Hormonal status in different phenotypic forms of Black Sea trout Salmo trutta labrax

ISSN 0032�9452, Journal of Ichthyology, 2010, Vol. 50, No. 11, pp. 985–996. © Pleiades Publishing, Ltd., 2010.

985

Many species of salmonids (Salmonidae) evenwithin one population manifest different life strate�gies—anadromous and resident—and, accordingly,have different phenotypic forms (as reviewed by Pav�lov and Savvaitova, 2008). Morphological, physiolog�ical, biochemical, and ethological traits of formationof such morphs are still subjects of numerous investi�gations (Hoar, 1953, 1988; Barannikova, 1975;Thorpe, 1986; Thorpe et al., 1989; Pavlov andMaslova, 2006; Nechaev et al., 2007; Pavlov et al.,2007a, 2007b, 2008a, 2008b, 2008c, 2008 d, 2009,2010).

Black Sea trout Salmo trutta labrax exists in twophenotypic forms: resident form (trout) and migratoryform (kumzha). The migratory form of this subsepciesis entered in the Red Data Book of Russian Federa�tion. Kumzha and trout make “a general salmonid�trout stock”—in the progeny of fish of one form, thespecimens of both forms regularly appear (Barach,1952; Panov, 1958). Differentiation into these forms isretained under conditions of artificial propagation.External characteristic traits of differentiation of parrsof Black Sea kumzha are observed at the age 1+. Atthis age, kumzha undergoes parr�smolt transforma�tion and is preparing for downstream migration to the

sea. Morphophysiological and biochemical particu�larities of fish at this age should be a subject of specialinvestigations as this information would elucidate themechanism of differentiation of parrs.

The present study is aimed at investigation of bio�chemical parameters (content of dopamine, norad�renalin, serotonin, thyroxin, triiodothyronine in thebrain and cortisol, growth hormone, an adrenocorti�cotropic hormone in fish blood) and morphophysi�olgical parameters (length, weight, sex, and stages ofgonad maturation) in different phenotypical forms ofBlack Sea trout.

MATERIAL AND METHODS

Investigations were conducted on Black Sea troutof fish�farm and on wild fish of natural origin fromJune to September 2008 and in August 2009.

The farm stock was formed at the Adler fish farm ofdescendants of several pairs of spawners caught in theMzymta River in November 1997. Genetic investiga�tion demonstrated that the farm stock generallyretained the genetic structure characteristic of naturalpopulations (Kholod et al., 2004). The fish investi�gated in the present study belonged to the second gen�eration of artificial propagation. The trout was kept inoutdoor concrete tanks at the water temperature 12–14°C. From June to September 2008, once a month,

Hormonal Status in Different Phenotypic Formsof Black Sea Trout Salmo trutta labrax

D. S. Pavlova, V. V. Kostina, I. V. Nechaeva†, V. A. Yankovskayab, N. N. Shindavinac, V. Ya. Nikandrovc, E. V. Moiseevab, and Ya. V. Kondratenkob

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

b Adler Forel farm, Russia c Federal Selection–Genetic Center of Fish Culture, Russia

Received April 14, 2010

Abstract—In three phenotypic forms (parrs, trout form, and kumzha form) of fish�farm Black Sea trout (age1+) and wild Black Sea trout (age 1+ and 2+), Salmo trutta labrax, inhabiting the basin of the Mzymta River,the content of monoamines (dopamine, noradrenalin, and serotonin) and of their metabolites (3,4�dihy�droxyindolacetic acid, 3�methoxy�4�hydroxyphenyl glycol, and 5�hydroxyindolacetic acid) was investigatedin brain regions (forebrain, optic tectum, brainstem, hypothalamus, and hypophysis) and the level of cortisol,thyroxin, triiodothyronine, growth hormone, and adrenocorticotropic hormone was investigated in blood.Data on length and weight of fish body and maturation stage of gonads are indicated. The hormonal level dif�fers in the fish of different phenotypic forms. It is the highest in specimens of the kumzha form which com�pleted parr–smolt transformation. Among wild fish, numerous mature females at age 1+ were found whichindicated the presence of a dwarf form of the Black Sea trout in the Caucasus in the Mzymta River.

DOI: 10.1134/S0032945210110032

Key words: hormonal status, monoamines, maturity stage of gonads, the Black Sea trout, phenotypic forms.

†Deceased.

986

JOURNAL OF ICHTHYOLOGY Vol. 50 No. 11 2010

PAVLOV et al.

the 1+ old fish were taken for investigation. Alto�gether, 566 specimens were investigated. Of them,samples for biochemical analysis were taken from270 specimens.

Fish of natural origin were caught in the MzymtaRiver, its tributary (the Chvezhips River) and in thePsakho River. For correct comparison with the farmfish, the wild fish of natural origin were caught in thesame season as the season of investigation of the farmfish. Water temperature in July–middle of Augustfluctuated within 16.6–17.8°C, in August–Septemberit decreased to 13.3–15.2°C, and in late September itwas 12.8°C. Depth in the Mzymta was 70–150 cm andin the Chvezhips and the Psakho it was 20–50 cm.First catches were taken in the middle of July. Themain part of the material was collected in late August–September 2008, predominantly in the Chvezhips,tributary to the Mzymta. Additional material on theage, size, and sex composition of fish in this tributarywas collected in August 2009. Fishing was made withhook�and�line gear at several river stretches of 2.5–4.0 km. Altogether, in 2008, 176 specimens wereinvestigated and, in 2009, 29 specimens were investi�gated. Samples for biochemical analysis were takenfrom 173 specimens.

In the fish, weight (in farm fish only), fork length(AC), sex, maturity stage of gonads, and phenotypicform were determined. Then, specimens of each phe�notypic form were dissected, and organs and tissueswere taken for subsequent biochemical analysis andscales were taken for determination of age.

According to biochemical analysis, differentregions of the brain were investigated: forebrain, opti�cal tectum, brainstem, hypothalamus, and hypophy�sis. Determinations comprised the level of monoam�ines—dopamine (DA), noradrenalin (NA), and sero�tonin (5�HT)—and of their metabolites—3,4�dihydroxyphenylacetic acid (DOPAA), 3�methooxy�4�hydroxyphenyl glycol (MHPG), 5�hydroxyindola�cetic acid (5�HIAA). In samples of blood, the level ofcotrisol, thyroxin (T4), triiodothyronin (T3), growthhormone (GH), and adrenocorticotropic hormone(ACTH) were determined.

The level of monoamines and of their metabolitesin the brain was investigated by high performance liq�uid chromatography (HPLC) (Shimadzu LC�10AVP,Japan) with application of an electrochemical detec�tor DECADE II. NA, MHPG, DA, DOPAA, 5�HT,and 5�HIAA were determined by the modified(Nechaev, 2004) Magnusson method (Magnussonet al., 1980). Supernatant homogenate was introduceddirectly to the chromatograph, omitting usual adsorp�tion operations. Columns Nucleosil C18 (5 µm) wereused. Potential of the detector was 0.8 V. Mobile phasewas: citrate buffer (pH 4.25) with methanol (8.2%)and hexyl sulfate (1.7 × 10–3 M).

Cortisol was determined by HPLC using chro�matographic columns Nucleosil 5NO2. Mobile phasewas: dichloromethane, ethanol, and water in the ratio

500 : 12 : 1, flow rate 1.5 ml/min at pressure 180 bar.Cortisol was determined at 242 nm.

Concentrations of T4 and T3 were determined bydirect radioimmune method (Dickhoff et al., 1978);measurement range was for T4 2–60 ng/ml, for T3—0.5–18 ng/ml.

Growth hormone in blood plasma was determineby a standard radioimmune method (Bjornsson et al.,1989); determination range was within 0.2–45.0 ng/ml. The hormonal status was used as a com�plex parameter of the state and level of activity of hor�monal systems of the organism. It was calculated onthe basis of standardization of the obtained values ofconcentrations according to the previously publishedmethods (Pavlov et al., 1998). The level of the value ofhormonal status (Gs) was determined separately forfarm fish, for wild fish, and for comparison of farm andwild fish by the equations:

where Ci is a set of standard concentrations of sub�stances for a given fish group (e.g., for parr in June); Nis number of Ci; and i is the number of a given sub�stance in a given region of the brain or in blood(through numbers, e.g., DA in the forebrain is no. 1and in the optic tectum it is no. 6).

Standard concentration was determined by theequation:

where Kij is mean concentration of a particular sub�stance in a give region of the brain or in blood in fish ofa certain group, Kj is a set of values of Kij for a give sub�stance in a given region of the brain or in blood, minand max are minimum and maximum values of Kj, i isnumber of a given substance in a certain region of thebrain or in blood (through numeration), and j is num�ber of the investigated fish group.

Statistical treatment was made by the standardmethod (Lakin, 1980) using statistical software andoriginal extensions Microsoft Excel.

RESULTS AND DISCUSSION

Morphofunctional State of Farm Fish

General characteristics. Three forms of fish werediscerned in the Black Sea trout of the age 1+, reflect�ing their morpho�physiological state at the moment ofinvestigation: parr, trout form (trout), and kumzhaform (kumzha, smolts). In addition, fish in a transi�tional state occurred rather often too—those withcharacters of several forms. Special traits of colora�tion, by which specimens were attributed to pheno�typic forms, are indicated below.

Gs

Ci∑N

��,=

CiKij min Kj( )–

max Kj( ) min Kj( )–��,=


HORMONAL STATUS IN DIFFERENT PHENOTYPIC FORMS 987

Parr. The body is gray with olive shade and clearblack transverse bands along the body. No round redand black spots.

Trout form (trout). Color is olive from dark on thedorsal side to light on the belly, with bright red spots allover the body alternating with small black spots ofirregular form.

Kumzha form (smolt, kumzha). Uniform silverycolor all over body. With formation of the kumzhaform, large round black spots appear all over the bodyand the belly remains light, without spots.

In addition, specimens in transitional states werefound. Color of their body had characters both of parr,trout, and kumzha in various combinations. Speci�mens were found with signs of trout and kumzha andabsence of characters of parr, probably due to theirdesmoltification.

Number of fish of different phenotypic forms dif�fers from year to year. For example, in August 2008,among 538 specimens, all aforementioned forms werefound in the ratio 20 : 22 : 21 : 37 (as listed) and thosein August 2009 (n = 447) were found in the ratio 0 : 66 :23 : 11.

In parr and in the fish in transitional state, malesslightly prevailed, 59.6 and 56.6%, respectively(Table 1). Males prevailed significantly (p < 0.05 by theStudent’s test for fractions) among fish of the troutform (67.2%). Females prevailed among fish of thekumzha form (66.1%).

The state of gonad in females was almost identicalin fish of the investigated forms, all females were atmaturity stage I–II of gonads. At the same time, thestage of gonads of males of different forms was inho�mogeneous. In fish of the kumzha form, the testeswere at maturity stage I–II. In most parr and the fishof transitional forms, most specimens were at the samestage, but more mature specimens were also notedamong them—4.5% (stage III) of transitional formsand 16.4% (stage III–IV) of parr. In the trout, almost

2/3 of males had testes at maturity stage IV–V andonly 37.5% were at stage I–II.

Great diversity by weight and length was foundamong females and males of each form (Table 1). Thebody length and weight increased in the series parr—trout—kumzha (Fig. 1). The fish in the transitionalstate occupied an intermediate position.

Length and weight of females and males of differentforms were different (Fig. 1, Table 2). In parr, malesand females were almost of the same length at a higherweight of females. In trouts, males surpassed females

Table 1. Body length and weight and the level of gonad development of the farm Black Sea trout Salmon trutta labrax at the age1+ (16 months) in August 2008

Parameters

Parr Trout Kumzha Transitional specimens

males(n = 65)

females(n = 44) males females males females males females

Weight, g

Length, cm

Maturity stageof gonads(part of fish, %)

I–II (83.6)III–IV (16.4)

I–II (100%)

I–II (37.5%)IV–V

(62.5%)

II (100%) I–II (100%)

I–II (100%) I–II (95.5%)

III (4.5%)

I–II (100%)

Note: Above the line⎯mean value of a parameter and mean square deviation; under the line⎯variation range of a parameter; n⎯numberof investigated fish.

37.1 10.2±

16.0–56.4�� 42.1 11.5±

32.5–59.9�� 75.7 27.4±

28.5–148.0�� 59.9 15.7±

40.5–89.0�� 83.7 18.3±

49.5–136.5�� 112.1 32.9±

43.5–222.0�� 60.0 29.3±

32.0–103.0�� 67.3 15.3±

32.0–84.0��

13.6 1.4±

10.0–16.2�� 13.9 1.4±

11.2–16.2�� 16.9 2.4±

13.2–21.7�� 16 1.1±

14.5–18.0�� 18.9 1.5±

16.5–21.2�� 20.4 2.5±

15.0–24.8�� 15.7 2.8±

11.2–19.6�� 17.0 1.7±

13.1–18.6��

25

20

15

10

5

0

120

100

80

60

40

20

0

Weight, g

Length, cm

Forms of yearlings KumzhaTrout Parr

(b)

(a)

Fig. 1. (a) Length and (b) weight of males andfemales of different forms of the farm Black Sea trout

Salmon trutta labrax at the age 1+.

988


PAVLOV et al.

by weight and length. In fish of the kumzha form andtransitional form, the body length and weight weregreater than those in males.

Thus, at the second year of live (1+) in juveniles ofthe Black Sea trout there was differentiation into phe�notypic forms in the process of growth and develop�ment under conditions of artificial propagation. A partof parr either underwent parr–smolt transformation(passed over to the kumzha form) or developed intothe trout form. Presence of parr and of numerous fishin transitional state indicates to incompleteness of thisprocess at the age 16 months or to desmoltificationstarted in some specimens. All these forms differed inbody length and weight. In the series parr—trout—

kumzha, both the body length and weight increased.The females belonging to different phenotypic groupshad the same maturity stage of gonads. Males of differ�ent forms differed by development of gonads too.Early maturation of testes was noted (up to maturitystage V) in some males of the trout form. Early matu�ration is one of characteristic features of specimens ofthe dwarf form characterized by retardation of subse�quent growth. No mature females at the age 1+ werefound.

Hormonal status. The results of investigation ofconcentrations of hormones in regions of the brainand in blood of fish belonging to different phenotypi�cal forms are shown in Table 3.

Dynamics of concentrations of the investigatedsubstances in fish belonging to different forms was dif�ferent and reflected differences in their growth anddevelopment in this period. For example, in fish of thekumzha form from June to September there was aconsiderable increase in concentration of growth hor�mone in blood (Fig. 2). In trout, this parameter washigher in June, then decreased (not significantly), andremained at this level until August. In parr, the contentof growth hormone was the lowest in comparison withother forms.

Dynamics of concentrations of the investigatedhormonal substances in regions of the brain and inblood was extremely diverse (Table 3). Most similarchanges in the content of different hormonal sub�stances were characteristic of juveniles of the kumzhaform. In most cases, there was a tendency to increasein concentration of hormones from June to Septem�ber. The quantity of DOPAA increased significantly inthe forebrain, optical tectum, hypothalamus, andhypophysis. The content of particular substanceschanged insignificantly. The exception was the signifi�cant decrease of concentration of cortisol in blood. Inmost cases, the content of hormones in kumzha washigher than in parr and trout, with some exceptions.For example, the level of concentration of dopaminein the forebrain in June was maximal in parr; in thehypophysis and hypothalamus, the maximum levels ofthis substance were in trouts in all months of the inves�tigation (Table 3). Still higher diversity of dynamicsand ratio of levels of concentration of the investigatedsubstances was in parr and trout.

For elucidation of the most general trends, theresults of biochemical analysis were standardized—the level of hormonal status for the investigated fishgroups was calculated. It was highest in specimens ofthe kumzha form in all months of the investigation(Fig. 3). In trout and parr, it was lower; in July theywere identical as to this status. Dynamics of this statuswas different in fish of different phenotypical forms. Inkumzha and parr, the level of hormonal statusincreased, obviously due to growth of these fish. Introut, this status decreased in July and increased toSeptember. It is possible that the value of these param�

Table 2. Significance levels of differences in mean values oflength and weight in the farm Black Sea trout Salmo truttalabrax at the age 1+

FormForm

Parr Trout Kumzha

Fish weight

Parr 0.02 <0.001 <0.001

Trout <0.001 0.001 0.11

Kumzha <0.001 <0.001 <0.001

Transitional state <0.001 0.01 <0.001

Fish length

Parr 0.27 <0.001 <0.001

Trout <0.001 0.03 <0.001

Kumzha <0.001 <0.001 0.001

Transitional state <0.001 0.001 <0.001

Note: Insignificant values are shown in bold type; the marked diag�onals of the table indicate the results of comparison of malesand females of one form; the results of comparison of param�eters of males of different forms are indicated above thesediagonals and of females is shown below them.

5

June0

July September

GH concentration, ng/g

10

15

20

Months

12

3

Fig. 2. Dynamics of concentration of growth hormone(GH) in fish blood (1+) of different phenotypic forms ofthe farm Black Sea trout Salmon trutta labrax at the age 1+in June�September: 1—parr, 2—trout, and 3—kumzha.



eters in them reflects prevalence of processes of gener�ative metabolism when this form is shaped.

With consideration of the results of biochemicalinvestigations shown in Table 3, cluster analysis was

made. By hormonal status, the most distinct compactcluster consisted of specimens of the kumzha form inall months of the investigation (Fig. 4). The highestsimilarity was found in the fish which completed the

Table 3. Concentrations of hormones and of their metabolites (M ± σ) in regions of the brain and in blood of the farm Black Seatrout Salmon trutta labrax at the age 1+ in the fish of different phenotypic forms

Substances,ng/g

Parr Trout Kumzha

June July June July September June July September

Forebrain

DA 80.3 ± 4.6 38.4 ± 5.9 38.1 ± 2.3 32.5 ± 4.7 41.3 ± 4.3 61.5 ± 2.2 68.4 ± 4.5 75.3 ± 4.7

DOPAA 7.5 ± 0.6 4.1 ± 2.2 4.2 ± 0.4 5.3 ± 1.2 9.4 ± 1.6 4.2 ± 0.4 9.2 ± 1.7 11.6 ± 2.2

NA 164.3 ± 11.4 167 ± 18.5 225.1 ± 12.5 187.3 ± 17.6 165.4 ± 21.0 252.1 ± 21.6 259.0 ± 19.5 248.5 ± 21.5

MHPG 0.21 ± 0.05 0.28 ± 0.09 0.53 ± 0.06 0.44 ± 0.08 0.56 ± 0.11 0.43 ± 0.06 1.05 ± 0.14 1.14 ± 0.17

5�HT 76.1 ± 11.4 74.3 ± 19.3 100.5 ± 12.2 77.7 ± 6.9 80.4 ± 7.8 111.6 ± 11.8 110.6 ± 9.9 110.2 ± 11.2

5�HIAA 15.9 ± 0.8 16.6 ± 4.7 23.5 ± 1.1 14.2 ± 3.4 16.7 ± 3.3 31.1 ± 5.4 26.6 ± 4.6 28.4 ± 3.9

Optic tectum

DA 46.7 ± 1.4 48.8 ± 11.8 46.4 ± 1.2 35.7 ± 3.9 34.4 ± 4.0 38.6 ± 2.7 36.4 ± 4.7 43.1 ± 3.8

DOPAA 1.2 ± 0.1 1.9 ± 0.9 1.4 ± 0.2 3.1 ± 0.6 3.6 ± 0.5 1.3 ± 0.1 4.7 ± 1.0 5.1 ± 1.1

NA 66.6 ± 1.5 76.2 ± 14.7 85.4 ± 1.4 79.2 ± 6.5 77.4 ± 8.8 86.8 ± 9.5 86.5 ± 10.6 88.8 ± 9.6

MHPG 0.23 ± 0.05 0.27 ± 0.11 0.31 ± 0.04 0.49 ± 0.08 0.51 ± 0.09 0.71 ± 0.05 0.73 ± 0.11 0.94 ± 0.13

5�HT 30.3 ± 1.5 34.6 ± 13.5 35.5 ± 1.6 36.4 ± 3.2 36.7 ± 5.4 47.3 ± 7.4 49.4 ± 8.8 51.2 ± 5.7

5�HIAA 6.5 ± 0.9 7.2 ± 2.9 7.9 ± 1.0 8.0 ± 1.2 7.4 ± 2.1 11.2 ± 1.2 12.3 ± 3.2 12.4 ± 2.6

Brainstem

DA 36.8 ± 1.3 40.2 ± 11.2 50.1 ± 1.7 43.3 ± 2.8 34.4 ± 4.6 42.1 ± 5.9 44.6 ± 4.7 45.0 ± 5.6

DOPAA 0.52 ± 0.07 0.57 ± 0.14 0.45 ± 0.05 0.43 ± 0.06 0.55 ± 0.11 0.84 ± 0.07 1.03 ± 0.21 1.01 ± 0.17

NA 87.4 ± 1.8 94.2 ± 14.5 107.5 ± 1.9 91.2 ± 4.7 82.6 ± 5.2 95.8 ± 9.8 114.1 ± 12.6 122.5 ± 11.6

MHPG 0.52 ± 0.08 1.06 ± 0.22 0.71 ± 0.11 0.55 ± 0.16 1.94 ± 0.36 1.75 ± 0.12 2.27 ± 0.22 3.11 ± 1.01

5�HT 65.5 ± 9.1 71.4 ± 15.6 71.5 ± 6.8 54.4 ± 7.7 45.7 ± 6.2 77.3 ± 9.3 64.1 ± 7.4 67.7 ± 8.1

5�HIAA 15.0 ± 1.2 15.7 ± 3.2 10.5 ± 1.3 6.7 ± 1.8 9.4 ± 1.9 18.4 ± 1.5 11.3 ± 2.0 12.6 ± 2.7

Hypothalamus and hypophysis

DA 160.2 ±13.6 171.4 ± 26.3 202.8 ±18.7 187.3 ± 11.4 232.3 ± 18.5 160.8 ± 13.4 159.7 ± 16.6 174.4 ± 12.5

DOPAA 5.1 ± 0.6 5.3 ± 2.1 1.7 ± 0.5 7.5 ± 1.2 11.4 ± 2.2 4.1 ± 0.6 10.5 ± 2.3 11.3 ± 3.1

NA 129.1 ± 11.4 121.0 ± 21.0 131.5 ± 12.0 124.6 ± 12.4 134.7 ± 11.9 118.0 ± 10.1 163.4 ± 14.2 162.7 ± 19.3

5�HT 111.7 ± 10.9 152.5 ± 27.7 204.9 ± 17.8 179.5 ± 14.3 235.6 ± 18.6 131.6 ± 12.2 134.2 ± 11.3 137.7 ± 12.4

5�HIAA 6.7 ± 1.0 13.7 ± 4.6 12.6 ± 2.3 16.5 ± 2.0 18.6 ± 3.4 11.8 ± 2.5 12.5 ± 2.8 11.9 ± 1.9

Blood

Cortisol 8.8 ± 2.5 7.6 ± 2.3 12.6 ± 2.7 18.4 ± 3.8 11.5 ± 2.8 80.2 ± 4.7 62.3 ± 11.2 37.4 ± 5.1

T3 4.8 ± 1.0 5.2 ± 1.8 4.1 ± 0.6 3.4 ± 0.7 3.6 ± 1.1 6.6 ± 0.5 9.1 ± 2.3 11.5 ± 1.9

T4 1.1 ± 0.3 1.7 ± 0.4 1.4 ± 0.3 1.2 ± 0.4 1.8 ± 0.6 6.7 ± 0.7 15.6 ± 2.9 19.8 ± 2.6

GH 6.2 ± 1.2 5.4 ± 1.5 10.0 ± 0.8 6.5 ± 1.7 6.9 ± 1.3 7.5 ± 0.8 12.2 ± 3.7 18.6 ± 3.0

ACTH,pg/ml

37.2 ± 4.9 29.6 ± 5.3 99.0 ± 8.3 42.5 ± 11.2 46.7 ± 9.6 68.0 ± 6.0 79.5 ± 10.6 84.3 ± 9.8

Note: M ± σ⎯mean value of a parameter and mean square deviation; DA⎯dopamine, DOPAA⎯3,4�dihydroxyphanylacetic acid,NA⎯noradrenalin, MHPG⎯3�methoxy�4�hydroxyphanyl glycol, 5�HT⎯serotonin, 5�HIAA⎯5�hydrooxyindilacetic acid,T3⎯triiodothyronin, T4⎯thyroxin, GH⎯growth hormone, and ACTH⎯adrenocorticotropic hormone.

990


PAVLOV et al.

process of parr–smolt transformation (July, Septem�ber). Parr and trouts made a mixed cluster in which thefish groups differed more than in the kumzha cluster.The minimum differences were recorded between parrand trout in July when the process of differentiation ofparr was almost completed.

Thus, the process of differentiation of parr into thekumzha form and the trout form was accompanied by

modification of their hormonal status—the complexparameter of the state of activity level of many hor�monal systems of the organism. In the series parr—trout—kumzha, this status increased. Smoltificationdrastically changed the activity of the investigatedhormonal systems. As a result of this, the fish readyfor migration to the sea (kumzha) drastically differedfrom the fish living only in fresh water (parr andtrout).

Morphofuncional State of River Fish

General characteristics. In July–September 2008in the Chvezhips, the Mzymta, and the Psakho rivers,176 specimens of the trout form of the Black Sea troutwere caught. From the beginning of the investigationto the end of August, the fish were caught on riffles andin river deep pools. In September, the fish were caughtin river deep pools only. Visually, the groups of 7–12 trout of various length were noted there. The groupbehavior might be related both to the decrease in the

water level in rivers1 and to the prespawning state of

fish.During the whole period of investigations, only fish

of the trout form of the Black Sea trout were found incatches. Absence of parr and of specimens of thekumzha form is obviously related to the time of catch�ing. Parr already were absent in the river as they passedover to the trout form of the kumzha form whose spec�imens migrated to the sea (Murza and Khristoforov,1988).

Among caught fish, males slightly prevailed(Table 4). The ratio of males and females in all periodsof investigation was statistically similar (p = 0.30, theStudent’s test for fractions). Mean size of fish caughtin August and September 2008 and in September 2009did not differ statistically (p > 0.05, the Student’s test).

The maturity stage of gonads is related both to sexand age of fish (Table 5). Over half of males attainedmaturity at the age 1+, and to the end of the third sum�mer they all had gonads at maturity stage IV and V. Itis interesting that almost a third of females attainedmaturity at the second year of life at the body lengthfrom 11.3 to 16.5 cm (Fig. 5). To the autumn of the

1 For example, in the Psakho River in September 2008, the waterdepth in the channel was 3–15 cm and up to 1 m in deep pools.

Table 4. Body length of wild specimens of the Black Sea trout Salmon trutta labrax

ParametersAugust 2008 September 2008 August 2009

males females males females males females

Number of fish, specimens 59 36 44 37 15 14

Length, cm

Note: Above the line⎯mean value of a parameter and mean square deviation; under the line⎯variation limits.

11.8 1.6±

9.5–14.8�� 11.3 1.9±

8.5–16.5�� 12.3 1.8±

9.8–18.4�� 11.5 1.8±

8.7–16.4�� 12.6 2.3±

10.1–17.4�� 14.2 2.5±

11.0–19.0��

1.0

0.8

0.6

0.4

0.2

0

Hormonal status

MonthsSeptemberJulyJune

Fig. 3. Hormonal status in phenotypic forms the farmBlack Sea trout Salmon trutta labrax at the age 1+ in June–September: —Parr, —Trout, and —Kumzha.

20

K90

K7 K6 T9 T6 T7 P7 P6Fish groups

40

60

80

100

120Euclidean distance, %

Fig. 4. The results of cluster analysis of the investigatedphenotypic forms of the farm Black Sea trout Salmon truttalabrax at the age 1+ by concentration of hormonal sub�stances in regions of the brain and in blood in June–Sep�tember: P6 and P7—Parr in June and in July, respectively;T6, T7, and T9—Trout in June, July, and September,respectively; K6, K7, and K9—Kumzha in June, July, andSeptember.



third years of life, the part of females with gonads atmaturity stage IV increased to 50%. Generally, in males,the number of fish with mature gonads (stages IV–V) washigher than in females (p < 0.001, the Student’s test forfractions).

In the fish caught in September 2008, the level ofgonad maturity was higher than in August: in males,the number of specimens with gonads at maturity stageIV and V increased from 81.2 to 93.2% and that infemales increased from 16.7 to 45.9%. This indicatesto maturation of gonads and preparation for spawning.Probably, maturation of gonads was the cause of thelow growth rate of trouts noted above. It is known that

at intensification of generative metabolism in theperiod of maturation of gonads, the growth of theorganism is retarded. Obviously, this explains theabsence of differences in length in the fish caught inAugust and September 2008.

According to Murza and Khristoforov (1988), fromAugust 27 to September 21, 1987, in the MzymtaRiver and in its tributary the Chvezhips, 51 femalesand 63 males of the Black Sea trout were caught withthe mean body length 16.2 and 16.7 cm, respectively.In 1987 and 2008, the area of fish capture and theperiod of work were almost identical. During thepassed 21 years the mean length of fish decreased by

(a)

(b)

Fig, 5. Dwarf forms of females of the Black Sea trout Salmo trutta labrax at the age 1+ caught in August in the Mzymta basin:(a) in 2008 and (b) in 2009.

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PAVLOV et al.

4.2 cm in males and by 4.7 cm in females. The differ�ences in the mean length of males and females in 1987and 2008 were highly significant (p < 0.001 by the Stu�dent’s test). In 1988, among 114 captured specimensof the Black Sea trout there were no specimens withgonad at maturity stages IV and V. In 2008, among81 specimens, 58 specimens were found with gonads atthese maturity stages. These differences were also sig�nificant (p < 0.001 by the Student’s test for fractions).Comparison of these materials indicates to acceleratedmaturation and to the related retardation of growth ofthe trout form in the Mzymta basin, i.e., to formationof the resident dwarf form of the Black Sea trout.

Table 5. Maturity level of gonads in wild specimens of thetrout form of the Black Sea trout Salmon trutta labrax(August–September 2008–2009)

Sex Age, years

Number of fish, %

Maturity stage of gonads

I II III IV V

Females 1+ 28.6 39.3 0 25.0 7.1

2+ 7.1 35.8 7.1 50.0 0.0

Males 1+ 5.6 22.2 19.4 33.4 19.4

2+ 0 0 0 53.3 46.7

Table 6. Concentration of monoamines and of their metabolites in regions of the brain of the wild specimens of the trout formof the Black Sea trout Salmon trutta labrax with gonads at different maturity stages, late August–September 2008

Substances,ng/g

Maturity stages of gonads

males females

II IV V II IV V

Forebrain

DA 37.7 ± 3.0 39.3 ± 4.1 29.0 ± 2.7 37.1 ± 3.2 36.5 ± 3.3 24.2 ± 2.3

DOPAA 4.4 ± 0.6 8.4 ± 1.3 5.3 ± 0.9 4.0 ± 1.1 4.1 ± 1.2 2.2 ± 0.7

NA 142.1 ± 10.2 159.4 ± 19.1 138.0 ± 15.1 136.5 ± 13.7 101.4 ± 10.2 107.2 ± 9.6

MHPG 0.32 ± 0.03 0.57 ± 0.08 0.41 ± 0.09 0.29 ± 0.05 0.24 ± 0.06 0.23 ± 0.07

5�HT 62.3 ± 5.4 84.4 ± 8.3 64.2 ± 7.7 60.1 ± 6.5 61.3 ± 5.7 65.8 ± 6.3

5�HIAA 9.2 ± 2.6 17.5 ± 3.6 8.7 ± 2.5 8.4 ± 1.3 8.8 ± 1.8 12.4 ± 2.6

Optic tectum

DA 31.1 ± 3.0 28.2 ± 2.4 26.1 ± 1.9 29.3 ± 2.0 26.5 ± 3.2 26.1 ± 2.7

DOPAA 4.5 ± 0.8 4.2 ± 1.1 3.8 ± 1.2 3.6 ± 0.9 3.6 ± 1.1 3.4 ± 0.9

NA 87.2 ± 9.3 80.0 ± 9.1 76.0 ± 7.4 82.4 ± 8.1 79.2 ± 8.3 77.2 ± 7.5

MHPG 0.73 ± 0.13 0.62 ± 0.08 0.61 ± 0.10 0.71 ± 0.12 0.66 ± 0.11 0.63 ± 0.10

5�HT 47.5 ± 7.1 47.9 ± 6.8 45.5 ± 5.6 43.3 ± 6.1 39.1 ± 5.4 39.0 ± 4.8

5�HIAA 10.2 ± 1.7 9.4 ± 1.3 9.0 ± 1.4 9.4 ± 1.9 8.3 ± 1.2 8.2 ± 1.3

Brainstem

DA 45.7 ± 2.5 45.4 ± 3.7 34.1 ± 4.0 38.3 ± 3.2 40.1 ± 4.0 47.4 ± 5.1

DOPAA 0.52 ± 0.04 0.72 ± 0.06 0.32 ± 0.09 0.44 ± 0.06 0.48 ± 0.08 0.69 ± 0.11

NA 106.5 ± 7.4 110.2 ± 11.1 103.3 ± 9.4 82.3 ± 6.9 96.3 ± 8.2 99.2 ± 7.7

MHPG 0.75 ± 0.15 0.84 ± 0.13 0.68 ± 0.11 0.61 ± 0.09 0.67 ± 0.06 0.89 ± 0.12

5�HT 58.8 ± 7.1 56.6 ± 8.4 60.2 ± 7.7 57.4 ± 7.2 56.8 ± 8.1 62.6 ± 7.0

5�HIAA 7.3 ± 2.0 8.4 ± 1.6 10.4 ± 2.2 6.9 ± 1.4 6.9 ± 1.8 10.1 ± 2.2

Hypothalamus and hypophysis

DA 193.6 ±13.7 212.6 ± 14.3 204.3 ± 15.8 184.3 ± 13.4 171.1 ± 12.3 162.4 ± 11.3

DOPAA 10.8 ± 1.8 16.3 ± 2.4 16.0 ± 2.6 7.7 ± 2.1 12.6 ± 3.1 16.4 ± 2.7

NA 100.5 ± 10.5 108.8 ± 11.9 114.5 ± 9.9 82.5 ± 8.4 104.2 ± 10.0 71.5 ± 5.9

MHPG 1.4 ± 0.1 2.3 ± 0.2 2.9 ± 0.5 1.8 ± 0.7 3.4 ± 1.0 4.2 ± 1.2

5�HT 164.5 ± 13.4 153.3 ± 12.6 160.3 ± 12.9 177.6 ± 11.9 161.3 ± 10.7 152.4 ± 9.8

5�HIAA 19.3 ± 2.6 18.1 ± 3.1 20.2 ± 2.6 12.1 ± 1.9 17.4 ± 2.6 19.3 ± 2.4

Note: See Table 3.



Thus, the investigation demonstrated that, in theMzymta basin and in the Psakho River in August–September, the gonads in small males and females oftrout attained maturation at the age 1+. A high occur�rence of mature males and females of trout at this ageat the body length up to 17 cm indicates to the exist�ence of a dwarf form of the Black Sea trout in theMzymta basin.

Hormonal status. The concentration of hormonesand of their metabolites in regions of the brain was dif�ferent in the fish with gonads at different maturitystages (Table 6). In males with maturation of gonadsfrom maturity stage II to stage IV, the concentration ofinvestigated metabolites usually increased reflectingactivity of the corresponding hormonal systems. Atmaturity stage V, this activity decreased (Fig. 6). Infemales, any trend was not found in this process: theactivity of hormonal systems might increase, ordecrease, or differently change.

General trends in modification of the individualhormonal state at maturation of gonads were revealedin the course of analysis of the hormonal status of fish.In males with any of the investigated maturation stagesof gonads, this status was higher than in females(Fig. 7). In the fish of different sex, not only the levelof the hormonal status differed but also the form of itsrelation to the maturation stage of gonads. In males,the maximum was observed at stage IV and the mini�mum was observed at stage V. In females, the oppositerelationship was recorded. The maximum level of thehormonal status was in specimens with ovaries atmaturity stage V and the minimum level was observedat IV.

However, the hormonal status was different inmales and females and similar in the fish of the samesex with gonads at one stage of maturation (Fig. 8).The cluster of males was more compact than that oneof females. Minimum differences of this status were inmales with gonads at maturity stages II and V and infemales at stages IV and V.

Thus, the level of the hormonal status by monoam�ines in four regions of the brain was different in malesand females, being higher in males. The relationship ofthe status with maturity stages of gonads was nonlinearbut an opposite one: in males at stage IV, the hormonalstatus was the highest, in females, it was the lowest; atstage V, it decreased in males and increased in females.It should be noted that we investigated those hor�mones that, according to literature, were responsiblefor formation of phenotypic forms. Therefore, theirrelation to maturation of gonads seems to be indirect.

Comparison of Wild Fish and Farm Fish

Comparison of farm�raised and wild fish of thetrout form demonstrated that the body length of wildfish not only in August but also in September was sig�nificantly smaller (p < 0.05) than in farm�raised fish(Fig. 9). This is true both of males and of females and

5

II0

IV V

Fo

rebr

ain

15

20

25

Maturity stages of gonads

1

2

3

10

2

4

6

8

10

12

14

16

0

Bra

inst

em

Fig. 6. Modification of activity of dopaminergic system(DOPAA/DA) in the forebrain in (1) males and(2) females and in the brainstem in (3) females of the BlackSea trout Salmo trutta labrax from the investigated rivers.

Females0 Males

0.70.60.50.40.30.20.1

Hormonal status

II IV V

Fig. 7. Hormonal status in wild males and females of theBlack Sea trout Salmo trutta at different stages of gonadmaturity. Here and in Figs. 8, 10, 12: II–V—maturitystages of gonads.

30

V20

IV II IV V II

40

50

60

70

80

90

100

110Euclidean distance

Males Females

Fig. 8. The results of cluster analysis of wild females andmales of the Black Sea trout Salmo trutta labrax withgonads at different maturity stages (by the concentrationsof hormonal substances in regions of the brain).

×10–3×10–3

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PAVLOV et al.

reflects the differences in life conditions of fish, first ofall, probably, food availability.

The fish at the age 1+ significantly differed also bymaturity stages of gonads (Fig. 10). Among farmmales, 62.5% had testes at stages IV and V; among wildfish, there were 10% less of such specimens. Stillgreater differences were found between farm femalesand wild females. In all farm females, the gonads wereat stage II, while, among the fish caught in the river,32% of females were ready for maturation.

Comparison of the hormonal status in farm fishand river fish was made by concentrations of hormonalsubstances in regions of the brain in September. Thehighest of this status was in farm specimens of thekumzha form and the lowest was in wild trouts(Fig. 11). The farm specimens of the kumzha form dif�fered from all investigated resident groups of both farmfish and wild fish (Fig. 12). Obviously, this is related tothe beginning of smoltification which involves manyphysiological processes in the organism. The farm

trout differed both the farm kumzha and from wildfish. Thus, the process of parr–smolt transformationcaused greater changes in the activity of hormonal sys�tems than different life conditions in the river or at thefarm.

Thus, comparative analysis of farm fish and wildfish demonstrated that the farm fish differ in a highergrowth rate and their hormonal status was higher. Thefarm females attained maturity later than the wildfemales. Females of the dwarf form were not recordedat the farm; however, more mature males were present.The length of these males was 5–6 cm longer than thatof river males. Thus, the mature farm males of trout atthe age 1+ cannot be attributed indisputably to thedwarf form. Probably, these are male of the trout formin which the maturation time at the age 2+ is shiftedcloser to January. Under natural conditions, presenceof dwarf males of salmons indicated insufficiency ofresources for growth of all specimens of the new gen�eration.

18

16

14

12

10

8

6

4

2

0

Length, cm

FemalesMales

Fig. 9. The body length of wild and farm specimens of thetrout form of the Black Sea trout Salmo trutta labrax: —farm Trout in August, —Trout from rivers in August,and —Trout from rivers in September.

100

80

60

40

20

0Males Females

farmwild

Part of fish, %

IV–

V

III

I–II

Fig. 10. Maturity stages of gonads in wild and farm speci�mens of the Black Sea trout Salmo trutta labrax of the Troutform at the age 1+ in August.

0.1

Farm Kumzha0

Farm Trout Wild Trout

0.20.30.40.50.60.70.80.9Hormonal status

Fig. 11. Hormonal status in farm and wild specimens of theBlack Sea Trout Salmo trutta labrax in September.

120

K V IV II IV V II T

100

80

60

40

20

0

Euclidean distance, %

Wild females Wild males

Fig. 12. The results of cluster analysis of the investigatedgroups of farm and wild specimens of the Black Sea troutSalmo trutta labrax (by concentrations of monoamines inregions of the brain), K and T—farm Kumzha and Trout.

wild farm



CONCLUSIONS

Under conditions of artificial cultivation, juvenilesof the Black Sea trout differentiate into phenotypicforms characteristic of fish from natural populations:parr, trout phenotype, and kumzha phenotype. Someindividuals have traits of several forms (transitionalforms). They all differ in body length and weight. Inthe series parr—trout—kumzha, the length andweight of fish increase. Males of different phenotypesat the age 1+ differ in gonad development. At this age,most males of the trout form attain maturity. Maturefemales at the age 1+ are not found. Generally, thefarm stock retains the characteristics of genetic struc�ture of natural populations (Kholod et al., 2004).

In June, at the Adler fish farm, the process of dif�ferentiation of parr of the Black Sea trout into troutform and kumzha form which terminated in Augustwas observed. The growth rate of juveniles of thekumzha form increases towards autumn; their size andweight surpass the parameters of fish of other forms. Inthe process of parr–smolt transformation, the activityof hormonal systems becomes more intensive; in Sep�tember, in comparison with the fish of other forms, thespecimens of the kumzha form have a high level ofhormonal status (increased concentration of almost allinvestigated hormones). The minimum values of thelevel of this status are observed in fish of juvenile phe�notypic form (parr). From June to July, in the processof formation of phenotypic forms, the similarity of thehormonal status of parr and trouts increases.

Among fish caught in the river, only specimens ofthe trout form are found, with slight prevalence ofmales. Over half of males attain maturity at the age 1+and to the end of the third summer they have gonads atmaturity stages IV and V. Almost a third of femalesattain maturity at the age 1+. Towards autumn of thesecond year of life the part of females with gonads atmaturity stage IV reaches 50%. The body length offemales that attain maturity at the age 1+ varies within11.3–16.5 cm. Their size is significantly smaller thanthat of fish caught in the same season and in the samestretch of the Mzymta River almost 20 years ago(Murza and Khristoforov, 1988). These authors notedalso that mature females at the age 1+ were not presentin catches. Decrease in body size and accelerated mat�uration of trouts in the Mzymta basin indicates to thepresence of the dwarf form of the Black Sea trout inthe Mzymta River.

Possibility of formation of dwarf forms is present inthe genotype of many salmonids. Realization of thisadaptive norm depends much on environmental con�ditions. Presence of dwarf males and especially ofdwarf females in the Mzymta basin may be related todeterioration of environmental conditions for thepopulation of the Black Sea trout in rivers. The resultsof investigation of the initial farm stock may supplyprerequisites of early maturation of females at the age1+. Thus, in November 2000, Nikandrov and Shin�

davina (2007) found 14% of females of this age readyfor maturation.

The hormonal status of the investigated wild fishchanges in the process of gonad maturation. Thesechanges are different in males and females and in dif�ferent regions of the brain. Special traits of the hor�monal status depend more on sex than on maturationstages of gonads. Differences by the hormonal statusbetween the investigated groups of wild fish are smallerthan those between wild fish and farm fish. The wildspecimens are close to the farm fish of the tout form,i.e., to those which developed without smotification.The hormonal status of smoltificated specimens of thekumzha form significantly differs from that in speci�mens of the trout form both of farm fish and wild fish.

In construction of olympic objects started in theMzymta basin, anthropogenous impact drasticallyincreases. This would unavoidably influence the abun�dance of the Black Sea trout entered in the Red DataBook. The significance of the farm stock increases, asa source of restoration of its abundance. Closeness offarm trouts and wild trouts in the hormonal status con�firms a possibility of use of the farm stock for restora�tion of the population of the Black Sea trout in theMzymta River after the Olympics of 2014.

ACKNOWLEDGMENTS

We are grateful to K.V. Kuzishchin (MSU) andV.Yu. Ponomareva (Institute of Ecology and EvolutionRAS) for help in determination of the age of wild spec�imens of the Black Sea trout. The study is supported bythe Russian Foundation for Basic Research (08�04�00927�a) and by the Federal Agency for Science andInnovations within the scope of the Federal TargetProgram “Research and Scientific�Pedagogical Per�sonnel of Innovation Russia” for 2009–2013, Gos�contract 02.740.11.0280.

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Documents

Hormonal status in different phenotypic forms of Black Sea trout Salmo trutta labrax