This paper not to be cited without prior reference to the author

International Council for theExploration of the Sea

C.M.1969

Special Meeting

"The Biochemical and SerologicalIdentification of Fish Stocks"

No.4

•

Recent Physiological, Biochemical and Immunological Studies on the

Problem of Intraspecific Differentiation in Marine Fish

by

Yu. P. Alturllov x)

X)Mr. Yu. P. Altukhov,Marine Biology Department,Academy of Scienc~ of U.S.S.R.,Vladivostok,U.S.S.R.

'.:

•

•

- 1 -

The gonetical trend in marine biology, aimed at studying intraspecificdifferontiation of fish on the basis of immunologica1, biochenica1 andphysio10gical characters, began, perhaps, not more than 10 years aga.

Tho pecu1iarities of tbe immuno10gical approach were more or loss fully .scrutinized in 0. series of communications (Marr and Spraguo, 1963; .CushinG, 1964; A~t.~ov ot a1i~, 1964:, A1tukhov, 1969; Suz~~i, 1967).

The constnnt1y growing number of works on the biochemica1 genetics offish populations require synthesis. However, certain detai1ed studies indi­cate thc o~v::'ous advancos in this fie1d (Sick, 1961, 1965a;1965b~ lT0l::..cr~1963;llaovda1, 1968; do Ligny, 1968; Fujino and Kang, 19680., 1968b, and many others).

In tho worl:s by Soviot authors in the fie1d of co11 physio10GY ofpoiki10thorma1 animals, 0. nou feature, thormostabi1ity of iso1ated cella.(Ush~kov, 1959a,b), has been shown to be convenient for distinguishingtaxonomically close species (within one Genus) and, in certain cases , forintraspGcific groups, if spociation takes place already. Same biochereica1and im~t~010Gica1 data (V. B. Ushakov, 1963, 1965; Altukhov, 1965a,b) showthat the heat death of iso1ated cells, tested by the irreversiblo lass ofe1ectrical oxcitation, is duo to the damago of so~uble sarcoplasmatic proteinn.Recont1y thopolygenic nature and horitability (h ) of the said foature wereestablishod (Altukhov et a1ia, 1967c; Altukhov and Ratkin, 1968; Ushakovet ~,1967). Tho par~icu1ars of this cytophysio10gica1 trend in the resea~chconnected with spociation are discussed in Ushakov's papers (19590., 1964, 1967).

This report SUDS up tho resu1ts of some recent works accomp1ished onthe basis of the three approaches mentioned above, on intraspecific differ­entiation in certain species of marine fish, such as the Black Sea horsemackoreI, tho i1marinus" and "mentel1a" redfish from the North Atlantic, theNorth Sea herring and the European anchovy inhabiting the Black and Azov Seas.

1. Studies on the differentiation of "large" and "small" formsof the Black Sea horse mackcrel

In the 1940's, large numbers of big horse mackerel (50 cm and more)were discovorod in the Black Sea. They were bio10gically considerab1y diff­eront from the sma11 mackore1 (loss than 20 cm) commonly found thoro. Thus,"Thereas tho "mnall" form 00.turos in i ts socond year and spawns in coasta1'wators, tho "largo" fish matures at four yoars of ago and spmms in tho opensoa.

However, duo to thc absence of external morpho1ogical differonces, bothtypeo were odducod to the same specios, Trachurus moditerraneus Stdr.(Humann, 1956; A100v, 1956, 1957, 1959). Aleev (loc. cit.) oaintains that"larGe" horso mackerol may be considered an independent southern (Anatolian)"loenJ. stock" difforing bio10gica11y from tho "10ca1 stocks" of the northern(Crir:ean) and oastorn (Co.ucasian) "small" forms. No dofinito do.ta havo beoncitod on "largo ll horse mackorol oxisting bcyond tho Black Sea.

Cytophysiological, immunological and biochomica1 investigationo of thoB1ack Soa horso 8~ckorolgavo tho fol1owing rosu1ts.

1. "Soall" horoo mackerplof both tho northorn and oastorn "local stocks"da not diffor as far as thermostability of isol~tod nU3clo tissue is con­cerncd, ~vhercaf3, the "large" tJ.rpe (araund 40 cm lang) differs sharpl:{ fromthom in this rospoct. Soasonal changos of tho abovo-oentioned foaturo takeninto account (Altukhov, 19630.), tho difforenco in cell thormostabilityX) of"largo" and ":::I:lall" horse mackorel roaches 2°C of the test tenporaturo scale~

i.e., it appoars to bc tho same as that botwoon taxonomically closo species

x) "Coll thermostability" i::: synonymaus with "muscular thornostabilit:r"since muscle heat death is tostod with irreversiblo lass of oxcitntio~

by separato fibres most rosistant to heat. With brovity in view, weaha11 torm the feature "CT", tho preparation survival tine ntdifferent tooporatures.

> ••. ~~ ..

"'.It t , ,~ '10. ."

- 2 -I. 1" \ I~", \

''/

•

•

(Altukhov, 1962a, 1967a; A1tukhov and Glushankova, 1966; see also Kusakina,1959 1960; Ushakov, 1964; 1961). The above difference is due to genotypicaladaptation fourtd on the oel1ular level. A.higher CT is characteristic of themore heat-loving "largo" mackereI.2. The CT analysis cf several hundred horse mackerel less than 20 cm long,established the heterogene!ty of the samples.taken from populations inhabitingthe Black Sea coastal wators. The distribution of the above-montioned featureis binodal the menn value of the right hand side of the variation curve beingidentical to the cell theroostability'lovel peculiar to the "Iarge" fish.This fact testifying that younß' "larß'oli horse oackerel live in mixed popul­ations with "small " fish,was used to elucidato pcculiarities of wintordistribution of the yoting iilarß'e" forms off the Caucasian and Crimean coasts(Altukhov, 1963b). It likewise allowed us to find the difference in thothermostability of t:l.ctomy6sin proteins of the forms (Glushankova, 1963), asweIl as in the otolith ration (Altukhov nnd Mlkha~ev, 1964).

3. The cytophysiological difference between the "Iarge" and "small" horsemackerel correlates with their differentiation determined in serological tests.Respective muscle water-salt extract titres, obtained by the ring-test pre­cipitation method, showed that the Black Sea horse mackerel differ from eachother essentially rio less than from the mackerel Trachurus trachurus L., whichis known to be an independent species (Altukhov and Apekin, 1963). Lator,when the CT of Trachurus trachu1:'Us was successfully studied in the l-Torth Seß,and thc data obtainod conpared with the investigation results for the BlackSea horse mackoreI, we found the same picture (Altukhov, 1967b).

4. Essential differences within ihe Blück Sea horso mackerel werG likewisofound when studying tho antigenic properties of their erythrocytes (Lioansky,1965) and serUm heteroagglutinins (LioUnsky, 1961). When o.gglutinating humanerythrocytes id th mackerel sera, the "Iarge" forms proved to differ sharplyin this respect fron noarly 0.11 the tlutually identical "small" forms frou"local stocks ll •

Howover, paper electropho~esis tests of seran proteinb itidic~tod o~lta slight difference between "Iarge" rind ,isDall j, mackerel in the cx ..globulin~6no(Golovko, 1964). If one takes irito account therather low resolutionof the above oothod, as ~ell as recent data on the character of proiein diff­erenco in sibling-species (Hubby and ThrockDorton, 1968), then ono oay'oxpectto find 0. still uore essential differen~iation of horse mackerel in the futurewith electrophoretical analysio of their proteins, priuarily such as oyogensand haemoglobins •

5. The SUD total of the exarained facts, indicating a deop divergence of"Iarge" and "1300.11" nackerel fron 0. whole series of genetical features, bothpolymeric and alternative, does not pormit UD to consider these forns as"local stocks". Bearinß' in uind the striking outer sinilarity of the saidforns, they should bo adduced to the sibling-species, one of which, the "larffe",is in all probability 0. nigrant from the Mediterranean (Altukhov, 1962a,b).Reccntly this viewpoint was again corroborated in the roport that "Iarge"mackerel are known to exist beyond the Black Sea (Slastnenko, 1965).

II. Studios on the differentiation of the North Atlanticredfish "oarinus" and "oentel1a"

Cytophysiological, inounological andbiocheoical studies were conductcdin order to elucidatc the differonce botween "marinus" and "nentella" redfis11(genus Sebastes), there being differing opinions regarding their taxono~(Travin, 1951; Andriyashev, 1954; Kotthaus, 1961).

1. The CT of over 1000 redfish caught in the waters off Iceland, Greenland,Labrador and tho Barents Sea was studied from 1964 to 1966 aboard researchvessels. In this respoct "marinus" and "montella" differ no less than theindependent species, the "uentella" cells being noro resistant to the daoagingeffect of heat. This result was obtained with fish saoples both in the North­Western (Altukhov ~ alio., 19670.) and North-Eastorn Atlantic (Payusova andllefyodov, 1968). Taking the exact corrospondence of the CT level to habitattemporature as the rule established for more than 300 poikilothern . species

•

•

...... - ..- .

.;. 3 -

(see Ushakov, 1964, 1967), one nay infer that "nehtella" are more thern.ophile.

2. Tho CT analysis for those re~fish,which, due to thoir external structuro,occupy an internediary position between "narinus" and "mentella", disclosesthe biDodality of the feature distribution. Möreover, the CT of the "inter­mediary" redfish (22.75 :t 0.75 Din at 28°C) likewise provos to be "interDodiary"for the respoctive values, obtainod at the same test teDperature for "Darinu~"

(13.6 ~ 0.69 Din) and "nentella" (27.8 ~ 0.69 tlin) in the Iceland area.. .

It io eooential to stress that the \-Tost Greenland "tlarinus" redfishhas a CT (20.05 :: 0.58 Din) vory cl~se to that of the "intermediary" redfish.H011evor, the feature distribution curve has one maxiouo. This fact, inco~pariso~ 1~ith tho biological data (Zakharov, 1962) on tho juvenal natureof thc fe r..1eles belonging to the West Greenland "oarinus" population, leadsUR to assune tlle hybrid (Fl) origin of such fiah. Tho absence of maturationin \;Teot Grcenland "rmrinus" fonales , as weIl as in "giant" redfish fonalosfrequontly encountcrcd therc, has beon proved inmunologically: their ovovitellinsynthesis is ouppressed (Altukhov et ~, 1967b). .

3. Aga~ gel electrophoresis of "marinus" and "nentella" blood serun proteins,as weIl ao of "giants'i, showod thc respective foro diffcrence to be in accordancewith thc frcquency of a scrics of protein conponents (Altukhov and Nefyodov,1967). Polynorphisn, probably heroditary and two-allolic, has been noted inthc redfish albUIJin zone•. At thc aane tiDe, the low conccntration of "slow"albunin in the blood of assuned heterozygotos, and the snall volune of sanplcs,give no ground for considering thc previous conclusion as final. Thc hereditaryvariability ofdectrophorctic nobility in thc redfish serUIJ proteins secns norDcertain for sone haptoglobin types, thc frcquoncics of which hclpcd find thcdistinctions bct'\-Tcen "narinus" and "nentclla" (lfefyodov, 1969).

On the wholc, our biochenical data are in COIJDon .with the rcsults ofprevious investigations by O'Rourke (1961) and Schacffer (1961), who deterninedthe differenco bct1'1een "narinus" and ,','tiimtella" by the antigenic properticsof thc b100d oerun end tho protoin anino-acid conposition of thc gil1 nucusand muscles~ The new infornation doa1s with tho "giant" redfish. Notwithstandingthc otrong outward siDila~dty with 'Imarinus", thoro is no biochor::lical idontitybotwccn thc two forns (Altukho~ and Nefyodov, 1967). This.fact io in accordancewith tho asounption of the hybrid origin of t~o "giants" (soo 2)~

4. Thus, tho exaninod cytophysiological, biochooico.l and iru::lUnoiogical " .data indicn.te a decp divergenco bctwoen "oarinus" and "oentella,j. redfish. Thiriio also in oound agroeIJont with tho gonorally known Dorphological ahd ecologidalpoculiarities of thc said forns, which oay ostensibly bo considored as spcciooin 8tatu nascend~.

III. Studies of Atlantic horring blood ~roups

1. Studios of crythrocyte antigens of Atlantic herring (Clupe~ harengus L.),inhabitinc tho North Soa, were begun in 1966 (Altukhov et alia, 1968)~Experioonts 'vith natural hetero-antibodios (hunan ABO sera;-änd lectins (oxtractof LiDa bean oeeds (oort "Palevopjootraja"» differentiated three ß'roups ofcrythrocytüo. They are convcntionally designated as Al (strong reaction withall rcagonts), 11.2 (wüak agglutination with sera of 0, A and B groupo: absenceof roactiono with certain AB-sera):, and 11.0 (absonco of agglutination withall rüagcnto). The antigenic character of thio variability wao proved byDüano of agglutination tosts with inoune rabbit antisera.

Analyois of herring phonogroup distribution throughout tho North Seaduring the sunner-autunn period of 1966 brought to liß'ht a certain hetero­gonoity. Tho rare groups, 11.2 and Ao , wore practically absent in saoples takonin tho aroa of tho Norweßian Deep. Only Al and 11.2 group fish were found offtho Shetland and Orkney Islands. ,All three blood groups wero representod inthe horring caught in othor invostigatcd o.roas of thc sea. Subsequcnt survcysby Dr. Truvollor (1969 - personal cODDunication) corroborate tho notcd diff- .orences, at least with Bank autuon-spawning and Atlanto-Scandian sprinß' spawninghorring. Furtherooro, in February 1967, a rathor high 11. 0 group frcqucncy (upto 40%) was found in asoall saoplo (n=48) in thc English Channel (Zcnkin,1968 - porsonal cot1I:lunication).

- 4 -

." 2. As is generally khowri, a closely related system of erythrocyte anti­gens in Atlantic herring from the Gulf of Haine was described in 1959 bySindermann and I-lairs, ,,,ho designated this variability as the "O-system".The frequency of Haine Bay "0" positive fish 'Those cells were agglutinatedby norDal lobster (Homarus americanus)sorum.or immune rabbii antiseren, wasfound to have essentially interpopulational differences~ Meantime, analysisof 3000 North Sea herring did not revoal differences in the frequency ofthe "0" antigen in sOJI1ples taken to the oouth of the central part of the seaon Dogger Bank, SaIldetti6,and in the English Ohannel (de Ligny; 1962, 1969 ­personal coonunication).

Unfortunately, when boginning our work, the W. de Ligny data worenot available and We were not able to take them into consideration in ourpublication (Altukhov et alia, 1968). However, simple comparison of tho .North Sea "A" positive fish and "0" frequencies alone, suggests thc identityof "A" and"O" antigeno, though Sindormann and Hairs (!Q.2.. cit.) did not dcs­cribe the subgroup antigen in their work. Quite recently, special testswere perforned on Georges Ban.lc herring, proving the identity of "A" and "0"factors in parallel agglutination of the cells of tho same fish with lobsterand human ABO sora (Zenkin, 1969 - personal coonunicntion).

3. The data examinod above, 0.0 weIl as the results achieved by Dr. Zenkin

•who is workinC with tho Ealtic herring subspecies (Olupen harengus membras)indicate considerablo uniformity of "0" factor frequencies (approximateaverage: 97% in all parts) over the huge area inhabited by the species. Thiscircuostancc, together with sone other unclarified conclusions regardingthe influence of tcnperature on thc lack of agglutination of horringcrythrocytcs (Tibbo, 1965), apparcntly limits tho possibility of using the

"O"antigen as 0. reliablo population characteristic. Eut at the same time,analysis of 0. sufficiont nuober of samplos and sufficiently nuoorous trnwlstations, rcvcals 0. certain hoterogoneity of oeemingly homogenoous NorthSon herring communitics, as was pointcd out abovo. This io the subject ofDr. Truveller's roport at the prcsent Synposiun. .

•

IV. Immunogonetical ·study of intraspecies differentiation ofthc European anchovy inhabitinR the Blnck and Azov Seas.

Thc European anchovy (Engraulis encrasicholus Linne) populations inthc Azov and Black Seas were at one time described as tho Azov (li.Q. maeoticusPusanov) and Elack Sea (E.Q. uonticus Aloxandrov) subspecies. In additionto morphological differences, these geographical racos essentially varyecologically. Thue, if the Elack Sea anchovy is found thoro the whole yearround, the Azov race only winters there, and migrates to the Azov Soa tomultiply and nature. Largo schoole of anchovy nigrating through thoKerch Straits for wintering are objocts of intensive fishery, 0. practice oflong standing. ~.,o questions constantly ariso - how nany isolated anchovyracos are on the spawning grounds, and whethor it is possiblo that the ElackSea anchovy penotratos to the Azov Sea, thus influoncing tho strength ofthe Azov race.

In addition to certain morphological works we (Altukhov, Limnnsky etalia, 1969a,b) conducted innunological studies of the anchovy with thefollowing rosults.

1. In heterohaonoagglutination tests with natural (horse and pig sera)and immune (rabbit serum) antibodios, threc blood groups were found inthe anchovy, Al' A2 and Ao.

2. This was used to determine essential differonces betwoen the anchovyraces. The A~ov anchovy is represcnted by all the phenotypos with thefollowing rJean frequencios, Al - 0.4867 : Ao - 0.4109. The Black Sea raceincludos only individuals with blood groups Aland A2 (frequencios oqual to0.9512 and 0.0428 respectively). .

3. A dctailod analysis of anchovy blood group distribution in thc AzovSoa (n=5936), nade fron 1963-66, showed the hetorogeneous character of theAzov population, which provod to bo roprosonted by three subpopulations:Azov proper, part of the Black Sea race Wllich had ponetrated thore, and 0.

mixed group~ The greatest migration of the Black Sea anchovy into the Azov Sen.~__ .J~~ ~_~ ~_ 'O~~

•

•

- 5 -

4. Biological and inmunological studios of fish saoplod fron oach trawldiscloso a furthor split of the subpopulations into still smaller, indivisiblogroups - "olooentary populations". Despite the absence of any {Seographicalisolation, these groupings actually differ in respect of frequoncy of bloodgroups. Such an isolation has a biological character due to the fact thatanchovy spawning is tine-consuning.

We stlggest that Dr. Naevdal's data on the frequency distribution ofhaeoo{Slobin and transferrin alleles in sprats, from which'no marked geographicaltrond could be discovered and in sone casos great differences were found amonssanpIes fron adjaoont areas" (1968, p.178), could be oxplained by postulatingthat the said cipecies possesses the SD.rn.e "elemontary populations" as tho D.nchovy.

Our data indicate that elonentary fish populations play an importantrole in the differentiation and integration of the species gene pool. On theone hand, these populations support the entity of self-sustaining races, andon the other, stimulato gene exchange between then.

Conclusion

We have scrutinized sone recent physiologo-biochemical studios of S07ietauthors on tho probIen of intraspecific differentiation of marine fish.Although tlle results of all the worko are the same, that is, differences werefound unon{S tho compared populations, the evaluation of the character of theform of divorgence is, however, far fron being sinple in overy respect. Thus,wheroas the differences in CT, determined ao the opecies cytophysiologicalcharacter of poikilothermal aninals may indicate ovolutionary changes, thedifference in blood group froquencioo or certain proteins with a non-highdecrree of species specificity merely attest {Srouping isolation. To prove thoevolutionary significance of such variability, a complex, i.e., composite~pproach, adequate to the conplicated probIen of speciation io essential.

Thus, two approaches appear valid for solving the probleo of intra­spocific differentiation of fish, nanely, (1) the evolutionary-taxonomicaland (2) genetico-populational. Strictly speaking, they naturallY'cannot beopposed to each other since the second trend is a new edition of the oldichthyological "race" probIen, beginning with Hein·cke. At the SD.rn.e tine, theanalysis of the {Senetico-populational structure of fish species is aseparateprovince for research. We still cannot always assess the evolutionarysignificnnce of population divergence by gene frequency. Nevertheless, thoreco{Snition and identification of such {Sroupingo io extronoly essential forunderstanding the poculiarities of species biology and consoquently, forelaborating the scientific foundations of rational fishery.

In this line, the results of ancho\7 inmunological studies deserveattention, since the fish in question cloarly show t''10 types cf intraspeci::i.cgroupings, differin{S in {Sene frequoncy. Firstly, "races" strietly oustainedwithin the reopective {Senorations and oecondly, lass resistant, but actunllye'lCisting "elenentary populations", in all probability, fornally eorrespondj.ngto Mendolian populations,rnthonatieally postulated by S. vTright (1931). Succintraspocific differentiation beeoIJes elear only with sufficiently detailoä.study of the variability of gene frequeney in time and spaee. An analysis ofrando~ sanpIes nay lead to erroneous conelusions on the character of thegenetie differentiation of the respeetive speeies.

The probIens of populational structure and evolutionary significaneeof fish biochooical polynorphisD have under{Sone further detailed scrutinyin our reeent publieations (Altukhov, 1969; Altukhov ~ alia, 1969b).

AcknouledgeIJe.:.!!i

I 'Icnt to express ny gratitude to Miss W. de Ligny for infornationconcernin~ her interesting data on the blood groups of herring, und alsofor other cODDunications in this fiold.

1965b

•

•

Aleev, Yu. G.

Aleev, Yu. G.

Aleev, Yu. G.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P.

Altukhov, Yu. P., &Apekin, V.S.

Altukhov, Yu. P., &Mikhalev, Yu. A.

- 6 -

References

1956 "On the systematic position of the horse mackerelof the Black Sea". Voprosy ikhtyologii,1:114-185.

1951 "Horse mackerel (Trachurus) of the seas of theU.S.S.R.". Trudy Sevastopol.Biol.Stantsii,2:161-242. .

1959 "On spawning of the Black Sea horse mackerel ofsouthern local stocks in the northern area of theBlack Sea". Ibid., 12:211-285.

19620. "A study of the thermostability of isolatedmuscles of "Iarge" and "small" horse mackerelfrom the Black Sea". Cytology, U.S.S.R.,.1: (1)12-13.

1962b "A study of the thermostability of isolatedmuscles of "large" and "small" Black Sea horsemackere1 and a serological analysis of the

·same". Trudy Karadag.Biol.Stantsii, 18:3-16.

19630. "Seasonal changes in thermostability of theisolated muscle tissue of horse mackerel fromthe Black Sea". Cytology, U.S.S.R., 2,:(2) 241­243.

1963b "Cytophysiological analysis of the distributionof young "Iarge" horse mackerel in the northernand eastern areas of the Blo.ck Sea". J.zool.,U.S.S.R., ~:(4)586-592.

19650. "Antigenic content of water-salt oxtracts fromthe normal and heated skeletal muscles of frog,Rana temporaria". Coll.: Thermostability ofanimal cells. Nauka,Moscow-Leningrad, pp. 16-81•

"Immunological analysis differentiating twospecies of frogs, Rana temporario. L. and~ridibunda PalI.". l!?.!2:..,pp.203-201.

196130 "Cytophysiological and serological analysis ofintraspecies differentiation of the Black Seahorse mackereI". In: The Coll and EnvironmcntalTemperature. Ed. by Troshin.356-360. PergamonPress, Oxford.

1961b "A study of the thermostability of isolatcdmuscle tissue in two species of horse mackerelfrom the B1ack and North Seas". Dok1.Akad.NaukSSSR,112:(2)461-469.

1969 "Immunogenetical approach to the probIen ofintraspecific differentiation in fish". Coll:Advances in modern genetics. Nauka, Moscow,pp.161-195.

1963 "Serologico.l analysis of "Iarge" and "small"horse nackerel from the Black Sea". Voprosyikht,yologii,i:(1)39-51.

1964 "Differences in otoliths of thc Black Sea "largc"and "small" horse mackcrel". In Coll: VoprosyFisiologii Ryb Chernogo i Asovskogo Morei,Moscow,pp.23-29.

1964• A1tukhov, Yu. P.,Apenkin, V.S., &Limansky, V.V.

A1tukhov, Yu. P" &G1ushankova, M. A.

A1tukhov, Yu. P.,Nefyodov, G. N., &Payusova, A. N.

A1tukhov, Yu. P.,Artemjewa, K. F.,Borisowa, T. V., &Nefyodov, G. N.

- 7 -

"The basie princip1es of sero10gica1 investi­gations of intra and interspecifie different­iation in fishes". Ibid.,pp.53-71.

1966 "Thermostabi1ity of iso1ated musc1es and ofaetomyosin in some speeies of the Azov Gobius".Cyto10gy, U.S.S.R.,8=(4)516-519.

1967a "A eytophysio10giea1 analysis of divergeneebetween Sebastes marinus Linne and~. mente11aTravin from the Northwest At1antie". In Co11:Variabi1ity in ce11u1ar heat resistanee ofanima1s in ontogenesis and phy10genesis.Leningrad,pp-82-98.

1967b "Immuno10gica1 analysis of serum proteins ofredfish (genus Sebastes) in conneetion withmaturation". ICNAF Res.Doc.,67/47:1-9.

•A1tukhov, Yu. P., &Nefyodov, G. H.

1967 "11. study of b100d serum protein composition byagar-ge1 e1eetrophoresis in marinus and mente11~

types of redfish". ICNAF Res.Doe.,67/52:1-9 •

A1tukhov, Yu. P.,Nefyodov, G. N., &Payusova, fl. N.

A1tukhov, Yu. P.,Truvo11er, K. fl.,Zenkin, V. S., &G1adkova, N. S.

fl1tukhov, Yu. P., &Ratkin, E. V.

A1tukhov, Yu. P.,Limansky, V. V.,Payusova, A. N., &Truve11or, K. A.

A1tukhov, Yu. P.,Limansky, V. V.,Payucova, A. N., &Truvo11er, K. fl.

Andrijashev, A. P.,

Cushing, J. E.

Fujino, K., &Kang, T.

Fujino, K., &Kang, T.

G1ushankova, M. fl.

1967e "Thermostabi1ity of iso1ated musc1e tissue indetermining the taxonomie relationship of thomarinus and mente11a types of redfish, SebasteR".ICNAF Res.Doc.,67/48:1-14.

1968 "The A-system of b100d groups in At1anticherring (C1upea harengus L.)". G,.anetics, U. S. S.R. ,.4= (2)155-167.

1968 "fl study of genotypie foundations of the indi­vidual variabi1ity in thermostabi1ity of iso1atedce11s". Cyto1ogy, U.S.S.R., 10:(12)1546-1554.

19690. "Immunogenetica1 analysis of intraspeeiesdifferentiation of the European anchovy from theB1ack and Azov Seas. I. The b100d groups and .possib1e meehanism of genic contro1. The diversityof the Azov race". Geneties, U.S.S.R.,6:(4)50-64.

1969b "Immunogenetiea1 analysis of intraspeciesdifferentiation of European anchovy from theB1ack and Azov seas. II. IE1ementary populations'of anchovy and its p1ace in genetico-popu1at5.onaJ.structure of speeies". lli.i!.., .§.:(5)265-278.

1954 "The fishes of northern seas of the U.S.S.R".Moseow-Leningrad~

1964 "Thob1ood groups of marine anima1s". In: Adv.in Mar.Bio1.,2:85-131.

19680. "Serum esterasegroups of Pacifie and At1antietunas". Copeia,1968, 1:56-63.

1968b "Tro.nsferrin groups of tunos" • Genetics, 59: 79-91.

1963 "Examination of the thermostabi1ity of o.cto­myosin preparations and the iodino number ofiso1atod lipids in Trachurus meditorraneusfrom the B1o.ck Sea". Cyto1ogy; lI.S.S.R.,2.: (2)244-246.

•

•

Golovko, N. T.

Hubby, J. L., &Throckmorton, H. H.

Kotthaus, A.

Kusakina, A. A.

Kusakina, A. A.

Ligny, '1;1. de

Ligny, '1;1. do

Limansky, V. V.

Limanksy, V. V.

Marr, J. C., &Sprague, L. 1'1.

Nrevdal, G.

Nefyodov, G. N.

Numann, '<f.

O'Rourke, F. J.

Schaoffer, H.

1964

1968

1961

1959

1960

1968

1962

1965

1961

1963

1968

1968

1969.

1956

1961

1961

- 8 -

"An electrophoretical study of blood serumproteins composition by "large" and "small"forms of mackerel from the North Soa". In Col1:Voprosy Fisiologii Ryb Tschernogo i AzovskogoMorei. Moscow,pp.13-94.

"Protein differences in Drosonhila. IV. A studyof sibling species" • .fun.Nat.,102:(925)193-205.

"Contribution to the race problem of rodfish".Rapp.P.-v.Reun.Cons.perm.int.Explor.Mer,150:43-44.

"Cytophysiological analysis of tho muscle tiscueat tho heterosis for some interspecies hybridsof fishes". Cytology, U.S.S.R., 1:(I)111-120.

"Thermostability of the musculaturc of someforms of thc Atlantic salmon and taimen".Voprosy cytologii i protistologii, Moscow­Leningrad,pp.l01-111.

"Polymorphism of plasma esterases in flounderand plaice". Gen.Res., .!!,:119-182.

"Contribution to the serology of marine fish".Contr.8th Conf.Eur.Soc.Anim.Bloodgroups,Llubljana.

"Difforences in erythrocytes antigens of the"largo" and"small" forms of horse mackerel fromthe Black Sea". Voprosy iYJltiologii,5:695-691.

"A study of serum agglutinins of the horsemackerel from tho North Sea and western coast ofAfrica". In Coll: 11etabolism and Biochemistryof Fishes. Moscow,pp.308-310.

"The use of blood group characteristics instudying subpopulations of fishes". ICNAF Spcc.PubI., 4:308-313.

"Genetic diversity in spawning cod alona thcNorwegian coast". Hereditas, 60:1-32.

"Studies on hemoglobins and serum protcins insprats from Norwegian waters". FiskDir. Skr. SD:'~.

Havunders.,1!:160-182.

"Serum haptobglobins of redfish (genus Seb~Qt9J2.)11.

Vestnik Moskovskogo Universiteta, BioloGi~.

1:,:104-101.

"Biologische Untersuchungen über die stockerdes Bosporus, des Bohw~zQn~eeres und derHarmara". Istanbul Universitesi Fon Fah.'"Ultes.iHidrobiol. Arastirma Enstitusu Layiniarindan,i: (I)3-41.

"An immunological and chromatographic'study ofSebastes marinus and Sebastes mentella". Rapp.P.-v.R6un.Cons.perm.int.Explor.Mer, 150:104-110.

"11. biochemical contribution to the redfishproblem". Rapp.P.-v.Reun.Cons.perm.int.Ex~lor.

Mer, 150:104-110.

•Siek, K.

Siek, K.

Siek, K.

Sindermann, C. J.

1961

1965a

1965b

1964

- 9 -

"Haemog1obin polymorphism in fishes". Nature,192:(4805)894-896.

"Haemoglobin polymorphism of cod in the BaJ.ticand the Danish Be1t Sea". Hereditas, 54,:19-48.

"Haemoglobin polymorphism of cod in the UorthSea and the North Atlantic Ocean". Ibid.,.2!:49-73.

"Immunogenetic and biochemical approach to theidentification of marine subpopulations". Occ.Publ.Grad.Sch.Oceanogr.,Univ.Rhode Island,~: 33-38.

Sindermann, C. J., 1959& Mairs, D. F.

Slastenenko, E. P. 1965

e Suzuki, A. 1967

Tibbo, S. N. 1965

Travin, V. I. 1951

"A major blood groups system in At1antic herring".Copeia, 1959, 2:228-232.

"The species composition of genus Trachuru~ inthe Black Sea". Rapp.p.-v.Reun.Com.int.Explor.Sci.Mer Med., 18:(2)269-272.

"Blood types of fishll .Bu11.Jap.Soc.Sci.Fish,2.2.: (4) 372-381.

lIReport of subcommittee on herring and otherpe1agic species". ICNAF Redbook, 1965, 24.

"A new species of redfish in the Barents Soc.(Sebastes mentella Travin sp. nov.)n. DokladyAkademii Nauk U.S.S.R., 77:741-744.

Ushakov, B. P.

Ushakov, B. P.

Ushakov, B. P.

Ushakov, B. P.

Ushakov, B. P.,Amosova, I.,Pashkova, I., &Chernokozheva, I.

Ushakov, V. B.

Ushakov, V. B.

\vright, S.

Zakharov, G. P.

19590.

1959b

1964

1967.

1967

1963

1965

1931

1962

llPhysiology of cell and problem of species inzoologyll. Cytology, U.S.S.R., I:(5)541-566.

llThermostability of the tissues as the criterionof species of poikilotherma1 anima1s". J.Zoo1.U.S.S.R., 38:(9)1292-1302.

"Thermostabi1ity of cel1s and proteins ofpoikilotherms and its significance in speciation".Physiol.Rev.,44:(3)518-560.

"Thermostability of cells and protoplasmaticproteins in poiki1otherma1 anina1s in relationto the problem of species ll • In: The Cell andEnvironmental temperature. Ed. by Troshin.322-334. Permagon Press, Oxford.

llQuantitative evaluation of individual variabilityin the hdat resistances of ce11s and theircontractile models". J.Exp.Zool., 16~:381-390.

"A possibile cause of the thermal death ofske1etal museIe". Cyto1ogy, U.S.S.R.,5:(2)204-211.

"The thermostability of excitab1e and contracti1esystems of a museIe fibre ll • In Co11.: Eeatresistanco of cells of animals. Moscow-Leningrad,.pp.55-60.

"Evolution in Mendelian populations". Genetics,16:(2)97-159."On biology of the West Greenland Sebastesmarinus". In Coll.:Sovetsk.Rybokhoz.issledovan. vsevero-zapadnoi tschasty Atlantitscheskogo okcana,Moscow, pp.319-330.