) | Ja 4

Cover: Rafflesia arnoldii R. Br. Central Kalimantan, Bukit Raya area. Photograph W. J. J.O. de Wilde, 1982.

Editorial Committee:

C. Kalkman P. F. Stevens D.W. Kirkup W. J. J.O. de Wilde H.P. Nooteboom

Requests for scientific information to be addressed to:

Rijksherbarium / Hortus Botanicus P.O. Box 9514, 2300 RA Leiden, The Netherlands e-mail: kalkman @rulrhb.leidenuniv.nl

Board of the Foundation Flora Malesiana:

M.A. Rifai, Bogor, chairman K. Larsen, Aarhus

P. Baas, Leiden, vice-chairman A. Latiff Mohamad, Bangi M.C. Roos, Leiden, secretary / treasurer D.A. Madulid, Manila Aprilani Soegiarto, Jakarta Ph. Morat, Paris

J. Burley, Cambridge USA F.S.P. Ng, Rome

J. Dransfield, Kew D.H. Nicolson, Washington O. Gideon, Lae H. van der Werff, St. Louis A. Hay, Sydney J. West, Canberra

K. Iwatsuki, Tokyo

Subscription orders and requests for sample copies to be sent to:

Publications Department

Rijksherbarium / Hortus Botanicus

P.O. Box 9514

2300 RA Leiden

The Netherlands Fax )S27351

LIBRARY THE NEW YORK BOTANICAL GARDEN BRONX, NEW YORK 10458

Flora Malesiana

Series I Seed Plants

Volume 13 1997

Raf flesiaceae

(W. Meijer pp. 1—42)

Boraginaceae

(H. Riedl pp. 43-144)

Daphniphyllaceae (T.-C. Huang pp. 145-168)

Illiciaceae & Schisandraceae

(R.M.K. Saunders pp. 169-184 & 185—207)

Loranthaceae & Viscaceae

(B.A. Barlow pp. 209-401 & 403-442)

CAT\ ete (ESo.

VAS

ISBN 90 -71236 -33-1 All rights reserved © 1997 Foundation Flora Malesiana

No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, or by any information storage and reirieval system, without written permission from the copyright owner.

PUBLISHER’S NOTE

Starting this volume, the subdivision of the volumes into parts will be abandoned. It has appeared that hardly anywhere, not even in libraries, the parts are bound together into the thick green volumes we were familiar with in the beginning of the project. Every issue, covering one or more families, will from now on be called a volume.

ABSTRACT

Flora Malesiana. Series I, volume 13 (1997) vi + 1—454, edited by C. Kalkman et al., published by Rijksherbarium/ Hortus Botanicus, Leiden, The Netherlands, under the aus-

pices of Foundation Flora Malesiana. ISBN 90 -71236-33-1

Contains taxonomic revisions of seven Flowering Plant families for Malesia, i.e. the area covering the countries Indonesia, Malaysia, Brunei Darussalam, Singapore, The Philip- pines, and Papua New Guinea.

W. Meijer, Rafflesiaceae, pp. 1—42.

The family as here circumscribed covers the genera Mitrastema (1 species), Rafflesia (13), and Rhizanthes (2), all parasitic plants. The logo of Flora Malesiana is based on Rafflesia and is found on most of our publications.

The general part of the treatment covers 10 pages and includes paragraphs on palynology by R.W.J.M. van der Ham, and on phytochemistry by R. Hegnauer.

Family, genera, and Malesian species are described and annotated. Keys to the genera and species are given. Under Rafflesia a historical review of the discovery of this remark- able genus is given, and also a paragraph on ex situ cultivation. The name Rafflesia titan Jack is considered to be an incompletely known species.

One new combination is formally made, on p. 23: Rafflesia arnoldii R. Brown var. atjehensis (Koord.) Meijer, comb. et stat. nov. (Basionym: Rafflesia atjehensis Koord.)

Illustration is (apart from the cover photo) by 4 half-page colour photographs, 3 black/ white photographs, and 8 line drawings mostly less than full-page.

H. Riedl, Boraginaceae, pp. 43-144.

This widespread family of over 2,000 species has only 77 species in Malesia of which 64 are indigenous, the remainder having been introduced for economical or ornamental use or as weeds. In Malesia 12 genera are represented, as follows: Borago (1 sp., cult.), Bothriospermum (1, intr.), Carmona (1, also cult.), Coldenia (1), Cordia (6 indig., 3 intr.), Cynoglossum (12 indig., 1 cult.), Ehretia (12), Heliotropium (6 indig., 5 intr.), Myosotis (1 indig., | intr.), Omphalodes (1, intr.), Rotula (1), Tournefortia (7), Trichodesma (2), Trigonotis (15). One dubious genus (Crucicaryum) is mentioned and one genus of uncertain affinities (Preleocarpa) 1s treated fully.

The general part of the treatment covers 19 pages and includes paragraphs on vegetative anatomy by P. Baas, on palynology by R.W.J.M. van der Ham, and on phytochemistry and chemotaxonomy by R. Hegnauer.

The family, genera, and Malesian species are described and annotated. There are keys to the genera and species.

Illustration is by 14 line drawings, some of them full-page, and 4 photographs.

Tseng-chieng Huang, Daphniphyllaceae, pp. 145-168.

A monogeneric family, possibly closest related to Hamamelidales or even belonging to that order. The only genus, Daphniphyllum, has 16 species in Malesia.

The general part of the treatment covers 6 pages and includes paragraphs on vegetative anatomy by P. Baas, on pollen morphology by R.W.J.M. van der Ham, and on phyto- chemistry and chemotaxonomy by R. Hegnauer.

The genus and its Malesian species are described and annotated; a key to the species is included.

The illustration contains a distribution map of the genus and its two sections, two photographs, and five (+) full-page line drawings.

R.M.K. Saunders, Illiciaceae, pp. 169-184.

A monogeneric family, closely related to Schisandraceae (see next entry), the two recognized as a separate order //liciales. Of the only genus, //licium, 7 species occur in Western Malesia and the Philippines.

The general part of the treatment consists of 11 printed pages and includes a paragraph on pollen morphology by R.W.J.M. van der Ham, and a paragraph on phytochemistry and chemotaxonomy also covering Schisandraceae by R. Hegnauer.

The genus and its Malesian species are described and annotated; a key to the species is included.

Illustration is by one full-page line drawing.

R.M.K. Saunders, Schisandraceae, pp. 185-207.

In this family two genera are distinguished, Kadsura and Schisandra. The former has 9 species in Malesia, the latter only 2.

The general part of the treatment consists of 6 pages and contains a paragraph on pollen morphology by R.W.J.M. van der Ham. Phytochemistry and chemotaxonomy are summarized in the treatment of //liciaceae (see entry above).

The family, genera, and Malesian species are described and annotated; there are keys to the genera and species.

Illustration is by two full-page line drawings.

B.A. Barlow, Loranthaceae, pp. 209—401.

Of this predominantly tropical family 23 genera and nearly 200 species occur in the Malesian region, as follows: Amyema (59 species), Amylotheca (3), Barathranthus (2), Cecarria (1), Cyne (6), Dactyliophora (2), Decaisnina (21), Dendrophthoe (21), Distrian- thes (1), Elytranthe (2), Helixanthera (11), Lampas (1), Lepeostegeres (9), Lepidaria (8), Loranthus (1), Macrosolen (24), Papuanthes (1), Scurrula (8), Sogerianthe (4), Taxillus (1), Thaumasianthes (1), and Trithecanthera (5).

The general part of the treatment consists of 20 pages and includes paragraphs on vegetative anatomy by P. Baas and L. van den Oever, and on pollen morphology by R.W.J.M. van der Ham. Phytochemistry and chemotaxonomy is treated for this family and Viscaceae together, see also next entry.

The family, the genera, and the Malesian species are described and annotated; for complete synonymy the reader is often referred to earlier publications by Danser or Barlow. There are keys to the genera and to the species; in the largest genus Amyema there are also some regional keys to the species. A key to Loranthaceae and Viscaceae, covering all Malesian taxa, is also included.

Illustration is by 32 line drawings, several full-page but often smaller, and by 15 photo- graphs. The drawings are mostly redrawn from earlier publications.

B.A. Barlow, Viscaceae, pp. 403-442.

This family, nowadays usually separated from the Loranthaceae, has far fewer spe- cies in Malesia, viz. 26, divided over 4 genera: Ginalloa (6 species), Korthalsella (5), Notothixos (6), and Viscum (9).

The general part of the treatment covers 9 pages and includes paragraphs on vegetative anatomy by P. Baas and L. van den Oever, and on pollen morphology by R.W.J.M. van der Ham. For phytochemistry the reader is referred to the pertinent paragraph under Loranthaceae, where both families are considered.

The family, the genera and the Malesian species are described and annotated. There are keys to the genera and to the species. A key to Loranthaceae and Viscaceae, covering all Malesian taxa, is also included.

Illustration is by six line drawings, mostly smaller than full-page, and by 7 photographs. The drawings are mostly redrawn from earlier publications.

Index to scientific plant names of taxa treated in this volume (accepted names and synonyms) on pp. 443-452.

List of revised families in Flora Malesiana on pp. 453-455.

i So. Pees

i} AiR oy) enor bog

; ; y + ine = Pree eto & ; i ee tame em rman ww Ss 1 Vie ed ; en Fu tie i

® ‘va 7 ¢ ' \ , i pan a ee ; rs j 7 : iva Por ' sire Art Baa)

= A

: if) Tui ee m 14) - ae

j oli ter Mat Loonagued

> Ot A ae a ae oe

th Dio 7 lo ant! ive @rarts i, hee, 1]

Tre ten | | fi i i {' fi) Gi UOITD ae? ie | ot ao} ola

behulani welt <i Pil nel rf - bd | H LL ab wish Fi FA) at vith oul AAF, ve 7} Cea wht

7 aw Niduydtohtcs pind viens eee

7 _

ss : ; ' Hii, © on a Bae gong pay! w) . Be ni bg ier) wa! {5 ¥5tdou anally stints oe @d a ri, 3 DOT MAY wom

P | _ ais on 1 "arty

m= | ad feb it fey 0, habe A wa b - ; al pile ~~

7 -

eee os

he

Flora Malesiana, Series I, Volume 13 (1997) 1—42

RAFFLESIACEAE (W. Meijer, Lexington, U.S.A.)!

Rafflesiaceae Dumort., Anal. Fam. Pl. (1829) 14; Koord., Bot. Overz. Raffles. Ned.- Indié (1918) 1-128; Meijer in Kubitzki (ed.), Fam. & Gen. Vasc. Pl. 2 (1993) 557— 563; Hansen in Fl. Thailand 2 (1972) 182—184; in Fl. Camb., Laos & Vietnam 14 (1973) 59-64; Kiu & Wing in Fl. Reipubl. Pop. Sin. 24 (1988) 246—248; Dell in Fl. Austral. 22 (1984) 147-150.

Parasitic plants, rootless, without chlorophyll, always rich in tannins, monoecious or dioecious. Endophytic body as strings (chains) or plates of cells inside host plant. Flow- ering buds or flowering branches vascularized, bursting through the cortex of the host and terminating in a single flower or in short racemes or spikes, with series of scales (bracts) at the base of the buds. Flowers uni- or bisexual; perianth single (perigone), often tubular or saucer-shaped at base, in Rafflesia and Sapria the apex of the tube part- ly closed by a diaphragm; stamens grouped around a central column representing part of the pistil in female and bisexual flowers, often joined with that column; ovary uni- locular, in general inferior but in some cases semi-inferior or superior (Mitrastema), with 4—6 or numerous parietal placentas. Fruits berry-like. Seeds minute, surrounded by pulp, testa hard, often thickened and pitted, embryo few-celled, undifferentiated.

DISTRIBUTION

As defined here the family is subdivided into two subfamilies with a total of nine genera and about 40 species, mainly in tropical regions, although some species occur in sub- tropical and even temperate parts of the world. The three genera of the tribe Rafflesieae of the subfamily Rafflesicideae are only known from Indomalesia, the other two tribes of that subfamily (Cytineae and Apodantheae) occur in America, Africa, the Mediterra- nean region (including Iran and Iraq), and SW Australia. The subfamily Mitrastemot- deae has only one genus, Mitrastema, originally found in E and SE Asia, but later also recorded from Mexico, Guatemala, and Colombia (Meijer 1993).

HABITAT

All Malesian species are restricted to moist, evergreen, lowland or montane, primary or adjacent secondary forests.

1) With contributions by R.W.J.M. van der Ham, Leiden (palynology), and R. Hegnauer, Leiden (phy- tochemistry). Most original drawings are by Janis Atlee, Lexington, one by Herbert Lee, Tenom (Sabah). Photographs are from different sources as indicated. Inclusion of the colour plates was made possible through a substantial financial contribution by the author.

(1)

to

Flora Malesiana, Ser. I, Vol. 13 (1997)

ECOLOGY

The ecology of Rafflesiaceae is of course closely interwoven with the host-parasite rela- tionship, the chances of survival and the specific ecological requirements of the host plants, pollination efficiency, seed dispersal and dormancy, and germination chances. Between the production of about 100-150 seeds in a peppercorn-sized fruit of Pilostyles and a fist-size fruit of Rafflesia with several millions of seeds exists an enormous range of seed production per flower.

Mitrastema is most consistently reported as parasitizing the roots of Fagaceae: Quer- cus, Lithocarpus, Trigonobalanus, and Castanopsis and, if collectors’ notes are accurate, occasionally adjacent tree roots of other families. All three genera of the tribe Rafflesieae (Rhizanthes, Rafflesia, Sapria) are obligate parasites of the genus Tetrastigma in Vita- ceae. Where species names are mentioned in the treatment, they must be considered as preliminary, since identification of herbarium specimens is difficult and nomenclature uncertain.

Literature: Banziger, H., Nat. Hist. Bull. Siam Soc. 39 (1991) 19-52; ibid. 43 (1995) 337-365.

TAXONOMY

Since Dumortier (1829) most systems of plant families of the world have treated Raffles- iaceae in a wide sense. Lindley (1836) and Richard (1838) considered Cytinaceae to be a separate family with Pilostyles as part of the Rafflesiaceae and the very closely related Apodanthus in the Cytinaceae. Van Tieghem (1890) elevated Apodanthaceae to the rank of family and Makino (1911) put his new genus Mitrastema in its own family. More re- cent accounts, as Thorne (1992), Beaman et al. (1992) and Meijer (1993) treat the fam- ily in a wide sense. Takhtajan et al. (1985) considered Rafflesiaceae sensu lato as a heterogeneous group, both macromorphologically and palynologically, and expressed the idea that the four tribes recognized by Harms (1935) deserve to be treated as separate families:

Rafflesiaceae: Rafflesia, Rhizanthes, Sapria

Apodanthaceae: Apodanthes, Pilostyles

Cytinaceae: Bdallophyton, Cytinus

Mitrastemaceae: Mitrastema.

Studies of ribosomal RNA of parasitic plants carried out by Dr Daniel Nickrent in Carbondale (University of South Illinois) are still preliminary but already support the removal of Cytinaceae from the Rafflesiaceae and ultimately may support the family system of Takhtajan et al. (1985). The ribosomal DNA data (Nickrent & Duff, in press) make it clear that the tribe Cytineae deserves to become a family at its own. Results on Apodanthes and Pilostyles are not yet available but it is quite possible also that they can- not easily be compared with the Rafflesia tribe (or family sensu stricto).

Solms-Laubach (1901: 7) warned not to rush to conclusions about the taxonomy and relationships of parasitic plants, which could hide their real ancestry in their strong reduc- tions and adaptations required to survive as parasites. We can safely restrict ourselves

Meijer Rafflesiaceae 3

here to the tribe Rafflesieae and the subfamily Mitrastemoideae and leave it to future re- search as to how closely or distantly they might be related.

Literature: Beaman, R., et al., in: G. Ismael (ed.), Proc. Int. Conf. For. Biol. & Cons. Borneo (1992) 109. Brown, R., Ann. Sc. Nat. 2, 1 (1834) 369-370; Trans. Linn. Soc. London 19 (1844) 221-239, 5 pl. Dumortier, B.C.J., Anal. Fam. Pl. (1829) 14. Harms, H., in Engler & Prantl, Nat. Pflanzen- fam., ed. 2, 16b (1935) 243-281. Lindley, J., Nat. Syst. Bot., ed. 2 (1836) 389-392. Makino, T., Bot. Mag. Tokyo 25 (1911) 254-257, pl. 7. Meijer, W., Rafflesiaceae, in: K. Kubitzki (ed.), Families & Genera of Vascular Plants, vol. 2: K. Kubitzki, J.G. Rohwer & V. Bittrich (eds.), Flow. Pl., Dicot. (1993) 557-563. Nickrent, D.L. & R.J. Duff, Proc. 6th Parasitic Weed Symp. April 1996, Cordoba, Spain (in press). Richard, A., Nouv. Elem. Bot., ed. 6 (1838) 1518-1520. Solms-Laubach, H., in Engler & Prantl, Nat. Pflanzenfam. 3, 1 (1889) 274-282; in Engler, Pflanzenr. 5 (1901) 1-19, 13 illus. Takhtajan, A.L., N. Meyer, R. & V.N. Kosenko, Bot. J. Leningrad 70 (1985) 153-162. Thorne, R.F., Aliso 13 (1992) 365-389. Van Tieghem, P.E.L., Traité Bot., ed. 2 (1890) 1577-1579.

PHYLOGENETIC AFFINITIES

As suggested before, considerations of this subject are still very speculative and depend on how natural the family in a wide sense really is. Takhtajan (1980) placed the two fam- ilies Hydnoraceae and Rafflesiaceae in the order Rafflesiales in the superorder Rafflesia- nae (subclassis Magnoliidae). The closest relationship may well be with Aristolochia- ceae which already Linnaeus (1753), Robert Brown (1821) and Solms-Laubach (1901) considered possible or likely. Nickrent & Duff (in press) in their preliminary work link Hydnoraceae with ‘paleoherbs’ like Aristolochiaceae. The position of Rafflesiales be- tween Santalales and Celastrales in Cronquist’s system (1981) might be at variance with the evidence from floral morphology and pollen morphology. As mentioned earlier Takh- tajan (1985) proposed to raise all the tribes from the system by Harms (1935) to the rank of family, based on his studies of pollen structure. Thorne (1992), however, stuck to Takhtajan’s family system of 1980 but ranked his Rafflesianae between Nymphaeanae and Caryophyllanae. The cladistic analysis of Beaman et al. (1992) was also based on Takhtajan’s circumscription (1980) of the family and hinges on the selection of the most primitive genus and the most closely related family: Hydnoraceae or Aristolochiaceae. The old family circumscription as followed in this flora can only be maintained when reversals are assumed.

Literature: Beaman, R., et al., in: G. Ismael (ed.), Proc. Int. Conf. For. Biol. & Cons. Borneo (1992) 109. Brown, R., Trans. Linn. Soc. London 13 (1821) 201—234, 8 pl. Cronquist, A., Integr. Sys- tem Class. Flow. Plants (1981) 703-704. Harms, H., in Engler & Prantl, Nat. Pflanzenfam., ed. 2, 16b (1935) 243-281. Linnaeus, C., Spec. Pl. (1753) 442. Nickrent, D.L. & R.J. Duff, Proc. 6th Parasitic Weed Symp. April 1996, Cordoba, Spain (in press). Solms-Laubach, H., in Engler, Pflanzenr. 5 (1901) 1-19, 13 illus. Takhtajan, A.L., Bot. Rev. 46 (1980) 225—359. Takhtajan, A.L., N. Meyer, R. & V.N.Kosenko, Bot. J. Leningrad 70 (1985) 153-162. Thorne, R.F., Bot. Rev. 58 (1992) 225-348.

VEGETATIVE MORPHOLOGY AND ANATOMY

The vegetative parts are a kind of tissue mass often compared with fungal mycelia. The cells have remarkable large nuclei and form the so-called endophytic system within the

4 Flora Malesiana, Ser. I, Vol. 13 (1997)

stems and roots of the host plants, especially inside the living bark close to the cambium of the host. From there, special strings (so-called sinkers) can penetrate through rays of the host into the deeper lying xylem, while these cell strings inside the host cambium in general keep pace with the secondary growth of the host. In Pilostyles thurberi the endo- phytic body stays at a uniform distance from the apical meristem of the host (Rutherford 1970), in the Cytineae generally near the ground level and in the Rafflesieae in the roots as well as high on stems, though in general close to the ground. When the host cam- bium is reactivated, it may succeed to put a xylem layer on top of the parasite tissues. In general the parasite can migrate through the rays into the new host tissues, as described by Forstmeier et al. (1983) for Cytinus.

The simple cell strings do not contain vascular tissues; in many genera these occur mainly in cell cushions from which flowering structures originate, connecting ultimately with the staminal or ovary structures.

Solms-Laubach (1869) described the situation in Cytinus where the parasite forms a kind of tissue sleeve between cambium and xylem of the Cistus host root. In a rhythmic way, parts of the parasite tissue are covered by xylem layers, apparently and for un- known reasons turning the cambium activity off from time to time. The resulting more mature closed cylinder sleeve of the parasite consists of a cambium and two surround- ing layers of tissue: an inner medullary and outer cortical plate. In the latter many irreg- ular weak vascular bundles occur. Flowering structures originate inside swollen paren- chyma tissues and cause gall-like growth above connections with the vascular bundles of the host plant, in general at least 2—3 years after the first infection of the host. The host tissues are filled with starch at this place except in a few cell layers close to the parasite tissue. These and similar situations were observed by Cartellieri (1926) in Rhi- zanthes, Brown (1912) in Rafflesia manillana, Haak (1889), Schaar (1898) and Hunzi- ker (1920) in Rafflesia patma, Endriss (1902) in Pilostyles ingae, Rutherford (1970) in Pilostyles thurberi and Meijer & Behnke (unpubl.) in Rhizanthes, while the old classical study by Solms-Laubach (1875) is still of value. If the family is polyphyletic we are dealing here with remarkable convergences in growth morphology.

Kuijt et al. (1985) discovered sieve elements in the endophytic body of Pilostyles thurberi, apparently in a discontinuous system which they considered to be a vestigial cell type. In older studies such elements were in general overlooked.

Weak vascular tissues are reported from the endophytic bodies of species of Pilo- styles. Floral tissue cushions contain rings of concentric vascular bundles in Rafflesia and Rhizanthes.

Most of the tissues are parenchymatous and these cells also never contain starch. In all genera the parenchymatous tissues are rich in tannins.

Stomata are known from scales of Pilostyles and Cytinus and also from Rafflesia and Rhizanthes (see Cammerloher 1920). Glandular hairs are known from the bracts of Cy- tinus and also in some species from the perigone. The function of the so-called ramenta, the outgrowths inside the flower tubes of species of Rafflesia and from the upper part of the diaphragm of Sapria is still unknown; their different forms have diagnostic taxonom-

Nn

Meijer Rafflesiaceae

ic value (Winkler 1927). The osmophoric and nectarial structures of the family still need more comparative anatomical studies.

Literature: Brown, W. H., Philipp. J. Sc., Bot. 7 (1912) 209-224, pl. 12—21. Cammerloher, H., Oesterr. Bot. Zeitschr. 69 (1920) 153-164, t. 3. Cartellieri, E. von, Bot. Archiv 14 (1926) 284-311, 7 pl. Endriss, W., Flora, 91, Erg. Band (1902) 209-236, t. 20. Forstmeier, L., F. Weberling & H.C. Weber, Beitr. Biol. Pflanzen 58 (1983) 299-312. Haak, J., Observ. Rafflesias (1889) 14 pp. Hunziker, J., PhD Thesis Freiburg (1920). Kuyt, J., D. Bray & L.R. Olson, Canad. J. Bot. 63 (1985) 1231-1240. Rutherford, R.J., Aliso 7 (1970) 263—288. Schaar, F., Sitzungsber. K. Akad. Wiss. Wien, Math.-Naturw. KI. 107 (1898) 1039-1056. Solms-Laubach, H., Bot. Zeitung 27 (1869) 185-190; Abh. Naturf. Ges. Halle, 13, 3 (1875) 40 pp., t. 24-27. Winkler, H., Planta 4 (1927) 1- ine

FLOWER MORPHOLOGY

Only in the genus Bdallophyton do the flowering structures (inflorescences) have a well developed long axis. In all other genera they are more or less fascicles or very short uni- flowered shoots, surrounded by a few whorls of scaly dark brown or blackish leaves. In Rafflesia and Rhizanthes there are in general 3 whorls of 5 scales (bracts), in Pilo- styles the whorls are 3—6-merous. Apodanthes has a regular structure of 2 outer bracts, 4 calyx-like bracts followed by 4 perigone lobes and an ovary with 4 placentas. Only in the tribus Cytineae inflorescences are developed like racemes, spikes or umbels, some- times with bracts and bracteoles.

Flowers are in general unisexual. In Rhizanthes zippelii unisexual flowers occur be- sides bisexual ones. Bdallophyton oxylepis has bisexual flowers and B. americanum unisexual ones on different plants; Mitrastema is always bisexual and protandrous.

Perigones can be partly tubular at their bases and the lobes are imbricate (Rafflesia) or valvate (Rhizanthes). Rafflesia and Sapria possess as unique organ the diaphragma. Staminal structures always have the thecae interconnected in a ring like in Hydnoraceae, though never in phalanges, and are in various ways connected with the central column. In some cases in Pilostyles they occur in 2—4 rings. The detailed anatomy of the anthers in various genera shows also some variation (see Fig. 1).

Literature: Koorders, S.H., Bot. Overz. Raffles. Ned.-Indié (1918) 206-215. Meijer, W., in: K.

Kubitzki (ed.), Families & Genera of Vascular Plants, vol. 2: K. Kubitzki, J.G. Rohwer & V. Bittrich (eds.), Flow. Pl., Dicot. (1993) 557—563.

Cc

Fig. 1. Comparison of anther structures in different genera, schematic. a. Rafflesia; b. Sapria; c. Rhi- zanthes; d. Mitrastema. Drawing Janis Atlee.

6 Flora Malesiana, Ser. I, Vol. 13 (1997)

PALYNOLOGY (R.W.J.M. van der Ham)

The most detailed account of Rafflesiaceae pollen is that of Takhtajan et al. (1985), which includes light and electron microscopic data of 25 species belonging to 7 genera. Others deal with one or a few species only. Straka (1978), Straka & Friedrich (1984) and Valdes et al. (1987) provide pollen descriptions with light and scanning electron micrographs of a few species of the most diverse genus Cytinus.

Pollen of the four tribes, as recognised by Harms (1935), is so different that it can- not be easily covered in a single description. Pollen grains of the Rafflesieae (Rafflesia, Rhizanthes, Sapria) are subspherical to ellipsoidal, 12—21 um large monads, with one distal pore or short colpus. The exine consists of a lamellate endexine (2—4 sublayers) and a loosely attached, sporopollininous perine-like outer layer. Pollen of Rafflesia arnoldii also has a homogeneous ectexine. The ornamentation is finely to very coarsely rugulate-verrucate.

Pollen grains of the Apodantheae (Pilostyles; pollen of Apodanthes and Berlinianche still unknown) are prolate (P x E = 18-28 x 10—20 um), tricolpate monads. The colpi are long and narrow. The exine consists of a homogeneous ectexine and an endexine that is often lamellate in its outer part. Locally the ectexine may be differentiated into tec- tum, columellate infratectum and foot layer. The ornamentation is + psilate.

Pollen grains of the Cytineae (Cytinus, Bdallophyton) are monads (Cytinus, Bdallo- phyton), or they are united in tetragonal, rhomboidal or tetrahedral, calymmate or aca- lymmate tetrads or, sometimes, dyads (Cytinus). The grains are subspherical to ellipsoi- dal, subiso- to heteropolar, 11-24 um large, with 2—4 + equatorial pori or short colpi (Cytinus), or (2) 3—4 long meridional colpi (Bdallophyton). The exine consists of a tectum, a distinct columellate infratectum and a nexine. The endexine is very thin, and recognisable only in the apertural areas. Cytinus pollen is sometimes semi- or intectate. The ornamentation is verrucate, perforate or + reticulate in Cytinus, and perforate in Bdallophyton.

Pollen grains of the Mitrastemoneae are triangular-ellipsoidal, 25 —28 um large mon- ads, usually with 3 equatorial(?) pores. The exine mainly consists of endexine, which is lamellate near the apertures. The ectexine is represented by small isolated verrucae. The ornamentation 1s psilate to scabrate.

The heterogeneity of Rafflesiaceae pollen led Takhtajan et al. (1985) to the concept that the family should be split into four natural families: Rafflesiaceae sensu stricto, Apo- danthaceae, Cytinaceae and Mitrastemaceae (see also p. 2). They did not indicate if these families form a monophyletic taxon. The single distal (monosulcate, ulcerate) aperture and the throughout lamellate endexine of the pollen of the Rafflesieae primitive features within the dicotelydons suggest that this group belongs to the subclass Magnoliidae, near the Aristolochiaceae (Takhtajan et al. 1985). With respect to the monophyly of the Rafflesiaceae sensu lato, it is important to determine whether the (2-) 3- (4-)porate and -colpate pollen types of the other tribes are ‘monosulcate-derived’ or ‘tricolpate-derived’ (Walker & Doyle 1975), and also if the monosulcate/ulcerate aperture type of the Raf- flesieae represents the original, primitive state of the aperture in Magnoliidae pollen.

Meijer Rafflesiaceae 7

References: Harms, H., in Engler & Prantl, Nat. Pflanzenfam., ed. 2, 16b (1935) 243 281. Straka, H., Pollen et Spores 20 (1978) 162-163. Straka, H. & B. Friedrich, Trop. Subtrop. Pflanzenwelt 51 (1984) 545-546. Takhtajan, A.L., N.R. Meyer & V.N. Kosenko, Bot. J. Leningrad. 70 (1985) 153-162. Valdes, B., M.J. Diez & I. Fernandez, Atlas polinico de Andalucia Occidental (1987). Walker, J.W. & J.A. Doyle, Ann. Missouri Bot. Gard. 62 (1975) 664-723.

POLLINATION

The foetid smell of the flowers of Rafflesia attracts carrion-flies of the genus Lucilia (Docters van Leeuwen 1929; Ross in Meijer 1985; Beaman et al. 1988; Banziger 1991). The smell is produced by fresh flowers, especially during sunny warm periods of the day. Beaman et al. suggested they observed green flies in action in Rafflesia at the upper part of the gullies in the column leading to the anther cavities between rows of hairs (Meijer 1985). The actual act of pollination is well illustrated by Banziger (1991), see Fig. 2. Still nobody has fully documented with a video camera what the flies do: laying eggs, collecting nectar (Haak 1885) or just using the carpet of ramentae as a mating ground (as insects do inside the odorous inflorescences of aroids: Croat, verbal comm.). The flies carry the pollen on their backs but have not been observed to use it as food. The actual source area (Osmophore) of the bad odour is also still not yet known. Banziger (1991) suggested from his own observations that the smell originates from the perigone lobes. Maybe the stomata described by Cammerloher (1920) have a function after all.

Douglas Warren Stevens noticed during his exploration of Nicaragua a faint smell from the flowers in Bdallophyton americanum (verbal comm.) and Rutherford (1966) reported this also from the masses of flowers of Pilostyles thurberi, both genera which like Cytinus and Mitrastemon also produce nectar. Honeyeater birds use flowers of Mitrastemon in New Guinea as nectar source (Beehler 1994).

Banziger (1995: 352—356) gave interesting new data on solidification of the liquid pollen of Rhizanthes on the back of pollinating insects and reliquefying by profuse stig- matic fluid and viability over a period of 3 weeks. He also gave details with more recent names of the pollinating carrion flies now classified as Calliphoridae.

a b c d

Fig. 2. Schematic pictures of flies picking up pollen in a male flower of Rafflesia kerrii (a, b) and striking it off on the stigma of a female flower (c, d). ss: stigmatic surface. Reproduced with permission from Banziger (1991).

8 Flora Malesiana, Ser. I, Vol. 13 (1997)

References: Banziger, H., Nat. Hist. Bull. Siam Soc. 39 (1991) 19-52; ibid. 43 (1995) 337-365. Beaman, R., et al., Amer. J. Bot. 75 (1988) 1148-1162. Beehler, B.M., Biotropica 26 (1994) 459—461. Cammerloher, H., Oesterr. Bot. Zeitschr. 69 (1920) 153-164, t. 3. Docters van Leeuwen, W.J., Trop. Natuur 18 (1929) 43—45. Haak, J., Weekbl. Pharmacie 3 (1885) 19 pp., 2 pl. Meijer, W., Nat. Geogr. 168 (1985) 136-140. Rutherford, R.J., PhD Thesis Claremont Grad. School, USA (1966).

LIFE “CYCLE

If we assume that the species of Rafflesia do not vary much in their life cycles we can reconstruct from data supplied by Teijsmann (1856a, b, 1858), Docters van Leeuwen (1929), Meijer (1958 and recent unpublished observations) that the total life cycle in that genus from seed to seed is about 3—4.5 years. New experiments started in Bogor and in temperate greenhouses in 1991 with seeds of R. gadutensis from West Sumatra, so far have not produced results. The life cycles of other genera of this family in Malesia are still incompletely known, except that Banziger (1995) observed for buds of Rhizanthes lowii (Rh. zippelii sensu Banziger) that it took an estimated 200-255 days from the point of breaking through the host tissue at a circumference of 3.7 to 4.1 cm to opening of the flower.

References: Banziger, H., Nat. Hist. Bull. Siam Soc. 43 (1995) 337-365. Docters van Leeuwen, W.J., Trop. Natuur 18 (1929) 43-45. Meijer, W., Ann. Bogor. 3 (1958) 33-44. Teijsmann, J.E., Nat. Tijds. Ned. Indié 12 (1856a) 279-281; Hook. J. Bot. & Kew Gard. Misc. 8 (1856b) 371-374; Ann. Hortic. Bot., Fl. Jard. Roy. Pays-Bas (1858) 27-30.

FRUITS AND EMBRYOLOGY

Field observations in 1981 and 1983 in the Ulu Gadut area near Padang, West Sumatra have shown that ripening of fruits of Rafflesia gadutensis takes about 8 months. Two fruits were monitored for periods of 6-7 months and the eldest had ripe seeds in Febru- ary 1984. Meijer’s guide Satar, who was monitoring this fruit below his hut, mentioned that it was visited by a ‘tupai kuning’ (most likely a tree shrew), the same species which was eating his young chickens. In Sumatra as well as Borneo we noticed male buds be- ing opened by squirrels or/and tree shrews and it looks as if one shrew sitting on the exit of such a vandalized bud was captured on the lens on Kinabalu near Poring; see Attenborough (1995). It sits on a bud not at the entrance of a flower as the legend in the book asserts. The holes made are too small for most squirrels.

From a very obscure report by R.H.C.C. Scheffer in a letter to Solms-Laubach [cited in Solms-Laubach (1875: 27)] it might appear that actual pollination is not necessary for fruit set. Scheffer wrote to Solms (translated): “Only one of the buds made it into a flow- er, only 3 years after the inoculation. Notwithstanding this was a female one, and with- out having a male flower nearby it still developed seeds. These were used to infect an- other plant of Cissus scariosa [= Tetrastigma leucostaphylum] and this was successful.”

Solms asserts that Scheffer suspected that the rudimentary anthers might have pro- duced some pollen. That is very unlikely. Meijer’s unpublished field observations showed that unfertilized female flowers, several months after flowering, had produced no seeds with embryos. Ovaries with very little pollination may be stimulated to grow

Meijer Rafflesiaceae 9

Fig. 3. Mature seeds of Rafflesia rochussenii Teijsm. & Binn. (left) and Rhizanthes zippelii (Blume) Spach (right). Scanning electron micrographs F. Bouman, courtesy Hugo de Vries-Laboratorium, Uni- versity of Amsterdam.

into fruits, but they can be full of seeds without embryos as observed from a fruit of Rafflesia keithii outside the Kinabalu National Park, August 1993 (seeds tested by F. Bouman, Amsterdam). Possibly there were other flowers of Rafflesia open in the garden or on Mount Salak about 120 years ago, to account for Scheffer’s observations. Real parthenocarpy of Rafflesia has never been proven.

Ovule and seed development stages have been studied for Rafflesia and Rhizanthes (Solms-Laubach 1898; Ernst & Schmid 1913). Pollen tetrads form according to the suc- cedaneous system; the tapetum of anthers consists of 2 or 3 layers of cells. The stigma is in Rafflesia and Rhizanthes situated in a ring around the rim of the column disk, often more or less papillose; the ovary shows in these genera a maze of placental plates which fill the ovary cavity. For the development of the embryosac see Ernst & Schmid (1913) and Olah (1960). The outer integument is reduced. Ovaries grow into berry-like fruits, with whitish pulpa around the seeds. The seeds (Fig. 3) are small and with hard scales [see Harms (1935: 255) and Bouman & Meijer (1994)]. Rafflesia patma has a 2-cell suspensor and an embryo consisting of 3—5 layers of 2—4 cells, often only 6 cells in total. Endosperm is nuclear and consists of 30—40 cells in R. patma. Endosperm and em- bryo mostly contain oil, see also Schuerhoff (1926: 526). Mitrastema also has cellular

endosperm, but ovules with only one integument.

References: Attenborough, D., The private life of Plants (1995). Bouman, F. & W. Meijer, PI. Syst. Evol. 193 (1994) 187— 212. Ernst, A. & E. Schmid, Ann. Jard. Bot. Buitenzorg II, 12 (1913) I-58, t. 1-8. Harms, H., in Engler & Prantl, Nat. Pflanzenfam., ed. 2, 16b (1935) 243-281.

Olah, L.V., Bull. Torrey Bot. Club 87 (1960) 406—416. Schuerhoff, P.N., Zytol. Bliitenpfl. (1926). Solms-Laubach, H., Abh. Naturf. Ges. Halle 13, 3 (1875) 40 pp., t. 24-27; Ann. Jard. Bot. Buiten- zorg 9 (1891) 184—246, 28 pl.; ibid., Suppl. 2 (1898) 11.

10 Flora Malesiana, Ser. I, Vol. 13 (1997)

DISPERSAL

Watanabe (1933, 1936) assumed long range seed dispersal of Mitrastema by birds. Ob- servations of jungle walkers working for Meijer (1958, 1983) at the sites of Rafflesia in West Sumatra showed that ground squirrels and tree shrews like to eat the contents of the white pulpy ripe fruits of these plants. These observations have been confirmed now by Emmons, Jamili Nais and Ali Briun (1991) and documented with colour photographs from a hide erected in August 1989 near a fruit of Rafflesia keithii on Mt Kinabalu. The fruits of Rhizanthes.also have white pulp, but they are hidden under the old perigones and predation has never been observed yet.

In analogy with other root and stem parasitic plants it is assumed that only distur- bance and damage to the organs of the host can deliver the signal for seeds in contact with them to germinate (Bouman & Meijer 1994).

References: Bouman, F. & W. Meijer, Pl. Syst. Evol. 193 (1994) 187-212. Emmons, L., et al., Biotropica 23 (1991) 197-199. Meijer, W., Ann. Bogor. 3 (1958) 33-44, fig.; Essays on Rafflesia- ceae (1983) 1-20. Watanabe, K., Bot. Mag. Tokyo 47 (1933) 798-805; J. Jap. Bot. 12 (1936) 603-618.

PHYTOCHEMISTRY (R. Hegnauer)

This mainly tropical family of parasitic plants is badly known at present from a chemical point of view (see Hegnauer 1973, 1990). Cytinus hypocistis yielded isoterchebin, an ellagitannin, as its yellow pigment and pelargonidin 3-galactoside and petunidin 3-gluco- side as red flower pigments. The sole crystalline compound isolated from acetone ex- tracts of Psilostyles thurberi turned out to be sucrose. Pollination biology of Rafflesia- ceae is still poorly known. Recent observations with Rafflesia pricei suggest that optical and olfactory mimicry may offer the clue. Flower pigments and odorous principles em- anated from flowers attract carrion-flies; they seem not to be compensated for their polli- nation activities by nurture or suitable breeding sites. Most authors are convinced that Rafflesiaceae belong to or are affiliated with Polycarpicae sensu Wettstein. However, synthesis and accumulation of ellagitannins do not favour such an assumption, because polymeric proanthocyanidins (i.e. ‘condensed tannins’) are the characteristic tannin-like metabolites of Polycarpicae. In this respect Rafflesiaceae are similar to Nymphaeaceae s.str. which produce ellagitannins and possibly Cabombaceae which produce gallic acid and probably gallotannins. Therefore it is noteworthy that Takhtajan (1980) has Aristolochiales, Rafflesiales, Nymphaeales (Cabombaceae, Nymphaeaceae s.str. and Ceratophyllaceae) and Nelumbonales as numbers 5—8 in his subclass Magnoliidae, and that in Thorne’s (1992) classification Aristolochiaceae are incorporated in Magnolianae— Magnoliales—Magnoliidae and the superorders Nymphaeanae and Rafflesianae immedi- ately follow Magnolianae. Nelumbonales and Ceratophyllales are treated by Thorne as orders of Magnolianae. Synthesis and accumulation of gallo- and ellagitannins may have evolved in a number of taxa now considered as outgroups of true polycarps.

References: Hegnauer, R., Chemotaxonomie der Pflanzen 6 (1973) 9; 9 (1990) 314-315. Takhta- jan, A.L., Outline of the classification of flowering plants (Magnoliophyta), Bot. Rev. 46 (1980) 225— 359. Thorne, R.F., Classification and geography of flowering plants, Bot. Rev. 58 (1992) 225-348.

Meijer Rafflesiaceae 11

KEY TO THE GENERA

la. Ovary superior, staminal structure a tube surrounding the pistil with a series of an-

thers above each other. Host plants in general Fagaceae .... Mitrastema (p. //) b. Ovary inferior or half-inferior, staminal structures different. Host plants species of ie erA EMEDICINE ee hee cin iehs ary sn SEs poise a. 2p Se eS Ler 2

2a. Mature flower buds oblong. Perigone without diaphragm, lobes 16-18, valvate, ending in bayonets (elongate stiff pointed appendages), which are hidden in a cav-

ity at apex of the column while flowers are in the bud stage . Rhizanthes (p. 37)

b. Mature buds more or less globular. Perigone with a diaphragm, the lobes imbricate,

mE ee cite we eis nets Ey Oe ac Me aye ais gk aes ok de eee 3

3a. Perigone lobes 5; ramenta only inside the flower tube ........ Rafflesia (p. 13)

b. Perigone lobes 10; ramenta on top of the diaphragm ... Sapria (Continental Asia) MITRASTEMA

Mitrastema Makino, Bot. Mag. Tokyo 23 (1909) 326 (‘Mitrastemma’). Mitrastemon Makino, Bot. Mag. Tokyo 25 (1911) 225, orth. mut., nom. inval.; Jochems, Rec. Trav. Bot. Néerl. 259 (1928) 203; Harms in Engl. & Prantl, Nat. Pflanzenfam., ed. 2, 16b (1935) 274; Yamamoto, Bot. Mag. Tokyo 50 (1936) 539; Watanabe, J. Jap. Bot. 13 (1937) 154; Matuda, Bull. Torrey Bot. Club 74 (1947) 133; Meijer in Kubitzki (ed.), Fam. & Gen. Vasc. Pl. 2 (1993) 560; Meijer & Veld- kamp, Blumea 38 (1993) 221-229. Type species: Mitrastema yamamotoi Makino (‘Mitra- stemma’ ).

Chlorophyll-less endoparasites with fungus-like endophytic body. Stems unbranched. Leaves scale-like, decussate. Flowers solitary, terminal, bisexual. Perianth much reduc- ed, collar-shaped. Stamens numerous, completely connate into a tube, below the sterile apical part with several vertical series of rings of c. 10 anthers each; pollen dicolpate, with reduced ectexine. Ovary superior, 1-locular, ovules numerous, anatropous, uni- tegmic. Fruit a slightly woody, berry-like capsule, horizontally dehiscing. Seeds sticky, testa hard. Fig. 4, 5.

Distribution Two species, one in Asia, from Japan to Taiwan, Yunnan, Bhutan, Assam, Indo-China, and Malesia: Borneo, Sumatra and New Guinea; a second, very closely related species (?) from Chiapas (Mexico) to Alta Vera Paz (Guatemala) and Antioquia (W Colombia).

Habitat In montane oak-chestnut forests, altitude 1400—2000 m.

Ecology The Asian species parasitic on roots of Fagaceae, probably the American species too. Pollination by insects and birds, seed dispersal most likely by birds and small mammals.

Notes 1. According to Matsuura, J. Fac. Sc. Hokkaido Imp. Univ. V, Bot. 3 (1935) 189, and Watanabe, J. Jap. Bot. 12 (1936) 769, f. 26P, the chromosome number is n= 20.

2. About the orthography of the genus name, see Meijer & Veldkamp, l.c.

12 Flora Malesiana, Ser. I, Vol. 13 (1997)

Mitrastema yamamotoi Makino

Mitrastema yamamotoi Makino, Bot. Mag. Tokyo 23 (1909) 326, fig.; P. Royen, Nova Guinea, Bot. 14 (1963) 243-245, pl. 17; Hansen, Bot. Tidsskr. 67 (1972) 149; in Fl. Camb., Laos & Vietnam 64 (1973) 62, t. 9; Tang Shui Liu & Ming You Lai in Fl. Taiwan 2 (1976) 582, t. 414; Meijer & Veldkamp, Blumea 38 (1993) 227. Syntypes: Tashiro s. n., Bando s. n., Yamamoto s. n. (TI holo), Japan, Kyushu.

Mitrastemon sumatranum Nakai, Icon. Pl. As. Or. 4 (1941) 338, t. 113 ((sumatranus’ ). Type: Jochems s.n. (TI holo), Sumatra, Karo Mts.

For more complete synonymy and references, see Meijer & Veldkamp, l.c.

Plants about 2.5—15 cm long and up to 3 cm in diameter. Basal part a corky pustular cupule, up to c. 2 cm high and in diameter, the margin an irregularly low lobed rim; stems 5—15 mm diam. Leaves (also called bracts or scales) in 3—4(—7) decussate whorls, increasing in length from the base of the plant upwards, broadly to narrowly ovate, at apex blunt-rounded, (4—)10—20(—28) by (5—)10—15(—25) mm, cream (turning ebony) coloured with brown spots, the lowest often purplish brown. Flowers up to 20 mm long, with a foetid smell. Perigone 5—10 by 6—17 mm, truncate or slightly 4-lobed. Sta- minal tube tubular, wide and globose in the basal part, 14—20 mm long, the minute an- thers in a 2—5 mm broad ring in the upper part, the whole collar early caducous. Ovary ellipsoid, c. 8 by 3 mm, style ovoid-ellipsoid, 2—8 by 3—6 mm, stigma 2—5 by 4—6 mm; 8—15 radial placentas. Fruit up to c. 20 by 10 mm, opening along a horizontal ring about halfway. Seeds c. 0.25 mm diameter, with a small funicle, yellowish or dark brown. Fig. 4, 5.

Distribution India, Thailand, Cambodia, Vietnam, China (Yunnan), Japan, Taiwan; Malesia: Sumatra (Aceh, East Coast), Borneo (Sabah: Mt Kinabalu; Sarawak: 4th Divi- sion), Papua New Guinea (W and E Highlands, Morobe, Milne Bay Provinces).

anthers stigma

staminal tube

perianth ovary

bracts

Fig. 4. Mitrastema yamamotoi Makino. Full open flower, habit and length section, with indication of flower parts. True size up to 15 cm high. Drawing by Janis Atlee after the type description by Makino.

Meijel Rafflesiaceae 3