Biochemical Systematics and Ecology, Vol. 14, No. 5, pp. 463-467, 1986. 0305-1978/86 $3.00 + 0.00 Printed in Great Britain. © 1986 Pergamon Journals Ltd.

Carotenoids in Lichens from the Taimyr Region of North Siberia*

B. CZECZUGA and R. P. SHCHELKUNOVAT Department of General Biology, Medical Academy, 15-230 Bia~ystok, Poland;

?Scientific Research Institute of Agriculture of the Far North, 663-305 Norilsk, U.S.S.R.

Key Word Index--Lichens; North Siberia; carotenoids; distribution.

Abstract--The carotenoid content in the thalli of 15 species of lichens from North Siberia was determined. Twenty-one carotenoids were found and their distribution recorded.

Introduction Lichens are found worldwide, being particularly abundant in the temperate and colder climatic zones. They are widespread in the far north of the U.S.S.R. where they are a food resource for reindeer, an important part of the husbandry in the region [1]. In Taimyr (northern Siberia), the fruticose lichens produce approximately 15 million tons dry weight annually [2], about one third of the total supply of reindeer fodder in the region [3]. Thus, the distribution and quantity of lichens determines reindeer husbandry in the far north [4].

It was with this in mind that we'decided to study the carotenoids (provitamins As) in the lichens of the Taimyr region. In addition we wished to study the effect of the specific ecological conditions in the far north on the presence of the various carotenoids which are found in the thalli of species occurring in other latitudes.

Results The results of chromatographic analyses of the lichen thalli collected from Taimyr (Table 1) are given in Table 2. The thalli of Pelt/gem aphtosa contained seven carotenoids, of which zeaxanthin constituted the largest amount (29.0%). The total carotenoid content was 14.6

*Part 13 in the series "Investigations on Carotenoids in Lichens". For Part 12 see Czeczuga, B. and Cifuentes, B. (1986) Acta Soc. Bot. Pol. 55.

(Received 29 December 1985)

mg'g -1 dry wt. Stereocaulon paschale thalli (Stereocaulaceae), contained six carotenoids, zeaxanthin again comprising the largest amount (47.0%). The total carotenoid content was 1.6 rag" g-1 dry wt. Nineteen carotenoids were identified in six species of the Cladoniaceae. Of these, the most interesting is neurosporene in Cladina sylvatica. The total carotenoid content ranged from 5.7 (CI. arbuscula) to 27.8 rag. g-1 dry wt. ( Cl. sylvatica).

Table 2 shows that 13 carotenoids were identified in the three lichen species of the Parmeliaceae. J]-Cryptoxanthin, lutein epoxide and astaxanthin were common to all these species. There were differences in the distribution of the various carotenoids and in their total content in Cetraria cucullata from different environments. The total carotenoid content in the thalli of the Parmeliaceae species investigated varied between 5.4 (C. islandica) and 40.1 mg. g-1 dry wt (C. cucullata).

The results of an analysis of the carotenoid content of the thalli of four species of the Usneaceae show that 17 carotenoids were identified. ~-Cryptoxanthin and lutein epoxide were present in the thalli of all four species. The presence of rhodoxanthin in Alectoria nigricans thalli is worthy of note. The total carotenoid concentration varied between 5.7 (Alectoria nigricans) and 31.3 mg.g -1 dry wt (Dac~lina arctica).

Discussion All the carotenoids found jn the thalli of the species under investigation have been found in

463

464

TABLE 1. SPECIES OF LICHENS INVESTIGATED FROM TAIMYR

6. CZECZUGA AND R.P. SHCHELKUNOVA

Family and species Collected from the vegetable complex

Peltigeraceae Peltigera aphtosa (L,) Willd.

Stereocaulaceae Stereocaulon paschale (L.) Hoffm.

Cladoniaceae Cladina arbuscula (L.) Web. Cladina rangiferina (L.) Web. Cladina stellaris (L.) Hoffm, Cladina sylvatica (L.) Hoffm. Cladonia amaurocraea (FIk.) Sch. Cladonia cenotea (Ach.) Schaer.

Parmeliaceae Cetraria cucullata (Bell.) Ach Cetraria cucullata (Bell.) Ach. Cetraria Jslandlca (L.) Ach. Cetraria nivalis (L.) Ach.

Usneaceae Alectoria nigricans (Ach.) Nyl. Alectoria ochrolema (Hoffm,) Mas. Dactylina arctica luck. Thamnolia vermicularis (Sw) Ach.

Shaggy--lichenic tundra

Mossy sallow

Shaggy--lichenic tundra Shaggy--lichenic tundra Shaggy--lichenic tundra Birch--sallow, shaggy-lichenic, spotted tundra Sha99y--lichenic tundra Mossy sallow

Mossy sallow Mossy Ernica Shaggy--lichenic tundra Lichenic alder

Shaggy--lichenic (alectoriales), spotted tundra Birch--sallow, shaggy--lichenic, spotted tundra Shaggy--lichenic tundra Shaggy--lichenic tundra

those of other lichens [5-11]. Most of them belong to the group of carotenoids commonly found in lichens, whereas others are somewhat rare, for example, neurosporene, 0c-carotene, 0c-cryptoxanthin and rhodoxanthin. Neuro- sporene, on the other hand, is a carotenoid

frequently found in fungi [12] but has not so far been found in algae. This carotenoid has been shown previously in lichens; in the thalli of Cladonia pyxidata [5] and a few species of the Usneaceae [6]; in two species of Peltigera [7] and in the thalli of a representative of the

TABLE 2. CAROTENOID DISTRIBUTION IN LICHENS

Family and species Carotenoids (see Fig. 1) Major carotenoids (%) Total content (mg. g ' dry wt)

Peltigeraceae Peltigera aphtosa 2,5,6,8,9,17,21 8(290) 14.6

Stereocaulaeeae Stereocaulon paschale 5,8,9,14,21 8(47.0) ! 6

Cladoniaceae Cladina arbuscula 6,7,8,9,10,14,18 6(44.6) 5.7 Cladina rangiferina 3,6,8,9,10,16,20 10(24.6) 12.3 Cladina stellaris 4,6,8,12,14,15,16, 8(27.2) 23.4 Cladina sylvatica 1,3,6,8,9,17,19 17(58.3) 27.8 Cladonia amaurocraea 6,7,8,9,10,13,14,20 9(26.4) 7.7 Cladonia cenotea 2,4,6,8,9,1t,13,15 15(34.9) 13.2

Parmeliaceae Cetraria cucullata 2,6,9,13,15,16,18 15(34.6) 40.1 Cetraria cucullata 4,5,6,9,15,20 15(30.0) 15.6 Cetraria islandlca 2,4,5,6,9,15,20 6(32.7) 5.4 Cetraria nivahs 4,6,8,9,15,17,18,19 15(40.6) 24.7

Usneaceae Alectoria nigricans 6,7,9,12,15,16,21 6(31.5) 5.7 Alectoria ochrolema 6,8,9,14,19,20 9(25.2) 12.0 Dactylina arctica 2,5,6,7,9,10,11,15,16,20 15(16.8) 31.3 Thamnolia vermicularis 4,6,7,9,19,20 6(27.0) 10.4

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466 B. CZECZUGA AND R. P. SHCHELKUNOVA

Parmeliaceae, Pseudovemia furfuraceae [8]. As for 0c-carotene, this is somewhat rare in both lichens and algae: it has been found in some representatives of Peltigera [7]. 0c-Cryptoxanthin, a derivative of 0~-carotene, has been noted in the thalli of two species of the Parmeliaceae (8) and in some species of green algae [13]. Rhodoxanthin has been observed in some aquatic plants [12], horsetails and ferns [14] and in gymnosperms [15]. Where lichens are concerned, this ketocarotenoid group has been found in two species of Xanthoria [10] and some species of Cladonia [11]. In the gymnosperms, rhodoxanthin is noted, particularly in autumn [15].

In northern Siberia, as we have said, lichens constitute an important source of fodder for reindeer [16]. The amount of carotenoids in these plants is therefore very important since they are a source of vitamin A for the animals. On comparing the data on other species of lichens growing in Europe under different climatic conditions, it can be said that the thalli of lichens from Taimyr investigated in the present work are very rich in these substances, particularly Cetraria cucullata, C/adina stellaris, Cladina sylvatica and Dactylina arctic& Not all carotenoids act as provitamin A [17]. Of the

carotenoids found in the Taimyr lichens, cz- carotene, I]-carotene, l~-cryptoxanthin and mutatochrome are precursors of vitamin A. As can be seen from Table 3, the carotenoid content of this group varied between negligible

i amonts (Stereocaulon paschale) to 7.8 mg-g dry wt (Cetraria nivalis). Our investigations revealed that the thalli of Thamno/ia vermicularis (Usneaceae) contained over 60% of the total number of carotenoids of the vitamin A-provitamin type.

It should also be noted that in the Cetraria cucullata collected for analysis from different phytological groups, differences in the occurrence of the various carotenoids, their total content and the quantity of carotenoids of the vitamin A-provitamin type were noted. As our previous studies have shown [9], the intensity of sunlight and the spectral composition of the light have a significant effect on the total carotenoid content. Where the light is lower, the amount of carotenoids increases in all species except those of Xanthoria [10]. This may explain the comparatively large amount of carotenoids in the thalli of Taimyr lichens.

Experimental Fifteen lichen species collected (5-15 g dry wt) from Taimyr

TABLE 3. CAROTENOID CONTENT RELATED TO VITAMIN A IN LICHENS

Family and species Total content of carotenoids Provitamin A (mg'g dry wt) (mg'g ' dry wt)

Peltigeraceae Peltigera aphtosa 14.6 3.0

Stereocaulaceae Stereocaulon paschale t.6 [race

Cladoniaceae Cladina arbuscula 5.7 2.5

Cladina rangiferina 12.3 2.4 Cladina stellaris 23.4 5.3 Cladina sylvatica 27.8 6.2

Cladonia ama urocraea 7.7 0.7 Cladonia cenotea 13.2 5,4

Parmeliaceae Cetraria cucullata 40.1 4.4

Cetraria cucullata 15.6 2.8 Cetraria islandica 5.4 2,2 Cetraria nivalis 24.7 7.8

Usneaceae Alectoria nigricans 5.7 1,8 Alectoria ochrolema 12.0 1,9 Dactylina arctica 31.3 2.6 Thamnolia vermicularis 10.4 6.9

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provitamin A

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11

18 42 32

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66

CAROTENOIDS IN LICHENS 467

(the left bank of the Yenisey River, lat. 69°N and long. 80°E) were investigated (Table 1). The carotenoids were separated from the thalli of the lichens according to earlier methods [5, 18], and their identification was achieved by column chromatography and TLC as described earlier [19]. Quantitative determination of the concentrations of carotenoid solutions were made from visible absorption spectra [19].

References 1. Khodachek, E. A. (1969) Bot. Zh., Leningrad54, 1059. 2. Shchelkunova, R. P. (1976) Byull. nauchn, techn, inf NIISKH

Kraynego Severa 11, 10. 3. Shchelkunova, R. P. (1979) Bot Zh., Leningrad64, 84. 4. Pospelova, E. B. and Vasilyevskaya, V. D. (1985) Bot. Zh.

Leningrad70, 188.

5. Czeczuga, B. (1979) Nova Hedwigia 31, 337. 6. Czeczuga, B. (1979) Nova Hedvvigia 31, 349. 7. Czeczuga, B. (1980) Cryptog, Bryol, Lichenol. 1, 189. 8. Czeczuga, B. (1980) Nova Hedvw'gia 32, 105. 9. Czeczuga, B. (1981) Nova Hedwigia 35, 371.

10. Czeczuga, B. (1983) Biochem. Syst Ecol. 11, 329. 11. Czeczuga, B. (1985) Biochem. Syst Ecol. 13, 83. 12. Goodwin, T. W. (1980) The Biochemistry of the Carotenoids.

Chapman & Hall, London. 13. Liaaen-Jensen, S. (1977) Mar. Nat. Prod. Chem, 1, 239. 14. Czeczuga, B. (1985) Biochem. Syst. Ecol. 13, 221. 15. Ida, K. (1981) Bot Mag., Tokyo 94, 41. 16. Shchelkunova, R. R (1980) Dissert. Abstr. 43, Novosibirsk. 17. Bauernfeind, J. C. (1972) J. Agric. Food Chem. 20, 456. 18. Czeczuga, B. and Czerpak, R. (1968) Eur. J. Biochem. 5, 429. 19. Davies, H. S. (1976) Chemistry and Biochemistry of Plant

Pigments (Goodwin, T. W. ed.). Academic Press, London.