Glandular hairs in the genusDrosera (Droseraceae)

P1. Syst. Evol. 194:163-172 (1995) Plant

Systematics and

Evolution © Springer-Verlag 1995 Printed in Austria

Glandular hairs in the genus Drosera (Droseraceae)

R. LANGER, I. PEIN, and B. Kope

Received March 21, 1994; in revised version October 19, 1994

Key words: Droseraceae, Drosera. - Glandular hairs, anatomy.

Abstract: On the leaves and sepals of 52 species, representing all sections of the genus Drosera except one, 14 different types of glandular hairs were found: two-celled papillae, peltate scales, several types with unbranched, bi- or multiseriate stalk with a two- or multicellular gland, and one type with a multiseriate stalk and a two-armed gland. The combination of these hairs and the presence of non-glandular hairs confirm the actual classification of the genus. In combination with simple morphological characters (e.g., the type of insertion of the petiole) glandular hairs facilitate the identification of species even in the pharmaceutically important cut crude drug.

The dried aerial parts of Drosera rotundifolia L. are traditionally used in therapy against affections of the respiratory tract, especially in case of convulsive cough or whooping-cough (CzYOAN 1989). The active substances are mainly derivatives of 1,4-naphthoquinone (e.g., plumbagin, 7-methyljuglone, ZENK & al. 1969). Due to the actual rarity of its habitat D. rotundifolia as well as the other species of Cen- tral Europe (D. anglica HuDs., D. intermedia HAYNE) are protected by law. Although extensive studies for in vitro cultivation and propagation of D. rotundifolia were carried out (BLEHOVA & al. 1990, BOBAK & al. 1990, WAWROSCH & al. 1993), the production of the required quantity of the pharmaceutically important crude drug Herba Droserae in this way is not yet possible. Therefore, species from the southern hemisphere (South Africa, Australia) such as D. madagascariensis DC. and D. peltata SM. still substitute the European species in the crude drug (LXNoER & al. 1994).

The identification of species in the crude drug is very difficult. In the pharmacognostical literature only the above mentioned species are described, and the data originate from commerical samples (ScHIER & al. 1987). The majority of the approximately 120 species has not been considered. In botanical as well as in pharmacognostical literature only morphological characters are cited, but most of them are not applicable to cut plant pieces. Anatomical details are limited to tentacles and to the glandular hairs of the species of Central Europe (DmLs 1906, SOLEREDER 1899) and stem anatomical details of some Australian species (DEBUnR 1977). A screening of anatomical characters of a great number of species should provide the base for the identification even in the cut crude drug. The material rep- resents all sections but one (sect. Stelogyne) published in the family monograph by DIELS (1906).

164 R. L;~N~Ek & al.:

Material and methods

The vouchers are loans from W. Most of the specimens had been revised by DIELS (1906). Because of this irretrievable value maximal care was taken to the herbarium specimens. Therefore, anatomical details of flowers cannot be given for all examined species, vascu- lar anatomy of stems had to be neglected totally. Additionally, living material cultivated in the Institute of Pharmacognosy, University of Vienna, was available from D. rotundifolia, D. capensis, D. ramentacea, D. dielsiana, D. pygmaea, and D. binata. The identity of all species was verified according to the Floras related to their distribution (CLARKE 1879, CODD & al. 1970, DIELS 1906, GRAY 1868, KERAUDREN-AYMONIN 1982, MARCHANT & al. 1982, SANTOS 1980, SONDER 1859--1860).

List of specimens: D. adelae F. MUELL.: Australia, Rockingham's Bay, det. DIELS; D. affinis WELW.: Sambia, Kinebe, det. DIELS, X. 1899; D. anglica HuDs.: Austria, Paznaun- tal, VIII. 1975; Austria, Otztaler Alpen, Venetberg, VII. 1975; BRD, Berlin, Grunewald, VII. 1878; Sweden, Norrbotten, Mt Rovavaara, VII. 1960; Finland, Helsingfors, VII. 1897; D. auriculata BACKH.: Australia, Victoria, Genoa Creek Track, XII. 1971; Australia, Canberra, Black Mountain, XI. 1952; D. binata LABILL: Australia, NSW, Avon River, II. 1969; D. bulbosa HooK.: Australia, Distr. NW Plantagenet, det. DIELS, VI. 1900; D. burkeana PLANCH.: Mozambique, Nyassa Highland, 1911; D. burmanni VAnL: Vietnam, Hue, Tourane, VI. 1927; Thailand, Chieng-Mai, Doj-Sutep, IV. 1905; D. caIedonica VIEILL.: New Caledonia, Nakety, X. 1884; D. capensis L.: South Africa, Cape, det. DIELS; D. capil- laris PoIR.: USA, Florida, Jacksonville, det. DIELS, IV. 1894; D. cistiflora L.: South Africa, Hopefield, IX. 1894; South Africa, Hopefield, det. DIELS, IX. 1894; D. cuneifolia L.: South Africa, Transvaal, Zuurbraak, I. 1893; South Africa, Cape, Koude River, det. DIELS, XII. 1896; D. dielsiana EXELL & LAUNDON: South Africa, Mariepskop, I. 1959; D. erythrorrhiza LINDL.: 9, det. DIELS; D.filiformis RAF.: USA, Massachusetts, Harwich, VII. 1918; D. gigantea LINDL.: Australia, Swan River, det. DIELS; D. glabripes (HARv.) STEIN: South Africa, Vogelgat, det. DIELS as D. ramentacea BuRcn., XI. 1896; D. glanduligera LEnM.: Australia, Ravensthorpe, X. 1955; D. graminifolia ST. HIL.: Brasil, Minas Geraes, det. DmLs; D. heterophylla LINDL.: ?, det. DmLs; D. hilaris CnAM. & ScnL: South Africa, Stel- lenbosch, X. 1960; Zwarteberg, det. DIELS, X. 1886; D. huegelii ENDL.: Australia, Distr. SW Plantagenet, det. DIELS, VII. 1901; D. indica L.: Vietnam, Hue, V. 1927; D. intermedia HAYNE: Austria, Tirol, Kitzbtihel, VIII. 1952; Finland, Paimio, Vartsala, VII. 1973; Finland, Kustavi, Kaurissalo, VIII. 1976; D. macrantha ENDL.: Australia, Distr. Swan, Darling Range, det. DIELS, VII. 1901; Australia, Distr. Avon, det. DIELS, VII. 1901; D. mac- rophylla LINDL.: Australia, Distr. Avon, det. DIELS, VIII. 1901; ?, det. DmLs; D. madagascariensis DC.: Tansania, Marengo, I. 1936; Madagascar, Imerina, det. DinEs, I. 1881; Madagascar, det. DmLs; D. menziesii R. BR.: Australia, Distr. Swan, X. 1901; Australia, Victoria, det. DIELS as D. planchonii HooK.; Australia, Moore, IX. 1906; D. microphylla ENDL.: Australia, det. DIEI~S; D. montana ST. HIL.: Brasil, det. DIELS; D. neesii LEI-IM.: Aus- tralia, Murchison, det. DmLs, IX. 1901; Australia, Distr. SW Plantagenet, det. DIELS aS D. sulphurea LEHM., XI. 1901; D. pallida LINDL.: Australia, Swan River, det. DIELS; D. pauciflora BANKS: South Africa, Cape, det. DmLs; D. peltata SM.: Singapore, det. DIEKS; Tasmania, Khasia, det. DmLs; China, Canton, det. DIEKS, III. 1868; India orientalis, det. DmLs; D. petiolaris R. BR.: Australia, Norman River, det. DIELS; D. ramellosa LEHM.: ?, det. DIELS; D. ramentacea BuRcH.: ?, det. DIELS; D. rosulata LEHM.: Australia, Distr. Swan, det. DIELS, V. 1900; D. rotundifolia L.: Austria, Tirol, Iselsberg, VIII. 1988; Czech Repub- lic, Nova Bystrica, VIII. 1923; Czech Republic, Jindrichuv Hradec, VIII. 1972; D. scorpioides PLANCH.: Australia, ?; D. sessilifoIia ST. HIL.: Brasil, Rio Beason, det. DIELS; D. spathulata LABILL.: Australia, Jervis Bay, II. 1953; D. subhirtella PLANCH.: Australia, Moore, det. DIELS, VIII. 1901; D. stenopetala HooK.: New Zealand, 1891; D. stolonifera ENDL.: Australia, det. DIELS; D. tracyi Mc. F.: USA, Florida, DeFuniak, V. 1906; D. trinervia

Glandular hairs in Drosera 165

SPRENG.: South Africa, det. DIELS, X. 1894; D. whittakeri PLANCH.: Australia, Rockleigh, Mt Lofty Range, VII. 1964; D. villosa ST. Hm.: Brasil, Sao Paulo, Serra do Mar, X. 1927.

Species cultivated in the Institute of Pharmacognosy, Vienna [seeds from the Botanical Gardens Munich, Leipzig, and Sch6nbrunn (Vienna)]: D. capensis, D. pygmaea DC., D. dielsiana, D. binata, D. communis ST. Hm., D. hilaris.

Small pieces of the leaf, the petiole, the pedicel and the sepals were cleared for micro- scopical observation by boiling with a 60% solution of chloral hydrate. Figures of hairs were drawn with a drawing tube.

Results

In contrast to the plenty of different kinds of glandular hairs other anatomical sur- face characteristics are rare. Non-glandular trichomes are present on the abaxial side of leaves in 19 of the examined species. Shape, structure and length of these hairs are similar. More restricted is the presence of non-glandular trichomes on the sepals, they were found in seven species. The numerous different kinds of glandular hairs can be classified into 14 types which we arrange in seven groups:

(a) Papillae. The most simple and common type of glandular hairs in the genus Drosera (type 1, Fig. 1) is a papilla (diameter appr. 30-50 ~m), which is vertically divided in two secretory cells. In aged specimens the resinous secretion under the cuticle looks like a multicellular head, but the comparison with fresh plant material confirmed the two-celled structure.

(b) Scales. The huge sessile glands of D. sessilifolia and D. burmanni (type 2, Fig. 1) consist of a short stalk of two parallel cells and a multicellular gland (diameter appr. 130 ~m). Often the cuticula is removed.

(c) Unbranched glandular hairs, stalk bi- or multiseriate, gland vertically divided (biseriate, Fig. 2). Type 3, which can be found mainly in species of sect. Rossolis, can be defined as biseriate, short, stalk two- or three-celled, thin or slightly thickened (e.g., D. burkeana), gland vertically divided. The gland cells are elongated, emarginated or laterally protruted. In type 4 the spherical gland, which is placed on a short biseriate stalk, is both vertically and horizontally divided into four (D. capensis) or eight (D. caledonica) cells. The stalk of hairs of type 5 is short or long, biseriate, at the base often multiseriate (e.g., in D. bulbosa and D. erythrorrhiza, length 150 ~m up to 1 mm). The biseriate gland is composed of three or four cells in each row and is spherical or slightly elongated (then the two terminal secretory cells are laterally protruted, D. indica).

(d) Unbranched, short glandular hairs, stalk bi- or multiseriate, gland spherical, basal biseriate with two very short cells, 5-8 secretory cells (Fig. 3). The fol- lowing hairtypes are similar in the arrangement of the secretory cells, but different in their stalks. In type 6 the stalk is built of two elongated parallel cells (e.g., in D.

Type 1

50 tim

Type 2 Fig. 1. Drosera. Glandular papilla, type 1; glandular scale, type 2

166 R. LANGER ~; al.:

Type 3

50 pm

Type 4

I Type 5

y

Fig. 2. Drosera. Unbranched glandular hairs, stalk bi- or multiseriate, gland vertically divided (biseriate), types 3-5

Type 6

Type 9 I , I

50 pm

Type 7 % Type 8

Fig. 3. Drosera. Unbranched short glandular hairs, stalk bi- or multiseriate, gland spherical, at base biseriate with two very short cells, 5-8 secretory cells, types 6-9

burmanni). The types 7 and 8 are characterized by several, biseriate arranged stalk cells, in type 7 they are very short (D. affinis), in type 8 elongated (D. erythrorrhiza). The coarse, multiseriate stalk of hairtype 9 is typical for the glandular hairs of the sepals of D. burmanni.

(e) Unbranched, short, stalk biseriate, gland multicellular (Fig. 4). The stalk


i i

50 pm

Type 10

Fig. 4. Drosera. Unbranched short glandular hairs, stalk biseriate, gland multicellular, type 10

~ 50 pm Type 13

Type 12

Fig. 5. Drosera. Fimbriae of sepals: unbranched glandular hairs, stalk bi- or multiseriate, gland multicellular, types 11-13

Type 14

t

50 pm

Fig. 6. Drosera. Two-armed, multicellular glandular hair, type 14

168 R. L a ~ o e a & al.:

. o . :

0

~D

. a < = ~

,-~ 0) z

O ~ A..2, m eo "v]"

,..: ~ o > Z

©

¢1I

i

0

Z

i

©

#

¢1.)

Z

~ ~ . ~

d ~ . ~ < .~ < . ~ . ~ . ~ . ~ = ~ ~ ~ . ~ < . ~

< < ~ m < m < Z Z ~ Z Z < Z ~ ~ ~

I I I I I I I I I I I I I I I + I I I + I + I

I I I I I I I I I I I + I + I + + + + + + + +

• ,"'~ ¢¢3 Z < ..1

~-q ~

¢ q t"q tt'3

¢9 ~ rO r..) r,.) Z Z

O © © 0 © ~ % % % % %

g

< t "~ ~

~ 1 ) " ~ ~ ) ~ "~ ~0 ~ ~ -.a . ~ ~ . ~ ~ . ~ ~..~,.~ ~ , . . ~ ~ ' ~ - ~ , . . o ,..0 " ~


N

N ~

~ ~ Z < < ~ ~ < < < < < < < < < < < < < < < <

I I + + + I I I + I E I I I I 1 l I I I I I I I I I I 1 1

+ + + + + + + + + 1 I I 1 1 1 1 I I I I I I I I I I I I I

, .0 , .0 ~ ,..0 ~ ,..0

© © © © © ©

; . ~ ; . ~ ; . ~ : - ~ ; - ~ . ~ ;_~

t"- t--- t"- t'-- P-- ~.~

Z

~ ' ~ ' ~ ' ~ " ~ ~ ~ ~ - ' ~ ~ : ~

• ~ ~ a ~ ~ . ~ ~ . ~ ~ . • ~ . ~

170 R. LANGER 8Z al.:

cells of type 10, which is very common especially in sect. Rossolis, are arranged alternately, their cell wall is either thin or slightly thickened. The shape in side- view of the multicellular gland ranges from spherical or mushroom-like to fan- shaped (D. indica).

(f) Fimbriae of sepals: unbranched, stalk bi- or multiseriate, gland multicellular (Fig. 5). Fimbriae are usually very long hairs, partly with a trachea at the base of the stalk (not to be confused with the tentacles on the leaf!). They differ in the number of cell rows in the stalk and the shape of the capitulum. The fimbriae of most of the members of sect. Polypeltes (type 11) consist of a multiseriate, long stalk and a spherical, multicellular gland. The stalk cells are usually thin-walled. The fimbriae of D. scorpioides and D. pauciflora are characterized by a biseriate, long stalk with strictly symmetrical, elongated and thickened cells (type 12). In contrast, the stalk of the fimbriae of D. heterophylla is short, multiseriate, as long as broad, the multicellular, spherical gland is as long as the stalk (type 13).

(g) Two-armed, multicellular glandular hairs (Fig. 6). This type of glandular hairs could only be found on the leaf of D. indica. The two-armed gland is placed on a multiseriate stalk (type 14).

In Table 1 the distribution of the types of glandular hairs of the species examined is shown in connection with the presence of non-glandular hairs, the distribution and the dominating 1,4-naphthoquinone-derivative.

Discussion

The taxonomic classification of DIELS (1906) is based mainly on characters such as presence of tubers and the morphology of bracts and styles. Differences in the vas- cular anatomy within subg. Ergaleium led to a partition of sect. Erythrorrhiza (DEBuH~ 1977). The presented screening of anatomical details like the distribution of different types of glandular hairs on leaves and sepals confirms the actual classification in its main parts. Only simple glandular hairs are found in most species of the northern hemisphere, which belong to subg. Rorella sect. Rossolis. How- ever, the majority of species of this taxon grows in South America and South Africa and is characterized by biseriate stalked hairs with numerous secretory cells on the sepals. Within subg. Ergaleium most members of sect. Polypeltes are distin- guished from those of the other sectt, by the presence of fimbriae on the sepals (not found however in D. gigantea and D. microphylla). Drosera heterophylla is exceptional, the hairs on the margins of sepals are very short with a globular gland. The species of sectt. Erythrorrhiza and Stolonifera are uniform in their indumentum, only sessile glands of type 1 are present on sepals. Glandular scales are restricted to the two examined members of sect. Thelocalyx (D. sessilifolia, D. burmanni). Although the types of glandular hairs are identical, differences in the type of the main naphthoquinone confirm the separation of D. binata (plumbagin) from most members of sect. Rossolis (7-methyljuglone). The glandular hairs of D. cistiflora and D. pauciflora, representing subg. Ptycnostigma, do not allow a dif- ferentiation from most of the species of sect. Rossolis.

Between the members of the other sections considerable differences were found. For example, in sect. Arachnopus we find D. indica with two-armed glandular hairs and D. adelae with the common hemispherical papillae only.


Non-glandular hairs do occur only within sect. Rossol is , free of such hairs are only D. f i l i formis , D. tracyi and the three European species. The latter ones additionally deviate in the absence of stalked glandular hairs on the sepals. Because of these dissimilarities the systematic position of D. rotundifol ia, D. angl ica, and D. in termedia should be discussed.

In consequence of the correlations between hairtypes and classification of the genus the anatomical investigation of D ro sera -p i ece s as present in the crude pharmaceutical drug gives first hints for an identification. For practical use keys were constructed based on hairtypes and simple morphological characters, e.g., the insertion of the petiole, and length of internodes (LXNGER & Koep 1995).

R e f e r e n c e s

BLEnOVA, A., SOMgAKOVA, V., BOBAK, M., 1990: Anatomical studies of the development of new plants from the leaves of the sundew (Drosera spathulata L.) in in vitro conditions. - Acta Fac. Rer. Nat. Univ. Comenianae, Physiol. Plant. 26: 33-41.

BOBAK, M., BLE,OVA, A., ERDELSK'~, K., CHOLVADOVA, B., SOMgAKOVA, V., 1990: Morphogen- esis of the plastid apparatus ill the process of organogenesis at the leaves of the sundew (Drosera spathulata L.), cultivated in in vitro conditions. - Acta Fac. Rer. Nat. Univ. Comenianae, Physiol. Plant. 25: 33-40.

BONNET, M., COUMANS, M., HOFINGER, M., RAMAUT, J. L., GASPAR, T., 1984: High-perfor- mance gas chromatography of 1,4-naphthoquinones from Droseraceae. - Chromato- graphia 18: 621-622.

CLARKE, C. B., 1879: Droseraceae. - In HOOKER, J. D., (Ed.): Flora of British India, 2, pp. 423-425 . - London: Reeve & Co.

CODD, L. E., DE WINTER, B., KmLICK, D. J. B., RYCROFT, H. B., (Eds), 1970: Flora of South- ern Africa, 13. - Pretoria: Bot. Res. Inst., Dep. Agr. Water Suppl., Rep. South Africa.

CZYGAN, E-C., 1989: Sonnentaukraut. - In W~CHTL, M., (Ed.): Teedrogen, pp. 462-465. - Stuttgart: Wissenschaftliche Veflagsgesellschaft.

DEBuHR, L. E., 1977: Sectional reclassification of Drosera subg. Ergaleiurn (Drosera- ceae). - Austral. J. Bot. 25: 209-218.

DmLs, L., 1906: Droseraceae. - In ENGLER, A., (Ed.): Das Pflanzenreich, 26, pp. 1-136. - Leipzig: Engelmann.

DURAND, R., ZENK, M. H., 1974: The homogenisate ring-cleavage pathway in the biosyn- thesis of acetate-derived naphthoquinones of the Droseraceae. - Phytochemistry 1 3 :

1483-1492. GRAY, A., 1868: Manual of the botany of the Northern United States. - New York: Ivison,

Phinney, Blakeman. KERAUDREN-AYMONIN, M., 1982: Droseracees. - In LEROY, J.-F., (Ed.): Flore de Madagascar

et des Comores, pp. 54-62. - Paris: Museum National d'Histoire Naturelle. L~NGER, R., KoPP, B., 1995: Qualit~itsprtifung yon Herba Droserae. 1. Grundlagen ftir die

botanische Identit~tsprtifung. - Deutsche Apotheker Zeit. 135 (in press). - KRENN, L., KoeP, B., 1994: Qualit~itsprtifung an Handelsmustem yon Herba Droserae. -

Sci. Pharm. 62: 99. LECLERCQ, J., ANGENOT, L., 1984: Apropos du Drosera peltata et de la standardisation de la

teinture de Drosera. - J. Pharm. Belg. 39: 269-274. LUCKNER, R., LUCKNER, M., 1970: Naphthochinonderivate aus Drosera ramentacea BORCH.

ex HARV & SOND. -- Pharmazie 25: 261-265. MARCnANT, N. G., ASTON, H. I., GEORGE, A. S., 1982: Flora of Australia, 8, pp. 9-64. - Can-

berra: Australian Government Publishing Service. SANTOS, E., 1980: Droseraceas. - In Rnfz, R., (Ed.): Flora illustrada Catarinense,

pp. 3-23. - Santa Catarina: Itajai. SCHmR, W., SCHULTZE, W., 1987: Sonnentau: zur Handelsware yon Droserae herba. -

Deutsche Apotheker Zeit. 127: 2595-2598.

172 R. L~NGER • al.: Glandular hairs in D r o s e r a

S OLEREDER~ H., 1899: Systematische Anatomie der Dicotyledonen. - Stuttgart: Enke. SONDER, W., 1859--1860: D r o s e r a c e a e . - In HARVEY, H., SONDER, W., (Eds): Flora Capensis,

1, pp. 75-79. - Dublin: Hodges, Smith. WAWROSCH, C., STEINBERGER, B., MARKOTAI, J., KopP, B., 1993: In vitro propagation of D r o -

s e r a species. - Planta Med. 59 Suppl.: A 653. ZENK, M. H., F~R~RINGER, M., STEGHCm W., 1969: Occurrence and distribution of %meth-

yljuglone and plumbagin in the D r o s e r a c e a e . - Phytochemistry 8:2199-2200.

Address of the authors: Dr REINHARD LJ~NGER and Prof. Dr BRIGITTE KOPP, Institut ftir Pharmakognosie, Universit~it Wien, Pharmaziezentrum, Althanstrage 14, A-1090 Wien, Austria.

Accepted November 8, 1994 by F. EHRENDORFER

Documents

Glandular hairs in the genusDrosera (Droseraceae)