Morphology, anatomy, and taxonomic position of Pagameopsis (Rubiaceae-Rubioideae)

Morphology, anatomy, and taxonomic position of Pagameopsis (Rubiaceae-Rubioideae)

FREDERIC PIESSCHAERT, l STEVEN JANSEN, IVAN JAIMES,

ELMAR ROBBRECHT, AND ERIK SMETS

Piesschaert, E (Laboratory of Plant Systematics, Institute of Botany and Mi- crobiology, Catholic University Leuven (K.U.Leuven), Kasteelpark Arenberg 31, B-3001 Leuven, Belgium; present address: Institute for Nature Conservation, Kli- niekstraat 25, B-1070 Brussels, Belgium; email: [email protected]), S. Jansen (Laboratory of Plant Systematics, Institute of Botany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leuven, Belgium; email: steven. [email protected]), I. Jaimes (Laboratory of Plant Systematics, Institute of Botany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leu- yen, Belgium; email: [email protected]), E. Robbrecht (National Botanic Garden of Belgium, Domein van Bouchout, B-1860 Meise, Belgium; email: el- [email protected]) & E. Smets (Laboratory of Plant Systematics, Institute of Botany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leu- yen, Belgium; email: [email protected]). Morphology, anatomy, and taxonomic position of Pagameopsis (Rubiaceae-Rubioideae). Brittonia 53: 490- 504. 2001.--Morphological and anatomical features (including wood anatomy and pollen morphology) of the small neotropical genus Pagameopsis (Rubiaceae- Rubioideae) are discussed and illustrated. The fused ovaries, fenestrate corolla tube, basally attached anther filaments, and absence of raphides are especially noteworthy. Pagameopsis is definitely not a member of the Psychotrieae because of significant differences in wood anatomy and gynoecial and fruit structure. A close affinity with Gaertnereae seems doubtful for similar reasons. The taxonomic affinities of Pagameopsis remain obscure. The genus shows similarities with several taxa of the Rubioideae, such as Coccocypseleae, Morindeae, Hedyotideae, and Metabolos. The absence of raphides, on the other hand, makes a position in the Rubioideae doubtful.

Key words: anatomy, morphology, Pagamea, Pagameopsis, Psychotrieae, Ru- biaceae, taxonomy.

Introduction

Pagameopsis (S tand l . ) S t e y e r m . is a small neotropical genus of the Rubiaceae. It c o m p r i s e s two spec ies , bo th sma l l , branched shrubs with leaves that are clustered at the top of the stems. The interpe- tiolar stipules are fused into a short, tim- briate, persis tent sheath. The most ly termi- nal, thyrsoid inflorescence is composed of small, dense or sl ightly branched clusters of

Author for correspondence

light blue to lavender-purple, small flowers. Pagameopsis is restricted to the Guayana Shield; it occurs in southern Venezuela and adjacent Brazil (Steyermark, 1974). It is a common genus in broad- leaved meadows mixed with low shrubs, e.g., on the Auy4n tepui and the summit of Cerro Huachama- cari and Cerro Aracamuni (Huber, 1995). Standley (1931) descr ibed the first species of Pagameopsis as Pagamea garryoides Standl. Al though no arguments were given, Standley probably included this species in Pagamea Aubl. because of its sheathing

Brittonia, 53(4), 2001, pp. 490-504. �9 2001, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

ISSUED: 28 Feb 2002

2001] PIESSCHAERT ET AL.: RUBIACEAE-RUBIOIDEAE 491

stipules, which is one of the distinguishing features of Pagamea in the tribe Psycho- trieae (Taylor, 1996). However, he remarked that Pagamea garryoides differs conspicu- ously f rom most of the other species of Pa- gamea in its densely pubescent leaves. Steyermark (1965) noticed that Pagamea garryoides also differs in many other and more important features. It has, for exam- ple, dry fruits derived f rom an inferior ovary instead of fleshy fruits coming f rom a superior ovary. Moreover, the ovaries of adjacent flowers are often more or less fused. He therefore established a separate genus Pagameopsis in the Psychotrieae, including P. garryoides and P. maguirei Steyerm. The latter is very variable and was described with two subspecies and two varieties (see also Steyermark, 1974). Later, Steyermark (1987) reevaluated the subspecies and varieties of Pagameopsis maguirei, but the position of the genus in the Psycho- trieae was never questioned. Taylor (1996) emphasized the unusual features of several neotropical genera of the Psychotrieae, including Pagamea and Pagameopsis, but retained them in this tribe. Jansen et al. (1997) noted that there are pronounced wood anatomical differences between Pa- gameopsis and the core genera of the Psy- chotrieae (Psychotria L., Chassalia Comm. ex Poir., Chazaliella E. M. A. Petit & Verdc.), without describing the wood of the genus in detail.

In recent years, the taxonomic landscape in the subfamily Rubioideae and the Psy- chotrieae in particular has changed pro- foundly, mainly because of new insights provided by macromolecular data. For ex- ample, evidence has been accumulating to reestablish the tribe Gaertnereae for Paga- mea and its p a l e o t r o p i c a l s i s t e r -genus Gaertnera Lain. The G a e r t n e r e a e were o r ig ina l ly e s t ab l i shed by B r e m e k a m p (1966), based on the occurrence of a stipular sheath and superior ovaries, but later authors included Gaertnera and Pagamea in the Psychotrieae (Igersheim et al., 1994; Robbrech t , 1988, 1994). Jansen et al. (1996a) noticed wood anatomical and pollen morphological differences between Pa- gamea and Gaertnera on the one hand and the Psychotrieae on the other. They sug-

gested creating a new subtribe Gaertnerinae wi th in the P s y c h o t r i e a e . Sequence da ta f rom rbcL and ITS (Bremer, 1996; Nepok- roeff et al., 1999) and sequence data of the rpsl6 intron (Andersson & Rova, 1999) confirmed these differences. Andersson and Rova (1999) proposed to reestablish the Gaertnereae as a separate tribe at the base of the Psychotrieae/Morindeae-clade. Sev- eral other genera (e.g., Lasianthus Jack., Saldinia A. Rich. ex DC., Trichostachys Hook. f., Ronabea Aubl.) have also been excluded f rom the Psychotrieae on the basis o f both macromolecular and morphological data (Bremer, 1996; Andersson & Rova, 1999; Nepokroef f et al., 1999; Piesschaert et al., 2000a); they occupy a place near the base of the Rubioideae. The neotropical genus Declieuxia Kunth was recently transferred f rom the Psychotrieae to the Cocco- cypseleae s.1. (Piesschaert et al., 2000b).

In the present study, wood anatomical and pollen morphological descriptions are presented for Pagameopsis. A fixed collec- tion of P. garryoides allowed us to observe and document leaf and floral anatomical characters as well. The taxonomic position of Pagameopsis is reconsidered and discussed in view of the important generic re- arrangements in the Psychotrieae and Ru- bioideae outlined above and considering the new morphological and anatomical data presented here.

Mater ia l and M e t h o d s

This study is based on herbarium material f rom U and VEN and on a fixed col- lection of Pagarneopsis garryoides f rom VEN. The fol lowing specimens were examined:

Pagameopsis garryoides (Standl.) Stey- erm. Venezuela. T.F. A m a z o n a s : Cerro Duida, N of La Esmeralda, alto Rfo Ori- noco, 03~ 65~ Tillet & Talukdar 752120 (U). Bolivar: La Gran Sabana, near Kavanay6n , 05~ 61~ Ramfrez 779 (VEN, fixed material).

Pagameopsis maguirei Steyerm. Vene- zuela. T.F. A m a z o n a s : Cerro de La Neb- l ina, a b o v e Rfo M a r a n i n u m a , 0 0 ~ 66~ Steyermark & Luteyn 129832 (U);

492 BRITTONIA [VOL. 53

Amazonas , Cerro de La Neblina, 00~ 66~ Stein 1615 (VEN).

For the wood anatomical study, the following wood samples of Pagameopsis were used (Tw numbers are sample numbers of the xylar ium of the Royal Museum for Cen- tral Africa at Tervuren, Belgium):

Pagameopsis maguirei Steyerm. subsp. neblinensis Steye rm . var. angustifolius Steyerm. Venezuela. T.F. A m a z o n a s : Cer- ro de La Neb l ina , cumbre , 00~ 66~ Maguire et al. 42119 (Tw 36517, juvenile wood f rom a branch with diam. 15 mm), 42129 (Tw 36619, mature wood).

Wood blocks were sectioned and macer- ated according to standard methods and LM and SEM observat ions were carried out following Jansen et al. (1998). Vessel e lement and fiber lengths were measured f rom mac- erations in 30 elements per sample. Aver- ages are bracketed for quantitative data. Quantitative data were determined f rom the mature wood sample. Terminology follows the IAWA list ( IAWA Committee, 1989).

The " a l u m i n o n " test (Chenery, 1946, 1948) was applied to leaves of Pagameop- sis garryoides and P. maguirei subsp, neblinensis, and the chrome azurol-S test, a chemical spot-test for A1 accumulat ion in wood (Kukachka & Miller, 1980), to both wood samples.

Methods for LM preparations follow Piesschaert et al. (1997). Leaf and flower anatomical data are f rom the fixed collec- tion of P. garryoides.

Pollen of Pagameopsis garryoides was obtained without any treatment f rom fixed anthers (flowers just before anthesis) and air-dried on a stub. For P. maguirei, anthers from herbar ium material were first rehy- drated with Agepon 1:200, critically point dried (CPD 030 Critical Point Dryer, Bal- zers), mounted on a stub, and opened to re- lease the pollen grains. The material was spu t t e r - coa t ed wi th gold ( S p i - m o d u l e T M

Sputter Coater). These different treatments should be taken into account when considering the measurements . Observat ions were made with a Jeol JSM-6400 scanning electron microscope.

Resul ts

A detailed description of the general morphology of the two species of Paga-

meopsis is given by Steyermark (1965, 1974, 1987). Here we present our new anatomical data and some morphological features that are treated in greater detail.

WOOD ANATOMY

The wood lacks growth rings (Figs. 1, 2). Vessels are diffuse and exclusively solitary. Vessel outline is round to oval. Vessel width is 40(51)65 Ixm and vessel e lement length is 500 (626 )850 txm. T h e r e are 18(22.5)25 vessels per mm. Perforation plates are simple. The vesse l - ray perfora- tions are frequently scalariform or irregular (Fig. 3). Vessel pits are alternate, minute, and vestured. Ground tissue is composed of f iber-tracheids, with numerous distinctly bordered pits on the tangential and radial fiber walls (Fig. 4). Chambers of the fiber pits are 3 -5 Ixm diam. Fiber length varies in the range of 680(786)900 txm. Axial parenchyma is scanty paratracheal and sparsely diffuse (Fig. 2). The rays are heterocellular, uni-, bi-, or triseriate and with long uniseriate margins (Fig. 5); uniseriate rays were exclusively found in Tw 36517. They are composed o f procumbent and square ray cells with several rows of u p r i g h t / square cells (Fig. 6). Calcium oxalate crystals and silica bodies are absent in the wood.

LEAF ANATOMY

The leaves are hypostomatic. The upper epidermis consists of relatively small, flat- tened cells and is covered with a cuticula. Below the upper epidermis there is a conspicuous hypodermis , consisting of 2 or 3 layers of isodiametric ceils (Fig. 7). The di- ameter o f the hypodermal cells increases toward the palisade parenchyma. The palisade pa renchyma is two-layered. In the chlorenchyma, small druse-like crystals or large, loose aggregates of randomly orien- tated needle-l ike crystals are found. In the palisade parenchyma, similar but smaller crystalline aggregates occur. Some isolated small prismatic crystals also may occur. True raphides, defined by the IAWA Com- mittee (1989) as a bundle of parallel nee- dies, are absent.

2001] P I E S S C H A E R T E T AL.: R U B I A C E A E - R U B I O I D E A E 493

FIGS. 1-6. Wood ana tomy of Pagameopsis maguirei. 1. Transverse section showing solitary vessels. 2. Transverse section, axial pa renchyma cells sparsely present (arrows). 3. Irregular vessel-ray perforation plate. 4. Detail of bordered fiber pits with small vestures, g. Tangential section, heterocellular rays, 1-3 cells wide. 6. Radial section, ray cells procumbent , upright or square. (1-4 , Maguire et al. 42119; 5, 6, Maguire et al. 42129. Scale bars: 1 = 200 Ixm; 2, 5, 6 = 100 Ixm; 3, 4 = 10 ixm.)

ALUMINUM ACCUMULATION

None of the species accumulates aluminum (A1) in its leaves. The chrome azurol- S test also proved to be negative for the wood samples of Pagameopsis maguirei. Although blue or bluish fruits and flowers are to a certain extent diagnostic for A1 ac- cumulators in general (Chenery, 1946,

1948) and also in Rubiaceae (Jansen et al., 2000), this correlation does not apply to Pa- gameopsis.

INFLORESCENCE AND FLORAL MORPHOLOGY/

ANATOMY

The branches of Pagameopsis bear ter- minal, frondobracteose, thyrsoid inflores-

494 BR1TFONIA [VOL. 53

FIGS. 7-11. Leaf and flower anatomy of Pagameopsis garryoides (Ramfrez 779). 7. Cross section of leaf with multilayered hypodermis. 8. Cross section of three fused gynoecia. Oxalate crystals in endocarp lightened with polarized light. 9. Longitudinal section of floral bud. Stamens are attached at the base of the corolla or very superficially fused with it. Also note the papillate disk. 10. Longitudinal section of floral bud showing bilobed papillate stigma. 11. Longitudinal section of ovule with knee-shaped funiculus. (Scale bars: 7 = 0.1 mm; 8 = 1 ram;9, 10 = 0.5 mm; 11 = 0.2 mm.)

cences . T h e s e are dense ly conges t ed , bu t their t r i c h o t o m o u s b ranch ing is st i l l r e c o g - n izable , e s p e c i a l l y at the base o f the inf lo- rescence . The t e rmina l units are t r iads or ra re ly p a i r e d f lowers wi th m o r e o r less fused ovar ies . The sub tend ing b rac t s are fused wi th the two outer f lowers o f a t r i ad and sh i f ted upward . Brac teo les a re m o s t l y r e d u c e d or they o c c a s i o n a l l y occu r as sca ly r emnan t s in the fused c o m p l e x .

F lower s o f Pagameopsis are 4 - 6 - m e r o u s . The ca lyx consis ts o f a short tube and wel l - deve loped lobes that are longer than the tube. The lobes are cil iate, subequal , and triangular to s l ight ly spathula te wi th an acute

to subacumina te , s l ight ly r ecu rved apex. Col le ters are often, though not a lways , found in the s inuses be tween the ca lyx lobes. The upper ha l f o f the ins ide o f the coro l l a tube, the coro l la throat , and the adaxia l s ide o f the corol la lobes are dense ly cove red wi th mo- n i l i fo rm t r i chomes (sensu Robbrech t , 1988; Figs. 9, 10). On the outside, the co ro l l a is g labrous excep t for some short uniser ia te hairs at the top o f the coro l la lobes ; these hairs d i s appea r at matur i ty . The coro l l a tube o f ma ture f lowers is d is t inc t ly fenes t ra te (i.e., p r o v i d e d wi th longi tud ina l slits between the peta ls ) at the base after anthesis , a fea ture that apparen t ly has been over-

2001] P I E S S C H A E R T ET AL.: R U B I A C E A E - R U B I O I D E A E 495

looked in the past. The anthers are dorsi- medifixed and exserted. In the upper part of the corolla tube, the glabrous anther filaments are superficially attached to the corolla; at the height of the corolla fenestrations the filament is free, and at the very base the filament is again fused with the corolla (Fig. 9). It should be noted that in bud stage the filament is already clearly free from the corolla at the height of the fenestrations; the fenestrations themselves become discernible only after anthesis. The filaments are visible from the outside of the mature corolla through the fenestrations.

The ovaries of adjacent flowers are par- tially to fully fused, forming clusters of two to three flowers (see also above; Figs. 8, 12, 13). The ovary is bilocular and each locule contains one ovule attached at the basal cor-

ner at the septal side (Fig. 12). The placenta (or funiculus) is knee-shaped, i.e., it has an abaxial protrusion that can be interpreted as an obturator (Fig. 11). A papillate to pubescent disk surrounds the base of the style (Fig. 15). The outermost papillae are clearly longer than those on the inside. They all have a striate surface pattern (Fig. 16). The stigma is bilobed and the adaxial surface of the stigmatic lobes is papillose (Fig. 10). Just below the stigma lobes, the style has ve ry short, papi l la - l ike , ep idermal out- growths, which are absent toward the base o f the style. N u m e r o u s druse- l ike and small, prismatic crystals are found in the tissue of the disk and the endocarpic layers (i.e., the cell layers constituting the wall of the locules; Fig. 8), which become scleri- f i ed in the fruit. Raphides are absent.

FIGS. 12-16. Gynoecium and fruit morphology of Pagameopsis garryoides. 12. Longitudinal section of two fused gynoecia with solitary, basally attached ovules. 13. General view of young fruits. Calyx lobes removed to show the papillate disk. 14. Pyrene of a fruit, exo- and mesocarpal layers removed. Note the conspicuous beak at the apex. Part of the endocarpal or pyrene wall was removed to show the immature, basally attached seed. 15. Papillate disk. Outer papillae are clearly longer than the inner ones. 16. Detail of the striate surface of the papillae. (12, Ramfrez 779; 13-16, Tilliet & Talukdar 752120. Scale bars: 12, 13 = 1 mm; 14, 15 = 0.1 mm; 16 = 10 I~m.)


FRUIT STRUCTURE

The fruits o f Pagameopsis are dry and indehiscent (Steyermark, 1974). There is a clear structural difference between the bony endocarp and the exo- and mesocarp, which are more or less fleshy and easily removable from the endocarp. Except for the degree of inflation of the mesocarpic layers, the structure of these dry fruits is identical to that of a drupe and they should be interpreted as an intermediate stage between a drupe and a capsule. The bilocular bony pyrene is more or less triangular with an acuminate base and truncate apex. It is crowned by a conspicuous, two-lobed beak, which is an endocarpic outgrowth. Each locule contains one basally attached seed (Figs. 13, 14). Unfortunately, the structure of the endosperm and seed coat anatomy could not be investigated due to the lack of mature seeds.

POLLEN MORPHOLOGY

Pagameopsis garryoides and P. maguirei are rather different in pollen morphology. Pollen grains in both species are oblate to oblate-spheroidal, medium-sized, 2 0 - 3 0 • 3 0 - 4 0 Ixm in SEM-preparations, tricolporate with a granular colpus membrane . In P. garryoides the ectocolpus ends are often (though not always) fused at the apocolpium, and consequently the pollen grains are syncolporate (Figs. 17, 18, 20). Other grains of this species are parasyncolporate, which means that the apices of the colpi divide and fuse toward the apocolpium, leaving a more or less isolated area of the sexine known as the apocolpial field (Punt et al., 1994; Fig. 19). Syncolporate or parasyncolporate pollen, however, were not observed in P. maguirei (Figs. 21, 22). The sexine pattern is also different: P. maguirei has a reticulate to microreticulate sexine with smooth muri (Fig. 24). In P. garryoides, the sexine is also reticulate to microreticulate, but small projections pointing toward the lumen occur at the inside of the muri (Fig. 23). According to Pire (1997), this is a transitional stage between a simple and complex reticulum (i.e., a ret iculum differentiated into a psilate suprareticulum and spinulate infrareticulum).

T a x o n o m i c Pos i t ion o f Pagameopsis Pagameopsis is a representative of the an-

cient flora of the Guayana Highlands, a region reputed for its high degree of endemism and many highly adapted life forms (Takh- tajan, 1986; Huber, 1995). The region also holds "exceptionally great interest for the history of floras, partly for the verification of past floristic connections with paleotropical regions" (Takthajan, 1986: 258). As demonstrated by Puff et al. (1993) in the Schradereae, affinities between paleo- and neotropical taxa are more easily overlooked than intracontinental alliances. This might be part of the reason why the relationships of many Guayanan endemics remain uncertain.

Besides Pagameopsis, 12 other small (monospecific or with few species) genera of the Rubiaceae are confined to the Gua- yana region. Most of them belong to the problematic Rondeletieae-all iance (Chale- pophyllum Hook. f., Dendrosipanea Ducke, Holstianthus Steye rm. , Neblinathamnus Steyerm., Sipaneopsis Steyerm.), but the monospecif ic genera Coccochondra Raus- chert and especially Aphanocarpus Stey- erm. and Coryphothamnus Steyerm. are more interesting in the present context. Just like Pagameopsis, the latter three genera are included in the Psychotrieae (Rob- brecht, 1988, 1994; Taylor, 1996), despite the fact that they have one or several features which are atypical for the tribe. The taxonomic history of Aphanocarpus and Coryphothamnus is identical to that o f Pa- gameopsis. They were originally described as species of Pagamea (Standley & Stey- ermark, 1953) but were later raised to ge- netic rank (Steyermark, 1965). Standley and S t e y e r m a r k (1953) b e l i e v e d that Aphanocarpus, Coryphothamnus, and Pa- gameopsis are closely related to each other, probably because they have the same peculiar habit. In the following paragraphs, we will have a closer look at these and other possible relatives of Pagameopsis within and outside the Rubioideae.

A GENUINE MEMBER OF THE RUBIOIDEAE?

The absence of raphides casts doubts on the position of Pagameopsis in the Rubioi- deae. Nevertheless, a comparison with the


FIGS. 17-24. 17--20, 23. Pollen morphology of Pagameopsis garryoides. 21, 22, 24. Pollen morphology of P. maguirei. 17. Polar view. 18. Polar view of a syncolporate grain. 19. Polar view of a parasyncolporate grain. 20. More or less equatorial view of a syncolporate grain. 21. Polar view. 22. Equatorial view. 23. Detail of microreticulate sexine with small projections into the lumina. 24. Detail of microreticulate sexine. (17-20, 23, Ramfrez 779; 21, 22, 24, Stein 1615. Scale bars: 17-22 = 10 Ixm; 23, 24 = 1 Ixm.)

s u b f a m i l y wi th w h i c h it has t r ad i t iona l ly been a s soc i a t ed is neces sa ry .

The ana tomica l and morpho log i ca l features o f Pagameopsis undoub ted ly demon- strate that the genus does not be long to the Psychot r ieae . Pagameopsis differs signifi- can t ly f rom the Psycho t r i eae in the s tructure o f its wood: so l i t a ry vesse l s vs. radial mul - t ip les in Psychot r ieae , f iber t racheids vs. l i- b r i fo rm fibers, and the p resence o f sparse ly d i f fuse axial p a r e n c h y m a vs. absence o f pa- r e n c h y m a (Table I). The g y n o e c i a o f adjacent f lowers are mos t l y fused. This fea ture does not occur in the Psychot r ieae , a l though

acc iden ta l ly two fused fruits m a y be found among the no rma l ones in Psychotria (pers. obs.) . Dry , indeh i scen t fruits are also ve ry unusua l in the f l e shy - f ru i t ed Psychot r ieae , a l though they do not p rov ide s t rong evidence to exc lude Pagameopsis f rom this tr ibe. Severa l authors have po in ted to the var iab i l i ty o f frui t s t ructure in re la ted taxa o f the Rub io ideae (Bremer & Er iksson, 1992; Bremer, 1996). Never the less , the d ry fruits add to the genera l d i f fe rence be tween Pa- gameopsis and the Psychot r ieae . The exc lu- s ion o f Pagameopsis undoub ted ly makes the Psycho t r i eae a m o r e h o m o g e n e o u s tribe.


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Should Pagameopsis then be included in the Gaertnereae, as a close relative of Pa- gamea, from which it was segregated? Sheathing stipules and fiber tracheids favor this hypothesis, al though in Pagameopsis the stipules are very short and the fimbriate sheath is reduced a lmost to a r im of tissue between the leaf bases, whereas the stipular sheath of the Gaer tnereae is usually long and well-developed. Moreover, Pagameop- sis lacks most of the morphological features distinguishing the tribe Gaertnereae, namely the banded wood parenchyma, the secondarily superior ovary, and the conspicuous endexine costae bordering the pollen endoapertures (Jansen et al., 1996b; Iger- sheim et al., 1994). The Gaertnereae also have fleshy drupes instead of dry indehiscent fruits. Consequently, the inclusion of Pagameopsis in the Gaertnereae is not supported.

The fusion of gynoecia, as in Pagameop- sis, is a wel l -known feature of the Morin- deae-al l iance (i.e., Morindeae, Mitchella/ Damnacanthus-group, and the Prismato- merideae; Igersheim & Robbrecht, 1994). M o r i n d e a e also h a v e fenes t ra te co ro l l a tubes in common with Pagameopsis (see further). The fused ovaries are only superficially similar. The Morindeae have two ovules per locule separated by a massive placenta (Igersheim & Robbrecht, 1994), a peculiar gynoecial structure that is absent in Pagameopsis. In Mitchella L. and Damna- canthus Gaertn. f., the solitary ovules are campylot ropous and attached near the top of the septum instead of being basal and anatropous (Robbrecht et al., 1991). The structure of the gynoee ium of Pagameopsis comes closest to that of the Prismatomeri- deae. In the latter, however, the solitary ovules are attached near or slightly above the middle of the septum and the fruit is berryl ike (Igersheim & Robbrecht, 1994), making a close affinity with Pagameopsis equally doubtful.

The above-mentioned groups of the Ru- bioideae all have predominantly white flowers, which is the most common situation in the Rubiaceae (Robbrecht, 1988). Blue flowers, as in Pagameopsis, occur far less frequently, but they are found, e.g., in the Coc- cocypseleae s.1. This tribe comprises the

genera Coccocypselum P. Browne, Hindsia Benthe. ex Lindl., and Declieuxia P. Browne (Piesschaert et al., 2000b). The latter was traditionally included in the Psychotrieae (Robbrecht, 1988, 1994; Taylor, 1996). The centre of diversity of Coccocypseleae lies in southeast Brazil (Piesschaert et al., 2000b). According to Huber (1995), the Brazilian Shield and Guayana have distinct phytogeo- graphical affinities. They share several char- acteristic genera, among which is Declieux- ia. The two most distinguishing features of Coccocypseleae are the pollen grains with a complex reticulate sexine sculpture and stipules with a central colleter-tipped awn (Pies- schaert et al., 2000b). The transitional stage between simple and complex reticulum in pollen of Pagameopsis garryoides is also present in Hindsia (compare Fig. 23 with fig. 3E in Piesschaert et al., 2000b). Other similarities are found in the fruit structure (tran- sition between drupes and capsules in De- clieuxia) and calyx (presence of colleters in the sinuses of the calyx lobes in Hindsia and Coccocypselum), but the taxonomic value of these characters is restricted. The stipular structure of Pagameopsis seems not to be in agreement with that of the Coccocypseleae. The central awn is absent and, insofar as they are visible on dried material, the tim- briae of Pagameopsis stipules are not colleter-tipped. It can be concluded that, except for the stipular structure and the absence of raphides, there is not much evidence against a relation between Pagameopsis and the Coccocypseleae, but neither are there very strong arguments in favor of it.

As mentioned before, Standley and Stey- ermark (1953) placed Coryphothamnus and Aphanocarpus in the Psychotrieae, close to Pagameopsis. There are indeed some morphological similarities, such as the peculiar habit with the leaves clustered at the top of the stems, blue flowers, and shortly sheathing fimbriate stipules. On the other hand, the slightly inferior to superior ovary of Coryphothamnus is two-celled with six to eight ovules on an axil lary placenta. The septum is very thin and weakly developed and consequently the ovary and fruit may seem unilocular. The dry fruit is septicidally dehiscent and contains two to four rugulose seeds (Steyermark, 1974). Aphanocarpus


has a one-celled ovary with one basal, erect ovule and dry and indehiscent fruits (Stey- ermark, 1974). These features clearly dis- tinguish Coryphothamnus and Aphanocar- pus f rom the Psychotrieae as well as f rom Pagameopsis and make a close relation doubtful. Taylor (1996) believed that the unusual fruits o f Coryphothamnus point to a relationship with the Spermacoceae. De- tailed morphological and anatomical data are desperately needed for these taxa. Es- pecially the presence or absence of raphides should be carefully reinvestigated.

Coccochondra is the fourth " o d d " Guay- anan genus (besides Aphanocarpus, Cory- phothamnus, and Pagameopsis) that was referred to the Psychotrieae in the past. It has white (vs. blue) flowers. The most distinc- tive character of the genus is the nonfleshy fruit with crustaceous endocarp, which dis- tinguishes it f rom the typical drupes in the rest of the Psychotrieae (Steyermark, 1974). Kirkbride and Robbrecht (1984) found the highest phenetic similarity for Coccochon- dra with Pagarneopsis. They considered Coccochondra as an obvious m e m b e r of the Psychotrieae, inter alia, based on the presence of raphides and the bilocular ovary with solitary, basal erect ovules. Indeed, of the four " o d d " Guayanan genera, Cocco- chondra most probably is the only one to be retained in the Psychotrieae. The dry fruit wall is the only notable difference, and as we noted before, this feature is very variable in the Rubiaceae. This also implies that Pagameopsis and Coccochondra are not closely related to each other.

The dry and beaked fruits of Pagameop- sis are morphological ly very similar to those found in some members of the Hed- yotideae, e.g., in Pentas Benth. (Verdcourt, 1953). The structure of the fruit wall is tax- onomical ly not very reliable, but as far as we know, beaked fruits have a very restricted occurrence in the Rubiaceae. The only other record we are aware of is the Mada- gascan genus Payera Baill. (Buchner & Puff, 1993), traditionally included in the Hedyot ideae but now of uncertain position (Andersson & Rova, 1999). The Hedyoti- deae also have fimbriate stipules, but the fimbriae are usually colleter-tipped, a feature not observed in Pagameopsis. Papillate

to hairy disks and fenestrate corolla tubes are found in certain Hedyotideae as well.

Several morphological and anatomical s imi lar i t ies occu r be tween Pagameopsis and Metabolos Blume (= Allaeophania Thwaites), an Asian monospecif ic genus that was associated with the Hedyot ideae (viz. Neanotis W. H. Lewis) by B r e m e k a m p (1939). Puff and Igersheim (1994) rejected Bremekamp ' s suggestion because Metabo- los has tricolporate (vs. pluricolporate) pollen. They described the exine of Metabolos as reticulate, but their photographs (see Puff & Igersheim, 1994: fig. 6) clearly show that it is a complex reticulum, consisting of a psilate suprareticulum and spinulate infrar- et iculum (e.g., Pire, 1997; Piesschaert et al., 2000b). The complex reticulum is a typical sexine pattern of the Spermacoceae sensu Bremer (1996), which include the Hedyot i - deae of Bremekarnp (e.g., Pire, 1997; S. Huysmans & S. Dessein, unpubl, data). Therefore a relation between Metabolos and the Hedyot ideae certainly cannot be over- ruled on the basis of palynological data. Most authors (Robbrecht, 1988, 1994; Puff & Igersheim, 1994) placed Metabolos in the tribe Psychotrieae, near the genus Lasian- thus Jack. Several macromolecular analyses have shown, however, that Lasianthus does not belong to the Psychotrieae at all but to a more basal clade of the Rubioideae (rbcL data: Bremer , 1996; N e p o k r o e f f et al., 1999; rps l6 - in t ron data: A n d e r s s o n & Rova, 1999; Piesschaert et al., 2000a). Me- tabolos undoubtedly also has to be removed from the Psychotrieae and probably is to be included in either the Lasianthus-clade or the Hedyotideae.

As ment ioned earlier, the exine of Pa- gameopsis garryoides can be considered as a transitional stage between a complex and simple reticulum. Other similarities with Metabolos are the bluish flowers, unequal calyx lobes often with colleters in the sinuses, papillate disk, ovules with a distinct obturator, and fruits with a dry (vs. fleshy) mesocarp (Puff & Igersheim, 1994). Mor- phological differences between Metabolos and Pagameopsis include axillary (vs. ter- minal) inflorescences and a tetralocular (vs. bilocular) gynoecium. The taxonomic value of most o f the above-ment ioned characters

2001] PIESSCHAERT ET AL.: R U B I A C E A E - R U B I O I D E A E 501

is restricted, but the similarities indicate that Metabolos should be included in future (e.g., molecular) analyses as a possible relative of Pagameopsis.

OR SHOULD WE BROADEN OUR HORIZON?

Since Bremekamp ' s (1952) first use of the character, the occurrence of raphides has been considered a very important character defining the subfamily Rubioideae. In the Cinchonoideae and Ixoroideae raphides are very rare. Nevertheless, there are some ex- ceptions to this rule: the Hamelieae, Hil- lieae, and Coptopsapelta Korth. do have raphides but are included in the Cinchono- ideae instead of the Rubioideae; Raritebe Wernham and Amphidasya Standl. do not possess raphides but are now considered to be at the base of the Rubioideae (Anders- son, 1996; Andersson & Rova, 1999). Al- though Pagarneopsis would thus not be the first ex-raphidiate genus of the Rubioideae, the absence of raphides still remains a very strong argument against its inclusion in the subfamily. The loose complexes of needle- like crystals that occur in Pagameopsis are also found in Colletoecema E. M. A. Petit, a basal genus of the Rubioideae (Pies- schaert et al., 2000). Similar druselike, ag- gregate crystal complexes as in Pagameop- sis occur in Lasianthus and the Pauridian- theae (unpubl. data).

Supposing that the absence of raphides suppor t s the exc lus ion o f Pagameopsis f rom the Rubioideae, can we then detect possible relatives in the Cinchonoideae or Ixoroideae? Two uncom m on features may be useful for this purpose, namely, the papillate to tr ichomatous disk and the corolla fenestrations combined with the basal filament attachment.

Robbrecht (1988) mentioned the occurrence of a papillate or hairy disk in certain Isertieae, Rondeletieae, Hedyotideae, and Urophylleae. Except for Rondeletia odorata Jacq. (hairy disk illustrated: fig. 35E in Robbrecht, 1988), no species or genera were specified. This makes it difficult to de- duce how common the feature really is in these tribes, especially since the delimitation of Isertieae and Rondelet ieae was problematic at the t ime of Robbrecht 's work

(e.g., Andersson, 1996; Bremer & Thulin, 1998). In the Urophyl leae and closely related Pauridiantheae, hairy or pappilate disks are very c o m m o n (HallE, 1966). In the other groups cited by Robbrecht, the feature seems more restricted. Apart f rom Rondeletia L., it was mentioned by Halle (1966) in Oldenlandia L. and Otomeria Benth. of the Hedyotideae. We could not find any examples in the Isertieae.

Besides in the tribes listed by Robbrecht (1988), a papillate to hairy disk occurs in four monotypic genera: a shortly papillate disk is present in Metabolos and the African Colletoecema E. M. A. Petit (Piesschaert et al., 2000a); a hairy disk is found in Strump- fia Jacq. (Igersheim, 1993) and in the Am- azonian genus Dialypetalanthus Kuhlm. (Piesschaert et al., 1997), which was recently included in the Rubiaceae (Fay et al., 2000). Colletoecema, Strumpfia, and Dialy- petalanthus are morphological ly very distinct and isolated taxa and none of them seems directly related to Pagameopsis. It can be concluded that hairy or papillate disks are uncommon in the Rubiaceae. The feature seems to have developed in several unrelated lineages of the family and is o f little use for identifying the relatives of Pa- gameopsis.

According to Robbrecht (1988), fenestrate corolla tubes are rare in the Rubiaceae, but they occur in Heinsia DC., Mussaenda Burm. ex L., and Pseudomussaenda Wern- ham (all Mussaendeae sensu Bremer & Thulin, 1998) and in Sacosperma G. Taylor, Pentas, and Pentodon H o c h s t . ( H e d y o t i - deae); he also reported it in Coelospermum Blume (Morindeae) and Paederia (Paeder- ieae). The feature is common in the Mor- indeae: Johansson (1994) found it in Coe- lospermum as well as in Morinda L., Gyn- ochthodes Blume , and Pogonolobus E Muell. Robbrecht et al. (1991: fig. 6B) illustrated fenestrate corolla tubes in Mitch- ella L. and Damnacanthus C. E Gaertn. This confirms the suggestion of Andersson & Rova (1999) to include this genus pair in the Morindeae.

In Pagameopsis, the anther filaments separate f rom the corolla tube near its base. Robbrecht (1988) listed this peculiar feature in the tribes Hamelieae, Argostemmateae,


and Chiococceae, in some genera of the Condamineeae, in Joosia Karst. and Alseis Schott (Cinchoneae), in Paederia L. (Pae- derieae), and in Xanthophytum Reinw. ex Blume (Hedyotideae). The anemophi lous Anthospermeae should be added to this list (Puf f & I g e r s h e i m , 1991). A n d e r s s o n (1997) only recorded two Joosia species out of 11 in which the anthers are actually inserted below one-third f rom the base of the corolla tube. Puff and Igersheim (1991) argued that the situation in Paederia is intermediate between that of flowers with basally attached stamens and flowers with tru- ly sessile stamens. The free filament portion is mostly short, but clearly discernible strands of filamentlike tissue fused to the corolla run down to the base of the tube.

The H a m e l i e a e and A r g o s t e m m a t e a e were traditionally included in the Rubioi- deae (Bremekamp, 1966; Bremer, 1987; Robbrecht, 1988), but recently the Hame- lieae have been transferred to the Cinchon- oideae (Bremer & Jansen, 1991; Bremer, 1996; Andersson & Rova, 1999). Argos- temmateae are maintained in the Rubioi- deae (Bremer, 1996). Robbrecht (1988) included the Chiococceae in the Anthirheo- ideae, which has proven to be an artificial subfamily (e.g., Bremer et al., 1995; Bre- mer, 1996). The Chiococceae are now gen- erally accepted as a member of the Cin- chonoideae, al though the circumscription of the tribe remains a point of discussion. Bre- mer (1992) included the subtribe Portlan- diinae of the Condamineeae in the Chio- cocceae s.1. Although not explicitly stated, the genera of the Condamineeae referred to by Robbrecht (1988) as having filaments inserted at the base of the corolla tube most probably belong to this subtribe. Delprete (1996) includes the Portlandiinae in the Ca- tesbaeeae. An elaborate discussion of the delimitation of Catesbaeeae vs. Chiococ- ceae is found in Delprete (1996) and is be- yond the scope of this study. It suffices to know that the basal at tachment of the anther filaments is prevalent in the subfamily Cin- chonoideae and more specifically in the widely circumscribed Chiococceae of Bre- mer (1992), but it also occurs in several representatives of the Rubioideae.

One must conclude that the flower mor-

phological peculiarities of Pagameopsis occur in several unrelated taxa of Cinchono- ideae as welt as Rubioideae. Consequently they are of not much help for determining the taxonomic position of Pagameopsis.

A final character of Pagameopsis that needs some consideration is the solitary erect ovule. This feature is largely restricted to the Rubioideae. In the Chiococceae, sin- gle ovules are also found but they are always pendulous. The taxonomic value of solitary vs. many and erect vs. pendulous ovules has been questioned by several authors (e.g., Bremer, 1996; Piesschaert et al., 2000a), but still erect ovules are atypical for the Cinchonoideae. They might indicate that Pagameopsis represents another ex- ample of an ex-raphidiate genus of the Ru- bioideae.

Conclusion

The only conclusion that can be drawn at present is that Pagameopsis belongs neither to Psychotr ieae nor to Gaertnereae. On the one hand, it shows morphological similarities with several taxa of the Rubioideae, such as Morindeae, Coccocypseleae, Me- tabolos, and Hedyotideae. On the other hand, the absence of raphides makes a position of Pagameopsis in subfam. Rubioi- deae questionable. The peculiar anther attachment and the absence of raphides might point to an alliance with subfam. Cinchon- oideae instead, but we were unable to find plausible allies in this subfamily. It is obvious that molecular data are needed to shed new light on the peculiar combinat ion of characters documented here in Paga- meopsis.

Acknowledgments

We are grateful to Ms. Anja Vandeperre for preparing wood and gynoecium sections and for her help in preparing the figures; to the Royal M u s e u m for Central Africa at Tervuren; to the curators of U and VEN; and to the reviewers Lennart Andersson, Piero G. Delprete, and Charlotte M. Taylor for their many useful comments and im- provements of the manuscript. Frederic Piesschaert is a research assistant o f the Fund for Scientific Research (EW.O.) Flan-

2001 ] P I E S S C H A E R T E T AL.: R U B I A C E A E - R U B I O I D E A E 503

ders. This study was supported by a grant f rom the Research Council of the Catholic University Leuven (K.U.Leuven; OT/97! 23).

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Morphology, anatomy, and taxonomic position of Pagameopsis (Rubiaceae-Rubioideae)

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