Issn 0704-3716 Canadian Translation of Fisheries

ISSN 0704-3716

CANADIAN TRANSLATION OF FISHERIES AND AQUATIC SCIENCES

No. 4728

Comparative analysis of embryonal-larval development of the European salmons of genus Salmo

by D.A. Pavlov

Original Title: Sravnitel'nyi analiz embrional'no-lichinochnogo razvitiya evropeiskikh lososei roda Salmo

From: Zool. Zh. 58: 674-684, 1979

1 Translated by the Translation Bureau ( -111 ) Multilingual Services Division Department of the Secretary of State of Canada

Department of Fisheries and Oceans Pacific Biological Station Nanaimo, B.C.

1981

26 pages typescript DEPARTMENT OF THE SECRETARY OF STATE SECRÉTARIAT D'ÉTAT TRANSLATION BUREAU BUREAU DES TRADUCTIONS

MULTILINGUAL SERVICES DIVISION DES SERVICES CANADA DIVISION MULTILINGUES c7-Fe 5 z/ 7 TRANSLATED FROM - TRADUCTION DE INTO - EN Russian English AUTHOR - AUTEUR Pavlov, D.A.

TITLE IN ENGLISH - TITRE ANGLAIS Comparative analysis of embryonal-larval development of the European salmons of genus Sem0.

TITLE IN FOREIGN LANGUAGE (TRANSLITERATE FOREIGN CHARACTERS) TITRE EN LANGUE ÉTRANGÉRE (TRANSCRIRE EN CARACTÉRES ROMAINS)

Sravnitel'nyi analiz embrional'no-lichinochnogo razvitiya evropeiskikh lososei roda Semo. REFERENCE IN FOREIGN LANGUAGE (NAME OF BOOK OR PUBLICATION) IN FULL. TRANSLITERATE FOREIGN CHARACTERS. RÉFÉRENCE EN LANGUE ÉTRANGÉRE (NOM DU LIVRE OU PUBLICATION), AU COMPLET, TRANSCRIRE EN CARACTÉRES ROMAINS. Zoologicheskii zhurnal

REFERENCE IN ENGLISH - RÉFÉRENCE EN ANGLAIS

Zoological Journal

PUBLISHER - ÉDITEUR PAGE NUMBERS 114 ORIGINAL DATE OF PUBLICATION NUMÉROS DES PAGES DANS DATE DE PUBLICATION L'ORIGINAL 'Academy of Sciences of the USSR YEAR ISSUE NO. 674-684 VOLUME PLACE OF PUBLICATION ANNÉE NUMÉRO NUMBER OF TYPED PAGES LIEU DE PUBLICATION NOMBRE DE PAGES DACTYLOGRAPHIÉES Moscow, USSR 1979 58 5 26

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Bureau No.-1\1 0 du bureau Language — Langue Translator (Initials) — Traducteur (Initiales) Nej 714382 Russian PJH - 6 1981

Source: Zoologicheskii zhurnal (Zoological Journal), Vol. 58,

No. 5 (1979), pp. 674 - 684 (USSR)

Comparative Analysis of Embryonal-Larval Development of the European Salmons of Genus Sate°

D.A. Pavlov

Problem Laboratory for Studying the Fish Productivity of Water Ecosystems, Moscow State University

U.D.C. 597.553.2 SaZmo:591.33/343

Among the papers devoted to the development of salmonid

fishes, there are very few comparative embryological studies. 674*

At the same time, such studies can lead to a more precise under-

standing of the systematic position and evolution not only of

major taxonomic units but also of certain species and intraspe-

cies forms. We shall attempt to demonstrate this, using as an

example the Atlantic salmons of genus Scuemo, within which are

grouped the Atlantic salmon S. ,eak L., the sea trout S. tkutta

L., the Lake Sevan trout S. ..cichchan Kessler and several

*The figures in the right-hand margin indicate page numbers of the original (Tr.).

SEC 5-25T (Rev. 6/78) 2

Mediterranean and Adriatic species. On the basis of a number of characters the forms of the first species are isolated into the

"4eak" group, and the sea trout, the Lake Sevan trout and the

Mediterranean species similar to it - into the utitutte group

(Savvaitova et al., 1973).

Information on the development of the Atlantic salmon is to be found in many papers, although there are few special studies

(Battle, 1944; Evropeitseva, 1960). There are data on the embryogenesis of the Baltic sub-species (Vernidub and Yandovskaya,

1955). The development of the sea trout has not been studied in

detail. On the other hand, the development of the Lake Sevan

trout has been quite fully described (Leshchinskaya, 1953). In

the present article, a comparative study is made of the Caspian

salmon and the Atlantic salmon (Smirnov, 1955), and also of the

Ladoga salmon, the Sevan trouts and the rainbow trout (Ryzhkov,

1976).

We studied developing eggs obtained during the period 1975- 1978. We collected eggs of the sea trout S. trtutta m. Zactl3t ,Li, inhabiting the lakes on Velikii Island which is in Kandalaksha Inlet of the White Sea, and of the diadromous sea trout and Atlantic salmon of the Nil l ma River (in the same region). Eggs of Atlantic salmon were also obtained from the collection points of the Umba fish hatchery and the Kola River, and eggs of the Baltic salmon - from collection points on the Daugava River. Eggs of two races of the Sevan trout (gegarkuni and the summer race) were taken at the "Lichka" fish hatchery in the Mortuninsk district of the Armenian SSR. 1

1 Valuable help in the collection and delivery of eggs was given by co-workers in the Department of Ichthyology at Moscow University V.V. Zuevskii, M.A. Bek and A.V. Borisov, the director of the Umba fish hatchery V.N. Shilov, the Head of the Production Dept., of the United Fishing Industry of Armenia E.A. Tigranyan, and the director of the "Lichke" fish hatchery M.M. Asatyan. To all these individuals I am deeply grateful. 3

Eggs of not less than 3 females of each population were studied. The study of embryogenesis was made after the transfer 675 of eggs that had already begun to develop, at the White Sea biological station of Moscow University and in the Department of Ichthyology of the Faculty of Biology at Moscow University. The eggs of each form were divided into 2 - 4 series which were then incubated at various temperatures in a Kanid'ev and Grachev apparatus, in a specially manufactured device with closed water circulation, and in cuvettes in which the water was changed every day. In this way, an attempt was made to establish opti- mal conditions for each species. Development was studied in live subjects and entailed the use of a vertical chamber, which made it possible to examine the eggs from the side (Chernyaev, 1962). Numerical data were derived from measuring 20 eggs or 10 fry or larvae of each series. The diameter of the yolk was mea- sured as the half sum of the horizontal and vertical diameters of the membraneless egg being examined in the vertical chamber. For the size of the periviterine space, its width at the animal pole of the egg was taken. The relative size of the perivitelline space was defined as the ratio of its absolute size to the diameter of the yolk. The diameter of the blastodisc was mea- sured in the 128 blastomeres stage. The stages of hatching were portrayed according to the state of the embryos at the time of mass hatching.

In accordance with the theory of stage differentiation ela- borated by Vasnetsov (1953), we distinguish the following stages in the development to the fry period of salmons of genus SaZmo:

I - swelling of the eggs, appearance of the perivitelline space and the formation of the blastodisc; II - cleavage; III - blas-

tulation (from the beginning of flattening of the blastodisc to the occurrence of asymmetry in its structure); IV - gastrulation;

V - organogenesis (from the establishment of the optic vesicles);

VI - beginning of mobility of the embryo and of pulsation of the heart; VII - beginning of erythrocytic embryonic blood circulation; VIII - hepaticovitelline circulation and preparation for hatching (in this stage the yolk is supplied with blood only

from the vena hepatica viteLeinae); Ix - endogenous feeding of

the free-moving embryo; X - mixed feeding.

Fig. 1. Stages in the development of the Atlantic salmon: a - emergence of 5 somites in the body (epiboly 2/3 complete, pbs - periblastic sinus); b - completion of vascularisation of the yolk, substantial reduction of the right blood vessel in the yolk (direction of the blood flow indicated by arrows); c - hatching stage; d - beginning of transition to the mixed feeding stage.

Table 1. Indices of development of European salmons

j),. 1.3e-mmmanelm- 5- Ïe/- ;I:mum Him nepoNo;,,,, 4Hamerp na6yxweil nwrum moaoro 4. .aomm HPefflmmum • . Li ne..m cemeirm, rire.,,,,,, i,,,,,,, Ha ememainwe nur,ffi:e, 1.1,, c:li) nrien III:PHI, MN1 npocTpancraa, -! !_1O r.ut MM I • MM COI- 14 ,11170B d6: dw 3HaambciThagtiitx BHA, cDopma IF cc • Ii• (> . 7. 'W' 0111111:1 7‘ ti„, 17 weam,mon G. 9 13 cpe,- 13 C1111111101,1 110M ■ 11 Or: OP061 ■ •'""" cPe;+" 1:•1,aminhe 111; mu ai5e. OTII. A° a n°111 3 . :Ic'.1 "" "°•le6 HoeGaminrl cpe:m. "Wle6a""" ePeAH • "Yea i men.> xe Ci. y Q ll'• 53,6 22,3--27.0 25,0 15--18 11--1 Cemra 5.2--6,3 5,8 0,84 0,16 0,25 16--22 14,5--18,4 17,2 34--36 22--24 ( q. 27,7--29,0 28,1 15--16 12-1 B.,,,neKlifi 2ococ 5,3--6,7 6,4 0,96 0,16 0,25 17--26 16,0-17,0 16,5 33--37 21-25 57,5 a.c. 57,7 21,5-25,6 23,6 13-16 10-1 1Cym ,.Ea npoxoaHaa 4,5--5,5 5,1 0,45 0,12 0,25 15--20 13,0--15,7 13,8 34--36 21-23 22,0-24,0 23,0 13-15 9--1 l■yma-ca oaepaà l 4,6--5,7 5,4 0,73 0,14 0,28 17--22 13,3--15,5 14,4 33--35 21-94 56,7 23,5 12-14 12-1 FerapKyaa IL 4,5--6,3 5,2 0,75 0,19 0,26 28--29 13,0--15,0 14,0 30-33 90-24 54,0 23,0-24.0 ,0 21.0 14-15 12 :1enudi 6axTaK2.3 3,8--5,3 4,5 0,86 0,21 0,37 ( 4--16 18,0-19,0 18,5 31--33 20--23 53,8 20,0-2 2

• riPeil.M141111K8 11AIITOSI Ha crapun HbixoAa Ha o60Homal. 5

Numbered key: 1. Species, form. 2. Diameter of swollen egg, mm. 3. Size of perivitelline space, mm. 4. Number of segments during stage when the yolk plug is closed. 5. Length of fry*, mm. 6. Range. 7. Mean. 8. Number of segments of fry. 9. To anus. 10. Posteriorly to anus. 11. Overall average. 12. Length at transition to mixed feeding, mm. 13. Number of rays. 14. On dorsal fin. 15. On anal fin. 16. Absolute. 17. Relative. 18. Atlantic salmon. 19. Baltic salmon. 20. Diadromous sea trout. 21. Lake trout. 22. Gegarkuni. 23. Summer race. *The fry is in the stage of having just emerged from the membrane.

In the development of species belonging to the "tan." and 676

"tnutte groups, the following variations have been discovered:

1. In the Atlantic salmon and the Baltic salmon the diame-

ter of the swollen egg is from 5.2 to 6.7 mm (table 1) and is as much as 7.9 mm in the Ladoga salmon (Ryzhkov, 1976). In the spe-

cies of the second group it is smaller and ranges from 3.8 to 6.3 mm. It is on the surface area of the yolk and consequently, on

the size of the egg that the rate of vascularisation (the "overgrowing" of the yolk by the blood vessels) is in large measure dependent. For example, the transition to stage VIII of the egg of the Atlantic salmon takes place when the degree of vasculari-

sation is 4/5, while in the smaller egg of the lake trout it occurs when this is 5/6.

2. The membrane of the forms belonging to the first group

is lustreless, while in the species of the second group it is

quite hyaline.

3. Although the ratio between the diameters of the blasto-

disc and the yolk (d :d ) does not differ in the Atlantic salmon b y 6

and the Baltic salmon, it fluctuates widely in the forms of each of the species of the "tnutta" group (table 1).

4. In all species of genus Semo, during the gastrulation

stage a cavity forms between the periblast and the superimposed

layers of cells. In the course of epiboly of the blastoderm

this cavity is isolated from the embryonic thorax, having been

transformed into a petiblastic sinus. At the beginning of the

organogenesis stage, this organ, situated anteriorly to the fore-

part of the body of the embryo, consists of a single layer of

large integ umentary cells. The periblastic sinus occupies a

larger area and is less high in the forms of the "at.ail." group

than in those of the "t/Lutta" group (fig. 1, a; fig. 3, a). This

speciation disappears in the first group when the degree of epi-

bolY is 2/3 to 3/4, and in the majority of the forms of the

second group by the time that the yolk plug has closed (fig. 3, b).

5. In the yolks of all of the Atlantic salmons, in stage

VII there develops initially a blood vessel discharging into the

auricle from the left side and subsequently, a second vessel,

carrying blood to the heart from the right. Both vessels collect

blood from the vena 4LLbLv e -tncttLs vitetlinae and subsequently, 677

also from the vena hepatica vitatinae, whereas in stage VIII

they collect it only from the latter. In the first group the

thickness of the right vessel decreases rapidly (fig. 2, b); it

receives blood from a smaller surface area of yolk and disappears

when the degree of vascularisation is 3/4 to 4/5. In the sea 7

Fig. 2. Stages in the development of the Baltic salmon: a - yolk half vascularised (emergence of posterior cardinal veins,, beginning of pigmentation of the eyes; arc. md . - mandibular arch of aorta, arc. hy. - hyoid arch of aorta, arc. br . - branchial arch of aorta); b - yolk more than half vascularised (appreciable reduction of vessel supplying the yolk from the right); c - hatching stage; d - yolk sac 1/3 reabsorbed (establishment of rays on paired fins.

trout and the Lake Sevan trouts there is no variation in the thickness of the right blood vessel until vascularisation is almost complete (fig. 3, c) and it only disappears after termination of the "overgrowing" of the yolk by the blood vessels.

6. The "4cdet." group is distinguished from the remaining

Atlantic salmons by the presence of a rounded spot with diameter 8

of about 1.5 mm which is situated on the caudal region of the

embryo and is more intensely coloured than the yolk. This formation appears at the site of closure of the yolk plug and

disappears during the second half of stage VII.

7. In the salmons of genus Semo, with the commencement of

blood circulation, in the branchial region the first to appear

are the paired mandibular arches of the aorta (akeu mandibuZa-

niis aoktae). Next to form are the branchial vessels (akcu

bkanchiaLiJs ao)ttae) and the hyoid arches of the aorta (akcu3 hy-

oideum aoktae). In the Atlantic salmon and Baltic salmon the

blood begins flowing across the hyoid arches and through the two

branchial vessels in stage VII (fig. 2, a). In the species of

the "tkutta" group the flow of blood across the hyoid arches is manifested at the beginning of stage VII, when 3 to 4 branchial vessels are already functioning (fig. 3, d).

8. In the hatching stage, the number of segments in each

of the forms in the "a.eak" group averages 57.5 to 58.6; in the

"t/Lutta" group the average is 53.8 to 57.7.

9. Evidently because of the larger size of the egg, in the

")seak" group the length of the freely moving embryos and larvae 678

in identical stages of development exceeds this index for the

"tkutta" group, and its mean values at the beginning of the mixed

feeding stage are 25.0 - 28.1 and 21.0 - 23.6 mm respectively.

10. During the reabsorption process the yolk sac in the forms of the first group is much elongated in the posterior part

(fig. 2, d); in the species of the second group this elongation

is not observed (fig. 3, e). 9

Fig. 3. Stages in the development of the lake trout (a, c, f) and diadromous trout (b, d, e): a - beginning of organogenesis (epiboly 1/3 complete); b - 14 segments (completion of epiboly, y.p. - yolk plug); c - completion of vascularisation of yolk; d - termination of vascularisation of the yolk (formation of first melanophores on the head and of hatching glands; emergence of erithrocytes in the hyoid arch of the aorta); e - reabsorption of yolk sac about 1/3 complete (establishment of rays on the pectoral fins); f - beginning of transition to the mixed feeding stage.

11. In the Atlantic salmon and the Baltic salmon the pre- anal fold disappears at the beginning of mixed feeding (fig. 1, d). In the sea trout and the Lake Sevan trout a vestige of this organ is preserved in this stage (fig. 3, f; fig. 4, e) and is ultimately reduced by the time that the transition to fully exo- genous feeding occurs. 10

12. In the larvae of the ")secte group the pigmented spots on the body are for the most part displaced downward in relation to the horizontal myoseptum (fig. 1, d). In the species of the

!Itnutta" group the myoseptum extends in the middle of the pigmented spots (fig. 3, f). This difference was also cited by

Smirnov (1955), in comparing the development of the Caspian salmon and the Atlantic salmon.

13. In the larvae of the first group the notch in the blade of the tail forms earlier than in the species of the second. In the mixed feeding stage and during the same stages of development it is larger (fig. 1, d; fig. 3, f; fig. 4, e).

14. As Mednikov showed (1977), the temperature dependence of the duration of development within the membrane can be ex- pressed by the equation lgN = lg A + kt, where N is the incubation period in days, A is a coefficient, numerically equal to the duration of development within the membrane at zero temperature, which is biologically meaningless in the case of the Salmonidae, k is the coefficient of thermolability, and t is the temperature.

Parameters of such equations, calculated by the method of least

Squares, are adduced for various species in table 2, constructed by the use of Ryzhkov's data (1976). From the graphs of these equations only an approximate judgment is possible with respect to the relationship between the rate of development of the various forms. This is because they hatch in different stages and the number of points (1) of the empirical lines of the regressions 1 1

1 me U Cl. (q_

Fig. 4. Stages of development of the Lake Sevan trout (a - e: summer race; f - g: gegarkuni): a - 14 segments (closing of the yolk plug, pb.s - periblastic sinus); b - 22 segments (beginning of formation of the eye cups, am - amnion); c - 30 segments (formation of cardiac tubule); d, g - hatching stage; e - larva in the mixed feeding stage; f - 42 segments (establishment of pectoral fins, beginning of contraction of cardiac tubule.

is small. In the Baltic, Ladoga and Atlantic salmons the spread of the points of the common regression line is very small, with the result that the error of the theoretical values of the 12

function (ty) is minimal. By reference to the coefficient of

thermolability the nut.tan" group is confidently distinguished

from the "tnuttan group. According to Mednikov's hypothesis

(1977), the highest thermolability is typical of groups with a marine origin. Ryzhkov (1976) considers that the high thermolability of S. .sean is associated with substantial temperature

fluctuations during the course of development of its egg. It can bè assumed that the most anadromous species, among which is S.

«cian, have a high thermolability.

Table 2. Parameters of the equations of the duration of development within the membrane of various species of European salmons.

BEA, cbopma A My

S. salar 13 260,0 --0,087 0,007 S. India 6 173,8 --0,060 0,023 rerapKynn 5 146,0 --0,053 0,049

MCTHal 6aXTaK 6 139,3 --0,050 0,058 S. ischchan 3 anunla 6axTaK 1.4 4 160,9 —0,056 0,041

Key: 1. Species, form. 2. Gegarkuni. 3. Summer race. 4. Winter race.

15. With respect to almost all of the indices, S. c cLJt is less variable than each of the species of the "tnutta" group

(table 1).

In the development of the Atlantic salmon and of the Baltic sub-species of S. 4aZan a strong resemblance is observed, although there are also the following differences. 13.

1. The swollen egg of the Baltic salmon is from 5.3 to 6.7

mm in diameter, which is, on the average, 0.6 mm larger than is

the case with the Atlantic salmon.

2. The yolk and the fat drops of the Baltic salmon are almost indistinguishable from the standpoint of the intensity of

coloration. They are either light yellow or yellow. The yolk

of the Atlantic salmon is light orange and the fat drops are

bright orange.

3. In the majority of the embryos of the Baltic salmon the

right blood vessel in the yolk becomes much narrower even at the

beginning of vascularisation (fig. 2, b) and disappears when the

degree of vascularisation is 3/4. In the smaller part of the

egg the right vessel is preserved almost until completion of vas-

cularisation of the yolk, at the same time remaining much narro-

wer than the left vessel. On the whole, the right vessel of the

yolk undergoes a greater degree of reduction than is the case

with the Atlantic salmon when they are in similar stages of

development.

4. Identical stages of development ensue in the Atlantic

salmon at a greater degree of vascularisation than is the case

with the Baltic salmon, which we attribute to the larger surface

area of the yolk in the second form. In the Atlantic salmon the

transition to stage VIII begins when vascularisation of the yolk

is 4/5 complete, and in the Baltic salmon when it is 3/4 complete.

5. In the Baltic salmon, hatching occurs at an earlier

stage of development than in the Atlantic salmon (fig. 1, c; 14 fig. 2, c). At this time the 16-17 mm long embryo has a larger yolk sac than does the Atlantic salmon, the operculum covers 2 branchial arches, the gill filaments are established on the branchial arches, the pelvic fin reaches half of the pre-anal fold, and numerous melanophores are situated on the head and dorsum of the embryo. The branchial-maxillary apparatus accom- plishes occasional movements. The pre-larvae are motionless and usually do not begin to move if they are disturbed.

In the hatching stage of the embryo of the Atlantic salmon the operculum covers three branchial arches, the fin fold is differentiated to a greater degree than in the Baltic salmon, rudiments of rays are visible in the tail blade, the pelvic fins reach the margin of the pre-anal fold, on the branchial arches there are fairly long gill filaments, melanophores cover not only the dorsal part of the body but also its flanks, as well as the upper part of the yolk sac. Respiratory activity is more pronounced than in the Baltic salmon. If the pre-larvae are disturbed they will continue to move for quite some time.

6. Because it hatches at an earlier stage, the larva of 681 the Baltic salmon at this time is on the average 0.7 mm shorter than the Atlantic salmon. At identical stages of development the juvenile of the Baltic salmon is larger, which is dictated by the larger size of its egg. Thus, during the transition to mixed feeding the length of the Atlantic salmon averages 25.0 mm, and of the Baltic salmon - 28.1 mm. 15

7. The unpaired fins in the larvae of the Baltic salmon are hyaline, whereas in the Atlantic salmon they are a light rose-coloured.

8. The rate of development of the Baltic salmon is somewhat slower than that of the Atlantic salmon since, notwithstanding the fact that the first form hatches at an earlier stage of development, its incubation period, as is also the case with the

Atlantic salmon, lasts for 91 days at 5.3 ° - 5.4 ° .

In the development of the Atlantic salmon in the populations of the rivers Umba, Nil t ma and Kola, only small differences are manifested in the diameter of the egg, the size of the larvae and the number of segments and rays on the fins.

The Sevan trout is distinguished from the sea trout by the following embryological characters:

1. The egg of the Sevan trout is light yellow or yellow, that is, it is paler than the egg of the sea trout, the intensity of whose colouring is almost identical to that of the Atlantic salmon.

2. In the egg of the Sevan trout the relative size of the perivitelline space is 0.19 - 0.21 mm. On the average, this is

0.07 mm larger than in the sea trout.

3. With respect to the ratio between the diameters of the blastodisc and yolk and the number of segments in the stage of closing of the yolk plug the forms of the sea trout are less variable than the races of the Sevan trout (table 1). 16

4. During the stage of termination of vascularisation the eyes of the Sevan trout are pigmented to a much lesser degree than those of the sea trout.

5. The average number of segments in the body, amounting to 53.8 - 54.0 in the pre-larvae of the Sevan trout, is approximately 3.3 less than in those of the sea trout, on account of the decrease in the number of pre-anal segments. The difference in the number of vertebrae as between these species is preserved in the adult forms and amounts to 51-59 and 66-60 respectively

(Vladimirov, 1940; Balon, 1968).

6. The number of rays on the anal fins in the larvae of the Sevan trout is 12-13, whereas in the sea trout it is 9-12.

Apparently, in the course of early ontogenesis in the Sevan trout there is a reduction of part of the established rays, since an inverse relation is observed among the adult forms, namely: 8-9 in the Sevan trout (Vladimirov, 1940) and 9-11 in the sea trout (Rounsefell, 1962).

7. During the mixed feeding stage the length of the larvae of the Sevan trout is 21-22.5 mm in the gegarkuni and summer race, and, according to Ryzhkov's data (1976), 16.9 - 17.2 mm in the winter race, that is, smaller on the whole than in the sea trout, the size of whose larvae ranges from 21.5 to 25.6 mm.

8. The larvae of the sea trout of all of the Atlantic salmons are most intensively pigmented (fig. 3, f). Their fins are more brightly coloured than those of the other species. The margin of the adipose fin is a vivid orange, while the margins 17

of the dorsal and anal fins are rose-coloured. The body and

fins of the Sevan trout are much more faintly coloured, while

the abdomen has a silvery hue (fig. 4, e).

9. The coefficient of thermolability is higher in the sea

trout than in the Sevan trouts, which tends to bring it closer

to the Atlantic salmon (table 2).

In the diadromous sea trout, as distinct from the lake form,

. on the average the diameter of the egg is 0.3 mm smaller and the

relative width of the perivitelline space is 0.02 mm smaller.

The magnitude of these indices, like the ratio between the dia-

meters of the blastodisc and the yolk in the egg and the number

of segments during the stage of closing of the yolk plug is

somewhat larger in the freshwater form as compared with the dia-

dromous (table 1). These forms also differ in the number of

rays on the anal fin: in the freshwater sea trout there are on

the average 1-2 fewer of them. The remaining differences in the 682

development of both forms of sea trout are negligible and are

associated with the different size of their egg.

Of the Sevan trouts the gegarkuni has the largest size of

egg, and in it the closing of the yolk plug occurs where there

is a larger number of segments as compared to the other species

and forms (table 1). The embryos of this race hatch in the same

stage of development as do those of the sea trout (fig. 4, g).

Here, the operculum covers 3 branchial arches, the rudiment of

the pelvic fin reaches half of the pre-anal fold, the fin fold 18 begins to be differentiated into unpaired fins, rays have not yet become established on the tail blade, melanophores are pre-

sent on only the dorsal part of the body, and the respiratory movements of the branchial-maxillary apparatus are feeble.

The eggs of the summer race are more faintly coloured than in the remaining races. This form differs markedly not only from the gegarkuni but also from the other Atlantic salmons in the comparatively large amount of vitelline plasma and in the peculiarities of development of the periblastic sinus. In the majority of representatives of genus Semo this organ is situated anteriorly to the head of the embryo and disappears prior to completion of epiboly of the blastoderm. In the summer race, by

the time that epiboly is completed the periblastic sinus is displaced towards the bsoundary of the zone of overgrowing, being situated to the right of the embryo or less frequently, either to the left of it or at the level of the caudal region (fig. 4, a). In all of the Atlantic salmons, the periblastic sinus, which has disappeared after the closing of the yolk plug, comes to be replaced by another temporary organ - the amnion. This latter organ is formed by the periderm that has exfoliated from the yolk and lies beneath the embryo and along both of its flanks.

This development can be regarded as an increased pericardial cavity, the dimensions of which become much smaller prior to hatching of the embryo (Pavlov, 1978). In the summer race the periblastic sinus is preserved after the manifesting of the amnion (fig. 4, b) and subsequently, being built from cells of the 19 integumentary layer, it becomes incorporated into it (fig. 4, c).

Her'e, the height of the amnion on one side of the embryo becomes greater than in the other forms such as the gegarkuni for ex'ample (fig. 4, f). Faint contractions of the cardiac tubule begin in the summer race when there are 37 - 39 segments of the body, and in the gegarkuni, as also in the other salmons, when there are 42 - 43 segments (fig. 4, f). The embryos of the summer race hatch at a relatively later stage of development when the length is 18 - 19 mm (fig. 4, d). At this time the yolk sac is considerably reabsorbed, the operculum covers 3 - 4 branchial arches, the pelvic fin almost reaches the edge of the pre-anal fold, rudiments of rays are visible on the tail blade, and melanophores are scattered on the head, dorsum and in part, on the flanks of the body. In the prelarvae vigorous movements of the branchial-maxillary apparatus are observed and they possess a higher degree of mobility. It is approximately in this stage of development that the embryos of the winter race hatch (Leshchinskaya,

1953).

A number of authors consider that the sea trout is the most generalised species in genus Scamo and the species that is closest to the ancestral form. In a number of indices the Atlantic salmon closely resembles the sea trout and probably originated from a common ancestor in the Pleistocene (Balon, 1968; Dorofeeva,

1975 et al.). In connection with this hypothesis the direction of evolution of the early ontogenesis in genus Sa.emo can be 20 envisaged in the following form: an increase in the diameter of the egg, a decrease in the dimensions and earlier disappearance of the periblastic sinus, reduction of the right- and more powerful development of the left blood vessel in the yolk, which corresponds to the principle of oligomerisation of homologous organs, a slowing of the rate of development and an increase in thermolability, a decrease in the range of the variability.

It is possible that the North Atlantic ancestors of the

Atlantic salmon underwent differentiation between Greenland and

America and subsequently spread towards the littoral of Europe where an ancestral form of the sea trout already lived (Balon,

1968), after which the populations of the European and American

Atlantic salmons became isolated. About 10 thousand years ago, as a result of the late glacial transgression and the retreat of the glacier, oceanic waters penetrated the Baltic Basin and the salt water Ioldiev Sea was formed, into which may have penetrated the form that gave the Baltic salmon its origin. This form entered the basin of the White Sea in consequence of its junc- tion with the Baltic basin where, as a result of a subsequent lowering of the water levels of the lakes and rivers a number of populations became isolated, after giving the lake form its origin (Behnke, 1972). The proto-Baltic genesis of the Ladoga salmon is confirmed by the similarity in the diameter of its egg with that of the Baltic sub-species.

The Baltic salmon and perhaps also the lake forms from the basin of the White Sea which closely resemble it are, in our 21 view, the most specialised in the "salar" group. With their divergence from the Atlantic salmon there was an increase in the diameter of the egg and the reduction of the right blood vessel in the yolk became even more pronounced. Under natural conditions the water temperature during development of the Atlantic salmon does not exceed 5; whereas during the development of the 0 Baltic salmon it reaches 7 (Evtyukhova, 1971; Kostylev, 1972 et al.). Because of the somewhat higher temperature in the course of embryogenesis and the larger size of the egg, and consequently, the smaller respiratory surface per unit volume of the embryo of the Baltic salmon, they probably experience less favourable oxy- gen conditions as compared to the Atlantic salmon. This may be the explanation for the earlier hatching of the embryos of the

Baltic sub-species, which provides for an improvement of the gas exchange between them and the environment.

With regard to the origin of the Sevan trout there exist two fundamental points of view: (1) divergence from the Kura salmon and (2) evolution from brook trouts. In the opinion of

Dorofeeva (1967), the second hypothesis is the more plausible, since the Caspian salmon is a highly deviant form. At the same time it is evident that the brook trouts are not direct descen- dents of the freshwater Eocene Thaumaturidae, but derivatives of diadromous forms and that they originated from an ancestor of the sea trout which had spread from the Mediterranean Sea into

European territory (Dorofeeva, 1967, 1968, 1975; Balon, 1968 et al.). With the transition to a lacustrine life the relative size -)

I of the perivitelline space in the egg increased, the number of

, vertebrae decreased and the colouration of the larvae became

lighter. The latter characteristic is possibly due to the fact

that, between two and three months after hatching the juvenile

begins to adopt a pelagic mode of life (Dadik'yan, 1962). In a

number of morphological characters, during the early periods of

development the gegarkuni preserved a large number of common

features with the sea trout and is evidently the closest to the

latter. In comparison with the other Atlantic salmons the sum-

mer race is capable of withstanding a higher temperature,

attaining in the opinion of Leshchinskaya (1953), 20 0 . It is

probable that this reproductive characteristic caused substantial

deviations in the course of the development of this race from

the original form. The hatching of the summer and winter races

in a late stage of development may be on account of the fact

that, due to the smallness of the egg, at the time when they are

developing within the membrane the embryos of these races enjoy

more favourable conditions of respiration than do the embryos of

the gegarkuni. 23

References

1. Vasnetsov, V.V. 1953. Stages in the development of bony fishes. Collection: "Essays on common problems in ichthyology," pp. 207-217. Iz-dvo AN SSSR, Moscow and Leningrad.

• Vernidub, M.F. and Yandovskaya, N.N. 1955. Instructions relating to the maintenance of brood stock, collection, fertilisation and incubation of eggs, and the maintenance and rearing of salmon larvae under the conditions obtaining in the northwestern part of the USSR: 1-48, Pishchepromizdat (Publishing house of the food industry), Moscow.

3. Vladimirov, V.I. 1940. A contribution to the study of the juvenile biology and reproduction of the Sevan trout (Scuemo i4chchan gegakkuni Kessl. biotypus a. Fort). Transactions of the Sevan hydrobiological station, 6:87-118.

4. Dadikyan, M.G. 1962. Information on the biology of juvenile Sevan trouts during the lacustrine period. Idem., 16:97-113.

5. Dorofeeva, E.A. 1967. Comparative morphological principles of the systematics of the eastern European salmons. Voprosy ikhtiologii, 7, 1(42):3-17,- 1968. Variability of some systematic characters in the evolution of the Sevan trouts (Samo i3hchchan Kessler). Vopr. ikhtiol. 8, 1(48):45-53 - 1975. Systematic relationships between the salmons of genus Scuemo. Zool. zh. 54, 4:583-589.

6. Evropeitseva, N.V. 1960. Stages in the individual development of juveniles of the Atlantic salmon. Vestnik Leningr. universiteta, ser. biol. 15, 3:83-95.

7. Evtyukhova, B.K. 1971. The Baltic salmon. Industrial- biological description: 1-46, Riga.

8. Kostylev, Yu. V. 1972. A biological description of the Atlantic salmon of the River Kem'. Collection "The , Salmonidae of Karelia," 1:25-29, Petrozavodsk.

9. Leshchinskaya, A.S. 1953. Embryonic development of the summer race of Lake Sevan. Trans. of the Sevan hydrobiological station, 13:227-237.

10. Mednikov, B.M. 1977. Temperature as a factor in development. Collection "The environment and the developing organism": 7-52, Izd-vo "Nauka", Moscow.

11. Pavlov, D.A. 1978. Development of the diadromous Kamchatka mikizha Sate() myki)m Walbaum and its position in the system of Atlantic salmons. Vopr. ikhtiol., 18, 6(113):1040-1054. 24

12. Ryzhkov, L.P. 1976. Morphophysiological mechanisms and the transformation of matter and energy in the early ontogenesis of freshwater salmonid fishes: 1-288, Petrozavodsk.

13. Savvaitova, K.A., Maksimov, V.A., Mina, M.V., Novikov, G.G., Kokhmenko, A.V., and Matsuk, V.E. 1973. The Kamchatka salmons: 1-118, Voronezh.

14. Smirnov, A.I. 1955. On the generic relationships between the Caspian salmon SClim0 t,Latta ca4paU Kessler and the salmon or Atlantic salmon S. c/...t.cut. L. Vestnik Mosk. un-ta, ser. fiz-mat i estest. nauk, 10, 10:131-134.

15. Chernyaev, Zh. A. 1962. A vertical chamber for observing the development of the eggs of salmonid fishes. Vopr. ikhtiol. 2, 3:558-560. References

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BaC1 10110B B. 13., 1953. 3Tanyt prim-m.11ln KouritcTi.ix pb16. C6. «OgepKii no o6mum Doupocam 11NTI 10:10r1 1 1 1»: 207-217, 143:k- 13o All CCCP, M.- JI. Bepiticty6 (1). ii 5Ina,oacKan H. H., 1955. IIncTpyKum-r no nbiRepauinainno c6opy, onmaontopeinno ii unKy6atuni iiipii, nuaepwitrianitio H no.apatunnanitio alumna]: aococn o ye.,10B1 1 SIX cenepo-aana,ation macTit CCCP: 1-48, fliimenpoNtita- aa .r, M.

Boaatimiipon B. H., 1940. 1K linguini° 6no.riortin :%10,J10,11 I H paaNnion:einin diope.lit-rerap- Kylin (Salmo gegarkuni Kessl. biotypus a. Fort). Tp. CenaticK. 1'111130CH 10.1. CT., 6: 87-118. ,r1a,rulKnii M. F., 1962. MaTepilambi no 6no.gormi Nio.m.zut cenaucKnx (pope.aeil 13 o3eptibi9 neplions. Tp. Celia 1ICK. rita.po6lion. CT., 16: 97-113. Ropockena E. A., 1967. CpaniniTeablio-mopclio.aornmecNne OC1 1013 131 clicTemaTium nocTottno- esponacKnx mococeii. Bonp. 1 1XT1 100., 7, 1(42): 3-17.- 1968. Hameittninocr, iteKo- TOpbtX clicTemaTitgecKnx riptianaKon 13 313031 1011 1 1 1 1 cenaticKnx (Sa/mo isrfichatz Kessler). Bonp. IIXT1 1031., 8, 1(48): 45-53.- 1975. CIICTONIaTimecmie ornometinit in- cocet po,aa Salmo. 3oo.g. )K., 54, 4: 583-589. Enponeiliteria H. B., 1960. 06 3TaM1X 11 1 1,1,1 1BI 1.1yailbH01 - 0 pa3Bl 1T1 1 31 mo.ao,iii tumatinittecKo- ro 11000CH. BeCTH. neinnirp. yn-Ta: cep. 6110J1., 15, 3: 83-95. EBTIOX0133 B. K., 1971. BurrniicKnii .gococn. flpombic..iono-Ono.aoriniecKan xapaKTeptteitiKa: 1-46, Pura. KOCTb1J1e13 10. B., 1972. BitonorintecKan xapaiereplicTitKa cutrit peRil Kemn. C6. «.1000CC- Bble (Salrnoniclac) Kape.unD>, /: 25-29, fIeTpoaanoacK. JleimiticKan A. C., 1953. 3m6pliona.abitoe paantrrne .aertiero 6axTaKa oaepa Cunt!. Tp CenancK. nuispo6ito.g., CT., 13: 227-237. Me,amiKon B. M., 1977. TemnepaTypa KaK cpaKTop pa:nit -run. C6. «Bnemumn cpe.-la it pa t- Entafflountrien oprainiam»: 7-62, 1 ,13,a-rio «HayKa», M. .11anzion A., 1978. Pa3B1ITIle npoxo,ana KamgaTcKoii iiiiiiiii Salina milkiss Walbatun hi ee no.noweime n clicTeme 6,aaropoatib1x .nococcii. Bonp. iixTito.a., 18, 6 (113 ): 1010- 1054. PbI)1:1:013 JI. 1-1., 1976. Moixkodmailonoriltieciote 331:01 10MeiMIOCTII 1h Tpaitupopmatinsi BellIe- CTBil II 911eprini hi pannem 011TOre0e3e 1.1pCCI 10130,11 MIX TIOCOCCB13IX pie): 1-288, FleTpo- saB0.3,C1C Caimairroaa K. A., M;1 KCIIN1011 13. A., Minia M. B., HonitNou F. F., KonictiNo A II.. it M•i- tiyK B. E., 1973. KamgaTcmie 6.1aropo,a111 ,1c aocoell: 1-118 , BoPoucw• Cmliption A. H., 1955. 0 pOACTIICIIHIAX oTtioweintsix KacrniiicKoro aococn Sei m.) ra..z.- pictiS Kessler it J1OCOCH 1 131 1 1 COMI'll S. sa ler I.. BOCT1 1. MOCK. yn-Ta, cep. t. \tat. It ecTecTit. intyK, 10,10: 131--134. qe111 MOH W. A., 1962. BerritKambrian Kamepa ,a.",151 10.:Iel 1 1 SI aa paanturnem Hubi nococe- 1311.:MbIX p1,16. Bonp. IIXT1 10:1., 2, 3: 558-560. Balon E. K.. 1968. Notes on origin and evolution of trouts and salmons with special reference to the Danubian trouts. Vest. Ces1:. Spol. Zool.. 32,1: 1--21. Battle 1-1. j.. 1941. The embryology of the Atlantic Salmon (Salmo salar nad, .1. Res., sect. D., 22: 105-125. - Behnke R. J., 1972. The systematics of salmonid fishes of recently glacis ted lake ,• .1. Fish. Res. Board. Canada, 29, 6: 639-671. Rounsefell G. A., 1962. Relationships among North Aniertcan Salmonidae. Fish. Bull Fis! and Wildlife, ser. V, 62: 235-270. 26

COMPARATIVE ANALYSIS OF EMBRYONAL-LARVAL DEVELOPMENT OF THE EUROPEAN SALAIONS OF THE GENUS SA LM

D. A. PAVLOV

Problem Laboratory for Studying Fish Productivity of Water Ecosystems, Stale t'ni: ,crsit,i of Moscozv

s u ni ni a r y

The Atlantic salmon forms differ distinctly by their embryonal-larval development from the sea trout and Sevan trout. These differences speak favourably for the isolation of the former in the group «solar» and of the latter in the group «India», In th y c o ur se of the Atlantic salmon and sea trout, in the former the egg diameter in- of divergence creased, the larval organs (periblastic sinus and right blood vessel on yolk) attained sanie degree of reduction, the development rate slowed down and the thermolability increased. In the group «solar» the Baltic salmon is Hie most specialized. In the cours,' of evolution of the Sevan trout which had talœn its origin from the sea trout, the relative size of perivitelline space in the egg increased, the colour of eggs and larvae became lighter, the number of vertebrae decreased. Among the Sevan trout forais the «gegarlmiii» is closer to the sea trout, whereas its summer race is characterized by some peculiarities due to differences in the ecology of reproduction.