d ARCHIVES

FISHERIES RESEARCH BOARD OF CANADA

Translation Series No. 266

DIFFERENCES IN THE BIOLOGY OF REPRODUCTION AND DEVELOPMENT OF RESIDUAL OR DWARF SOCKEYE AND ANADROMOUS SOCKEYE ( NERKA (WALBAUM)).

By A. I. Smirnov

Original title: Otlichiiâ v biologii razmnozhens.iâ i razvitii ostatochnoi ili karlikovoi i prokhodnoi nerki [Oncorhynchus nerka (Walbaum)].

Fromô Nauchnye Doklady Vysshei Shkoly, Biologicheskie Nauki, No. 3, pp. 59065, 1959.

Preliminary translation by W. E. Ricker

Distributed by the Research Board of Canada Biological Station, Nanaimo, B. C.

1960 At the present time quite a variety of material has been collected indicating wide intraspecific variability in salmonfl an example of this being the recognition of hiemal and vernal races9 and local stocks, From both a theoretical and a practical point of view j_t is of interest to discover whether intraspecific diffe-r® ences occur only in the final stages of the growthfl or whether they are evident throughout other stages of developmentfl even the- very earliest. It can be taken for granted that good material for shedding light on this question is afforded by the species which include both anadromous and freshwater forms a such forms being particularly sharply distinguished from each other.

During 1956 and 1957 the author studied the development of anadromous and the so-called residual Costatochna â] or dwarf sockeye (Oncorhynchus nerka (Walbaum)). The work was done at the Paratunka Stàtion of the Kamchatka bivision of the Pacific Research Institute for Fisheries and Oceanography (TINRO)fl which is situated on Lake Dalneen the latter being connected by means of a small river of the same name which drains from it to the bisin of the Paratunka, and thence flows into the Gulf of Avachin.

The characteristics of the development of anadromous sockeye have already been briefly described (Smirnov, l95$). In the present article some characteristics of the reproduction and development of the dwarf form are outlined, and a comparison is made with the anadromous form.

According to the observations of F. V. Krogius2^ males pre® dominate in number among the residual sockeye9 and they mature at ages from 2+ to 4+ 9 most frequently at 3+; the females for the most part mature one year later, most of ^hem at age 1++, and they have a fecundity of about 500 eggs, Ripe dwarf males are observed from the beginning of September and mingle with the anadromous sockeye during spawning, but the dwarf females mature about a month later. Both the male and the female dwarf sockeye feed up to the time of maturing9 whereas anadromous sockeye cease feeding at the mouths of the rivers, that is, quite a long time before spawning.

1The success of the work was greatly facilitated by the efforts of F. V. Krogius and E. M. Krokhin, to whom the author extends his heartfelt thanks.

2F, V. Krogius, 1952, Materials on the biology of the Oncorhynchus nerka (Walbaum), Fondy Kamchatskovo otdelenii Tikhookeanskovo n,-i-, in-ta rybn. khoz-va i okeanogr,

3 [Here and later peripe" is used to translate tekuchii, literally '1running"p presumably meaning fish with freely flowing milt or eggs.] - 2 -

In the years of our observations ripe dwarf male skeye were encountered beginning in the second 5-day period of September, whereas the first ripe females were caught only between the 6th and 10th of October. Judging by the capture of females with only a small quantity of eggs remaining, spawning lasted up to the beginning of November. In the same years the summer anadromous sockeye began spawning in the last 5-day period of August and they finished in the last 10-day period of October. The beginning of their spawning [page 60] coincided with a marked warming of the upper layers of water in the lake and also of the springs (ground water) the daily mean temperature of the water at the source of the river [outlet of the lake?] exceeded 14 0 9 and in the spring which supplied water for our hatching apparatus it was 4'. The spawning of the dwarf sockeye began when there had been some cooling of the upper layers of water (mean daily temperature at the source of the river fell to 5 or -6") and when the temperature of the ground waters began to decrease. Thus the completion of the maturation of the dwarf females and their spawning takes place at a lower temperature [than that of the anadromous fish]. The spawning place of dwarf sockeye has not been exactly determined. In earlier years and during the period of our work in Kamchatka no nest construction by them was observed in the shallow littoral area of the lake in places where the anadromous summer form spawns. Above Lake Dalnee there are no tributary bodies of water where spawning might take place, as has been observed for the kokanee type of dwarf sockeye [zhilaia karlikovafà nerka] in Lake Kronotsk and in certain American lakes (V. V. Ohernavin, 1921; E. M. Krokhin and F. V. Krogius, 1936; I. Fraser and A. Pollit, 1951); while in the river flowing from the lake no emigration of dwarf females for spawning has been observed. Inas- much as during the spawning period ripe dwarf females were cap- tured in fixed nets, placed near the shore, we may assume that they laid their eggs in the littoral region of the lake but in deeper water than the anadromous sockeye. Ripe dwarf individuals in Lake Dalnee are easily distinguished by external appearance from anadromous sockeye. It is widely known that mature males and females of anadromous sockeye assume an intense red colour, while their scales lose their luster and become deeply buried in the skin; the body of the males before maturity becomes compressed, on the back there appears a great hump, the jaws become greatly lengthened and tusk-like teeth grow out from them. Pre-spawning changes in the form of the body, skeleton and teeth of dwarf sockeye of Lake Dalnee are quite small (Fig. 1). The body covering of the dwarf sockeye also changes very little. It retains a distinct silveriness, while the scales are only slightly embedded in the skin and are easily removed. The general tone of the colour of the ripe spawners is dark grey. Dwarf sockeye males are usually of a dark olive shade on the body, with a weak narrow rosy stripe along the midline; among the females these marks [page 61] as a rule are lacking and a metallic blue-violet shade prevails. On the head and back of the dwarf 3

spawners there are weakly developed fine dark spots; similar spots are more clearly developed on the dorsal and caudal fins. On certain females there may be seen the rosy stripe along the lateral line which is characteristic of males, and an olive shade on the back. These characters do not occur on all of the males Ceither7. Becâ.use of this variability in colour, and the absence of differences in body form, it is not possible to distinguish the sex of some of the dwarf individuals by external characters.

An analysis of the pre-spawning changes in the body covering of Pacific , and the conditions under which they appear, has led me to the conclusion that they have an important adaptive function, permitting intensification of the dermal respiration which is necessary under the new environmental conditions and the changed physiological. circumstances for the spawners ( Smirnov, 1959)o Dwarf spawners, because of their small size, have a relatively large . body surface; therefore, among them it would seem that the necessa:ry increase in level of dermal respiration is achieved with-less change in structure and colour of the body covering. In addition , the spawning medium of the dwarf sockeye is not so radically different from the medium in which they feed during their active life; therefore the transition to the place of reproduction does not require such radical adaptive changes in the organism as takes place in the anadromous sockeye. Judging by the specimens which E. M. Krokhin has kindly provided me with, the Lake Kronotsk kokanee change more9 during the period of their maturation, than do the Lake Dalnee dwarf sockeye; spawning individuals are brightly coloured, they have heavier teeth and in the males a distinct hump is developed. As was remarked earlier, the stock of Kronotsk kokanee leaves the lake for spawning and enters the river and springs9,corresponding to this more severe change in spawning environment ( as compared with that of the Lake D.alnee dwarf sockeye) among them there occurs a more important change in the whole organism before spawning. Such an ecological -int,erp.retation of the causes of the differences in the degree of development of the somcalled breeding colours [brachnyi nariad], among different stocks of trout, has already been suggested (V. V. Chernavin, 1921). As we have seen, this approach is applicable also to our problem; however it is clear that a more detailed analysis of the causes of the development of pre-spawning changes in the dwarf and the anadromous forms of sockeye will require the undertaking of special physiological studies.

The majority of the dwarf males which were at my disposal were ripe, and data on the weight of their gonads, of course, are too low. The observed variation in weight of the testes is from 3.6 to 6.6% of the body weight. The maximum weight was observed in a male of stage IV of maturity ( weight 17$ g) whose testes weighed 11.7 g. According to the data of I. V. Kizevetter (194$), among,semi-mature anadromous sockeye the weight of the gonads varies among the males.from 2 to 6%, and among the females from 7 to 12% of the body weight. From the data cited we may regard the testes of the dwarf sockeye as being relatively larger than in the anadromous form. An exaggerated size and weight of testes, up to a quarter of the total weight, was observed by 0. Robertson (195'J^ among dwarf male . It is likely that this increased size and weight is generally characteristic of dwarf forms of salmon.

As F. V. Krogius (1952) has ob served, the fecundity of dwarf female sockeye is 5 times less than the fecundity of the anadroT mous ones. Among 14 females which were examined in 1.956 there were from 411 to 593 eggs (average 4$2..) . Weight of the ovaries varied from 10,0djo to 23.3% (average 1.5.7%) of the live weight of the fish. The ovaries fr.e uently weighed 25-30 g, and the heaviest ones were 40.2 ga female weighing 172.7 g). Even the average relative weight of the ovaries among the dwarfs was considerably greater than their maximum weight [relative to the body] in anadromous lake sockeye. Whereas in a l-L-kilôgram anadromous sockeye there are 1550 eggs per kilogram, and in a 2-kilogram sockeye there are about Upage 62] 1290 per,kilogram, the dwa•rf females produce on the average about 2$00 eggs per kilo- gram of live weight, which is about twice as many.• Thus the dwarf sockeye, with a smaller absolute fecundity, have a greater relative fecundity. This indicates an interesting direction of adaptation of the dwarf sockeye, consisting of intensification of the activity of the gonads under conditions of decreased food supply in the lake as compared with the sea. A relative increase in production by the gonads is permittéd by the fact that the dwarfs feed right up to the time of spawning, by the absence of any serious change of environment before reproduction and the radical reconstruction of the,organism which is associated with this, and by the absence of any extended pre-spawning migration which among anadromous fishes consumes a tremendous amount of energy.

A lower absolute fecundity of the Lake Dal,née dwarf sockeye, like the same phenomenon among the soacalled Kennerly?s salmon Ckokanee] of American lakes (L. Scattergood, 1949), must be con- sidered as testimony of increased survival rate under the condi- tions of freshwater life, and as an indication of the very low level of fecundity at which reproduction of salmon can be success- ful in the uniform conditions of the lake environment.

Running eggs of the anadromous Lake Dalnee sockeye weigh from $4 to 130 mg, on the average 103 mg, while among the dwarf sockeye the weight is from 51 to 69 mg, average 5$,5 mg, or almost two times less; the weight of the eggs, as we see, changes in fresh- water conditions less than the fecundity. This may be explained by the fact that the most important adaptive characteristic of salmon is the embryo4s need for a large quantity of material., for construction of its body and for energy, during the long period of development without external feeding while the eggs are buried in the gravel, For this reason there can be no important decrease in the size of the egg (quantity of yolk) since it must conform to the requirements of a type of development which is typical not only for this species but even for all salmon. The eggs of the dwarf individuals are of the same intense red colour as those of anadromous sockeye, which indicates the pres- ence in them of carotenoids and the capacity to develop under conditions of a considerable oxygen deficit [below saturation]. This has already been indicated9 earlier, by the strong develop= ment of the superficial system of capillary vessels w.hich are the embryonic organ of respiration. Thanks to the small size of the egg fl the diffusion surface is relatively large, which makes easier the task of supplying of the embryo with oxygen when it is at a low concentration in the watern and gives the embryo the property of great tolerance of low oxygen levels.

In the structure of the egg of the two forms being compared, no impôrtant differences have been observed. In the smaller eggs of thè dwarf females there is a correspondingly smaller size of the blàstodise, which in the sockeye has a characteristically depressed form; the blastodisc of the dwarf egg has the diameter of 0.$-1.15 mm, and in the anad--romous form 1.241.4 mm. The perivz- telline space in the dwarf egg is rather laxger.

As a x°esult of the small egg and the smaller amount of plasma (blastodisc). the embryos of dwarf sockeye at corresponding stages are of a rather small size. Embryos in the eggs of residual sock- eye develop along the same lines as embryos of the anadromous sockeye; although9 to be sure, among them the blastopore usually closes somewhat earlier9 at the 25-27 segment stage or less, but this has been observed also among some of the embryos from the smaller eggs of anadromous sockeyea However, the period of incu- bation of the dwarf sockeye is significantly shorter and is completed at an earlier morphological stage (Fig. 2). Thus in the experimental incubator, supplied with ground water of a very uniform temperature and uniform concentration of salts and gasesfl mass hatching of embryos from the eggs of the dwarf sockeye is observed at the age of 105 days, or 430 degree-days; under the same conditions (with the exception that the eggs of the anadromous sockeye were fertilized [pagè 64] earlier and began their develop- ment at a somewhat higher temperature) among the anadromous sock- eye massive hatching took place at the age of 174 days, or 535 degree-days, and was quite prolonged.

Of especially great inter est for us is the difference in the level of development of the embryos at the time they leave the egg. The embryos of the dwarf sockeye at this time have short fins,.bifurcation of the olfactory aperture is only barely indi- cateda the otic capsule is as close as possible to the eyes, the gill covers do not completely cover the weakly developed filaments Clepestki] of the last gill, teeth on the jaws are not apparent, and the short head occupies about 15% of the total length of the body. The unpaired fin-fold is strongly devel.oped. In the dorsal and anal fins there is only a weakly developed muscle bud, in the caudal fin can be seen 5-9 short rays and the beginning of the development of the net of vessels, the fold of the pectoral fins i s only outlined and in the pelvic fins there are as yet no r ays. The upper and lower cones of the myotomes are weakly drj,reloped. The yolk globule is large and has a strongly devéloped net of blood vessels. The embryo is weakly pigmented, the covering of the trunk has scarcely any melanophores, and on the head there are a few lipophores. Hatching of the dwarf embryos takes place all together.

During the period of the main hatch of anadromous lake sock- eye, the larvae are at a considerably later stage of development. Their head is larger and comprises about 1.7% of the body length, the snout is long, the olfactory apertures are divided, the ear capsule is far from the eye, the gill covers completely cover the gills which have well-developed branched filaments, and the teeth are well developed. The eyes move. In the well-developed dorsal and anal fins there is a complete number of rays, the adipose fin has been formed, while the embryonic fin-fold is much reduced. In the tail fin all the rays are formed, the larger of which have 3-4 joints. The pectoral fins are large, in the pelvic fins there are large rays. The size of the yolk sac is considerably decreased. The body of the.larva is covered with large melanophores and orange and yellow lipophores. For the anadromous sockeye it is typical to have a long incubation period and a very extended period of hatching. Embryos which hatch late are at an even later stage of devel.opment. But even embryos of the very earliest hatch are developed more than are embryos of dwarf sockeye at the hatching stage; for example, in the tail they have about 20 rays with 2 or 3 joints.

The early and concurrent hatching of the embryos from thé eggs of dwarf sockeye can be considered as a definite indication of an adaptation of the dwarfs to development under conditions of poor aeration and worsened water supply during the winter period. Hatching from the egg places the embryo in a new relationship to the surrounding worldq Among dwarf embryos this change of rela- tionships takes place early, something which cannot be without its effect on the further course of their development, inasmuch as the different stages of individual development of organisms follow definite patterns and are interdependent (S. G. Kryzhanovsky, 1950).

Thus the life of the dwarf sockeye, throughout the whole of its development under lake conditions, has resulted in important differences not only in the definitive morphological and ecologi- cal characters (small siz^e at maturity and low fecundity, very limited change in the form of the body and colour among mature individuals,..absence of a long pre-spawning migration, late spawning in deeper water), but also to changes at other stages of development, including the very earliest (small size of eggs and embryos, early and simultaneous hatching, hence a protracted period of nourishment by the yolk sac after hatching from the egg, etc.). This shows that adaptive changes among intraspecific groups°involve morphological and ecological characters of the early stages of development. 7

[page 65 1 In conclusion, it is important to observe that the dwarf sockeye which have been studied are a part of the progeny of the anadromôus sockeye of Lake Dalnee, in the same way as the Black Sea river trout Ccher°norechenska â forel7 are a part of a single'stôck of Black Sea salmon [chernomorskii losos]of that region (G. P- Barach, 1952; D. A. Panov, 1958), In this connec, tion, although there are also considerable differences in dwarf sockèye at different stages of development, they cannot serve as the basis for distinguishing it even as a morpha, and they only bear witness to the breadth and depth of intraspecific adaptive variability.

In the situation described we have an example where, not some insignificant deviation of particular individuals, but actual group c^flh n es which are undoubtedly favorable to survival under special^not necessarily lead to separation of the group and the production of a new specieso Though actually differing both morphologically and ecologically, the anadromous lake sockeye and the dwarf form not only are not beginning to split into separate bodies, but on the contrary clearly present quite the reverse picture. Because of the observed separation of the two forms in respect to place of feeding, time and place of spawning, and con- ditions of development, and a probable difference between them both in the size of their food objects and season at which the young start to feed, the sockeye as a species divides its "arena of l.ife'^ and thus acquires the capacity to survive under more varied conditions, which makes possible an increase in abundance of the species and its survival under changing environmental conditions.

The example studied, of differences in the development of migratory and residual or dwarf sockeye, and also previously described differences between the modes of development of cultured carp and wild carp (Smirnov, 1955), illustratè the importance of studies of this kind, which afford u.s a deeper understanding of the laws underlying the phenomena of the formation of stocks [porody] and species, and also of 'intraspecific relationships.

1. $

LITERATURE

Barach, G. P. 1952. [The significânce of the river trout in the reproduction of the stocks of Black Sea salmon (kumzha),] Zool. zhurn,fl Vol, 31, No, 6.

Kizivetter, I. V. 1948, [Concerning changes in the chemical composition of the body of the sockeye (nerka).] Izv, Tikhookeanskovo n.-i, in-ta rybn, khozmva i okeanogr.

Krokhin, E. M., and F. V. Krogius. 1936, [The lake form of sock- eye salmon (Onco.r.hynchus nerka) from Lake Kronotsk in Kamchatka, ] Dokl, AN SSSR, Vol, L. (13), No. 2,

Kryzhanovsky, S. G. 1950, `.The theoretical foundations of embryology,] Uspekhi sovrem, biologii, Vol, 30, No, 3 (6).

Panov, D. A. 195$, [Concerning the uniformity of the stocks of Black Sea salmon and river trout,] Nauchn, dokl, vysshei shkoly, ser. Biol. nauki, No, 1,

Smirnov, A. I. 1955. [Some characteristics of the development of the mirror carp.] Vopr. ikhtiologii, No. 3,

Smirnov, A. 1, 1958. [Some features of the biology of reproduc- tion and development of the sockeye salmon Qncorhynchus nerka (Walbaum), ,] Dokl, AN SSSR, Vol, 123, No, 2.

Smirnov, A. I. 1959. [The functional significance of prem spawning changes in the integument of salmon (as illustrated by the genus Oncorhynchus),] Zool, zhurn,;, Vol, 3$, No. 5,

Chernavin, V. V. 1921, [The origin of reproductive coloration in salmon.] Zhurn. Petrogr, agronomich, in-ta, No. 3-4,

Fraser, J. C,, and A., F. Pollit. 1951. The introduction of kokanee red salmon (Oncorhynchus nerka kennerlXi).into Lake Tahoe, California and Nevada. California Fish and Game, Vol, 37, No. 2,

Robertson, 0, H. 1957. Survival of precociousl y mature King salmon male parr ( Oncorhynchus tschawytscha) after spawning. California Fish and Game, Vol. 43, No. 2,

Scattergood, L. W. 194.9. Notes on the kokanee (Oncorhynchus nerka kennerlyi). Copeia, No. 4. -r-. ■ ?11"-liereeelgelek%& - -tege

Fig. 1 0 Males in Stage V of sexual maturity. A--anadromous sockeye; 6 --residual or dwarf sockeye. Fig. 2, Embryos at the hatching stage. A--from the egg of an anad- romous sockeye; 6--from the egg of a residual or dwarf sockeye.

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