The lipid status and feeding habits of yearlings of mykiss Parasalmo mykiss and coho salmon Oncorhynchus kisutch in autumn

ISSN 0032�9452, Journal of Ichthyology, 2010, Vol. 50, No. 7, pp. 543–551. © Pleiades Publishing, Ltd., 2010.Original Russian Text © D.S. Pavlov, N.N. Nemova, P.I. Kirillov, E.A. Kirillova, Z.A. Nefedova, O.B. Vasil’eva, 2010, published in Voprosy Ikhtiologii, 2010, Vol. 50, No. 4,pp. 561–569.

543

INTRODUCTION

In the life cycle of many salmonid species (Salmo�nidae), one of the most important periods is seawardmigration. The diadromous forms of salmonids differfrom resident forms in the presence of this period. Thefreshwater period of life in juveniles of diadromousforms of different species may be from several weeks toseveral years. The migration to the sea is accompaniedby the process of smoltification connected with pro�found morphophysiological restructuring of the fishorganism. There are numerous studies demonstratingthe difference between parr and smolts of salmonids inthe period of their seaward migration by means ofmorphological, physiobiochemical, and behavioralparameters. Smolts show changes in body propor�tions, appearance of silvery coloration, change ofhematological parameters, and in the content of lip�ids. The content of cortisol and thyroxin, the activityof gill ATPase, and tolerance to salinity increase. Thefish pass over from the territorial and bottom dwellingto pelagic dwelling (Shapovalov and Taft, 1954;Barach, 1960; Savvaitova et al., 1973; Matsuk, 1975;McCormick and Saunders, 1987; Hoar, 1988; Wede�meyer, 1996; Kazakov and Veselov, 1998; Pustovit andPustovit, 2005; Quin, 2005; etc.).

Investigations on the Atlantic salmon Salmo salarand the Black Sea trout Salmo trutta labrax rearing at

fish hatchery farms demonstrated that the juveniles aredivided into two groups a long time before smoltifica�tion. The distribution of juveniles of Atlantic salmonof the same age by length becomes bimodal at a mini�mum of 6 months before smoltification (Thorpe,1977). Biochemical differentiation of hatchery�rearedjuveniles, by the concentration of neuromediators andtheir metabolites, begins at a minimum of 4 monthsbefore visible signs of smoltification appear (Pavlovet al., 2009). For underyearlings of Black Sea trout,the behavioral division into two different groups wasrecorded at 9–10 months before smoltification (Pav�lov et al., 2010a). Such differentiation may be causedby different conditions of temperature and illumina�tion (Thorpe et al., 1989), by lower feeding intensity insome specimens (Metcalfe et al., 1992), by complexhierarchical interrelations between specimens, and bymanifestations of aggressive territorial behavior(Faush, 1984). It was supposed that the mechanismstriggering the smoltification process are analogous tothose triggering the maturation process (Thorpe,1986, 1989). The latter does not begin until the fatreserves of the fish would reach a certain level (Roweet al., 1991).

Earlier we had noted that the principal factor con�trolling presence or absence of smoltification and thetiming of smoltification is the trophic factor (Pavlov,1979; Pavlov et al., 2001). Feeding habits, growth rate,

The Lipid Status and Feeding Habits of Yearlingsof Mykiss Parasalmo mykiss and Coho

Salmon Oncorhynchus kisutch in AutumnD. S. Pavlova, N. N. Nemovab, P. I. Kirillova, E. A. Kirillovaa,

Z. A. Nefedovab, and O. B. Vasil’evab

a Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow 119071 Russia e�mail: [email protected]

b Institute of Biology, Karelian Research Center, Russian Academy of Sciences, ul. Pushkinskaya 11, Petrozavodsk, 185910 Russia

Received February 26, 2010

Abstract—Juveniles of coho salmon Oncorhynchus kisutch and mykiss Parasalmo mykiss at the age 1+ (year�lings) are differentiated by the content of different fractions of lipids (the lipid status), feeding habits, and bysize�weight characteristics even eight months prior to smoltification. The juveniles of coho salmon andmykiss with high lipid status consume more calorific food items and, as a rule, have higher (on average) bodylength and weight. The juveniles with low lipid status consume less calorific organisms and have lower bodylength and weight. It is supposed that a considerable part of juveniles with high lipid status will migrate sea�ward the next year. The role of feeding habits in formation of this differentiation and, accordingly, in deter�mination of timing of smoltification are discussed.

DOI: 10.1134/S0032945210070064

Key words: mykiss, coho salmon, yearlings, lipid status, feeding, differentiation, smoltification

544

JOURNAL OF ICHTHYOLOGY Vol. 50 No. 7 2010

PAVLOV et al.

and the complex of parameters of lipid metabolism(the lipid status) reflect the foraging conditions ofjuveniles and determine whether smoltification wouldtake place or not a long time before the beginning ofseaward migration. Scale analysis demonstrated (Kuz�ishchin et al., 2002; Pavlov et al., 2005; Pavlov andMaslova, 2006; Pavlov et al., 2006; Kirillova, 2009)that the growth rate of smolts in juveniles of mykissParasalmo mykiss and coho salmon Oncorhynchuskisutch in rivers of western Kamchatka is higher thanin parr of the same age and that these differencesbecome visible at least in the year preceding the sea�ward migration of smolts.

The lipid status seems to be a most reliable criterionof differentiation as it is a direct parameter of theintensity of metabolic processes in fish and an indirectparameter of life conditions of representatives of par�ticular groups. Biochemical analysis enables one toobtain a reliable quantitative estimation of the lipidcontent. Previously, we had obtained preliminaryresults indicating the presence of differentiation ofyearlings of coho salmon and mykiss by lipid statusand feeding habits (Pavlov et al., 2007) in autumn, i.e.,6–8 months prior to smoltification. To verify and con�firm the obtained results, additional investigations ofjuveniles of coho salmon and mykiss of the age 1+(yearlings) were conducted.

MATERIAL AND METHODS

The objects of investigation were juveniles of cohosalmon and mykiss from the Utkholok River (north�west Kamchatka, 57° N, 157° E). Only the diadro�mous form represents the coho salmon here. Smoltifi�cation of the juveniles starts at the age 1+ to 3+ at thebody length from 80 to 150 mm. Mykiss have morecomplex intraspecific and intrapopulation structureand is represented both by the resident form and themigratory form. Its smoltification in migratory formsis observed in the Utkholok River at the age 2+ to 6+at the size from 90 to 280 mm. Taking into consider�ation that the first age of smoltification in mykiss andthe principal age of smoltification on coho salmon is 2+(two�year�old), the samples of juveniles at the age 1+were collected for solution of the above�stated tasks.The material was collected in the middle reaches of theUtkholok River in 2005 (from September 4 to October 7)and in 2006 (from September 6 to September 26). Upto this time, the seaward migration of smolts was fullycompleted and in the river there only were the fish,which certainly would stay one more winter there. Thejuveniles were caught by gill nets (mesh size 10–15 mm), electrofishing (Smith�Root LR�24), andminnow seine (length 5 m, high 1 m, mesh size 5 mm).The fish with 70–135 mm fork length were selectedcorresponding to age 1+ (yearlings). Their age wasadditionally checked by scales before fixation. Onlyyearlings were used for analysis. Fork length (AC) was

measured with accuracy to 0.5 mm and weight wasmeasured with accuracy to 0.1 g.

The stomach content was preserved in 10% forma�lin solution for the subsequent examination of dietaccording to Methodical Instructions on Investigation ofFeeding and Trophic Relationships of Fish under Natu�ral Conditions (Methodical Guide, 1974).

The individual samples of juveniles of coho salmonand mykiss were fixed in 96% ethyl alcohol. In the lab�oratory, the samples were weighted and minced thor�oughly. Chloroform�methanol (2 : 1) mixture wasadded to homogenate. After that samples were storedin the cool place (at +4°C) until the analysis (Folchet al., 1957). The extracted total lipids (TL) were driedto constant weight in an exiccator over phosphorusanhydride (P2O5) in a cooling chamber (at +4°C).Defatted residue (DR), comprising proteins, carbohy�drates, nucleic acids, amino acids, and microele�ments, was dried to constant weight at room tempera�ture. The lipid fractions—total phospholipids (PL),triacylglycerols (TAG), cholesterol (CS), cholesterolesters (CSE)—were separated on Silufol thin�layerchromatographic plates (Kavalier, Czech Republic) inthe system of solvents: petroleum ether�sulphuricether�acetic acid (90 : 10 : 1). The content of PL,TAG, and CSE was determined by the hydroxamatemethod (Sidorov et al., 1972) and that of CS wasdetermined by the reaction with dyed reagent (Engel�brecht et al., 1974) and expressed in percentages of thedry weight of the sample (TL + DR).

The volume of the used material: 32 specimens ofcoho salmon and 31 specimens of mykiss in 2005 and41 specimen of coho salmon and 32 specimens ofmykiss in 2006.

Significance of difference of samples' means wasestimated by U�test of Mann�Whitney (Lakin, 1990).Difference between the investigated groups by the lipidstatus was estimated using discriminant analysis (Kari�mov, 2002), simultaneously using the data on the con�tent of four principal fractions of lipids—PL, TAG,CSE, and CS.

RESULTS

In both years of investigations, the content of TL injuveniles of coho salmon and mykiss varied within awide range. According to frequency distribution, twogroups of individuals were conventionally markedout—those with low and high lipid status (Table 1,Fig. 1). These groups of fish made a basis for furtheranalysis. In juveniles of coho salmon and mykiss withlow lipid status, the mean content of TL was similar inboth years. In juveniles of coho salmon and mykisswith a high lipid status, the mean content of TL in2006 was lower than in 2005. The differences in thecontent of TL in juveniles with low and high lipid sta�tus are significant (p < 0.001). The same significantdifferences are also characteristic to such fractions oflipids as TAG, PL, and CS (Fig. 2). The differences in


THE LIPID STATUS AND FEEDING HABITS OF YEARLINGS OF MYKISS 545

the content of CSE were significant only in mykiss in2005. No differences in the content of CSE in cohosalmon in both years of investigations and in mykiss in2006 are found.

Juveniles of coho salmon and mykiss in 2005 andjuveniles of coho salmon in 2006 with low lipid statushad, on average, significantly lower value of fork

length and weight (p < 0.01–0.001) than the individu�als with high lipid status (Table 2). Juveniles of mykisswith low lipid status in 2006 did not differ, on average,in length and weight from juveniles with high lipid sta�tus. Distribution of yearlings of coho salmon andmykiss with low and high lipid status by length is rep�resented in Fig. 3.

Table 1. Content of total lipids (% of dry weight) in yearlings of coho salmon Oncorhynchus kisutch and of mykiss Parasalmomykiss with low and high lipid status in 2005 and 2006

Year

Lipid status

Coho salmon Mykiss

low high low high

2005

2006

Note: Here and in Table 2: above the line is the mean value of a parameter and its standard deviation, in parentheses is the number of fish,and under the line is the variation range of the parameter.

12.98 2.57 17( )±

7.36–17.20�� 26.60 5.26 15( )±

19.43–35.48�� 13.93 4.58 14( )±

6.62–19.79�� 29.94 3.04 17( )±

23.57–35.06��

10.10 2.96 26( )±

4.62–15.67�� 20.49 4.01 15( )±

16.34–31.38�� 14.25 4.14 17( )±

6.06–19.39�� 22.40 1.95 17( )±

20.36–26.75��

14

12

10

8

6

4

2

0

9

8

7

6

5

4

3

2

1

0

16

14

12

10

8

6

4

2

0

10

9

8

7

6

5

4

3

2

00 5 10 15 20 25 30 35 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

0 5 10 15 20 25 30 35 40 0 5 10 15 20 25 30 35 40

(a)

(b) (d)

(c)

Num

ber

of fi

sh

Content of total lipids, % of dry weight

1

Fig. 1. Distribution of yearlings of coho salmon Oncorhynchus kisutch (a—2005 and b—2006) and of mykiss Parasalmo mykiss

(c—2005 and d—2006) with ( ) low and ( ) high lipid status by the content of total lipids.

546


PAVLOV et al.

Discriminant analysis of groups of coho salmonand mykiss with low and high lipid status by the con�tent of PL, TAG, CSE, and CS demonstrates that, inthe space of canonical roots, all groups form clear fac�tor areas (Fig. 4). Values of Wilks’ Lambda statistic(0.09 for coho salmon and 0.17 for mykiss) at the sig�

nificance level p < 0.001 confirm discrimination ofthese samples. It should be noted that, in 2005, thegroups of coho salmon and mykiss with low and highlipid status form nontransgressing factor areas, and, in2006, their factor areas transgress weakly. A consider�able transgression is noted for factor areas of juveniles

Fig. 2. The content ( ) phospholipids, ( ) triacylglycerols, ( ) cholesterol esters, and ( ) cholesterol in yearlings of cohosalmon Oncorhynchus kisutch (a—2005 and b—2006) and of mykiss Parasalmo mykiss (c—2005 and d—2006) with (1) low and(2) high lipid status.

Table 2. Mean fork length (AC) and weight Q of yearlings of coho salmon Oncorhynchus kisutch and of mykiss Parasalmo mykisswith low and high lipid status in 2005 and 2006

Year Parameter

Lipid status

Coho salmon Mykiss

low high low high

2005 AC, mm

Q, g

2006 AC, mm

Q, g

89.6 7.72 17( )±

78.0–108.0�� 111.4 16.25 15( )±

73.0–132.0�� 89.8 10.41 14( )±

68.0–103.0�� 102.1 14.48 17( )±

74.0–129.0��

8.5 2.56 17( )±

5.9–15.2�� 18.6 7.19 15( )±

5.0–29.5�� 9.1 3.14 14( )±

3.6–13.2�� 13.5 5.49 17( )±

5.8–27.0��

82.8 7.39 26( )±

67.5–99.0�� 98.3 6.24 15( )±

86.5–107.5�� 91.1 9.52 15( )±

74.5–106.0�� 93.6 9.16 17( )±

80.0–110.0��

7.43 2.19 26( )±

4.0–13.4�� 12.9 2.83 15( )±

9.2–19.2�� 9.5 4.10 15( )±

4.3–16.5�� 11.1 3.77 17( )±

5.9–18.6��

22201816141210

86420

22201816141210

86420

18

16

14

12

10

8

6

4

2

0

18

16

14

12

10

8

6

4

2

0

1 2

1 2 1 2

1 2

(a) (c)

(d)(b)

Con

ten

t of

lipi

ds,

% o

f dry

wei

ght

Lipid status



of coho salmon and mykiss with low lipid status caughtin 2005 and 2006.

The principal difference in food spectra of juvenilesof coho salmon and mykiss with low and high lipid sta�tus was that the latter consumed predominantly eggs ofPacific salmons and of charr of the genus Salvelinus(which spawn in September�October) and larvae ofDiptera (mainly maggots) (Fig. 5). The food spectrumof yearlings of coho salmon and mykiss with low lipidstatus was, as a rule, wider than in juveniles with highlipid status. The main food items of juveniles of cohosalmon with a low lipid status were various insects(imagoes of amphibiotic insects and aerial insects)whose chitin is not assimilated and is evacuated non�digested from the intestine. The part of insects (pre�dominantly Diptera) in the diet of mykiss with a lowlipid status was also very high.

DISCUSSION

Analysis of the material of two�year investigationsshows the presence of a wide range of variation amongyearlings of coho salmon and mykiss by such parame�ters as fork length, weight, feeding habits, and lipid

status. Let us discuss the reasons of such deviation ofthe aforementioned parameters.

Higher mean size of juveniles of coho salmon andmykiss with high lipid status certainly result from itshigher growth rate in comparison with juveniles withlow lipid status. Mykiss yearlings in 2006 make anexception. However, in spite of similar size of all indi�viduals of mykiss, in this year, they retained differenti�ation into groups with high and low lipid status. Itmight depend on separation of the somatic growth anddevelopment in fish; these processes require differentquantity of energy (Novikov, 2000), and the ratio ofthe used energy is epigenetically determined. Eitherthe environmental conditions in 2006 might favorrapid growth of individuals of mykiss with low lipidstatus or it was a consequence of the rapid growth atthe first year of life.

Differences in food spectra of yearlings of cohosalmon and mykiss depend on their dwelling in differ�ent biotopes differing in abundance and availability offood items. In autumn, the juveniles of mykiss stay intributaries of the Utkholok River where coho salmonand charr spawn in mass in this period, whose eggsmake their principal food in this season. In quiet

6

5

4

3

2

1

0

6

5

4

3

2

1

0

6

5

4

3

2

1

0

12

10

8

6

4

2

0

65 75 85 95 105 115 125 135 60 70 80 90 100 110 120 130 140

60 70 80 90 100 110 70 80 90 100 110

(a) (c)

(d)(b)

Num

ber

of fi

sh

Fork length, mm

Fig. 3. Distribution of yearlings of coho salmon Oncorhynchus kisutch (a—2005 and b—2006) and of mykiss Parasalmo mykiss

(c—2005 and d—2006) with ( ) low and ( ) high lipid status by fork length.

548


PAVLOV et al.

stretches of the river inhabited by juveniles of cohosalmon in autumn, some small quantity of eggs ofchum salmon O. keta remains (washed out of rediggedredds) and maggots are washed off from decomposingcarcasses of chum salmon and pink salmon O. gorbus�cha during frequent floods caused by rains. Imagoes ofinsects and other invertebrates are available in allbiotopes (they are washed off during floods or they fallonto the water surface at strong winds).

Narrower food spectra of yearlings of coho salmonand mykiss with high lipid status seem to follow fromthe dominant position of larger individuals over othersand from higher selectivity of feeding of the individu�als with high lipid status possessing a higher energeticpotential. In particular, greater energetic possibilitiesof these individuals are evidenced by a higher contentof TAG. It is known that in salmonids the principalstock of high�energy lipids (TAG) is concentrated inmuscles. The content of TAG clearly reflects the phys�

4

3

2

1

0

–1

–3

–4

–5

–2

–4 –2 0 2 4 6 8

1234

1

2

3

4

1

3

3

2

1

0

–1

–2

–3

–4–5 –4 –3 –2 –1 0 1 2 3 4 5

K1

K2

K2

Wilks’ Lambda: 0.09, p < 0.001

Wilks’ Lambda: 0.17, p < 0.001

(а)

(b)

2

4

Fig. 4. Canonical analysis of samples of yearlings of (a) coho salmon Oncorhynchus kisutch and of (b) mykiss Parasalmo mykiss bythe content of PL, TAG, CS, and CSE in the space of canonical roots: 1—with low lipid status, 2005, 2—with high lipid status,2005, 3—with low lipid status, 2006, and 4—with high lipid status, 2006. For designations of fractions of lipids see Fig. 2.

Fig. 5. Food spectra and the value (% by weight) of particular components of the food bolus in yearlings of coho salmon Onco�rhynchus kisutch (a, b) and of mykiss Parasalmo mykiss (c, d) with low (a, c) and high (b, d) lipid status in 2005 and 2006. Othercomponents of the food bolus: Diptera (pupae), Ephemeroptera (larvae), Ephemeroptera (imago), Gastropoda, Caviarium gas�tropoda, Trichoptera (imago), Lepidoptera (imago), Coleoptera (imago), Plecoptera (imago), Hymenoptera (imago), Collem�bola, Hemiptera (terrestrial), Arachnida (Acariformes, Hydracarina), scales, parts of plants, mineral particles, nonidentifiedmass.



162 3 5

2005 2006

7416

15

12

31

53 6

39

1.5

33

0.5

1118

36

1 4

16

1

6

72

265

2

3352 14

14

43 1 4 3

57

5

15

3 1

7699

1

Caviarium Oncorhynchii sp. et Salvelinii sp.

Diptera (imago)

Trichoptera (larvae)

Insecta (imago)

Hemiptera (Corixidae) imago

Myriapoda

Amphipoda

Oligochaeta

Lepidoptera (larvae)

Diptera (larvae)

Hymenoptera (imago)

(a)

(b)

(c)

(d)

Other

550


PAVLOV et al.

iological state of fish organism, including their loco�motor activity. In addition, the TAG level in the bodyof fish, particularly salmonids, reflects the level oftheir food supply (Sidorov, 1983; Shulman, 2001).Such juveniles obtain the advantage over subordinates(individuals with low lipid status) in selection of siteswith better food conditions and in selection of partic�ular food items (Ivlev, 1955; Faush, 1984; Metcalfe,1986; etc.). This assumption is also conformed by ourobservations on juveniles of coho salmon and mykissin aquaria: as a rule, larger individuals (dominants)aggressively drive away smaller individuals (subordi�nates) from food. Both eggs and maggots are suffi�ciently calorific food. In addition, the energy expendi�tures for obtaining eggs and maggots in dense aggrega�tions may be much lower than the expenditures forobtaining of dispersed imagoes of insects.

The summarized data for two years confirm ourpreliminary results on the presence of significant dif�ferences in juveniles of migratory (coho salmon) orhaving migratory forms (mykiss) salmonids by physio�logical and morphological parameters at least at8 months prior to smoltification and seaward migra�tion. It is found that the juveniles of coho salmon andmykiss with high lipid status have, as a rule, greater (onaverage) fork length and weight and consume morecalorific food. The juveniles with low lipid status havesmaller fork length and weight and consume less calo�rific organisms. With growth, they require more foodwhich may compensate not only the energy expendi�tures for its procuring but also to ensure furthergrowth. However, this becomes an increasingly com�plicated task for fish. As a result of this, the intraspe�cies and interspecies competition for food resourcesbecomes more acute. When certain size is attained,another behavioral program, aimed at smoltificationand seaward migration, is switched on. Realization ofthis program begins in the year preceding the migra�tion to the sea and, as we suppose, in the fish with highlipid status first of all. They would start seaward migra�tion already in June of the next year. The fish with lowlipid status continue feeding and would make seawardmigration later: coho salmon in July and mykiss wouldstay in the river at least for one more year.

Thus, the juveniles of salmonids a long time priorto the seaward migration are differentiated into twogroups differing in food habits, size�weight character�istics, and lipid status. Formation of such differentia�tion is based on well expressed separation of under�yearlings of the considered species into migrating andresident individuals in the period of their primary dis�persion (Pavlov et al., 2010b). Formation of suchgroups may make a component determining the originof intrapopulation diversity and, accordingly, influ�encing formation of the life strategy of fish and dates oftheir future smoltification and return for spawning.Further investigations of juveniles of salmonids in dif�ferent periods of ontogenesis would verify the causes

and role of differentiation in mechanisms of smoltifi�cation and of the subsequent seaward migration.

ACKNOWLEDGMENTS

The study was supported by the Russian Founda�tion for Basic Research (08�04�00927�a, 08�04�01140�a), the Biodiversity and Dynamics of GenePool Program of Fundamental Research of the Presid�ium of the Russian Academy of Sciences, the LeadingScientific Schools Program, and the State Support ofYoung Russian Scientists Program of the President ofthe Russian Federation (NSh�3731.2010.4; NSh�2104.2008.4, MK�1392.2009.4).

REFERENCES

1. G. P. Barach, “Dynamics of Downstream Migration ofJuvenile Salmon and a Unique Pool of Reproduction ofSalmon�Trout Schools of the Black Sea Basin,” Tr.Nauchno�Issled. Rybokhoz. St. Gruzii 5, 54–64(1960).

2. F. M. Engelbrecht, F. Mari, and J. T. Anderson, “Cho�lesterol Determination in Serum. A Rapid DirectionMethod,” S. Afric. Med. J 48 (7), 250–256 (1974).

3. K. D. Faush, “Profitable Stream Positions for Salmo�nids; Relating Specific Growth Rate to Net EnergyGain,” Can. J. Zool. 62, 441–451 (1984).

4. J. Folch, M. Lees, and G. H. Sloane, Stanley “A SimpleMethod for the Isolation and Purification of Total Lip�ids from Animal Tissues,” J. Biol. Chem. 226 (5), 497–509 (1957).

5. W. S. Hoar, “The Physiology of Smolting Salmons,” inFish Physiology, Ed. by W. S. Hoar and D. J. Randall(Acad. Press, New�York, 1988), Vol. 11B, pp. 275–343.

6. V. S. Ivlev, Experimental Ecology of Fish Feeding (Pish�chepromizdat, Moscow, 1955) [in Russian].

7. R. N. Karimov, Fundamentals of Discriminant Analysis(SGTU, Saratov, 2002) [in Russian].

8. R. V. Kazakov and A. E. Veselov, “Regularities of Smol�tification of Atlantic Salmon,” in Atlantic Salmon(Nauka, St. Petersburg, 1998), pp. 195–241.

9. E. A. Kirillova, Candidate’s Dissertation in Biology(IPEE RAS, Moscow, 2009).

10. K. V. Kuzishchin, O. P. Pustovit, D. S. Pavlov, andK. A. Savvaitova, “Morphobiological Traits of Down�stream�Migrating Juveniles of Parasalmo mykiss fromSome Rivers of the Western Kamchatka in Relation toSmolting,” Vopr. Ikhtiol. 42 (6), 751–762 (2002) [J.Ichthyol. 42 (9), 720–732 (2002)].

11. G. F. Lakin, Biometry (Vysshaya Shkola, Moscow,1990) [in Russian].

12. V. E. Matsuk, Candidate’s Dissertation in Biology(Mosk. Gos. Univ., Moscow, 1975).

13. S. D. McCormic and R. L. Saunders, “PreparatoryPhysiological Adaptations for Marine Life of Salmo�nids: Osmoregulation, Growth, and Metabolism,” Am.Fish. Soc. Symp. 1, 211–229 (1987).

14. N. B. Metcalfe, “Intraspecific Variation in CompetitiveAbility and Food Intake in Salmonids: Consequences



for Energy Budgets and Growth Rates,” J. Fish. Biol.28, 525–531 (1986).

15. N. B. Metcalfe, F. A. Huntingford, and J. E. Thorpe,“Social Effects on Appetite and Development in Atlan�tic Salmon,” World Aquaculture Workshops, No. 2,29–40 (1992).

16. Methodical Instructions on Investigation of Feeding andTrophic Relationship of Fish under Natural Conditions(Nauka, Moscow, 1974) [in Russian].

17. G. G. Novikov, Growth and Energetics of Development ofBony Fish in Early Ontogenesis (Editoreal URSS, Mos�cow, 2000) [in Russian].

18. D. S. Pavlov, Biological Foundations of Control of FishBehavior in a Water Stream (Nauka, Moscow, 1979) [inRussian].

19. D. S. Pavlov and E. A. Maslova, “Downstream Migra�tion and Feeding of Juvenile Coho Salmon Oncorhyn�chus kisutch in the Northern Part of Its Range on Kam�chatka,” Izv. Akad. Nauk, Ser. Biol., No. 3, 314–326(2006).

20. D. S. Pavlov, K. A. Savvaitova, K. V. Kuzishchin, et al.,Pacific Noble Salmon and Trouts of Asia (Nauch. Mir,Moscow, 2001) [in Russian].

21. D. S. Pavlov, K. V. Kuzishchin, P. I. Kirillov, et al.,“Downstream Migration of Juveniles of KamchatkaMykiss Parasalmo mykiss from Tributaries of theUtkholok and Kol Rivers (Western Kamchatka),” J.Ichthyol. 45 (Suppl. 2), 185–198 (2005).

22. D. S. Pavlov, E. A. Kirillova, P. I. Kirillov, et al.,“Downstream Migration of Juvenile Salmonids andCyclostomata in the Utkholok River Basin,” in Conser�vation of Biodiversity of Kamchatka and Coastal Waters,Materials of VII International Scientific Conference Ded�icated to the 25th Anniversary of Organization of Kam�chatka Division of the Institute of Biology of Sea (Kam�chatpress, Petropavlovsk�Kamchatskii, 2006),pp. 112–115.

23. D. S. Pavlov, N. N. Nemova, P. I. Kirillov, et al., “LipidStatus and Feeding Habits of Salmonid Juveniles in theYear Preceding Seaward Migration as Factors Control�ling Their Future Smoltification,” Vopr. Ikhtiol. 47 (2),247–252 (2007) [J. Ichthyol. 47 (3), 241–245 (2007)].

24. D. S. Pavlov, V. V. Kostin, I. V. Nechaev, et al., “Etho�Biochemical Mechanisms of Early Differentiation inJuveniles of the Atlantic Salmon Salmo salar,” J. Ich�thyol. 49 (11), 1081–1090 (2009).

25. D. S. Pavlov, V. V. Kostin, and V. Yu. Ponomareva,“Behavioral Differentiation of Underyearlings of theBlack Sea Salmon Salmo trutta labrax: Rheoreaction inthe Year Preceding Smoltification,” Vopr. Ikhtiol. 50(2), 251–261 (2010a) [J. Ichthyol. 50 (3), 270–280(2010a).

26. D. S. Pavlov, N. N. Nemova, Z. A. Nefedova, et al.,“The Lipid Status of Young of the Year Mykiss Paras�

almo mykiss and Coho Salmon Oncorhynchus kisutch,”Vopr. Ikhtiol. 50 (1), 120�129 (2010b) [J. Ichthyol. 50(1), 116–126 (2010b)].

27. N. S. Pustovit and O. P. Pustovit, “Some Hematologi�cal Parameters of Juvenile Kamchatka SteelheadParasalmo mykiss,” Vopr. Ikhtiol. 45 (5), 680�688(2005) [J. Ichthyol. 45 (8), 648–656 (2005)].

28. T. P. Quin, The Behavior and Ecology of Pacific SalmonTrout (Univ. Wash., Canada, 2005).

29. D. K. Rowe, J. E. Thorpe, and A. M. Shanks, “TheRole of Fat Stores in the Maturation of Male AtlanticSalmon (Salmo salar) Parr,” Can. J. Fish. Aquat. Sci.48, 405–413 (1991).

30. K. A. Savvaitova, V. A. Maksimov, M. V. Mina, et al.,Kamchatka True Salmon (Systematics, Ecology, andPerspectives of Use as an Object of Trout Husbandry andAcclimatization) (Voronezh. Gos. Univ., Voronezh,1973) [in Russian].

31. L. Shapovalov and A. C. Taft, “The Life Histories of theSteelhead Rainbow Trout (Salmo gairdneri) and SilverSalmon Oncorhynchus kisutch) with Special Referenceto Waddell Creek, California, and RecommendationsRegarding Their Management”, Fish. Bull. Calif.Dept. Fish. Game, No. 98 (1954).

32. G. E. Shul’man, “Ecological Physiology and Biochem�istry of the Black Sea Hydrobionts at the Beginning ofthe 21st Century,” in Sea Ecology, Collection of ScientificPapers of the Institute of Biology of Southern Seas of theNational Academy of Ukraine (2001), Issue 57, 68–74.

33. V. S. Sidorov, Ecological Biochemistry of Fish. Lipids(Nauka, Leningrad, 1983) [in Russian].

34. V. S. Sidorov, E. I. Lizenko, O. M. Bolgova, andZ. A. Nefedova, “Fish Lipids. 1. Methods of Analysis.Tissue Specification of European Cisco Coregonusalbula L.,” in Salmonidae of Karelia (Karel. Fil. ANSSSR, Petrozavodsk, 1972), Issue 1, pp. 152–163.

35. J. E. Thorpe, “Bimodal Distribution of Length of Juve�nile Atlantic Salmon under Artificial Rearing Condi�tions,” J. Fish. Biol. 11, 175�184 (1977).

36. J. E. Thorpe, “Age at Maturity in Atlantic SalmonSalmo salar L.: (Freshwater Period Influence and Con�flicts with Smolting,” Can. Spec. Publ. Fish. Aquat.Sci. 89 7–14 (1986).

37. J. E. Thorpe, “Developmental Variation in SalmonidPopulations,” J. Fish. Biol. 35 (Suppl. A), 295–303(1989).

38. J. E. Thorpe, C. E. Adams, M. S. Miles, and D. S. Keay,“Some Photoperiod and Temperature Influences onGrowth Opportunity in Juvenile Atlantic SalmonSalmo salar,” Aquaculture 82, 119–126 (1989).

39. G. A. Wedemeyer, Physiology of Fish in Intensive CultureSystems (Chapman & Hall, Int. Thompson Publ.,1996).

Documents

The lipid status and feeding habits of yearlings of mykiss Parasalmo mykiss and coho salmon Oncorhynchus kisutch in autumn