Directory UMM :Data Elmu:jurnal:B:Biochemical Systematics and Ecology:Vol28.Issue8.Oct2000:

Biochemical Systematics and Ecology 28 (2000) 751}777

Lipophilic exudates of Pteridaceae } chemistry
and chemotaxonomy
Eckhard Wollenweber!,*, Harald Schneider"
!Institut fuer Botanik der Technischen Universitaet, Schnittspahnstrasse 3, D-64287 Darmstadt, Germany
"Department of Botany, Field Museum, Roosevelt Road at Lake Shore Drive, Chicago, IL 60605-2496, USA
Received 26 July 1999; accepted 27 September 1999

Abstract
A number of fern species, belonging to several genera of Pteridaceae, exhibit a more or less
conspicuous farinose wax, which is mostly located on the lower leaf surface. Production of these
waxes is often correlated with the presence of glandular trichomes. Particularly during the past
two decades, a series of publications appeared on the chemical composition of these exudates.
The major components were found to be #avonoids (chalcones, dihydrochalcones, #avanones,
dihydro#avonols, #avones, #avonols), some of them with a complex substitution pattern,
including esters and C-methyl derivatives, and even bis#avonoids. Diterpenoids and triterpenoids can also occur in such exudates. It is the purpose of this paper to survey the chemical
composition of Pteridaceae exudates and their occurrence within the genera of the family. The
chemotaxonomic signi"cance of the #avonoid aglycones at the generic, speci"c and populational level is brie#y discussed. ( 2000 Elsevier Science Ltd. All rights reserved.
Keywords: Pteridaceae; Farinose exudates; Flavonoid aglycones; Terpenoids

1. Introduction
More or less conspicuous white or yellow coatings are long known to occur on the
lower leaf surfaces of a number of ferns, belonging to the genera Pityrogramma,
Cheilanthes, Notholaena and others. In the pteridological literature, these coatings

* Corresponding author. Tel.: #49-6151-163602; fax: #49-6151-166878.
E-mail address: wollenweber@.bio.tu-darmstadt.de (E. Wollenweber)
0305-1978/00/$ - see front matter ( 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 3 0 5 - 1 9 7 8 ( 9 9 ) 0 0 1 1 8 - 0

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E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

were described as wax, cera, powder, farina, resins, `pseudostearoptenesa (cf. Wollenweber, 1976a). It was found early that this material is excreted by glandular trichomes
(De Bary et al., 1877). Already in 1906, Zopf isolated some components from the
farinose exudates of Pityrogramma species, but only in 1961 Nilsson (1961a,b) identi"ed these products as chalcones and dihydrochalcones.
A series of papers dealing with the composition of farinose fern exudates have since
been published, in particular from the senior authors's laboratory; some papers of
other authors appeared, too. Information on this subject is hence scattered in the

phytochemical literature, a comprehensive survey is missing. Markham (1988), in
a chapter on `Flavonoid distribution in lower plantsa, listed most of the results
reported up to 1986, but his chapter covers both internal and external #avonoids. We
deem it desirable, therefore, to present here a complete compilation of all #avonoids
found to date in farinose (waxy) fern exudates and related epicuticular layers. In the
present paper we list the #avonoid aglycones, we report their distribution in the
relevant genera, and we discuss their chemotaxonomic implications. The terms wax
and farina are used synonymous throughout the text. Many species also exhibit
externally deposited terpenoids, which might have some importance as
chemotaxonomic characters, as will be discussed for the relevant taxa.

2. Experimental
The #avonoid aglycones as well as the terpenoids in question are all more or less
lipophilic, and they are deposited externally, on leaf surfaces. All these products can
hence be recovered unambiguously by brie#y rinsing the fern material with acetone,
sometimes with addition of toluene or methanol. Unless major components crystallize
spontaneously, the concentrated extracts are subjected to column chromatography on
silica and/or on polyamide and the components isolated are further puri"ed and
identi"ed as reported e.g. in (Wollenweber et al., 1978b; Roitman et al., 1993). When
the exudate constituents are known #avonoids, a small fragment of fern leaf is

su$cient for thin-layer chromatographic identi"cation by direct comparison with
markers. Terpenoids were also isolated by column chromatography, sometimes by
`#ash chromatographya. They are less suited for identi"cation by tlc comparisons, so
normally spectroscopic studies are required. (For details see e.g. RuK edi et al., 1989;
Appendino et al., 1992; Arriaga et al., 1996).
In some cases preservation treatment of herbarium specimen has eliminated the
exudate material, so these are of no use for phytochemical analysis. Especially, most
specimen collected in humid tropical regions lack farinose waxes, because they were
treated with alcohol or similar "xatives before drying. (In only 6 out of 50 collections
of Cheilanthes papuana from New Guinea and Moluccas Islands the farina is still
present). Due to di!erent solubility of farina components, such preservation treatment
may have changed the composition in some other specimens. These cases become
evident, however, when specimen of various origins are compared and they are not
considered for chemotaxonomic evaluation.

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753

3. Results

3.1. Components of farinose waxes in Pteridaceae
In this section we list in the "rst line all #avonoids so far reported as constituents of
farinose fern exudates (Table 1). They are grouped by #avonoid classes, and within
these classes they are sorted according to their substitution patterns as e.g. in
Wollenweber, 1994. Structural formulae of representatives of the #avonoid classes
concerned are given in Fig. 1. For standard numbering of #avones, #avonols, etc. on
the one hand, and of chalcones and dihydrochalcones on the other hand, see Fig. 2.
The latter also shows examples of a b-chalcone or bibenzyl and of #avonol-esters, as
well as the structure of the chalcone-like Pentagramma-product, ceroptene. In Fig.
3 the complex fern #avonoids reported so far are shown, and Fig. 4 shows the
methylene-bis#avonoids found in Pentagramma.
For the sake of completeness we also mention two dihydrostilbenes or bibenzyls
found in the exudate of Argyrochosma species, namely 5-OH-3,4@-diOMe-6-COOHbibenzyl or `notholaenic acida, and 3-OH-5,4@-diOMe-6-COOH-bibenzyl or
`isonotholaenic acida. Their structures are included in Fig. 1.
The terpenoids so far encountered accumulated on the leaf surfaces of Pteridaceae
comprise diterpenes and triterpenes. Some relevant structures are depicted on Fig. 5.

3.2. Morphological prerequisites for the production of farinose waxes
Farinose `waxesa in ferns are mainly the product of glandular trichomes with
a stalk of 1}6 cells and one enlarged apical glandular cell (For a brief review of earlier

descriptions see Wollenweber, 1978). These hairs are located on the lower surface in
most taxa, such as Argyrochosma, Cheilanthes, Chrysochosma, Pityrogramma, Pentagramma, but they may also occur on the upper leaf surface and even on the rachis, e.g.
in Pentagramma pallida. The impression of a farinose or waxy coating on the leaf
surface is caused by densely arranged glandular trichomes, whose glandular cells are
covered with microcrystalline platelets, rods, etc., much like in farinose Primula
species (Barthlott and Wollenweber, 1981).
Flavonoid excreting hairs are restricted to the outer surface of the pseudoindusium
in Onychium siliculosum and also in Adiantum poiretii. In farinose species of Cerosora
and Pterozonium, glandular trichomes are only found in contact to sporangia. They
are, therefore, classi"ed as paraphyses. Glandular paraphyses also occur in some
non-farinose species of Pterozonium and in the non-farinose closely related genera
Aspleniopsis KUHN, Austrogramme E. FOURN., and Taenitis WILLD. ex SPRENGEL.
On the other hand, there also exist taxa that exhibit #avonoid exudates, although
no glandular structures are observed. These species are discussed in Section 4. In this
context we also want to mention that related phenolic exudates are also known for
some fern taxa outside the Pteridaceae, e.g. in Grammitis SW. (grammitic acid, see
Wollenweber and Arriaga-Giner, 1991) and in Dryopteris ADANS. (see e.g. WideH n et al.,
1991; Wollenweber et al., 1998).

754

Table 1
Flavonoids found in fern exudates!

1
2
3

4
5

OH substitution
ring A only substituted
2@,4@,6@-triOH
ring B also substituted
(2@,4@,6@,4@-tetraOH)
b-chalcones (bibenzyls)
(2@,4@,6@,b,4-pentaOH)
C-methylated compounds
(2@,4@,6@-triOH-3@-CH )

3
(2@,4@,6@,4-tetraOH-3@-CH )
3
(2@,4@,6@,4@-tetraOH-3@,5@- diCH )
3

methyl ethers, C-methyl derivatives, esters
4@-Me, 2@-Me (cardamonin), 2@,4@-diMe (#avokawin B)
4@-Me (neosakuranetin), 4@,4-diOMe
2@,4@-diMe, 2@,4@,4-triMe
2@-Me, 2@,4@-diMe
4@-Me (triangularin)
4@-Me

Dihydrochalcones

1
2
4

OH substitution
ring A only substituted
(2@,4@,6@-triOH)
ring B also substituted
(2@,4@,6@,4@-tetraOH)
C-methylated compound
(2@,4@,6@,4-tetraOH-3@-CH )
3

methyl ethers, C-methyl derivatives, esters
4@-Me,
4@-Me, 4@,4-diOMe
4@-Me

Flavanones
1
2
3
4
5

6
7

OH substitution
5,7-diOH Pinocembrin
5,7,4@-triOH Naringenin
(5,7,3@,4@-tetraOH Eriodictyol)
(5,7,3@,4@,5@-pentaOH)
C-6 substituted
(5,6,7,4@-tetraOH)
C-8 substituted
(5,7,8-triOH)
(5,7,8,4@-tetraOH)
C-6 and C-8 substituted

methyl ethers, C-methyl derivatives, esters
pin-5-Me (alpinetin), 7-Me (pinostrobin), 5,7-diMe
nar-7-Me (sakuranetin), -4@-Me (isosakur.), 7,4@-diMe
erio-7-Me, 4@-Me (hesperetin), 7,3@-diMe, 7,4@-diMe, 7,3@,4@-triMe
7,3@-diMe, 7,3@,4@-triMe, 7,3@,5@-triMe, 7,3@,4@,5@-tetraMe

6,7-diMe, 6,7,4@-triMe
7-Me
7,8-diM, 7,8,4@-triMe

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Chalcones

8
9

(5,6,7,8,4@-pentaOH)
C-2@ substituted
(5,7,2@,4@-tetraOH)

6,8-diMe, 6,7,8-triMe, 6,8,4@-triMe, 7,8,4@-triMe, 6,7,8,4@-tetraMe
2@-Me

10
11

12
13

C-8 substituted
(5,7,8-triOH)
C-methylated compounds
5,7-diOH-6-CH strobopinin
3
5,7-diOH-8- CH cryptostrobin
3
5,7-diOH-6,8-di CH Desmethoxymatteucinol
3

7-Me-8-Ac
7-Me,
5-Me, 7-Me, 5,7-diMe

Dihydroyavonols

1
2
3

OH substitution
C-8 & C-2@substituted
(3,5,7,8,2@-pentaOH)
Ester (3,5,7,4@-tetraOH Aromadendrin)
C-8 and C-2@ substituted
(3,5,7,8,2@-pentaOH)

methyl ethers, C-methyl derivatives, esters
7,8-diMe
arom-7-Me-3-Ac, 7-Me-3-But, 7-Me-4@-But

7,8-diMe-2@-Ac

Flavones
1
2
3
4
5

OH substitution
5,7-diOH Chrysin
5,7,4@-triOH Apigenin
5,7,3@,4@-tetraOH Luteolin
C-2@substituted
(5,7,8,2@- tetraOH)
C-6 and C-8 substituted
(5,6,7,8,4@-pentaOH)

methyl ethers, C-methyl derivatives, esters
ap-7-Me (genkwanin), 4@-Me (acacetin), 7,4@-diMe
lut-7-Me, 3@-Me (chrysoeriol), 4@-Me (diosmetin), 7,3@-diMe (velutin),
7,4@-diMe (pilloin)
7,8-diMe (skullkap#avone I)
6,8-diMe (desmethoxysudachitin), 6,8,4@-triMe (nevadensin),
6,7,8-triMe (xanthomicrol)

Flavonols
1
2

OH substitution
3,5,7-triOH Galangin
3,5,7,4@-tetraOH Kaempferol

*continued

755

methyl ethers, C-methyl derivatives, esters
gal-3-Me, 5-Me, 7-Me (izalpinin), 3,7-diMe, 5,7-diMe
kae-3-Me (isokaempferid), 7-Me (rhamnocitrin), 4@-Me
(kaempferid), 3,7-diMe (kumatakenin), 3,4@-diMe (ermanin),
7,4@-diMe, 3,7,4@-triMe, 5,7,4@-triMe

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Esters

756

Table 1*continued
3

5
6

7
8
9
10
11
12
13

(3,5,7,8,3@,4@-hexaOH Gossypetin)
C-6 and C-8 substituted
(3,5,6,7,8,4@-hexaOH)
C-2@ substituted#C-8 substituted
(3,5,7,8,2@-pentaOH)
(3,5,7,8,2@,3@-hexaOH)
(3,5,7,8,2@,4@-hexaOH)
(3,5,7,8,2@,5@-hexaOH)
C-2@ substituted#C-6 and C-8 substituted
(3,5,6,7,8,2@,4@-heptaOH)

qu-3,7-diMe, 3,3@-diMe, 3,7,3@-triMe (pachypodol), 3,7,4@-triMe
(ayanin), 7,3@,4@-triMe, 3,7,3@,4@-tetra-Me (retusin)
6-OH-kae-6,7,4@-triMe (mikanin)
8-OH-gal-8-Me, 3,7-diMe
herb-7-Me (pollenitin), 8-Me (sexangularetin), 4@-Me, 3,7-diMe,
7,8-diMe, 3,4@-diMe, 8,4@-diMe (prudomestin), 3,8,4@-triMe,
7,8,4@-triMe (tambulin)
goss-7,4@-diMe
3,6,8-triMe (sarothrin), 6,7,8-triMe
3,7,8-triMe
3,7,8-triMe
7,8,4@-triMe, 3,7,8,2@-tetraMe, 3,7,8,2@,4@-pentaMe,
3,7,8-triMe, 3,7,8,2@-tetraMe
3,6,7,8,tetraMe, 3,6,7,8,2@-pentaMe, 3,6,7,8,4@-pentaMe, 3,6,7,8,2@,4@-hexaMe

Esters
14
15
16
17
18
19
20
21
22
23

C-8 substituted
(8-OH-Galangin)
(Herbacetin)
(Gossypetin)
C-8 and C-2@ substituted
(3,5,7,8,2@-pentaOH)
(3,5,6,7,2@,5@-hexaOH)
(3,5,7,8,2@,3@,4@-heptaOH)
C-methylated compounds
3,5,7,8-triOH-8-CH
3
3,5,7-triOH-6,8-diCH
3
(3,5,7,8-tetraOH-6-CH )
3
(3,5,7,4@-tetraOH-6,8-diCH )
3

8-OH-gal-7-Me-8-Ac, 7-Me-8-But
herb-7-Me-8-Ac, 7-Me-8-But, 7,4@-diMe-8-Ac, 7,4@-diMe-8-But
goss-7,4@-diMe-8-Ac, 7,4@-diMe-8-But, 3,7,3@-triMe-8-Ac
7-Me-8-Ac
3,7,8-triMe-2@-Ac
3,7,2@,3@,4@-pentaMe-8-Ac
3-Me, 7-Me
3-Me, 7-Me
3-Me, 7-Me, 3,7-diMe
7-Me

!For structural formulae and numbering system see Figs. 1 and 2, for complex #avonoids and methylene bi#vonoids see Figs. 3 and 4.

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

4

3,5,7,3@,4@-pentaOH Quercetin
C-6 substituted
(3,5,6,7,4@-penta-OH 6-Hydroxy-kaempferol)
C-8 substituted
3,5,7,8-tetraOH 8-Hydroxy-galangin
3,5,7,8,4@-pentaOH Herbacetin

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

757

Fig. 1. Representatives of di!erent #avonoid classes. Notholaenic and isonotholaenic acid.

The colour of the waxes varies from snow white, yellowish white and golden yellow
to orange (and even reddish-orange in Pterozonium). The greatest variability is
observed in Pentagramma triangularis. In species with scant wax production, the lower
leaf surface appears rather greenish-white. Some species show a characteristic colour,
while in others the colour may vary slightly from specimen to specimen. Yellow and
orange are often constant and typical, but transitions are found between yellowishwhite and greenish white. Also in species exhibiting snow-white waxes the composition of the exudate is often, but not always, constant. A correlation between
geographic range, aspect, height, edaphic requirements, the colour and chemistry of
the ceraceous exudate has been reported for Chrysochosma hookeri syn. Notholaena
standleyi (Seigler and Wollenweber, 1983).

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E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Fig. 2. Numbering of #avones, #avonols, etc., compared with numbering of chalcones & dihydrochalcones.
Examples of a b-chalcone and of #avonol-esters. Structures of ceroptene and a-diceroptene.

The colour of the waxes is largely correlated with the chemical composition.
Orange colour is normally caused by chalcones, and so is yellow colour in some cases.
However, yellow colour may also point to the presence of #avonols, in particular of
8-O-substituted #avonols. White exudate material can be composed of dihydrochalcones, #avanones, or #avones (and sometimes of diterpenes). Sometimes slight variations of the farina tint (e.g. faint pink instead of chalky white) are observed, that
cannot be attributed to the presence or absence of certain chemicals.
3.3. Distribution of farinose waxes in Pteridaceae, based on genus level
In the following we list all exudate #avonoids found in relevant genera, regardless of
their occurrence in certain species. Within a given genus, the #avonoid patterns can be
rather uniform (e.g. Pityrogramma), but they can also vary from species to species (e.g.
Chrysochosma), and also within a species (e.g. Cheilanthes argentea, Chrysochosma
trichomanoides).

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

759

Fig. 3. Complex Flavonoids from Pityrogramma spp.

Due to the extremely variable number of species concerned per genus as well as of
#avonoids encountered, the following inventory cannot be presented in a standardized manner. For genera comprising only few farinose species (and producing few
#avonoid aglycones), the #avonoids are cited in the text (e.g. Adiantum, Onychium),
while for others they are compiled in tables (e.g. Pentagramma, Argyrochosma,
Chrysochosma).
The classi"cation follows Tryon (1990) with the following exceptions. Pentagramma
has been accepted as an independent genus of the Cheilanthoideae (Schneider, 1996).
Argyrochosma is accepted, but the remaining species of Notholaena sensu R.M. TRYON

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E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Fig. 4. Methylene bis#avonoids from Pityrogramma triangularis var. triangularis.

are placed in Chrysochosma according to the reinterpretation of the type of Notholaena
R. BR. (Pichi Sermolli, 1989). Taxa of doubtful hierarchical status such as Aleuritopteris have been accepted as groups without taxonomic rank in the genus Cheilanthes.
The order of subfamilies and genera re#ects the diversity of farinose taxa.
1. Cheilanthoideae
1.1 Cheilanthes SW.
Tryon (1990) has included the following taxa in Cheilanthes s.l., but they are
monophyletic units with unknown phylogenetic relationships.
1.1.1. Aleuritopteris Group"Aleuritopteris FE& E * Cheilanthes subgen. Aleuritopteris FRASER-JENK.
This is a very diverse pantropical group which includes farinose species (Aleuritopteris ser. Aleuritopteris CHING) as well as non-farinose species (Leptolepidium HSING et
S.K. WU). The taxonomy and relationships of the group is poorly understood. The
Argentea group and Negripteris group may be close relatives. In farinose species, the

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

761

Fig. 5. Diterpenes and Triterpenes found in fern `waxesa (examples).

lower surface of the lamina is covered with mostly whitish, only rarely golden yellow
waxes. Almost all species have been analyzed for their exudate composition:
Cheilanthes agetae (SAIKI) C.M. KUO, C. albidissima FRASER-JENK., C. anceps BLANF.,
C. bicolor (ROXB. et GRIFF. ex FRASER-JENK., C. bullosa KUNZE, C. chrysophylla HOOK.,
C. dalhousiae HOOK., C. dubia OPE, C. farinosa (FORSSK.) KAULF., C. formosana HAYATA,
C. grisea BLANF., C. krameri FRANCH. ET SAV., C. kuhnii MILDE, C. papuana C.CHR., C.
platychlamys (CHING) FRASER-JENK., C. pulveracea C.PRESL, C. subdimorpha B.K.
NAYAR, C. welwitschii HOOK. ex BAKER. The following analyzed taxa are currently
plazed in Aleuritopteris: A. afra PIC.SERM., A. decursiva (FORSSK.) SAIKI, A. yava SAIKI,
and A. stenochlamys CHING.
Components: The #avonoid aglycones encountered in this group are compiled in
Table 2. The species show infraspeci"c as well as intraspeci"c di!erences in their farina
composition. Many unpublished data are available; the results of detailed analysis will
be published elsewhere. (Wollenweber, 1976b, c, 1977b, 1982a, 1997; Serizawa and
Wollenweber, 1977; Scheele et al., 1987).
1.1.2. Argentea Group"Aleuritopteris FEH E series argentea CHING.
The taxonomically poorly known group occurs from Korea, Japan, China, Taiwan,
Indochina to northern Thailand, and in the Himalayas. White or yellow waxes cover
the lower surface of the lamina. The non-farinose fern Cheilanthes concolor (LANGSD. et
FISCH.) R.M.TRYON et A.F.TRYON resembles Cheilanthes argentea (GMEL.) FEH E in many
morphological features. The group includes about 16 species (Ching and Shing, 1990).

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E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Table 2
Flavonoid aglycones found in `Cheilanthesa
Argentea group

Aleuritopteris group

Chalcones
2@,6@-diOH-4@-OMe (in var. sulphurea only)

2@,6@-diOH-4@-OMe

Dihydrochalcone
*

2@,6@-diOH-4@-OMe

Flavanones
5,4@-diOH-6,7-diOMe, 5-OH-6,7,4@-triOMe;
5,4@-diOH-7,8-diOMe, 5-OH-7,8,4@-triOMe,
5,6-diOH,7,8,4@-triOMe, 5,4@-diOH-6,7,
8-triOMe, 5-OH-6,7,8,4@-tetraOMe
Flavones
Scutellarein-6,7-diMe; 6-OH; Isoscutellarein-6,8diOMe/ 6,8,4@-triOMe-#avon/ 6,7,8-triOMe
Flavonols
6-Hydroxykaempferol-6,7,4@-triMe;
herbacetin-7-Me/ 7,8-diMe/ 7,8,4@-triMe;
3,5,4@-triOH-6,7,8-OMe

Pinocembrin-7-Me; 5,8-diOH-7-OMe-#avanone;
eriodictyol-7-Me/ 7,3@-diMe/ 7,3@,4@-triMe;
5,7,4@-triOH-2@-OMe-#avanone; 5,4@,5@-triOH-7,3@diOMe/ 5,5@-diOH-7,3@,4@-triOMe/ 5,4@-diOH7,3@,5@-triOMe/ 5-OH-7,3@,4@,5@-tetraOMe-#avanone
Apigenin/ 7-Me/ 4@-Me/ 7,4@-diMe

Galangin-7-Me; Kaempferol, kae-3-Me/ 7-Me/
4@-Me/ 3,7-diMe/ 3,4@-diMe/ (5,7-diMe)/
3,7,4@-triMe/ 5,7,4@-triMe; Quercetin-3,7-diMe/
7,3@-diMe/ 3,7,4@-triMe/ 7,3@,4@-triMe/
3,7,3@,4@-tetraMe

Only two species have been investigated chemically: Cheilanthes argentea (GMEL.) FEH E
and C. tamburii (HOOK.) CHING. C. argentea is part of a species complex, which need
further taxonomic studies.
Components: The analyzed specimens of C. argentea show a remarkable diversity of
farina components. Their #avonoid patterns indicate the existence of two chemotypes
(Wollenweber, 1982a; Wollenweber and Roitman, 1991). This result is also supported
by the existence of two di!erent diterpenes in the farina: specimens from Japane and
mainland Asia exhibit 3-hydroxy-anticopalic acid, while specimens from Taiwan
exhibit anticopalic acid (Wollenweber et al., 1982a). The #avonoid aglycones are
compiled in Table 2, compared with those of the Aleuritopteris group and the
Brandigei group. (Wollenweber et al., 1980).
1.1.3. Brandegei Group R.M.TRYON and A.F.TRYON
This group consists of "ve South American species (Tryon et Tryon, 1982). The
farinose indumentum on the lower surface of the lamina is often yellow to orange.
Only C. aurantiaca T. MOORE ("Notholaena aurantiaca) and C. aurea BAKER have
been studied chemically.
Components: Cheilanthes aurantiaca exhibits 2@,6@-diOH-4@-OMe-chalcone, while
C. aurea exhibits a so far unidenti"ed chalcone. (Wollenweber, 1977b, 1982a).

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

763

1.1.4. Negripteris Group"Negripteris PIC.SERM.
Pichi Sermolli (1946) has described this taxon as a distinct genus based on an
atypical sporangium, but other characters indicate close relationships to Aleuritopteris
group. The group is monotypic, the sole species N. scionana (CHIOV.) PIC.SERM.
occurring in East Africa and Arabia Whitish or slightly yellowish farina are found on
the lower surfaces of the lamina.
Components: Fragments of several specimens have been studied for their exudate
components,1 but these could not be identi"ed. Thin layer chromatograms indicate
a certain similarity to #avonoid patterns observed in Cheilanthes argentea.
1.1.5. Sinopteris Group"Sinopteris C. CHR. ET CHING
The group consists of only two species, endemic in China, with some unique
characters. It may be closely related to the Argentea-group. Only Cheilanthes albofusca
BAKER has been examined chemically.2
Components: One sample exhibits Kae-7,4@-diMe#apig-7,4@-diMe, whereas three
others exhibit luteolin-7,3@,4@-triMe. We do not dare to give any interpretation.
1.2. Argyrochosma (J.SM.) WINDHAM
Nearly all species of the genus exhibit a remarkable farinose indumentum. Most
species have been analysed for their exudate chemistry, but publications are scattered.
So far no comprehensive survey allowing comparisons has been published. Flavonoid
data are available for A. chilensis (FEH E and REMY) Windham, A. dealbata (PURSH)
WINDHAM, A. delicatula (MAXON ET WEATH.) WINDHAM, A. fendleri (KUNZE) WINDHAM,
A. incana (C.PRESL) WINDHAM, A. limitanea (MAXON) WINDHAM, A. microphylla (METT.
EX KUHN) WINDHAM, A. nivea (POIR.) WINDHAM, A. pallens (WEATH. in R.M. TRYON)
WINDHAM, A. palmeri (BAKER) WINDHAM, A. peninsularis (MAXON & WEATH.)
WINDHAM, A. pilifera (R.M. TRYON) WINDHAM. Since no material for analysis could be
obtained, A. formosa (LIEBM.) WINDHAM, A. jonesii (MAXON) Windham, A. lumholtzii
(MAXON and WEATH.) Windham and A. stuebeliana (HIERON.) WINDHAM have not yet
been checked. Notholaena bryopoda MAXON lacks an epithet but it is a member of the
genus. (Windham, 1987).
Components: All #avonoids found in representatives of this genus are listed in Table
3. Note: The species di!er greatly in the composition of their farinose waxes. Several of
them exhibit species-speci"c #avonoid patterns, some #avonoids even occur exclusively in one single species. The list of #avonoids found in the genus may insofar be
somewhat misleading.
In this context we also brie#y report the occurrence of dihydrostilbenes ("bibenzyls, see Fig. 1) and terpenoids in Argyrochosma exudates. A. chilensis, A. dealbata,
A. limitanea var. limitanea and A. nivea var. nivea exhibit isonotholaenic acid, while

1 Coll. ETS 36; Sodore Hot Springs, Awash-River Valley, Ethiopia, June 1970 [L].
2 Cavalarie 57, Tinla, S.W. China, 1911 [K]; China, Yunnan, Maire, C. Bonati 6105 B [ZT]; Yunnan,
Maire 6558 [US]; Yunnan, Rock 4879 [US].

764

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Table 3
Flavonoid aglycones (and bibenzyls) found in `Notholaenaa
Argyrochosma

Chrysochosma

Chalcones
2@,6@-diOH-4@-OMe/ 2@,6@-diOH-4@,4diOMe/2@,4-diOH-4@,6@-diOMe

*

b-Chalcones
2@,b,4@triOH-4@,6@-diOMe/ 2@,b-diOH4@,6@,4triOMe
Dihydrochalcone
2@,6@-diOH-4@-OMe
Flavanones
Pinocembrin, naringenin-7-Me/
4@-Me/ 7,4@-diMe; eriodictyol-7-Me/
4@-Me/ 7,3@-diMe/7,4@-diMe/
7,3@,4@-triMe

*

2@,6@-diOH-4@-OMe/ 2@,6@,4-triOH-4@-OMe/ 2@,6@-diOH-4@,
4-diOMe
Pinocembrin-7-Me; 5,8-diOH-7-OMe-#avanone; eriodictyol-7-Me/ 7,3@-diMe/ 7,3@,4@-triMe; 5,7,4@-triOH-2@OMe-#avanone; 5,4@,5@-triOH-7,3@-diOMe/ 5,5@-diOH7,3@,4@-triOMe/ 5,4@-diOH-7,3@,5@-triOMe/ 5-OH-7,3@,4@,
5@-tetraOMe-#avanone

Flavanone-ester
5-OH-7-OMe-8-OAc; 3,5-diOH-7,8-diOMe-2@-OAc;
Dihydroyavonols
Dihydroyavonol-esters
aromadendrin-7-Me-3-Ac/3-But/4@-But; 3,5-diOH-7,
8-diOMe-2@-OAc
Flavones
Apigenin-7-Me/ 4@-Me/ 7,4@-diMe;
luteolin-7,3@-diMe/ 7,4@-diMe
Flavonols
Galangin-3-Me/ 5-Me/ 3,7-diMe;
kaempferol/ 3-Me/ 7-Me/ 4@-Me/
3,7-diMe/ 3,4@-diMe/ 7,4@-diMe/
3,7,4@-triMe; quercetin-3,3@-diMe/
7,3@-diMe/ 3,7,3@-triMe/ 3,7,4@-triMe/
3,7,3@,4@-tetraMe

Flavonol-Esters
*

Dihydrostilbenes ("bibenzyls)
notholaenic acid, isonotholaenic acid

Apigenin/ 7-Me/ 4@-Me/ 7,4@-diMe; Scutellarein-6,7-diMe/
6,7,4@-triMe; Luteolin/ 7-Me/ 3@-Me/ 4@-Me/ 7,3@-diMe/ 7,4@diMe; 5,2@-diOH-7,8-diOMe
Galangin/ 3-Me/ 5-Me/ 7-Me/ 5,7-diMe; kaempferol/ 3-Me/
7-Me/ 4@-Me/ 3,7-diMe/ 3,4@-diMe/ 7,4@-diMe/ 3,7,4@-triMe;
herbacetin-7-Me/ 7,4@-diMe; quercetin-3-Me/ 7-Me/ 3,7diMe/ 7,3@-diMe/ 3,7,4@-triMe; myricetin-3,7,3@,4@-tetraMe/
3,7,3@,4@,5@-pentaMe; 5,2@-diOH-3,7,8-triOMe; 5,2@,3@-triOH3,7,8-triOMe; 3,5,2@-triOH-7,8,4@-triOMe/ 5,4@-diOH-3,7,8,2@tetraOMe/ 5-OH-3,7,8,2@,4@-pentaOMe; 5,2@,5@-triOH-3,7,8triOMe/ 5,5@-diOH-3,7,8,2@-tetraOMe; 5,2@,4@-triOH-3,6,7,8tetraOMe-#av., 5,4@-diOH-3,6,7,8,2@-pentaOMe/ 5,2@-diOH3,6,7,8,4@-pentaOMe/ 5-OH-3,6,7,8,2@,4@-hexa-OMe-#avonol.
8-OH-gal-7-Me-8-Ac/ 8-But; herb-7-Me-8-Ac/ 8-But, herb7,4@-diMe-8-Ac/ -8-But; goss-7,4@-diMe-8-Ac/ 8-But, goss3,7,3@-triMe-8-Ac; 3,5,2@-triOH-7-Me-8-OAc; 5,6,5@-triOH3,7,8-triMe-2@-OAc; 5-OH-3,7,2@,3@,4@-pentaMe-8-OAc;

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765

A. limitanea var. mexicana produces notholaenic acid (one specimen showed both isomers).
A. delicatula, A. incana, A. pallens, A. palmeri, A. peninsularis and A. pilifera produce
terpenoids instead (Wollenweber et al., 1993). Diterpenes from A. pallens and A. incana
were reported by RuK edi et al. (1989). For examples of terpenoid structures see Fig. 5.
(Roitman et al., 1992; Wollenweber, 1976c, 1977b, 1981, 1982a, 1984, 1989; Wollenweber and Favre-Bonvin, 1979; Wollenweber and Roitman, 1991; Wollenweber et al.,
1980,1993).
1.3. Chrysochosma (J.SM.) KUEMMERLE ("Notholaena SENSU R.M.TRYON non R.
BR.)
All species of the genus possess farina, except for C. ekmanii (MAXON) PIC.SERM.
Flavonoid data are available for C. aznis (METT.) PIC.SERM., C. aliena (MAXON)
PIC.SERM., C. ascherboniana (KLOTSCH) PIC.SERM., C. californica (D.C.EATON)
PIC.SERM., C. candida (M. MARTENS and GALEOTTI) KUEMMERLE var. candida, C.
candida (M. MARTENS and GALEOTTI) KUEMMERLE var. copelandii (C.C.HALL)
PIC.SERM., C. galapagensis (WEATH. and STENSON) PIC.SERM., C. galeotti (FEH E)
PIC.SERM., C. grayi (DAVENP.) PIC.SERM., C. greggii (METT. EX KUHN) PIC.SERM., C.
hookeri KUEMMERLE ("Notholaena standleyi MAXON), C. lemmonii (D.C. EATON)
PIC.SERM., C. neglecta (MAXON) PIC.SERM., C. rigida (DAVENP.) PIC.SERM., C. rosei
(MAXON) PIC.SERM., C. schawneri (E. FOURN.) PIC.SERM., C. sulphurea (CAV.)
KUEMMERLE, C. trichomanoides (L.) PIC.SERM.
Flavonoid data are listed in Table 3. The above comments to the #avonoid survey
of Argyrochosma also apply to Chrysochosma. A survey on the triterpenes found in C.
candida, C. grayii, C. greggii, C. neglecta, C. rigida and C. schawneri (cyclolanostane,
dammarane and hopane derivatives) is given in (Arriaga-Giner et al., 1997). For
examples of some structures see Fig. 5.
(Arriaga-Giner and Wollenweber, 1986, Arriaga-Giner et al., 1987; Iinuma et al., 1986a;
Jay et al., 1979a, b, 1981, 1982; Scheele et al., 1987; Seigler and Wollenweber, 1983;
Wollenweber, 1976a,b,c, 1977a,b, 1982a, 1984, 1989; Wollenweber and GoH mez, 1979;
Wollenweber and Roitman 1991; Wollenweber and Yatskievych, 1982; Wollenweber et
al., 1978a,b, 1982b, 1988).
The comparative table of exudate #avonoids in Argyrochosma and Chrysochosma
(Table 3) shows some noticeable features: Chalcones and b-chalcones are produced
only in Argyrochosma, whereas Chrysochsoma produces often dihydrochalcones.
Flavanone- and dihydro#avonol-esters as well as #avonol-esters are found only in
Chrysochosma. Further, Chrysochosma shows a greater variety of #avanones, #avones,
and #avonols. Dihydrostilbens, on the other hand, were reported only from Argyrochosma. These phytochemical results might underline the division of the previous
genus Notholaena sensu R.M. Tryon into two distinct genera.
1.4. Pentagramma YATSK., WINDHAM and WOLLENW EBER (1990)
All species/subspecies of the genus exhibit remarkable yellow or whitish farina,
mostly on the lower lamina surface (P. pallida, P. triangularis subsp. triangularis,

766

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

P. triangularis subsp. semipallida and P. triangularis subsp. maxonii), or a resinous
exudate (P. triangularis subsp. viscosa). They have been analysed in extensive studies
by D.M. Smith (1980) and by Wollenweber et al. (Refs. see below).
Components: An extremely high number of exudate #avonoids is known from
Pentagramma, but many of these occur only in certain species or subspecies. It does
not make sense, therefore, to list them for the genus in total. In the following we hence
give the #avonoid composition for the species.
P. pallida (WEATH.) YATSK., WINDHAM and WOLLENWEBER: Major #avonoids of the
abundant white farina are: 5,7-diOH-6-CH -#avanone (strobopinin), 5,7-diOH-83
CH -#avanone (cryptostrobin), 5,7-diOH-6,8-di-CH -#avanone (desmethoxymat3
3
teucinol). These C-methyl-#avanones are not produced by any other species, so they
are quite characteristic for P. pallida. Minor #avonoids are pinocembrin-5-Me,
pinocembrin-5,7-diMe, 7-OH-5-OMe-8-CH -#avanone, 2@,4@-diOH-6@-OMe-chal3
cone (carda-monin), 2@-OH-4@,6@-diOMe-chalcone (#avokawin B), 2,4@-diOH-6@OMe-3@-CH -chalcone, 2@-OH-4@,6@-diOMe-3@-CH -chalcone (aurentiacin).
3
3
(Wollenweber et al., 1979a, 1981a,b; Markham et al., 1987).
P. triangularis (KAULF.) YATSKIEVYCH, WINDHAM and WOLLENWEBER subsp. triangularis * The major and species-speci"c product is ceroptene (Fig. 2). This
chalcone-like compound exhibits brilliant yellow #uorescence and can, therefore, be
detected directly on fern material viewed under UV . Minor products: a-diceropten
366
(trace constituent only), 2@-OH-4@,6@-diOMe-chalcone (#avokawin B), 2@,6@,4-triOH4@-OMe-3@-CH -chalcone (triangularin), 5-OH-7-OMe-6-CH -#avanone, 5-OH-73
3
OMe-8-CH -#avanone, 8-hydroxy-galangin, 5,8-diOH-3,7-diOMe-#avonol (8-OH3
gal-3,7-diMe), 3,5,7-triOH-8-CH -#avonol, 3,5,7-triOH-6,8-diCH -#avonol, 5,73
3
diOH-3-OMe-8-CH -#avonol, 5,7-diOH-3-OMe-6,8-diCH -#avonol, 3,5-diOH-73
3
OMe-8-CH -#avonol, 3,5-diOH-7-OMe-6,8-di CH -#avonol, 3,5,8-triOH-7-OMe-63
3
CH -#avonol, 5,7,8-triOH-3-OMe-6-CH -#avonol, 3,5,7-triOH-8-OMe-6-CH 3
3
3
#avonol (pityrogrammin), 5,8-diOH-3,7-diOMe-6-CH -#avonol. Two methylene-bis3
#avonoids (Fig. 4, structures A and B) were the "rst representatives of this group of
substances found in nature (Roitman et al., 1993). Four further methylene-bis#avonoids were reported later (Fig. 4, str. C}F) (Iinuma et al., 1994, 1997).
(Dietz et al., 1981; Roitman et al., 1993; Vilain et al., 1987; Wollenweber, 1989;
Wollenweber and Roitman, 1991; Wollenweber and Smith, 1981; Wollenweber et al.,
1985; Yatskievych et al., 1990).
P. triangularis subsp. viscosa (NUTT. EX D. EATON) YATSKIEVYCH, WINDHAM and
WOLLENWEBER produces 2@,6@,4@-triOH-4@-OMe-3@-CH -dihydrochalcone, herbacetin3
3,7-diMe, and 3,5,4@-triOH-7-OMe-6,8-diCH -#avonol. (Wollenweber et al., 1979b).
3
P. triangularis subsp. semipallida (J. HOWELL) YATSKIEVYCH, WINDHAM and
WOLLENWEBER exhibits kaempferol-3,4@-diMe as major product, along with traces of
gal-3-Me, gal-5-Me, gal-5,7-diMe, and kae-3-Me.
P. triangularis subsp. maxonii (WEATH.) YATSKIEVYCH, WINDHAM and WOLLENWEBER
exhibits galangin and traces of some so far unidenti"ed #avonoids (some of which
might be identical with compounds found in P. triangularis var. triangularis).
Wollenweber et al. in 1985 reported the #avonoid patterns of two collections that
were not ascribed to distinct varieties or chemotypes. In addition to a series of

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767

#avonoids reported above for P. triangularis, these collections exhibit 2@,6@-diOH-4@OMe-chalcone, 2@,6@-diOH-4@,4-diOMe-chalcone, 2@,6@-diOH-4@-OMe-dihydrochalcone, 2@,6@-diOH-4@,4-diOMe-dihydro-chalcone, pinocembrin-7-Me, kae-7-Me, kae3,7-diMe, herbacetin-8,4@-diMe, herb-3,8,4@-triMe and 2@,6@,4-triOH-4@-OMe-3@,5@diCH -dihydrochalcone. } For a detailed discussion of #avonoid patterns in the
3
Pentagramma ("Pityrogramma) triangularis complex see Smith (1980). (Wollenweber,
1979; Wollenweber and Dietz, 1980).
2. Taenitidoideae (C.PRESL) R.TRYON
2.1. Pityrogramma LINK
All 14 species possess farinose greenish-white, white or yellow waxes on the lower
side of the sterile and fertile parts of the lamina. The composition of the farina was
analysed for most of the species: P. argentea (WILLD.) DOMIN, P. aurantiaca (HIERON.)
C. CHR., P. austroamericana DOMIN, P. calomelanos (L.) LINK, P. chrysoconia (DESV.)
MAXON ex DOMIN, P. chrysophylla (SW.) LINK, P. dealbata (C.PRESL) R.M.TRYON,
P. dukei LELLINGER, P. ebenea (L.) PROCTOR, P. lehmannii (HIERON.) R.M. TRYON,
P. pulchella (T. MOORE) DOMIN, P. sulphurea (SW.) MAXON, P. tartarea (CAV.) MAXON,
P. trifoliata (L.) R.M.TRYON, P. WILLIAMSII PROCTOR.
Components: 2@,6@-diOH-4@-OMe- and 2@,6@-diOH-4@,4-diOMe-chalcone, 2@,6@diOH-4@-OMe- and 2@,6@-diOH-4@,4-diOMe-dihydrochalcone (exceptional: 2@,6@,4triOH-4@-OMe-ch and 2@,6@,4-triOH-4@-OMe-dhch); galangin, gal-7-diMe, kaempferol-3,7-diMe, apigenin-7-Me and ap-7,4@-diMe (Wollenweber, 1972, 1976a, 1977a,
1979, 1980; Hitz et al., 1982). Note: chalcones and dihydrochalcones are major
products in all species, while #avones and #avonols are found as minor products in
only a few species. The complex #avonoids D-1 and D-2a/ D2-b (Wagner et al., 1979;
Donnelly et al., 1987; Iinuma et al., 1993) (see Fig. 3) are found in P. calomelanos, P.
chrysoconia, P. dealbata, P. sulphurea and P. trifoliata. (Wollenweber and Dietz, 1980.
Complex #avonoids X-1 and X-2 (Favre-Bonvin et al., 1980Iinuma et al., 1986b) were
detected in individual plants of P. austroamericana (" P. calomelanos var. aureoyava
[Hook] Weath. ex Bailey), P. sulphurea and P. tartarea (Wollenweber and Dietz,
1980). The structurally closely related `calomelanolsa A-J (Fig. 3) were reported from
P. calomelanos from Indonesia (Asai et al., 1992) [in fact, it might be P. austroamericana]. The complex #avonoids T-1, T-2, T-3 (Dietz et al., 1980) occur in P.
sulphurea, P. trifoliata and P. williamsii (Wollenweber and Dietz, 1980).
2.2. Pterozonium FEH E
At least three out of 14 species possess glandular paraphyses which excrete a more
or less obvious yellow or reddish-orange farina: P. brevifrons (A.C.SMITH) LELLINGER,
P. reniforme (MARTIUS) FEH E, P. scopulinum LELLINGER.
Components: P. brevifrons and P. scopulinum exhibit 2@,6@-diOH-4@,4-diOMe-chalcone along with an unidenti"ed chalcone, while P. reniforme shows an unknown,
less polar chalcone. The description of the paraphyses of P. linearis LELLINGER

768

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

(`cera brunneo-rubra a, Lellinger, 1967) suggests that the latter species also excretes
chalcone(s). (Wollenweber, 1979).
2.3. Onychium KAULF
Only one out of some eight species, namely O. siliculosum (DESV.) C.CHR.
("Onychium auratum KAULF.), exhibits a yellow farinose exudate on the outer surface
of the pseudoindusia.
Components: The farina is composed of 2@,6@-diOH-4@-OM-chalcone and 2@,6@diOH-4@,5@-diOMe-chalcone.
(Ramakrishnan et al., 1974; Wollenweber, 1982b). The corresponding #avanones
(pinostrobin and 5-OH-6,7-diOMe-#avanone, named onysilin), as reported by Wu et
al. in 1981, were shown to be artifacts (Wollenweber, 1982b).
2.4. Cerosora (BAKER) DOMIN
Only one of the three species, namely C. chrysosora (BAKER) DOMIN, shows
a farinose indumentum (yellow). The glandular hairs are placed between the sporangia
on the fertile lamina.
Components of the farina have not been analyzed, due to lack of material.
3. Adiantoideae (C.PRESL) R.M.TRYON
3.1. Adiantum L.
Farina is only known from Adiantum poiretii WIKSTR. var. sulphureum (KAULF.)
R.M.TRYON ("A. sulphureum KAULF.) with a more or less dense yellow wax on the
outer surface of the pseudoindusia and sometimes on parts of the lower surface of the
lamina. This variety is distinct from var. poretii only in the presence of farinose waxes.
Specimens with scarce farina have been collected in Chile. A. poiretii is widespread but
scattered distributed from southern South America to Mexico, from (temperate and
tropical) Africa to India. However, farinose plants (var. sulphureum) are only known
from southern South America (Chile) and in parts of Africa (Kenya, Tanzania,
Zimbabwe, South Africa). Detailed studies are needed to understand the evolution of
farinose coatings in this species.
Components: In some plants of A. poiretii var. sulphureum, 2@,6@-diOH-4@-OMechalcone and 2@,6@-diOH-4@-diOMe-dihydrochalcone are the major components,
accompanied by galangin and gal-7-Me (izalpinin). Other plants exhibit 2@,4@,6@trihydroxy-chalone along with pinocembrin and naringenin-7-methyl ether
(sakuranetin). The existence of two chemotypes should, therefore, be considered. No
correlation is observed between the exudate #avonoid pattern and the geographic
origin (Wollenweber, 1976b, 1979).

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769

4. Non-farinose species
Externally deposited #avonoid aglycones are also found in some non-farinose ferns.
4.1. Platyzomatoideae (NAKAI) A.F.TRYON
4.1.1. Platyzoma R.BR.
A monotypic genus, endemic in Australia (P. microphylla R.BR.). This fern does not
really produce a farina: `Two- or three-celled, capitate glands are abundant on the
pinnae, which usually have accumulations of yellowish exudate on the surface. Freshly
collected specimens have a characteristic scent and, when pressed, leave an oily stain
on paper.a (Wollenweber et al., 1987).
Components: Major #avonoids are 2@,6@-diOH-4@-OMe-chalcone and 2@,6@-diOH4@,5@-diOMe-chalcone. Minor components and trace constituents are pin-7-Me; gal5-Me, gal-7-Me, gal-3,7-diMe, kae-7-Me, kae-3,7-diMe, kae-3,7,4@-triMe. (Wollenweber and Roitman, 1991; Wollenweber et al., 1987).
4.2. Cheilanthoideae
Species of the genus Cheilanthes with glandular hairs (C. kaulfusii KUNZE, C.
micropteris SW., C. pilosa GOLDM., C. pruinata KAULF., C. viscida DAVENP.)
Cheilanthes kaulfussii. Components: Galangin, gal-3-Me, gal-3,7-diMe, kaempferol,
kae-3,7-diMe, kae-3,7,4@-triMe.
(Scheele et al., 1987; Wollenweber, 1997). (a diterpen is reported in RuK edi et al.,
1989).
Cheilanthes micropteris. One of the samples seen (Monberg, 1394) exhibts at least
two #avonoid aglycones, but these could not be identi"ed, due to the paucity of
material.
Cheilanthes pruinata. Components: Galangin and gal-3-Me (Wollenweber, 1998
unpubl.)
Cheilanthes viscida. Components: Apigenin, ap-7-Me, ap-4@-Me, ap-7,4@-diMe.
(Wollenweber, 1997).
4.3. Several species of the genus Pellaea LINK lacking glandular trichomes have
been found to exhibit external #avonoid aglycones: p. andromedaei-folia (KAULF.) FEH E,
p. brachyptera (T. MOORE) baker, p. bridgesii HOOK., P. mucronata (D.C.EATON) d.C.
EATON, p. quadripinnata (FORSSK.) Prantl and p. truncata GOODING ("p. longimucronata HOOK.).
Components: Galangin, gal-3-Me, gal-7-Me; Kaempferol, kae-7-Me, kae-4@-Me,
kae-3,4@-diMe, kae-3,7,4@-triMe; Quercetin-7-Me, qu-7,3@-diMe.
(Wollenweber, 1979 and unpublished data).

770

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

4.4. Taenitidoideae
Jamesonia HOOK.

ET

GREV.

A tropical American genus of about 19 species which is closely related to Eriosorus
FEH E. The leaves of both genera are usually densely pubescent and often the aglandular
hairs are mixed together with glandular ones. Tryon (1962) noted a vernicose or
crustoce upper surface of the pinnae for Jamesonia imbricata var. glutinosa (KARST.)
A.F.TRYON and J. scammanae A.F.TRYON. Traces of #avonoids were recovered in
specimens of J. imbricata var. glutinosa, but it was not possible to identify the
components. The lower surface of these species is densely covered with whitish hairs,
and whitish crusts are only detectable on the upper side and parts of the rachis. It is
not clear, however, if the observed traces of #avonoids are the products of the
glandular hairs and/or part of the relatively thick cuticle.
3.4. Chemotaxonomy
Farinose waxes are found in about 80 pteridophyte species out of 14 genera of only
one family, the Pteridaceae. The family is divied in six subfamilies with more than 800
species in about 35 genera. Farinose species are restricted to small fractions of its three
subfamilies Adiantoideae, Cheilanthoideae, and Taenitidoideae (for a synopsis see
Table 4). This scattered distribution suggests a polyphyletic origin of farinose waxes
within the family and subfamilies. Although no phylogenetic analysis exists for
Pteridaceae, proposed relationships (Tryon, 1990) indicate an independent evolution
of genera with farinsoe waxes. This hypothesis is further supported by recent cladistic
analysis of the subfamily Cheilanthoideae (Gastony and Rollo, 1995).

Table 4
Distribution of farinose ferns (only #avonoids considered) in four subfamilies of the Pteridaceae
Taxon

Number of farinose taxa
per subfamily or genus

Total number of taxa
per subfamily or genus

Cheilanthoideae
1.1 Cheilanthes
1.2 Argyrochosma
1.3 Chrysochosma
1.4 Pentagramma

4
30
20
17
2

15
150
22
17
2

Taenitidoideae
2.1 Pityrogramma
2.2 Pterozonium
2.3 Onychium
2.4 Cerosora

4
14
3
1
1

11
14
14
8
3

1
1

1
150

Adiantoideae
3.1 Adiantum

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

771

Farinose species often co-occur with non-farinose species in the same genus (e.g.,
Cerosora, Cheilanthes subgen. Aleuritopteris). Some genera such as Pityrogramma and
Pentagramma are characterized by the (almost) general presence of farinose waxes,
whereas in the neo-tropical Argyrochosma and Chrysochosma only a few species lack
such coatings. In Adiantum, only one out of more than 100 species exhibits a farinose
exudate (Adiantum sulphureum var. poiretii).
Within the genus Cheilanthes, the provisionally segregated "ve groups may represent monphyletic units. Non-farinose species are included e.g. in the Aleuritopteris
group, which otherwise mainly consist of farinose species. Previously, some authors
separated the non-farinose taxa as genus Leptolepidium S.K. Wu, but there exists
a close relationship to farinose species of the Aleuritopteris group (Fraser-Jenkins,
1992). Close a$nities of farinose and non-farinose species are also found in Cerosora,
in which two very closely related species di!er mainly in the presence (C. chrysosora)
or absence (C. sumatrana HOLTTUM) of glandular paraphyses producing farinose
coatings. These patterns again suggest a polyphyletic origin of farina production,
including the possibility of repeated loss and gain of this feature. Furthermore, the
development of waxes may be suppressed or stimulated by genetic factors. This is
indicated by the variability in the density of coatings in widespread ferns, such as
Pityrogramma calomelanos. Environmental factors, on the other hand, seem to play
a secondary role, if any. They may only in#uence the amount of waxes produced
(quantitative aspect), but not the chemical composition (qualitative aspect). No
matter, whether e.g. a sample of a certain Notholaena species is taken from a more than
hundred years old herbarium specimen, or freshly collected in the Sonoran Desert, or
clipped from a plant cultivated in a greenhouse in Europe, the #avonoid pattern is
constant, at least in qualitative respect.
The presence of glandular hairs is a prerequisite for the development of farinose
waxes. The suppression of trichome development results in the reduction or lack of
farinose waxes. Examples are the species of the proposed genus Leptolepidum, which
di!er from other species of Aleuritopteris only in the absence of trichomes on the
lamina. In other cases, e.g. in Pterozonium, hairs are present, but they lack a glandular
apical cell, or the glandular cells do not exude waxes. Therefore the lack of farinose
waxes can be the result of di!erent mutations (deletions). Some species of Cheilanthes,
which do not produce a farinose coating, possess glandular hairs (e.g. Cheilanthes
micropteris, C kaulfussii, C. viscida), thus indicating relationships to farinose species.
Analyses of C. kaulfussii and C. viscida (Scheele et al., 1987; Wollenweber, 1979) have
shown the presence of similar components in these glands. Such components are also
found accumulated on the leaf surface of non-farinose species with thick cuticles in the
genus Pellaea (Wollenweber, 1979 and unpublished results), where they are probably
excreted by unmodi"ed epidermal cells.
The colour of the waxes may be a useful character in the identi"cation of at least
some species, e.g. Cheilanthes chrysophylla and C. welwitschii, but in other taxa
infraspeci"c variation is also observed. The colour is determind by various
factors such as the chemical composition, the microstructure and size of crystals
of the quasi-crystalline material, and to a certain extent also to the density of
exudates.

772

Taxon

Chalcones

Dihydro-chalcones

Flavanones

Dihydro-#avonols

Flavonols

Flavones

Cheilanthoideae
1.1.1 Aleuritopteris Group
1.1.2 Argentea Group
1.1.3 Brandegei Group
1.1.4 Negripteris Group
1.1.5 Sinopteris Group
1.2 Argyrochosma
1.3 Chrysochosma
1.4 Pentagramma

#
#
#
?
!
#
!
#C-6,8

#
!
!
?
!
#
#
#C-6,8

#
#
!
?
!
#
#C-2,5 E
#C-6,8

!
!
!
?
!
!
E
!

#
#
!
?
#
#
#C-2,5 E
#C-6,8

#
#
!
?
#
#
#C-2,5
#C-6,8 B

Taenitidoideae
2.1 Pityrogramma
2.2 Pterozonium
2.3 Onychium
2.4 Cerosora

#
#
#
?

#
!
!
?

#
!
!
?

!
!
!
?

#
!
!
?

#
!
!
?

Adiantoideae
3.1 Adiantum

#

#

#

!

#

!

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

Table 5
Flavonoid aglycones in Pteridaceae, an overview of all genera with farina. Symbols: #"present,-"absent,?"unknown. Rare components are added as
O-2,5"2- and/or 5-O-substituted #avonoids, C-6,8"6- and/or 8-C-methylated #avnoids, E"#avonoid esters, B"bi#avonoids. The components are found
in one or more taxa of the genus/group, but mostly they are not present in all. Especially the rare components are often restricted to one or few species

E. Wollenweber, H. Schneider / Biochemical Systematics and Ecology 28 (2000) 751}777

773

Most of the farina components analyzed so far are derivates of the #avonoid
biosynthetic pathway, with the occasional accumulation of terpenoids in addition.
The composition of the farina may vary, as has already been exempli"ed in the
description of the respective genera and units (survey see Table 5). It may be
of interest that in many cases only chalcones constitute the #avonoid pattern.
Similarly, other exudates consist only of widespread components, such as apigenin
and galangin derivatives. Occasionally, rare components with a relative
complex substitution pattern such as C-6,8-disubstituted #avones and #avonols,
#avonoid esters, etc occur. They seem to be restricted to the cheilanthoid
genera Argyropchosma, Chrysochosma and Pentagramma in the New World,
and to the SE Asian Cheilanthes argentea complex, a fact that may have
taxonomic signi"cance. However, the chemical composition of the farinose waxes
o!ers generally only little information with regard to intergeneric relationships (Table
5). This may be correlated with the scattered distribution of farina and exudate
production within genera and the possibility of polyphyletic origin both of taxa and of
farina production.
The chemical composition of the farina proved to be useful in populational studies,
since some variability is observed, leading frequently to de"ning chemotypes (see
Table 7.1 in Wollenweber, 1995). This does not exclude the usefulness of such patterns
at the speci"c level. Some components, such as ceroptene, which is known exclusively
from Pentagramma triangularis var. triangularis., are de"nitively species-speci"c. The
#avonoid patterns often characterise closely relate