of population groups that yield differentforms and provide the maximum spatiotemporal sta�bility of the species. The presence of an intricate sys�tem of relationships between the forms can provide ahigh degree of stability of the system under the expo�sure to environmental factors (in particular, by chang�ing the ratio of different forms present in the waterbody as well as due to the emergence of new forms ofchars). The existing balanced system of groups of charsin the lake suggests that the described diversity can befurther broadened by performing a meticulousresearch of chars, particularly with regard to theirmicrogeographic variation (i.e., different areas of thelake or its deep horizons). Special attention in futurestudies should be given to the nosed char. The identifiedhigh heterogeneity of this form and new informationabout its diversity (D.S. Pavlov and G.N. Markevich,personal communication) give reason to assume thatthe morphological and genetic diversity of the nosedchar is higher than is known today.

The study of the genetic and phenetic diversity ofchars of the Kronotskaya riverine�lacustrine systemshowed that, by the morphological and genetic char�acters, the anadromous malma from the lower reachesof the Kronotskaya River is not isolated from thelacustrine chars. By the combination of plastic andmeristic characters, it occupies an intermediate posi�tion between all lacustrine forms (Figs. 3–5). This isprobably due to the downstream migration of juvenilesand some mature lacustrine chars through the rapidsof the Kronotskaya River and joint spawning of the lat�ter together with the anadromous malma. This is sup�ported genetically by the largest diversity of haplotypesidentified in the anadromous malma (Fig. 6; Senchuk�

ova et al., 2012), including all the widespread haplo�types of the lacustrine forms.

It is believed that the anadromous malma cannotovercome the rapids in the middle reaches of the Kro�notskaya River and that the lacustrine chars do notexperience the influence of the anadromous fish. Nev�ertheless, there is evidence that single specimens ofanadromous fish (malma, Coho salmon Oncorhynchuskisutch, sockeye salmon O. nerka) can still reach thelake. This was repeatedly mentioned by Kurenkov in anumber of reports of the Kronotskii National Park(1979). Therefore, the existence of a limited gene flowfrom the anadromous malma to the metapopulation oflacustrine chars cannot be ruled out. Theoretically, itmay restrain the development of isolation betweensome lacustrine forms. It is known that, if there is freeexit to the sea, the polymorphism of chars in lakes islow: the populations are strongly dominated by theanadromous form as is observed in Lake Kuril’skoe insouthern Kamchatka (Pichugin, 1991).

Thus, in the Kronotskaya riverine�lacustrin esys�tem, there is an anadromous malma, which inhabitsthe lower reaches of the Kronotskaya River, and ametapopulation of chars, which is represented by thelacustrine forms that are not completely isolatedgenetically. Currently, these forms are in a quasi�sta�tionary state, when an evolutionary stasis of the lacus�trine forms is ensured. This equilibrium can be easilydisplaced both in the direction of the complete isola�tion of the forms (in this case, they will acquired thespecies status) and in the opposite direction, when theboundaries between the forms may disappear. Appar�ently, the Kronotskaya riverine�lacustrine system is apeculiar evolutionary cauldron in which active micro�evolution processes take place literally beneath oureyes. This makes this water body and the chars living init unique objects to solve the fundamental problems ofmodern biology.

ACKNOWLEDGMENTS

We are grateful to T.I. Shpilenok, V.I. Mosolov,M.Yu. Repin, A.S. Kononov, G.N. Chichorin, andT.P. Egorov (Kronotskii State Nature BiosphereReserve) for their help in organizing and conductingthe field work; A.M. Malyutina and G.N. Markevich(Moscow State University) for their assistance in col�lecting the material; T.L. Vvedenskaya (Kamchat�NIRO) for kindly providing more detailed data on thediet of the white and nosed chars. Special thanks aredue to our colleagues, coauthors of the previousgenetic and other studies of chars of the Kronotskayariverine�lacustrine system: N.S. Mugue (VNIRO),M.N. Mel’nikova (Moscow State University),C.O. Ostberg (USGS), and L. Hauser (USGS).

This study was supported by the program “LeadingScientific Schools” (project no. NSh�719.2012.4) andthe Russian Foundation for Basic Research (projects



nos. 12�04�01358/12, 11�04�00778/12, and 12�04�10131).

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Translated by M. Batrukova

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Phenetic Diversity and Spatial Structure of Chars ...€¦ · A. L. Senchukova, and E. A. Pivovarov Biological Faculty, Moscow State University, Moscow, 119992 Russia email:[email protected]