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Chemical Lichens
Chemical Lichens
REVIEW
Abstract: Lichens produce a wide variety of secondary compounds formed by the oxidative coupling
metabolites which assist them in the colonization of terrestrial of methylphloroacetophenone units are found
h a b i t a t s . S u c h compounds a r e i m p o r t a n t i n t h e
in the cortex of many lichen species (Figure
chcmotaxonomy of lichens. Furthermore, lichen substances
exhibit antiherbivore, antimicrobial and antineoplastic
1). Anthraquinones, xanthones and
activities. This review highlights the different types of lichen chromones, are all pigmented compounds
substances and their activities, uses and t h e possible which occur in the cortex, which are also
ecological role. produced by the acetate-malonate pathway by
intramolecular condensation of long folded
Lichens a r e symbiotic organisms of fungi polyketide units rather than the coupling of
(mycobiont) and algae (photobiont) comprising phenolic units (Figure 2).
about 17,000 species. Lichens are unique because
they look and behave quite differently from their (b) The shikimic acid biosynthetic pathway
component organisms. They are classified and produces two major groups of pigmented
named according to their fungal partner, with compounds,which occur in the cortex: pulvinic
many thousands of species of lichens sharing a acid derivatives and terphenyl quinones
much smaller number of photobiont species. (Figure 3). Although most pulvinic acid
Lichens show a world-wide distribution commonly derivatives lack nitrogen, they a r e
growing on rocks and poorly developed soils such biosynthesized through phenyl alanine.
as those of arid lands and boreal-arctic regions or Nitrogen is strongly limiting to metabolic
as epiphytes on trees and shrubs. activities in most lichens, and nitrogen rich
metabolites such as alkaloids are unknown
Primary metabolites of lichens, which are among lichen substances.
intracellular, are proteins, amino acids, polyols,
carotenoids, polysaccharides and vitamins. (c) Terpenes and steroids are produced by the
Lichens produce a wide array of secondary mevalonic acid pathway. These include
metabolites (extracellular). There are over 700 compounds unique to lichens and many that
lichen substances reported to date1and many are occur in higher plants as well (Figure 4).
restricted to t h e lichenised s t a t e . Broadly
speaking, there are three major types of lichen Chemotaxonomy of lichens
substances based on their biosynthetic pathway^.^
The application of chemical discriminators to
(a) Depsides, depsidones and dibenzofurans lichen taxonomy is widely accepted. The secondary
formed by the acetate-malonate pathway. The metabolites in about 5000 species (33 % of all
most important of these are the esters and known species) have been studied and the data
the oxidative coupling products of simple are used in the routine identification of lichens
phenolic units related to orcinol and p-orcinol. than in any other group of organism^.^^^
Most depsides and depsidones are colourless
compounds which occur in the medulla of the Cortical chemistry: It has now been recognized by
lichen. However, usnic acids, yellow cortical many lichenologsts that some cortical substances
* Corresponding author
Veranja Karunaratne et al.
Figure 1: Structures of typical acetyl-polymalonyl lichen products derived from two or more
polyketide chains.
Lichens: a chemically important biota
Aliphatic acids
H02C, ,C02H
H " - H
H3C (CH2)11CH3
Figure 2: Structures of some acetyl-polymalonyl lichen products derived from a single polyketide
chain.
172 Veranja Karunaratne et al.
Terphenyl quinones
Figure 3: Structures of some lichen products derived from the shikimic acid pathway.
Terpenoids
Ergosterol (Steroid)
y-Carotene (Carotenoid)
Figure 4: Structures of typical lichen products derived from the mevalonic acid pathway.
are correlated with higher taxonomic ranks. For biosynthetically related to these two compounds.
example, vulpinic acid in Letharia (at the genus I t is therefore now recognized t h a t when
level) or anthraquinones such as parietin in biogenetic demarcations complement
Teloschistaceae (at the family l e ~ e l ) . ~ biogeographic variations, such taxa should be
recognized as separate species. Thus, the North
Medullary chemistry American taxon is named as P. c o n s ~ c i a n s . ~
However, it has been suggested that the best way
Variations in medullary constituents are used to recognize whether chemical variation is under
mainly as discriminators at the species level. Most genetic control or not is through sympatric
morphologically defined species have a constant chemical races which maintain their chemical
chemistry, regardless of their geographical integrity even when growing side by side."
location, substrate or ecology. Within a complex
of morphologically similar species, three common Chemosyndrome refers to a group of
patterns of chemical variation can be discerned: biosynthetically related lichen substances and the
(a) replacement compounds, (b) chemosyndromic major metabolite is accompanied by several minor
variation and (c) accessory type compound^.^ constituents which are biosynthetically relatede4
The compounds which are major constituents in
With replacement compounds, cogeneric one species may occur as minor constituents in
chemotypes show simple replacement of one related taxa and vice versa. These chemotypes can
substance by another. Morphologically these also be considered as sibling species5, where
lichen populations are sometimes reproductive isolation of a species often leads to
indistinguishable, but possess well-defined and ecological differentiation. This is a common result
constant variations in chemical compositions. For of evolution in animals and vascular plants.
example, Psuedovernia furfuraceae has three
chemical races. One race contains olivetoric acid The occurrence of accessory compounds
and is found in Northern Europe, a second is found may tend to complicate the above arguments.
in Southern Europe and Northern Africa and These compounds are found at certain times in
contains physodic acid and third containing species, usually i n addition to normal
lecanoric acid is found i n North America. constituents, a n d have relation to the
Biogenetically the first two compounds are closely morphological or distributional variation. Thus,
related because one can be derived from the other these compounds a r e not accorded
by one single step. But lecanoric acid is not chemotaxonomic significance. Such compounds
Veranja Karunaratne et al.
often occur as accessory compounds in more than by the position relative to the standards. Data are
one species and often vary in quantity. then sorted to find all compounds with the same
R,classes. Of these possibilities, those with similar
The following spot tests and microchemical spot characteristics (colour, fluorescence etc.,) are
methods will be used to garner taxonomical details compared chromatographically w i t h t h e
of lichen specimens: unknown. Additional solvent systems are used for
compounds that do not separate well in the initial
(a) Chemical (colour) tests conducted on lichen analysis. Two-dimensional TLC methods are used
thalli to evaluate structurally similar compounds.
Before spraying the dried plates are examined in
The common spot test reagents not only day light for pigments and for fluorescence or
indicate where particular compounds are located quenching u n d e r s h o r t (254 n m ) a n d long
in sectioned thalli, but may also indicate the wavelength (365 nm) ultraviolet (UV) light.
chemical nature of the substance. Subsequently the plates are sprayed with 10 %
Reagents for thalline spot tests: sulfuric acid and heated a t 110" C on a hot plate
for 10 minutes to develop the spots. The following
K = 10 % aqueous KOH solution solvent systems are used:
a. Turns yellow to red with most o-hydroxy
aromatic aldehydes Solvent A = Toluene: dioxane: acetic acid
b. T u r n s b r i g h t red to deep p u r p l e w i t h (180: 45: 5)
anthraquinone pigments Solvent B = Hexane: methyl tert. butyl ether:
C = saturated aqueous Ca(OCl), or common bleach formic acid (140: 72: 18)
NaOC1 solution Solvent C = Toluene: acetic acid (170: 30)
(iii) Gas Chromatography and Mass Spectrometry: suggests that these compounds act as light-
Xanthones, anthraquinones, dibenzofurans, screens, regulating the light intensity reaching
terpenes a n d pulvinic acid which lack the algal layer in the upper cortex. Usnic acid, a
thermolabile ester groups can be studied by gas yellow cortical pigment is the most widespread
chromatography coupled with mass spectrometry lichen substance found in thousands of lichens.
(GCMS). Xanthones in lichens were studied by Lichen populations having usnic acid which are
injecting a lichen extract directly into a mass exposed to the sun are yellow, while the shade
spe~trometer.~ More recently, the main terpenoid populations are grey-green, indicating a lower
components of t h e lichens of t h e family concentration of the depside. Cladonia subtenuis
Pyxinaceae have been studied by GCMS." and Parmeliopsis ambigua show concentrations
of usnic acid varying along concentration
Ecological role of lichen substances gradients.ll
(c) Biologically active compounds namely, erythrin and methylorsellinate have been
isolated from the dichloromethane extract of
The biological activity of lichen compounds very Roccella montagnei collected from
likely gives them a n ecological advantage in Bamunakotuwa in Kurunegala district.
colonization of terrestrial areas. Such compounds
have been used by man as well. Lichens have been I n g e n e r a l , e r y t h r i n showed lower
used in medicine by the ancient Chinese and antifungal activity when compared with benomyl
Egyptians.l"14 The medicinal use of lichens is not (Benlate- standard funpcide) in the TLC bioassay
prevalent at present, particularly since the testing technique. Apart from somewhat reasonable
of the atom bomb and the Chernobyl accident in activity shown a g a i n s t C o l l e t o t r i c h u m
1986 which have increased the concentrations of gleosporioides, erythrin exhibited moderate
radionuclides (137Cs a n d 40K) to a l a r m i n g activity against four fungi namely, Colletotrichum
prop~rtions.~%ccording to recent investigations, musae, Cladosporium cladosporioides, Curvularia
lichens possess a variety of biological activities: trifolii, and Monacrosporium ambrosium. These
results were corroborated by a spore germination
( i ) A n t i m i c r o b i a l a c t i v i t y : Although lichen a s s a y a g a i n s t C o l l e t o t r i c h u m m u s a e . The
substances are used as antibiotics, their activity germination was 70.1 %with erythrin at 10 ppm,
is found to be low compared to those isolated from while for the untreated control germination was
microorganisms. Furthermore, lichen antibiotics 74.2 %.
are not adequately water soluble for therapeutic
use. Depsides, depsidones and usnic acid are Methylorsellinate on the other hand,
active against Gram-positive microorganism^.^^ showed significantly higher antifungal activity as
Sodium salt of usnic acid was used as a drug in compared to erythrin (Table 1).Methylorsellenate,
Russia.17 Antiseptic creams such as "Usno" and when tested against Colletotrichum
"Evosin" contain usnic acid. Usnic acid acts by gleosporioides, Colletotrichum musae,
uncoupling phosphorylation and is effective Cladosporium cladosporioides and Curvularia
because animal cells are far less permeable to t r i f o l i i , showed g r e a t e r activity t h a n t h e
usnic acid than the microorganisms. commercial fungicide Benlate. Methylorsellinate
showed lesser activity against t h e fungus,
In S r i Lanka, lichens h a d remained Monacrosporium a m b r o s i u m as compared to
completely unexplored (both chemically and Benlate. Based on the diameter of inhibition
taxonomically) until 1996, when a systematic zones, methylorsellinate was significantly more
study to harness their biological and medicinal active than erythrin against C. cladosporioides.
v a l u e was i n i t i a t e d a t t h e D e p a r t m e n t of
Chemistry, University of Peradeniya. The antifungal activity of
methylorsellinate was also confirmed by a spore
Roccella montagnei is a fruticose lichen, germination assay using Colletotrichum musae.
which is pendulous or shrubby. It is sparsely to The germination percentage with
moderately branched and has shades of grey, methylorsellinate was 29.9 %while in the control
specially lilac grey. (Figure 5).lDifferent Roccella it was 74 %.
lichen species a r e used to prepare complex
mixtures of pigments for the preparation of litmus In order to show that methylorsellinate
paper (pH 4.5 red; pH 8.3 blue). Two compounds was not produced as a n artifact in the methanol
Erythrin Methylorsellenate
Lichens: a chemically important biota
Figure 5: Roccella montagnei lichen growing on the trunk of a coconut tree, Cocos nucifera
Colletotrichum musae 25 50
Colletotrichum gloeosporioides 20 44 25
Cladosporium cladosporioides 10 50 31
Curvularia trifolii 16 55 25
Monacrosporium ambrosium 10 36 48
extract by the methanolysis of erythrin, the lichen is found in large amounts in the lichen (4.9 % of
Roccella montagnei was extracted into ethyl dry weight) compared with methylorsellinate (0.3
acetate. Upon examination by TLC and co-TLC it % of dry weight). It is not uncommon that lichen
was evident that this extract also contained both substances are accumulated in amounts exceeding
erythrin and methylorsellinate, proving that the 20 % of the dry weight of the thallus. These
latter was indeed a natural product isolated from compounds are considered to impart a protective
Roccella montagnei and not an artifact. role against invading pathogens and herbivores.18
Ambewelamide A, R = (CH2),CH3
Ambewelamide B, R = (CH2),CH3
(ii) Anti tumour and anti mutagenic activity: (-1- potent in vitro cytotoxicity (Figure 6 ) . Bioassay
Usnic acidlg, protolichesterinic and guided fractionation of the Usnea sp. extracts led
nephrosteranic acids20,physodalic acid20~21, lichen to the isolation of ambewelamides A (1)and B (21,
g l u c a n ~and~ ~lichenin derivatives" have shown whose structures have been elucidated via a
anti tumour and anti mutagenic activity. Lichen combination of single crystal X-ray diffraction and
polysaccharides, the class of compounds to which spectroscopic a n a l y s e ~ . ~ ~ ~ ~ ~
the latter two belong are particularly interesting
due to their anti tumour activity. The mechanism Ambewelamides A (1)and B (2)are new members
of action of these lichen polysaccharides are not of a family of highly modified diketopiperazines
completely known, b u t a p p e a r s to be host that include fungal metabolites such as a r a n ~ t i n ~ ~ ,
mediated: such compounds a r e believed to apoaranotinZ7,emethallicinsZ8,exserohiloneZ9and
g e n e r a t e lymphoid cells, p l a s m a cells, SCH64847.30There are reports of anti allergenic
macrophages i n t h e vicinity of t h e grafted 28,anti viralz7,EGF receptor binding 30,phytotoxic
tumo~r.~~ 29 activity for t h e members of t h e family of
E epoxides and a diketopiperazine epidisulphide herbivores. Since these compounds are bright
bridge, suggesting that these functionalities might yellow in colour, their cortical position indicates
be necessary for cytotoxicity. The ambewelamides a n example of warning coloration. The medullary
are the first examples of the diketopyperazine fam- position of pulvinic acid derivatives i n t h e
ily isolated from a lichen. Stictaceae and two species ofParmelio. suggest a
defensive role against small, nonvisual1y.-oriented
(d) Anti-herbivore compounds invertebrate herbivores.ll
Both vertebrate and invertebrate herbivores In vascular plants, several studies have
consume lichens. The reasons for the low observed shown that sesqui- and diterpenoids may act as
levels of herbivory may be due to low nutrient defense restricting h e r b i ~ o r yThe . ~ ~nutrient rich
content of lichens, the difficulties in metabolising species of Pseudocyphellaria, Sticta a n d
lichens, and the sparse nature of lichens as a Nephroma show a surprising lack of herbivory
resource. Lichens comprise a major source of indicating that terpenes may play an important
winter food supply of' caribou and reindeer in role in protecting these species with high nitrogen
boreal a r e a s i n t h e Northern Hemisphere. content. l1
Although lichens are a poor source of proteins (2-
3 %), they are a n easily accessible carbohydrate Fumarprotocetraric acid is a b i t t e r
source when higher plant foliage is not a ~ a i l a b l e . ~ ~depside occurring in many lichens which appear
In addition, herbivory on lichens by insects, mites, to deter herbivory. For example, neither Caldonia
molluscs are i m p ~ r t a n t .Despite ~ ~ . ~ the
~ ~ lichens
~~ arbuscula nor C. rangiferina (both contain
being a potential food source for herbivores, fumarprotocetraric acid) are eaten by reindeer,
feeding on lichens is not common. In temperate while they s r e attracted to C. alpestris which has
evergreen forests, there is little evidence of no fumarprotocetraric acid.39Concentrations of
v e r t e b r a t e or i n v e r t e b r a t e herbivory. T h e f'umarprotocetraric acid vary greatly between
resistance of individual lichens toherbivory may younger and older thallus parts in Cladonia, with
be due to a variety of factors. Lichens with t h e g r e a t e s t concentration occurring in
gelatinous sheaths covering their surface are metabolically active growing tips." Species
relatively immune to herbiv01-y~~ as seen in some containing depsides and depsidones such as
species of Collemataceae. Thick cortical structure diffractic acid, physodic and physodalic acids and
with heavily agglutinated hyphae may also salazinic acid which are bitter are avoided by
provide some protection from small invertebrate Caribou in Canada.41
herbivores. Inorganic chelate agents present in
many saxicolous crustose lichens are toxic to P a r i e t i n , a n a n t h r a q u i n o n e lichen
numerous insects.36 F o u r groups of lichen substance appears to have a defensive role against
substances that have possible defensive functions herbivore^.^^ Lichen species of Teloschistaceae
in lichens are pulvinic acid derivatives, terpenes, contain relative high contents of ~ a r i e t i n . ~ ~
depsides and depsidones and anthraquinones.
(+)-Usnicacid isolated from a n Usnea sp.
Several studies support t h e primary i n t h e Ambewela a r e a 4 4showed significant
defensive role of pulvinic acid derivatives. Lichens antitermite activity (80 % mortality at 10 mg)
containing these compounds have relatively high against Glyptotermes dilatatus, which is a major
nitrogen content thus making them potentially a live-wood tea-termite a t low elevations. Although
valuable food source. Yet, feeding on these taxa usnic acid is a well-known antimicrobial
are virtually unknown. Vulpinic acid, the most compound16 t h e r e is only one report of t h e
widespread of these compounds is toxic to both insecticidal activity of usnic acid against the
vertebrates and invertebrate^.^^ The cortical polyphagous herbivorous insect Spodoptera
presence of most of the pulvinic acid derivatives l i t t o r ~ l i s . 'Currently,
~ the control methods of G.
is unusual since they show no variation along light dilatatus are focused on t h e development of
gradients. B u t t h i s histological position is r e s i s t a n t clones a n d t h e r e a r e no reported
consistent with their defensive role against chemicals which can be used in controlling the
180 Veranja Karunaratne et al.
pest, and as such search for such compounds are Many species of invertebrates live on and
imp~rtant.~" among lichens, using them for concealment,
shelter or food. Over half of the orders of insects
(e) Allergenic activity have associations with lichens.49
OH COOMe
Atranorin
Lichens: a chemically important biota
Vulpinic acid
The moth larvae of Lithosiinae feed on to soil a t a n amazing rate. The snails pass
epiphytic algae of trees or on the algal component significant amounts of rock through their digestive
of lichens.48A recent survey for the presence of tracts in the process of consuming the lichen. In
sequestered lichen compounds i n several addition, the snails were taking the nitrogen from
Lithosiinae species in Australia and Germany, the lichen and leaving it behind in the new
demonstrated t h a t t h e presence of lichen On the other hand, many lichen species contain
compounds is variable but wide spread in wild- bitter compounds that may discourage feeding by
caught imagines.48 invertebrate^.^^ Although the ecological role of the
sequestered compounds for the herbivores
Many snails and slugs (class: Gastropoda) remains unknown, it is thought that they may be
feed on lichens. In Israel, two species of snails utilized for chemical defense against predators or
that eat lichens growing under the surface of lime pathogen^.^^
stone rocks were discovered to be converting rock
Three species of lichen-grazing snails, During our studies of Sri Lankan lichens,
Baleaperversa, Chondrina clienta and Helicig-ona we discovered the sequestration of lichen products
lapicida were found to sequester lichen belonging to the crustaceous lichen Leproloma
compounds when feeding on the crustous lichen sipmanianum Kurnmerl & Leukert by t h e
species Aspicilia calcarea, Caloplaca atra and butterfly T. nyseus Guerin (red pierrot)
Xanthoria parietina. The lichen compounds such (Lycaenidae) in Beragala (80" 54' 30" E, 6"45' 30"
as (+)-usnicacid or a-collatolic acid were detected N), Uva province, Sri Lanka.58T. nyseus was found
in the feces of these snails, suggesting selective flying close to the extensive lichen thallus,
uptake of lichen compounds by the snails.57 growing on road side proterozoic rocks of gneiss
and quartz schist which are exposed at road-edges,
Lycaenidae is t h e largest family of and roosting on it periodically (Figure 8).
butterflies in Sri Lanka and consist of 40 genera,
comprising 8 1 species.50Some species of Pupae of the butterflies were also located
Lycaenidae live on plants, a few live or, scale- anchored to the thallus surface. T. nyseus were
insects, others feed on the larvae and pupae of collected from Beragala between the period from
the large red ant Oecophylla smaragdina, while September 1996 and March 2001.
many are actually tended by ants in their nests.
Some are cannibalistic, devouring larvae or the Out of seven butterfly collections made,
pupae of their own hnd.50Fruit-eating forms are on three occasions, five compounds namely, zeorin
also found in the Lycaenidae. 1, psitosterol 2, a long-chain fatty acid ester 3,
atranorin 4, and (+)-usnic acid 5, were present in
Talicada nyseus Guerin (red Pierrot) wild-caught imagines (Figure 9). The butterf ies
which belongs to the family Lycaenidae is which emerged from the pupae also contained
distributed from Sri Lanka to Indo-China. The Sri these compounds.
Lankan population belongs to the nominotypical
race, which flies through out the island below 4000 The presence of these compounds in the
feet. The butterflies love human settlement being butterfly was confirmed by comparative TLC
equally abundant in domestic gardens as it is in studies a n d GC-MS with authentic lichen
the It is plentiful all over the island all the substances isolated from t h e lichen L.
year round and flies slowly near the ground and sipmanianum.
settles f r e q ~ e n t l y .The
~ ~ natural food source of
its larvae is Bryophyllum calycinum (Sinhala: The butterflies found at the University of
akkapana; Tamil: malai-kalli) (Figure 7). Peradeniya and Kandy contained only psitosterol
CH3(CH2)4ICH20CCH2CH2CH2CH3
Me
H
3
CHO OH 0 0
2 (common plant sterol also found in the host plant the Central Province and in Ukgalkalthota (80"
B. calycinum) with no trace of other lichen 52' 30" E, 6" 39' 30' N) in the Uva Province.
compounds. It was concluded that the presence Butterflies were subjected to the same analysis
of lichen products of L. sipmanianum in adult T. protocol as described above using both TLC and
nyseus butterflies indicated that its larvae may GC-MS. Interestingly, the butterflies found at the
feed on the lichen although the natural food source University of Peradeniya and Kandy contained
is B. calycinum. only 0-sitosterol with no trace of other compounds.
However, those collected in Ukgalkalthota
Out of the seven butterfly collections made contained atranorin (4) and 0-sitosterol while
from Beragala, all five compounds, (1) - (5) were butterflies a t the foot-hills of Adam's peak
present in adult butterflies on three occasions. contained (+)-usnic acid (5) along with 0-
Importantly, on two occasions, the butterflies sitosterol. Examination of the extracts (hexane,
which emerged from laboratory-reared pupae also dichloromethane and methanol) of air-dried plant
contained compounds (1) - (5). (+)-Usnicacid (5) material (140 g) of BryophylLum calycinum by
was present only on three occasions and atranorin TLC and MPLC did not reveal the presence of
(4) four times. T. nyseus collected during all the lichen compounds (I), (3), (4) and (5). However,
field visits contained zeorin (I), 0-sitosterol (2) the dichloromethane extract (1.50 g) whose TLC
and the fatty acid ester (3). showed the presence of p-sitosterol upon MPLC
on silica gel (eluent: s t e p gradient from
In order to expand the scope of the study dichloromethane: hexane (2: 3) to methanol:
and investigate the presence of lichen products dichloromethane (1:79)) yielded fl-sitosterol as a
in T. nyseus in other areas of the island, butterflies colourless crystalline solid (0.021 g) confirming
were collected from four other locations: foot hills that B. calycinum contains p-sitosterol 2 and it
of Adam's peak in Central Province (80"30' 50" E, could be the source of the butterfly.
6" 50' N), Peradeniya University premises (80"35'
30" E, 7" 15' N), from a domestic garden in It may be concluded that the presence of
Aniewatta, Kandy (80"38' E, 7" 17' 30" N), both in lichen products found in L. sipmanianum in adult
Veranja Karunaratne et al.
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