FISHERIES RESEARCH BOARD OF CANADA
Translation Series No. 2882
Carotenoid pigments and the Taxonomic Status of Salmonids
by A. A. YarZhombek
Original title: Karotinoidnye pigmenty i sistematika lososevykh ryb
From: Trudy Vsesoyuznogo Nauchno-Issledovatel!skogo Instituta Morskogo Rybnogo Khozyaistva i Okeanografii (VNIRO) (Proceedings of the Ali-Union Research Institute of Marine Fisheries and Oceanography), 85(3) : 148-153, 1972
Translated by the Translation Bureau(YK5 Multilingual Services Division Department of the Secretary of State of Canada
Department .of the Environment 'Fisheries Research Board of Canada Biological Station, St. Johns, Nfld. BiOlogical Station, Nanaimo, , Bi.C. 1974
12 pages typescript' • d s
• DEPARTMENT OF THE SECRETARY OF STATE SECRÉTARIAT D'ÉTAT
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TITLE IN ENGLISH - TITRE ANGLAIS Carotenoid pigments and the Taxonomic Status of Salmonids
TITLE IN FOREIGN LANGUAGE (TRANSLITERATE FOREIGN CHARACTERS) TITRE EN LANGUE ÉTRANGÉRE (TRANSCRIRE EN CARACTàRES ROMAINS) Karotinoidnye pigmenty i sistematika lososevykh ryb.
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Trudy VNIRO
REFERENCE IN ENGLISH - RÉFÉRENCE EN ANGLAIS Publications of the A11-Union Scientific Research Institute of Marine Fisheries and Oceanography
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Trudy VNIRO (Publications of the All-Union Scientific Research Institute of Marine Fisheries and Oceanography), Vol. 85, No. 3, 1972, pp 148-153 (USSR)
Carotenoid Pigments and the Taxonomic Status
UNED:r.D TRANUATION of Salmonids For inforrnaion or,ly by A.A. Yarzhombek TRADUCTION NON R.VISEE UDC (597.08:001.8)+597-13 Inforrnafion soukwaclit The pigmentation of the external integuments is an important
taxonomie characteristic. Certain phyla of fishes have tissues with
specific pigmentations, e.g., in the bones of needlefishes there is
an accumulation of derivatives of biliary pigments; the liver of
certain percidae concentrates the red carotenoid pigment; many fishes
accumulate specific carotenoids, pterins, and melanins in their skin;
the majority of fishes concentrate carotenoids in the roe. •The salmonids
are characterized by an intense carotenoid pigmentation of their muscles.
The qualitative composition of carotenoid pigments of muscles,
ovaries and skin of salmonids has been investigated thoroughly by Steven
(1948), Loginova (1966), Bayley (1937), and Kanemitsu and Aoe (1958).
While working on the metabolism of carotenoid pigments of salmonids
(Yarzhombek, 1964, 1966 and 1970) this author has accumulated material
on the qualitative composition of pigments of a number of salmonids of
Europe, Asia and North America. In this article an attempt has been
made to compare the pigmentation of various tissues of salmonids and.
the existing taxonomie classification of these fishes. The author was
SOS-.200-10-31
75AD-714120-5332 interested in knowing the order of importance in taxonomy that would
correspond to the differentiation in pigmentation.
Salmonids belonging to four different genera were investigated:
Sakhalin taimen (Hucho perryi(Brevoort); Siberian char (Salvelinus leuco- maenis (Vallas), both the non- and diadromous; Dolly Varden char (S. malma (Walbaum), non- and diadromous; Atlantic salmon from the Kola
Peninsula and Baltic Sea (Salmo salar) (L.); salmon from the Kura River
(S. trutta caspius) (Kessler); rainbow trout (S. irideus (Gibbons);
mikizha (S. mykiss (Walbaum); Kamchatka trout (S. penshinensis (Pallas);
cutthroat trout S.clarkii (Richardson); steelhead (S. gairdnerii (Richard-
son); Sevan trout (S.ischchan (Kessler); pink salmon (Oncorhynchus gor-
buscha (Walbaum); chum (O. keta (Walbaum); coho (O. kisutsch (Walbaum);
sockeye,.anadromous and residual (O. nerka (Walbaum); chinook salmon
(O. tschawytsha) (Walbaum) and masu (O. masou) (Brevoort).
The qualitative composition of the carotenoids of skin, muscles,
and roe was determined by the method of Kanemitsu and Aoe (Kanemitsu, Aoe, 1958).
Pigments were identified by means of absorption spectra. The presence
and configuration of pigment cells in the skin were determined by
microscopic observation.
The skin of salmonids contains two types of lipophores (erythrophores
and xanthophores) and non-lipophoric pigment granules. Xanthophores are
encountered in the skins of all investigated genera in all stages of the
post-embryonal development. Erythrophores and non-erythrophoric pigment
granules, however, are not found in all species,nor in all stages of
ontogenesis. Xanthophores are'distributed on the skin surface in a fairly
manner, while the erythrfdiJhdeàand pigment granules can be dis- unifàrm . i„, tributed in various ways (Table1).,,,Thered pigment of the erythrophores
and pigment granules is invariablrepre?,sented by astaxanthin. 3.
1 • T a 6 .1 H Ix a 1 1 2. Haatme KpacHoro narmeHra Hoxe +1000Ceklb1X pt:46 3. Ileptio,i 6. 7. 4. BHA 5p11.16- nepe- 8,11oxamnatutti Hpacuoro mirbtewra tdopcKoil 1■013b1r1 • CTOBbirt 1 1-1 r.". 9 • Taftmenb +10 • glickbraHo pacnonœKemibte 3pirrpo- gtopu Ha Te.le R neatnut(ax 11.% abm a +12. 3pHTpo4topb4, pacnono)KeHHue 1113T- 'label H ,,Uttqt4ty3tio paa6pocannue izoaz,e u rutantetHax 13-1
31. nitnNtettanne. — eeTb Epacubni nurNteHT, —EpaCHblr1 11H1-1.1eHT Œrcyr- neyer 4."
1 - Table 1
2 - Presence of red pigment in the skin of salmonids 3 - Development stage 4 - Species 5 - Fry 6 - Sea 7 - Spawning 8 - Location of the red pigment 9 - Taimen 10 - Erythrophores distributed diffusely on body and fins 11 - Dolly Varden char 12 - Erythrophores, in spots and distributed diffusely in skin and fins 13 - Siberian char 14 - Same 15 - Atlantic salmon 16 - Salmon from Kura River 17 - Sevan trout 18 - Mikizha 19 - Concentration of erythrophores along lateral lines and on fins 20 - Kamchatka trout 21 - Rainbow trout 22 - Cutthroat trout 23 - Steelhead 24 - Coho 25 - Zones of pigment granules and erythrophores on the sides and fins 26 - Sockeye 27 - Masu 28 - Chum 29 - Pink salmon 30 - Concentration of erythrophores in form of red spots on the sides (according to data of 1962) 31 - Note: + and - denote presence and absence of red pigment, res41 pectively. 5.
• 1. T a 6a ta .2 2. KCaliT04314,111.1 uWWfl 11 11à44t14..ItTOK IPC0Ce3i4X
4, .mmtuubJ 5. 9Ancioericit 8. 8. 7 . 3. BHA 6 .3ea- 7. acsa- sea- Creta- ..tareitit Kl TeH II KC 8 h All KC8811111 KC 8 H TA H 11(CO Hill H
12. rartmein -r -4-
■■■ ■ ••■■•■ _ • •• •-• 13. Maisbua • 14. KyiwKa 4.
15. Mitxtinu ••••••••■ . + 16. (Dopeab 17. cea. aticxan - ._... •-,-* - 4- • 4* . 18. P.343moian --i- 4. • 19. KAaPKii _i_** • ..._._ ...1. i...•,., • 20. 6ypan ...... -4- 21. Itococb ..1._••••■ 22 craribnoroao. ablA 23. Kypiincioth •t- l• -4: 24. 45aernficxliA
25. KOJI bCKH /I 26. Cemrsa
■ ■ 27. hant,ocast ..1 ••• • • 28, xamvarce(an 29. ropbywa ■•■••••• 1- 30. Kera •••••■••• +
31. 1(11)firt + •••••••• 32. HePKa • 33. Oima i- 34, liaawm +
35 • • no.no6en.,m .eteunie. nozytienbi ratone normiosa (lee). 36. " .aatemde erteetut (Steven, 1 948). 37. ••• ,flannut BeA.an (Bailey, 19 38 ,•••• notto-61nde Raionie nanygenbi Tax.mte Kotiennny n AO, (Kapelnitut, 6.
1 - Table 2 2 - Xanthophyls of the muscles and egg cells of salmonidae 3 - Species 4 - Muscles 5 - Egg cells 6 - Zeaxanthin 7 - Lutein 8 - Astaxanthin 12 - Taimen 13 - Dolly Varden char 14 - Siberian char 15 - Mikizha 16 - Trout 17 - Sevan 18 - Rainbow 19 - Cutthroat 20 - Brown 21 - Salmon 22 - Steelhead 23 - From Kura River 24 - From Baltic Sea 25 - From Kola Peninsula 26 - Atlantic salmon 27 - From Kola Peninsula 2a - From Kamchatka 29 - Pink salmon 30 - Chum 31 - Coho 32 -' Sockeye 33 - Masu 34 - Chinook salmon 35 - Similar data were also obtained by Loginova (1966). 36 - Data of Steven (1948) 37 - Data of Bailey (1938) 38 - Similar data'were also obtained by Kanemitsu and Aoe (1958). o
7.
1. Ta6swas 3 2 • 1161zaa, nogemba tJI4 epopmw c pasurroirous tamer« pacnpeighestm Epacuoro ruarmeirra s KOMO y hococechtx parsinax ppAos
4. THu unmet-men 3 .pox 2 3 I 4
Hach() Salvelitius Sahli° Oncorilynchus
1 - Table 3
2 - Species, subspecies, or forms of various genera of salmonidae showing different types of distribution of red pigment.on skin.
3 - Genus
4 - Type of pigmentation
In the muscles and egg cells of the salmonidae, one finds three carotenoids of the pigment xanthophyl: astaxanthin, lutein and zeaxanthin.
Astaxanthin is present in the muscles of all fish species that were in- vestigated. Lutein or zeaxanthin can also be present. The qualitative composition of pigments of muscles and egg cells is usually the same
(Table 2).
The various types of distribution of the red pigment on the surface of the body can be divided into four categories (Table 3).
1. The pigment is concentrated in erythrophores, which are dis- tributed diffusely over sizeable segments of the skin and fins (juveniles of coho, fingerlings of sockeye, chars, trouts, taimen, i.e., the re- presentatives of all genera investigated): This type of pigmentation can occur in combination with other types.
2. The pigment is concentrated in erythrophores which conglomerate in round or oval formations of the size of a fish's eye or smaller (chars, 8.
Atlantic salmon, trout, and the Japanese endemic O. rhodurus).
j. The pigment is concentrated in erythrophores whicil group themselves along the lateral line (Pacific representatives of the genus
Salmo, or according to Vladykov, Parasalmo), and also the spawning dwarf sockeye from Lake Dal t nii in Kamchatka).
4. The pigment is concentrated in red zones, which are formed as a result of conglomerations of erythrophores and non-lipophoric pig- ment granules (representatives of the genus Oncorynchis, during the spawning period - breeding colours).
The representatives of the genus of the Pacific salmons exhibit all four types of pigmentation. The first type is encountered in the juveniles of sockeye and coho; the second, in the land-locked O. rhodurus; the third, in spawners of residual sockeye, and the fourth, in most species of this genus, during the spawning period. The representatives of the Atlantic salmon have three types of pigmentation: those originating from the Atlantic Ocean have the first and the second types, while the ones from the Pacific exhibit the first and the third. Chars have two types - the first and the second, while taimen has only the first one.
The presence of the same type of pigmentation on the members of different genera cannot be explained by convergence, since it would have to be assumed that identical mutations took place in the genetic systems of different populations at different times, which is highly unlikely. It is more likely that a characteristic, inherent in representatives of two or more different genera, indicates the Presence of a common ancestor, who possessed such a characteristic. All four genera have in common the first type of pigmentation, which is, possibly, a characteristic of their common 9. ancestor. All genera, with the exception of the taimens, share also the presence of the second type of pigmentation, i.e., the chars and the Atlantic and Pacific salmons could have had a common ancestor only after the taimens had established themselves as a reproductively isolated group. The Atlantic and Pacific salmons could only have had a common ancestor "younger" than the genus of chars, since the latter do not exhibit the third type of pigmentation, shared by the two former. The fourth type of pigmentation is encountered only in the genus of Pacific salmons, which compels us to place them at the top of the evolutionary ladder of the investigated group. Such conclusions are shared also by
Norden (1961) and Rownsefell (1962).
Examination of the composition of pigments of roe and muscle tissues leads also to some interesting generalizaiions. Interesting, because the controversial questions of the taxonomy of salmonidae in some cases concern fishes with various pigment composition. This applies, in particular, to the genus of Atlantic salmon.
1. The roe of the Baltic salmon contains two pigments, while that of the Kola salmon has only one. Both are now classified as belong- ing to the same species.
2. The roe and muscles of the rainbow trout (freshwater) contain two pigments, those of the steelhead (diadramous) have only one. Amrican research workers (Vladykow, 1963) consider both these fishes to be subspecies of one and the same species.
3. Kamchatka trout contains in its muscles and roe only astaxanthin, while the muscles of mikizha contain also zeaxanthin. There is evidence that both these fishes belong to the same species (Savvantova, Lebedev, 1966). 10.
4. Morphologically the Sevan trout does not differ from the
brook trout any more than it does from the trouts of other water basins
(Vladimirov, 1948). Both species have two pigments in their muscles
and roe - yellow and red. However, the yellow pigment of the brook trout
is lutein, and that of the Sevan trout is zeaxanthin.
To sum it up, then, differing pigmentations can be encountered
in fishes of the same species, but in all such cases the fishes belong
to different populations. One should keep in mind that criteria of
species are very conditional. Reliable morphological differences, differ-
ences in mode of life, even differences in the number of chromosomes are
often insufficient evidence for establishing independent species (Dorofeeva,
1965). Also this author does not consider differences in pigmentation of
• muscles and egg cells to be a basis for separation of taxonomic units, in
spite of the exceptional consistency of this ctiterion. Yet, it is to be
assumed that differences in pigmentation of muscles and egg cells indicate
the presence of a reproductive isolation among the investigated populations.
Spontaneous mutations resulting in changes in pigmentation are encountered
in nature, although not frequently. "Chromides" of the Caspian herring,
carp family, whitefishes, graylings, etc. are known. Specimens even of
'cod and pollock are encountered that have red meat like that of salmon
(Baalsrood). Whether of adaptive significance or not these mutations form
alleles that, as a result of automatic genetic processes and selection, may
become dominant in an individual population, form subspecies, species, and
even genus. The set of genes determining the qualitative composition of the
carotenoid pigments of muscles and ovaries has best chances of succeeding
when the composition of the carotenoids of the food is similar to the one
that is programmed into the genotype. For instance, the Pacific salmon and
the diadromous Atlantic salmon take in with their food a large quantity of 11. the red pigment of crustaceans - astaxanthin, and it is the accumiilption of this very pigment that is the most beneficial for them. Thé freshwatèr trout and chars feed to a considerable extent on molluscs and insects rich in yellow pigments, which corresponds to their genetic program.
Conclusions
1. The carotenoid pigmentation of the external integuments of the salmonidae changes in the course of their life cycle and is also dependent on their physiological state, mode of life and feeding, while being specific to each species. Different species and even genera have similar pigmentation features. This, however, should not be interpreted as a sign of convergence, but rather as a preservation of ancestral features.
2. Differences in the qualitative composition of carotenoid pigments of muscles and roe indicate reproductive isolation of populations.
3. Based on the distribution of the red pigment on the skin of salmonidae of different genera, the following conclusion has been made with regard to the chronological order in which these genera were established:
1 - taimen, 2 - chars, 3 - Atlantic salmon, 4 - Pacific salmon.
Bibliography
1. Vladimirov, V.I., The brook trout of Armenia and its relation to other members of the genus Salmo. Trudy Sevan. gidr. st ., vol. 10, 1948.
2. Dorofeeva, E.A., Karyological bases for the taxonomic positions of the Caspian and Black Sea salmons (Salmo trutta caspius (Kessler) and
S. trutta labrax (Pallas). "Vopr. ikhtiologii", vol. 5, No. 1, (34), 1965.
3. Loginova, T.A., The carotenoids of the rainbow trout. Pro- ceedings of the All-Union conference on the ecological physiology of fish. 1966.
4. Savvantova K.A., Lebedev, V.D., The taxonomic position of
12.
Kamchatka salmon S. penshynensis (Pallas) and mikizha S. mykiss (Walbaum)
and their relationship with the American members of the genus Salmo. "Vopr. ixhtiolog.", vol.6, No. 4 (41), 1966.
5. -Yarzhombek, A.A. Carotenoids and trout breeding. Coi. ONTI VNIRO., No. 6, 1964.
6. Yarzhombek, A.A., Dynamics of fats and carotenoid pigments of the gonads of Pacific salmon, "Vopr. ikhtiolog.", vol.6, No. 1, 1966.
7. Yarzhombek, A.A., The carotenoids of salmonidae and their
connection with the reproduction of these fishes Trudy VNIRO. vol. 59, 1970.
•' Boaanmupoo B. IL Pylibeaan cl3ope.ab Apmennii n ee ontomenne K.apyrnm npe,acrainvreasim pona Salmo. Tpy.abi Cenatt. limp. CT. T. X, 1948. Ropo (1) eena E. A. Kapno.-formiectote «loci-foramina nononcentin xacrutricKoro n ItepuomopcKoro aocoéefi (Salmo trutta caspius (Kessler), S. trutta labrax (Pallas). «BMW. IIXTH0.101':» T. 5. Bbm. I (34), 1965. Jlornnooa T... K..apoTationalf paRymoil flaopeinf. Bcecoloattoe coaentanue ' axorfortNeckoil (I)}uffionornit pleb TC3HCb1 ,aon.nazton, 1966. Caaaaur cilia K. A.. .11 e 6e j e a B. 21. 0 cucremartutecxom n000:Reinin Kam- ili*TCKOrl ceNtrii S. penshynensis (Pallas) n NIHK117KH S. mykiss (Walbaum) u nx naaitmo- • omonienite c amepincancatimit ripeRcrainfTemaNni pona Salmo. * Bd. Can. Vol. 18, No. 5, 1961. Rounsef f ell. G. Relationships among North American St:Imonidae. t. S. Fish N,‘ ildl. Serv. Fish. Bull. Vol. 62, No. 209, 1982. Slastenenk o, E. P. Freshwater fishes of Canada, Kiev Printers, Toronto, 1963 Steven, D. M. Carotcnoid pigmentation of trout. Nature, No. 160, London, 1947. Vladyko v, V. D. A revieu of sal:nonid genera and their broad geographycal .listribution. Trans. Roy. Soc. Canada, Ser. 4, Vol. I, Ottawa, 1963. Kanemitsu, T., A 0e, IL Studies of the carotenoids of salmon. I. Identificatiofi of the rimsde pigment. Bull. Jap. Soc. Sel. Fish., Vol. 24, No 3. 1958. CAROTENOID PIGMENTS AND THE TAXONOMIC STATUS OF: SAL MONIDS • A. A. Yarzhombek Summary • Differences in the qualitati‘e composition of c irotenoid pigments of the muscle tissue and ovocytes in the family Salmonidae can be observed at anv level of taxonomie differAces, the population le\ ,s1 included, whieh F. indicative of reproductive isolation in fish. Four distribution patterns have been found of the red pigment in the skin of salmonids. The presence or absence of these pigmentation patterns is discussed front the evolutionary point of view.