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2.

The Redfish; Gametogenesis and Migrations of the Sebastes marinus (L.)

and Sebastes m entella TravinBy

V. P. SOROKIN PINRO, M urm ansk, U.S.S.R.

T he redfish Sebastes marinus (L.) and Sebastes mentella Travin, are of great importance to the trawl fishery by their abundance and the size of concentra­tions they form. It is therefore easy to understand why so great and so fully justified an interest in the behavi­our of this fish has developed.

W ithin recent years a significant part of the life history of the redfish, inhabiting the Barents Sea and the Norwegian Sea, has been the subject of study. Age and rate of growth have been studied by N. P. Sma- ragdova (1936), V. V. Veshchezerov (1941), A. Kott- haus (1952), and E. I. Surkova (1957). Its distribution and its fisheries have been investigated by V. V. Vesh­chezerov (1941), N. A. Maslov (1944), V. I. Travin (1949, 1951, and 1957), and A. S. Baranenkova ( 1957). G. V. Boldovski ( 1944) reported on the redfish feeding behaviour.

V. F. Schmitt (1944) studied the development of the ovaries, embryonic development of the eggs, and the larval distribution after “spawning” . Similar studies have been carried out by K. H. Lüling (1951), who did not seem to know about the work of Russian inve­stigators (Schmitt and others), concerned with the life history of the redfish, as is seen from this quotation from the introduction to his paper: “We may say that we know almost nothing about the reproductive biology of the redfish Sebastes marinus.” Dr. J. Magnüsson (1955) and Sorokin (1956) m ade histological game- togenesis studies independently of each other.

T he present paper is not aimed at a critical analysis of all the data on the biology of the redfish. However, it was thought useful to try to assess how far the migra­tions of redfish in the Barents and Norwegian Seas are inter-related with the processes going on in the gonads.

T he distribution and migration areas of S. marinus, as described by N. A. Maslov ( 1944), still remain valid (see Fig. 1). Recent investigations have only completed and defined this general scheme.

In the Barents and Norwegian Seas, to the east of

Figure 1. Diagram of S.marinus (L.) migrations according to N. A. Maslov.

1 = “spawning” areas2 = areas of autum n/w inter concentrations of males and

females3 = areas of spring concentrations of males4 = migrations of females5 = migrations of males

the continental slope, S. marinus females liberate their larvae in the Lofoten Islands area and along the slope further north, as far as approximately 71°N. Liberation of larvae starts in the second half of April. I t is a t its height in May and comes to an end in the first half of June.

The spent S. marinus females m igrate to the feeding grounds. At least three such areas are known: the eastern Barents Sea as far as Goose Bank (Travin reports S. marinus being caught incidentally a t 73°N, 50°E) ; the Demidov Bank (Norwegian fishermen call

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it “T hor Iversen Banken” ) and adjacent northern and eastern areas; the third area includes the slopes of the Bear Island Bank and the continental slope of West Spitsbergen. S. marinus is sometimes found north-east of Hope Island (78°N ; Travin, 1949).

After liberation of the larvae, the ovaries become reduced in size and weight (m aturity factor — 0-2-1-1 % ),* and become flabby; the membrane is shrunken. C ut sections show connective tissues of the follicular membranes to be partly degenerate. Sometimes unfer­tilized eggs in the process of resorption occur in the ovaries. The stroma of such an ovary contains sex cells of several generations, beginning with oogonia and including oocytes with a follicle of one or two layers. In June certain females have oocytes in the ovaries, with yolk accumulating in the plasma. Yolk deposition in the oocytes of older generations is not simultaneous, i.e. the vitellogenesis is of an asynchronous nature.

Vitellogenesis does not appear to be very active during June, July, and August, and the m.f. does not show a significant rise (1-2 % on average) ; by August it increases to 1-8 % . T he diameter of the older genera­tions of oocytes varies from 200 to 300 ju during this period.

The shoals of males and females, formerly separated, unite during these three months of the feeding m igra­tion, and S. marinus disperses on the feeding grounds m entioned above.

C ut sections of ovaries suggest that in September vitellogenesis becomes more active; the yolk granules increase in size (12-19 ju), as also does the ovary-mass. M.f. averages 2-3 % and in some cases even reaches 2-6 %. During Novem ber/D ecem ber S. marinus leaves the feeding grounds, this being concurrent with and probably due to the beginning of w inter cooling of the water.

Yolk accumulation is completed in January-Febru- ary, sometimes in M arch. The oocyte is filled with large yolk granules; the nucleus loses its round form and becomes amoebiform; the nucleoli disappear and zona radiata begin to form. Diam eter of such (living) oocytes varies from 900 to 1100 u. T he follicular mem­brane is stretched and epithelial cells are stretched out and flattened. T he ovaries increase more in size and become heavier; the membrane stretches and becomes thin and transparent, so tha t oocytes can easily be seen through it. M.f. increases to 4 -6 % , whilst some females have been found to possess a m.f. of 10-2 % ; such fish occur from M urm an Bank to Finnm ark Bank; in the Norwegian Deep; in the Demidov Bank and Bear Island Bank areas.

L ater on, when the albumen components of the oocyte have taken up water, homogenization begins

* The gonad weight, relative to the total weight of the fish, expressed in % is called the “m aturity factor” or briefly m.f.

and the oocyte becomes transparent. Meiosis takes place, followed by ovulation and fertilization (gametic syngamy). The diameter of the oocyte in the ripe condi­tion attains 1500 ju. T he ovaries are of a greenish-gray colour. T he eggs lie free in the ovary-cavity and, if the belly of the female is lightly pressed, are discharged from the oviducts. T he ovaries grow larger still and occupy more than half of the body cavity. M.f. averages 7 % , some specimens attaining a m.f. of 12 %.

Females bearing ripe (and fertilized) eggs are found in February and M arch on the Finnm ark Bank and westwards, in the Kopytov area, and in the Western Deep. Females with eggs already fertilized are rarely found east of the Kola meridian or on the slopes of the Bear Island Bank. The author, at least, has never had an occasion to observe them.

Egg ripening and fertilization are followed by an active migration of females to the “spawning” places. This is also the period of formation of unisexual shoals.

After fertilization the period of embryonic develop­ment begins, also characterized by an increase in the size of the eggs and of the ovary as a whole. T he eggs’ spherical form changes into an elliptical one. T h a t is why V. F. Schmitt adopted the value of half the sum of diameters for characterizing the eggs’ growth. The largest egg size so measured (in fixed m aterial) varied from 1980 to 2150 ju.

As the eggs tend to be discharged from the ovaries when they have reached the embryonic stage, the weight of the ovaries cannot be determined exactly. Despite this fact ovaries were weighed and it was found tha t the mean m.f. of the great m ajority of specimens was not lower than 11-3 %. Figure 2 shows the varia­tion of the m.f. of S. marinus during the year.

Here a reservation must be made, in that observa­tions from this m aterial do not agree with Liiling’s opinion, th a t copulation would affect the growth-rate of oocytes.

Observations make it possible to suggest tha t the copulation period does not affect the rate of vitello­genesis and the period of fertilization of the oocytes. In the case of some females which rem ain unfertilized, vitellogenesis is not ham pered and ovulation takes place in the normal way. Unfertilized oocytes become de­generate or, eventually, abortive spawning takes place. Females with ripe bu t unfertilized oocytes have been found relatively often, bu t this problem will be dis­cussed elsewhere.

At the time when the females start liberating larvae, active spermatogenesis is observed in the testes of the males. In April numerous cells in the testes of most of the males are observed in the process of division, a t the metaphase or prophase of primary meiosis. Spermatids are already present in almost 50 % of the spermato- cysts, being especially numerous in the gonads of males

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June Ju ly Gu gust SeptemS. October November Decemb. January February March Qprit M ay June

fertilization sPawnin9

females

m ales 2 -

malesfem ales

Figure 2. Changes in the maturity factor of the redfish (Sebastes marinus (L .)) males and females during the year (% ).

caught during May, while in April they are rarely found. In June general transformation of the sperma­tids into spermatozoa is observed. The spermatocysts begin discharging sperm into the lumen of the ampullae and ductuli efferentes. The num ber of spermatocysts with fully formed spermatozoa increases continually; the amount of sperm in the lumen of the ampullae and ductuli efferentes also increases. By August spermato­genesis has ceased. All spermatogonia, which have begun to divide, are transformed to spermatozoa. Duc­tuli efferentes and ductus epididymidis are filled with sperm ; the male is capable of copulation. Insemination takes place on the feeding grounds between August and October. T he period of copulation indicated above does not coincide fully with the period reported by J. Magniisson. I t may be that the two populations obser­ved were of a different ecological character. The copul­ation period varies, probably owing to the circum­stances obtaining at the time of spermatogenesis.

The spermatozoa lie in the ovaries in the condition of physiological rest, influenced — as J. Magniisson supposed — by a secretion produced within the bladder of the male. Spermatozoa remain in this resting state until the oocytes have ripened and ovulated (February/ M arch). Ripening and ovulation are effected by changes in the pH of the ovarian fluids. According to the measurements of pH obtained from this material, pH changes from 6-5 to 7-0. As a result the resting sper­matozoa become active, and the oocytes are fertilized.

A cross-section cf a testis during the period following

copulation clearly shows two zones, a peripheral and a central one. The peripheral zone contains the empty ampullae after the discharge of sperm. In the central zone the ductuli efferentes, ductus epididymidis and part of the ampullae still contain sperm. Several speci­mens at this period (September) show the presence of some mitosis of spermatogonia undergoing division, but such testes occur only rarely. The remainder of the spermatozoa in the testes undergo phagocytosis. The role of phagocytes is played by epithelial cells lining the ductuli efferentes and ductus epididymidis. O n the cut sections plasmatic bulges can be seen “seizing” the spermatozoa with which the ductuli are filled. The duration of phagocytosis of the spermatozoa varies. It coincides to some extent with the feeding period, but occurs mainly during the winter migrations. In the m ajor part of the testes observed, phagocytosis was found to end by January/February. But there were some testes (May, 1954) in which spermatozoa of a new generation had been formed ; at the same time the ductus epididymidis contained “old” sperm, under­going phagocytosis.

By early October, secondary and later spermatogonia have already appeared in the spermatocysts, first in the peripheral zone of the testes. In November testes sec­tions sometimes show spermatocysts containing sperma­tids. Thus, during the winter migrations of the males, two processes are going on simultaneously in the testes : phagocytosis of the “old” sperm and a new wave of spermatogenesis. In D ecem ber/January, intensity of

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rt

11 lllllll}

Figure 3. Diagram of migrations of S. mentella Travin.1 = females 4 = migrations of females2 = males 5 = migrations of males3 ~ “spawning” areas

spermatogonal division increases and over all the testis spermatogonia of later stages can be observed. Sperma­tocysts with spermatids are by no means infrequent. In February spermatid formation intensifies, and by M arch it reaches its height. Figure 2 shows how the relative weight of the testes (m.f.) changes during the year.

Investigations have also been m ade into the history of gametogenesis of the S. mentella. Comparison of the data obtained showed tha t gametogenesis and m.f. are very similar for both species. I t has been possible, how­ever, to discover tha t the duration of gametogenesis is influenced by the ecological differences of the species reported by Travin (1951). I t has been found that spermatogenesis and oogenesis term inate earlier in S. mentella (Bear Island-Spitsbergen populations) than in S. marinus (inhabiting the Barents Sea). In 1959 this difference was at least one month.

As has been shown by Travin, the habitats of S. marinus and S. mentella are different and so are their routes of migration. A schematic chart of S. mentella migrations (Fig. 3) has been drawn, based on the data collected by scientific workers of P IN R O since 1946, (V. I. Travin, N. A. Khaldinova, T. S. Berger, A. S. Baranenkova, V. P. Sorokin). T he feeding areas of S. mentella include deep-water areas of the Western Deep (to the east and south-east of Bear Island), the south­ern and western slopes of Bear Island Bank, and the area northwards along the continental slope, including the West Spitsbergen area. Here S. mentella lives from

June/A ugust until February/A pril. In August/Sep- tember insemination of the females takes place; during January /February and partly in M arch, the oocytes ripen and are fertilized, and this coincides with the beginning of the active “spawning”migration of females to the “spawning” areas. T he migration of males begins approximately a m onth later than of females.

In 1959 the migrations of females reached their height by February, whereas mass migrations of males were observed only a t the end of M arch. At this time the formation of unisexual shoals takes place.

From the Spitsbergen area and the western slope of the Bear Island Bank, S. mentella moves southward along the slope; from the Western Deep area the fish move in a westerly and south-westerly direction, keeping to depths greater than 350 m. “Prespawning” female concentrations of S. mentella are already being formed at the beginning of M arch in the south-west part of the Kopytov region. This area lies between 71°50'-72°20'N , 15°00'-16°30'E. T he ovaries of females caught in this area contain embryos w ith the eyes pigm ented; the body is segmented and there are chromatophores on the ventral and dorsal side of the caudal part of the body. T he latest stage of embryo development observed in the area of “prespawning” concentrations can be characterized as follows: body length, 7-7 m m ; eye pigmentation is complete; num er­ous chromatophores are present on the dorsal and ventral sides of the body; the alimentary canal and the occipital region are pigmented. The pectoral fins are formed and the rays of the caudal fin can be seen. T he embryo lies in the egg membrane. Females with such embryos pass to the areas of liberation of larvae.

M aterial collected over several years by Baranenkova and others (1956) on the distribution of redfish larvae, as well as the samples taken in 1959, indicate that liberation of larvae by the females of the Bear Is land / Spitsbergen populations of S. mentella takes place in the area between 70°-71°N and 11°-16°E.

In 1959 the liberation of larvae belonging to this population began between 25. April and 2. May. During liberation S. mentella females are not found in concentrations suitable for commercial fishing. After liberating the larvae the females m igrate to the feeding grounds via the same route.

The S. mentella males do not undertake such long migrations. They remain in the northern part of the Kopytov area, north of 72°20'N. In early spring (M arch) shoals of males are observed at 25°E. In due course they move to the west, and by June reach 15°E. W ith their advancement to the west their concentration increases; the greatest density of shoals of males is observed in April. Throughout the whole migration period the concentrations of S. mentella males are fished intensively by the trawl fishery.

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^ ? / c 'S,

Figure 4. Sex ratio dynamics of the S. mentella Travin population during the 1959 spring migration.

1 = males 2 — females 3 = locality of capture

The migration dynamics can be clearly traced by the changes in the sex composition of the migrating stock. This is illustrated by Figure 4, where the results of three months’ observations on the sex ratio variations during the spring period of the migrations (M arch, April, May) are summarized.

Summary

Redfish oogenesis and spermatogenesis take place in different seasons. Spermatogenesis is completed by August; then copulation takes place, resulting in the females’ insemination. The spermatozoa are maintained in the ovary in a state of physiological rest until the moment of ripening of the oocytes, which occurs in February/M arch. Ripening and ovulation are accom­panied by a pH change of the ovarian fluid, which results in an intensification of the spermatozoan activ­ity and fertilization.

The extent of migrations of S. marinus and S. men- tella is different. The spring migrations of females have a “spawning” character, the migrations of males are

winter migrations. T he sum m er/autum n migrations of both are associated with feeding. The formation of unisexual shoals takes place in February/M arch.

The bulk of S. marinus m ature males inhabit the area eastward of the North Cape. S. mentella males generally inhabit the area north of 72°20'N. The males and females re-unite, after the liberation of larvae, in June-July, during their migrations to the feeding areas. The small num ber of males observed by Liiling in the Andenes, Langanes, M alangen areas (i.e. area of larval liberation by females, or the areas of prespawning con­centration) does not signify, as Liiling thought, tha t males are in the minority in the S. marinus population but is the result of differential distribution brought about by different behaviour of males and females in the period of spring migrations.

The time of the migration of females to the “spawn­ing” areas depends on the period of ripening of oocytes, their fertilization and subsequent embryonic devel­opment.

The duration and rate of migrations of males are determined by thermal conditions of the w ater masses in which they spend the winter. T he time of the begin­ning of the males’ and females’ migrations may change; it is not necessarily the same in different years.

These investigations perm it the conclusion tha t the sex ratio in a redfish population, not subjected to fish­ing, is unity (LI ) .

The actual redfish fishery results in an upsetting of the male : female ratio. M any years’ exploitation of the shoals of female S. marinus in the Lofoten Islands area has resulted in a reduction of females. The inten­sive fisheries for male S. mentella belonging to the Bear Island/Spitsbergen population has resulted in a reduc­tion of male S. mentella.

The general biological timing of the annual cycle of the redfish, as established with respect to S. marinus and S. mentella populations of the Barents and N or­wegian Seas, is apparently also valid for other Sebastes species accomplishing seasonal migrations.

ReferencesBaranenkova, A. S., 1957. “Materialy k raspredeleniu mor-

skykh okunei roda Sebastes. (Data on the distribution of redfish, Sebastes).” Dokl. Akad. Nauk S.S.S.R., 113 (2) : 468-71.

Baranenkova, A. S., Khokhlina, N. S., & Yudanov, I. G., 1956. “Raspredelenie lichnok morskogo okunia roda Sebastes v Norvezhskom more. (The distribution of larvae of Sebastes in the Norwegian Sea).” Dokl. Akad. Nauk S.S.S.R., Ill (2) : 489-90

Boldovski, G. V., 1944. “Pitanie morskogo okunia Barentsova moria. (Feeding of Redfish from the Barents Sea).” Trudy PINRO, 8: 307-30.

Kotthaus, A., 1955. “Age and growth in redfish (Sebastes m a r i n u s ) Biol. Anst. Helgoland. Fischereibiol., Bremer­haven.

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Liiling, K. H., 1951. “Zur intraovarialen Entwicklung und Embryologie des Rotbarsches (Sebastes marinus L.). Zool. Jahrb., Abt. Anat., 71: 145—288.

Magnüsson, J., 1955. “Mikroskopisch-anatomische Untersuch­ungen zur Fortpflanzungsbiologie des Rotbarsches (Sebastes marinus L .) .” Z. Zellforsch., 43: 121-67.

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Schmitt, V. F., 1944. “O razmnozhenii morskogo okunia. (On the reproduction of the redfish).” Trudy PINRO, 8: 280- 306.

Smaragdova, N. P., 1936. “Rost Sebastes marinus L. v Barents- ovom more. (Growth of Sebastes marinus h. in the Barents Sea).” Biul. Mosk. obshch. ispyt. prirody, otdel biol., N.S., 45 (5) : 331-37.

Sorokin, V. P., 1958. “O biologii razmnozhenia morskikh okunei Sebastes marinus i Sebastes mentella Travin v Ba- rentsovom i Norvezhskom moriakh. (On the reproductive

biology of Redfish, S. marinus and £. mentella in the Ba­rents and the Norwegian Seas).” Trudy Soveshchanii, Vyp. 8 (Trudy Soveshchaniya po Fiziologii Ryb, 1956), pp. 158-70.

Surkova, E. I., 1957. “Polovoi i vozrastnoi sostav okuniaklu- vacha (Sebastes mentella Travin) rayona Kopytova. (Sex and age composition of S. mentella in the Kopytov area).” Trudy PINRO, 10: 172-85.

Travin, V. I., 1951. “Novy vid morskogo okunia v Barents- ovom more (Sebastes mentella sp. T ravin). (A new species of redfish in the Barents Sea, S. m e n t e l l a ) Dokl. Akad. Nauk S.S.S.R., 77: 741-44.

Travin, V. I., 1957. “Promysel morskogo okunia v yuzhnoi chasti Barentseva moria i rayonie Kopytova. (The redfish fishery in the Southern Barents Sea and the Kopytov area).” Trudy PIN RO , 10: 161-71.

Veshchezerov, V. V., 1944. “Materialy po biologii i promyslu morskogo okunia v Barentsovom more. (Data on the biology and fishery of Redfish in the Barents Sea).” Trudy PINRO,8: 236-70.