[Advances in Marine Biology] Advances in Marine Biology Volume 16 Volume 16 || Pigments of Marine Invertebrates
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Adv. Mar. Biol. Vol. 16, 1979, pp. 309-381
111. Iv. V.
VIII. IX. X.
XII. XIII. XIV. xv.
XVIII. XIX. xx.
PIGMENTS OF MARINE INVERTEBRATES
G. Y. KENNEDY
The University of Shefield, Shefield, England
Introduction . . .. . . . . .. .. .. .. Protozoa .. .. .. . . . . .. .. .. Porifera. . . . .. .. .. . . .. .. .. Coelenterata . . . . .. . . . . . . .. .. Ctenophora . . .. .. . . . . .. .. .. Platyhelmiiithes . . .. . . . . .. .. . .
B. Acanthocephala .. .. . . . . . . ..
Nemathelminthes . . . . .. . . . . . . .. A. Nematoda . . . . .. . . . . .. ..
Rotifera .. . . . . . . . . . . . . . . Nemertini . . . . . . . . . . . . . . . . Annelida, Echiuroidea, Sipunculoidea, Priapuloidea and Phoronidea
A. Crustacea .. .. .. . . . . .. .. B. Arachnida . . . . . . . . . . .. ..
Mollusca .. .. . . . . .. .. .. . .
Arthropoda .. . . . . . . . . . . . . . .
C. Myriapoda . . . . . . . . . . . . .. Chaetognatha . . . . .. . . . . .. .. . . Brachiopoda . . .. .. . . . . .. .. .. Polyzoa .. . . . . . . . . .. .. .. Echinodermata .. .. . . .. .. .. .. Pogonophora . . .. .. . . . . .. .. .. Tunicata . . . . .. . . . . . . . . .. Comment . . .. .. . . . . . . .. . . Acknowledgements . . .. * . .. . . . . . . References . . .. .. .. .. . . .. ..
309 312 314 319 326 326 329 329 331 332 332 333 336 336 342 343 343 366 356 366 367 364 364 364 366 366
" 0 Sea! Old Sea! who yet knows half Of thy wonders or thy pride? "
Gosse: Aquarium 226-227.
I. INTRODUCTION Marine plants and animals are often very brilliantly coloured,
especially those from tropical waters. Even in temperate climes many animals of the sea-shore, when viewed in quantity as in a rock pool association, present a fine sight, but in warmer waters, corals and their attendant fauna and flora provide a pageant of great beauty. Marine organisms also display many examples of pattern, an aspect discussed
309 A.P.B.-16 11
The phylogenetic tree FIG. 1. The phylogenetio tree (from Scheuer, 1973).
PIGMENTS OF MARINE INVERTEBRATES 311
in most fascinating style by the late T. A. Stephenson (1944) in his beautiful little book Sea Shore Life and Pattern.
In his stimulating article on Marine Natural Products, Thomson (1978) writes : There is no clear explanation for chemists neglect of marine products, although several contributory factors come to mind. Chief among these is the relative difficulty of collecting material which may be compounded by the problem of identification. While collecting intertidal species is easy enough, in deeper waters diving, trawling or dredging is necessary, and in some parts of the world the local marine fauna and flora have not been studied, and there is no taxonomic literature available. Sometimes there is no local expertise to hand where it might reasonably have been expected: e.g. there is no algologist in Aberdeen and only one in the whole of South Africa. Hence it is not unusual to find in the current literature interesting compounds reported from unidentified sources. Later on : Numerous marine animals are brightly coloured but little is known about the pigments.
It is true that at times the study of natural pigments has been desultory and empirical but, as we hope to show in this chapter, a good deal is known about many of them, and we owe our knowledge of many quinone pigments to Professor Thomson himself, and his school in Aberdeen.
Marion Newbigin (1898) gave three reasons why the biologist should be interested in the colours of organisms :
1. Conspicuousness of colour phenomena in an objective survey of
2. Relation of these colours to current theories of evolution ; 3. Their importance in comparative physiology.
animals and plants ;
The colours of living things are the visual result of three different processes :
1. Chemical: the metabolic formation of natural pigments, or the storage of ingested pigments, both consisting of coloured molecules which reflect and transmit parts of visible light : i.e. chemical pigments.
2. Physical: colourless structures which include laminations, striations, ridges, air bubbles, crystals, particles etc. which split light into its con- stituent colours by reflection, scattering and interference : i.e. structural colours.
3. A combination of 1 and 2. In this review, we shall consider only the chemical pigments of
marine invertebrates by a discussion of their occurrence, phylum by
312 Q. Y. KENNEDY
phylum, with some mention of their metabolism and speculation on their functions. The order of classification followed is that of the Ply- mouth Marine Fauna List of the Marine Biological Association of the United Kingdom, 1957. There is a most useful table (Table 4.1) in the book by Needham (1974) embodying The major taxa of animals in relation to their chromatology.
Their colours and their forms were then to me an appetite . . . . . . . 1 ,
Wordsworth: Lines composed a few mil@ from Tintern Abbey .
11. PROTOZOA Very little has been done on the pigments of marine Protozoa,
possibly because in many instances it is very difficult to obtain quan- tities sufficient to make a thorough chemical examination.
The amoeba Janickina (Paramoeba) pigmentifera is parasitic in the coelom of the chaetognaths Sagitta and Spadella, and contains pigments which have not yet been identified (Hyman, 1959). Several blue-green, brown, yellow and purple pigments are found in some heterotrich ciliates ; some of these are fluorescent and photodynamic. Carotenoids have also been reported.
Stentor coeruleus has been extensively studied by Tartar (1961) in a comprehensive monograph which describes some marine species :
8. multiformis is reported from salt or brackish water, and is blue- green, with pigment stripes ; S. pygmaeus with a chitinoid case is found attached to some gamma- rids in the depths of the Sea of Baikal. This has a dark pigment; S. auriculata Kent and S. auriculatus Kahl were shown by Faur6- Fremiet (1936a) to belong to the genus Condylostoma; S. acrobaticus said to be found on a branch of Fucus-reported unpigmented.
Some chemistry has been done on the pigments of Stentor and its species and relatives. The blue-green pigment of S. coeruleus, stentorin, is probably also found in S. multiformis, S. amethystinus and S. introversus. Stentorin is very similar to hypericin (the pigment from some species of Hypericum, notably St Johns Wort, H . perforatum) in fluorescence and U.V. visible absorption spectra. The pigment has the structure of a tetra-cr-hydroxynaphthodianthrone. Another pigment, stentorol, was extracted from Stentor niger by Lankester (1873), and this yellow pigment was studied by Barbier, FaurB-Fremiet and Lederer (1956) who
PIGMENTS O F MARINE INVERTEBRATES 313
isolated it as a black powder giving a red solution in chloroform and red fluorescence in U.V. light. They suggested that it was a polyhydroxy- quinone.
Zoopurpurin extracted from Blepharisma undulans by Arcichovskij (1 905) and examined fairly recently by Sevenants (1 965) is a mixture of two compounds both very similar to stentorin and hypericin, and has been the subject of further study by Giese and Grainger (1970).
It may be seen from the discussion of these pigments that investiga- tion of the ma,rine species of Stentor and its relatives might be well worth while. The function of these pigments is still unkown. They may render the animals sensitive to light or, since they are toxic to other Protozoa, they may have some protective value. It is interesting that if Stentor engulfs another Stentor, the pigment of the victim is not assimi- lated but is ejected as a green excretion vacuole.
In the Folliculinidae, which often attach themselves to mollusc shells and tunicates, Faur6-Fremiet (1936b) found green, blue and red- dish-violet pigments which may be polycyclic quinones. In the blue Folliculina ampulla, closely related to the stentors, he found many blue granules close to the macronucleus. Another heterotrich Fabera salina, found in salt works in France and saline pools in Russia, Rumania and California, contains a dark pigment which, when extracted, is purple-red with a fine red fluorescence in U.V. (Fontaine, 1934). The yellow-green solution in pyridine gives absorption bands at 612 and 566 nm, and it has been suggested that this is also a polycyclic quinone.
Although the hypotrich ciliate Holosticha rubra (previously known as Kernopsis rubra) found in aquarium tanks at the Plymouth Labora- tory obviously invites investigation, nothing is known about its pig- ment ; there is also a yellowish variety H . rubra var. Jlava.
Some Protozoa require pterins, principally biopterin and neopterin, as co-enzymes for some redox systems (Kidder, 1967) and others need pteroylglutamic acid (Kaufman, 1967).
The hermit crab Eupagurus prideauxii is parasitized by ciliates Polyspira spp. and Gymnodioides spp., which take up blue caroteno- proteins from the host. The carotenoid is split off from the protein by digestion in the food vacuole and is attached to another protein, pro- ducing a new carotenoprotein which imparts a violet-red colour, or even blue or green, to the ciliate. This pigment is passed on to the daughter cells in fission. In similar vein, the copepod Idyafurcata contains a blue carotenoprotein in epidermis and retina, and a deep orange carotenolipo- protein in the blood and eggs. The parasitic ciliate Spirophrya takes up these pigments and reconstitutes them after digestion, to become pig- mented itself.
314 Q. Y. EBNNEDY
There is an unidentified ethanol-soluble red pigment in cytoplasmic granules in the foraminiferan Myxotheca arenilega-probably a caro- tenoid derived from the crustaceans on which it feeds. Newbigin (1898) drew attention to this pigment, and also to some species of the rhizopod Globigerina, which were described by Agassiz (1888) in his account of the cruise of the Blake, as " floating scarlet masses on the surface of the sea."
Radiolarians often have a pigmented body, the phaeodium, which suggests a brown colour.
It is well known that the protozoans Noctiluca miliaris and Pyro- cystis noctiluca have great powers of phosphorescence, produced from minute granules of the system :
luciferase Luciferin + oxygen - oxyluciferin + water + light
Less well known is the pink colour of Noctiluca which " may be thrown upon the shore in such numbers as to form a coloured layer along the beach, the shore water resembling thick tomato soup " (Russell and Yonge, 1975). The identity of this pigment is unkown, but it is likely to be a form of oxyluciferin. The luciferins of known structure are heterocyclic chain-linked molecules whose colours, in their oxidized forms, may range from yellow through red to purple.
The protozoan Opalina ranarum, parasitic in the intestine of frogs, does not fall within the marine category, but is mentioned because of its unique green pigmentation by biliverdin from the bile of the host. Another protozoan, Nassula, has a blue pigment which is probably derived from the Oscillatoria of the food.
Nusslin (1884) described a beautiful violet pigment in Zoonomyxa violacea from the Herrenwieser Lake. The protoplasm is filled with many small violet vacuoles which impart a violet colour to the whole animal. Amphizonella violacea contains a granular pigment which is similar in many ways to that of Zoonomyxa.
111. PORIFERA The sponges provide many fine examples of vivid pigmentation as
well as the more sombre browns, black and grey with off-white. The lipid-soluble nature of some of the yellow and red pigments of sponges was described by Krukenberg in 1880-1882 (see Krukenberg, 1882). MacMunn (1883, 1890) examined Halichondria albescens, Halma buck- lanai and Leuconia gossei and found " lipochromes '' giving one strong absorption band in his simple spectroscope. The pigments producing the most vivid coloration of sponges are predominantly carotenoids
PIGMENTS OF MARINE INVERTEBRATES 316
(Figs. 2, 3, 4), with a preponderance of carotenes over xanthophylls, but there are instances of the occurrence of other types of pigment.
Lonnberg (1931, 1932, 1933) examined many sponges (among other marine animals) for carotenoids, but his studies were not sufficiently
FIG. 2. Structures of some cmotenoids.
complete to enable the pigments in his extracts to be characterized; this is a great misfortune, considering the amount of work done. None of the absorption spectra given by Lonnberg are near enough to the accepted maxima of authentic carotenoids to identify his pigments. However, because of the striking coloration of many sponges, their
316 0. Y. KENNEDY
FIG. 3. Structures of carotenoids.
availability in quantity and the continuing active interest in carotenoids coupled with well-developed analytical methods, much of the work of Lonnberg has been repeated and extended.
Astacene (Fig. 3) was isolated and crystallized from the red " cocks- comb " Axinella crista-gulli by Karrer and Solmssen (1935) (but see later discussion on astacene). Lederer (1938), working with Suberites domuncula and Ficulina $GUS, reported that all the carotenoids in his extracts were epiphasic, even after saponification, and maintained that the pigments present were torulene (as in the red yeast Torula rubra), lycopene (Fig. 2) (as in the epidermis of the fruits of the tomato) and
CH CH, v CH, CH, / \
CH, '\ / /"\ I CH, C ~ C I I - C H ~ C - C H C H - C H ~ C - C H C H - C f i C H ~ C ~ C H - C H C H - C ~ C H - C 1 I ~ C CH,
HOCH I 11 C.CH, I1,C.k AHOF
I I1 BOCH C.Ct1,
Xant hophyll H&.d (!HOE
FIG, 4. Structures of carotenoids.
PIGMENTS OF MARINE INVERTEBRATES 317
a-, /3- and y-carotenes (Fig. 2) with a small fraction of xanthophyll (Fig. 4) in Ficulina only. A propos this report of torulene by Lederer, Fox, Updegraff and Novelli (1 944) often encountered this carotenoid in deep marine muds, and they suggested that the sponges which Lederer had examined may have ingested numbers of red Torula species known to occur in the sea (ZoBell, 1946.) If this is true, it seems odd that torulene has not been found in other detritus feeders, although of course there are isolated cases of specific retention of carotenoids and other pigments by marine animals.
Drumm and OConnor (1940) and Drumm, OConnor and Renouf (1 945) isolated and crystallized echinenone (4-keto-fi-carotene) from Hymeniacidon perleve ( = Hymeniacidon sanguinea) and also detected a-carotene in traces. Lederer (1938) also reported a brown-orange carotenoprotein in Ficulina Jicus.
There are many papers describing carotenoids of sponges, and reference should be made to the books of Karrer and Jucker (1950), Goodwin (1952)) Fox (1953, 1976) and the short review by Goodwin ( 1 96th).