Pollen morphology of the tribe Morindeae (Rubiaceae)

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1 Grana ISSN: (Print) (Online) Journal homepage: Pollen morphology of the tribe Morindeae (Rubiaceae) Jan Thomas Johansson To cite this article: Jan Thomas Johansson (1987) Pollen morphology of the tribe Morindeae (Rubiaceae), Grana, 26:2, , DOI: / To link to this article: Published online: 01 Sep Submit your article to this journal Article views: 141 View related articles Citing articles: 8 View citing articles Full Terms & Conditions of access and use can be found at

2 : Pollen morphology of the tribe Morindeae (Rubiaceae) JAN THOhlAS JOHANSSON Johansson, J. T Pollen morphology of the tribe hlorindeae (Rubiaceae). - Gram 26: , Uppsala 25 June ISSN This investigation represents a detailed account of the pollen morphology of 32 species from 10 genera in the tribe hlorindeae (Rubiaceae). Light microscopy, scanning electron microscopy, and, for three species, transmission electron microscopy are used. Seven pollen types are established and described and a key to their identification constructed. The tribe is eurypalynous; with some exceptions the pollen grains are tricolporate, suboblate to spheroidal and medium-sized and have a reticulate or microreticulate sexine. The pollenmorphological variation within the different genera is discussed. Most of the genera are stenopalynous, whereas Moritida, in particular, is markedly eurypalynous. The importance of pollen morphology for the taxonomy in hlorindeae is evident and this and other features are compared, in order to elucidate the problems of generic delimitation. The genera Appiiiiia and Pogonolobiis are re-established on the basis of pollen morphology and several other features. Jan Thonras Jolmnssoti, Palyiological Lnboratoty, Swedish hliiserrni of Natrrral Ilistoty. S Stoclilioliii 50, Sweden. (hfanirscript received 20 February 1986, revised version accepted 27 October 1986.) The Rubiaceae comprise c. 500 genera including c species (Willis 1973). The subdivision of the family has been disputed over the years. Thus Verdcourt (1958) divided the family into 3 subfamilies and 29 tribes, whereas Bremekamp (1966) recognized 8 subfamilies and 41 tribes in the Rubiaceae. The taxonomy is based mainly on characters such as stipules, type of inflorescence, flower shape, aestivation, placentation and number of ovules, type of fruit, testa cells and occurrence or absence of raphides. The tribe hlorindeae was described by hliquel / (1857), Whomcluded the genera Aloritida L., Tribracliya Korth. and Retitiellin Korth. According to Hooker (1873), hlorindeae comprised the genera Aloritida, Retitiellin, Tribracliya, Doriitiacatithirs Gaertn. fil., Pristnatomeris Thw., Coelosperriiirtii Blume, Gytioclithodes Blume, Tetralopha Hooker El., Apptitria Hooker fil. and Iitiatititra Hooker fil. Schumann (1891) included the genera Tetralophn, Coelosperriiirtn. Dat?itiacanthirs, Gytioclithodes, Prisnintorneris, Appirtiia and Aloritidn and this classification has been principally accepted by subsequent taxonomists. However, Merrill (1923) reduced Tetralopha to a synonym of Gytiochthodes, and Steyermark (1972) included Appirriin in Aforitida. The problems of generic delimitation in this tribe has not been solved by these authors and Bremekamp (1966) stated that the genera which were united in this tribe, are on the whole still imperfectly known. Even the delimitation of Morindeae itself in relation to other tribes, such as Coussareeae and Psathureae, should be subjected to a more critical investigation. During recent years studies of pollen morphology have been undertaken in order to elucidate the taxonomy of different groups of Rubiaceae. Important papers include those written by Chinnappa & Adam (1974), Chinnappa & Warner (1981, 1982), Danvin (1980), Keraudren-Aymonin et al. (1969), Lewis (1963, Lobreau-Callen & Leroy (1980), hlalplanche (1971), hlathew & Philip (1983), hlcdus & Sanokho (1974), hlelhem et al. (1974), hlitra (1969), Robbrecht (1982, 1984) and Verdcourt (1958). These and other investigations have revealed the importance of pollen morphology in the generic delimitation and infrageneric taxonomy of this ramily. No detailed account of the different pollen types

3 Pollen of hforiridene, Riibioceae 135 in the Morindeae has been published previously. pollen of some species have been illustrated in a few papers and regional pollen floras (see Danvin 1979, Huang 1972, Wang 1960), although most of the descriptions are very brief and based on light microscopy. The purpose of the present study is to give a general survey of pollen types of the genera which are usually included in the Morindeae. However, Sarcopygnie Setchell & Christoph. and Lasintithiis Jack have not been treated here. hlaterial of Sarcopygttie, a genus of uncertain taxonomic position confined to Samoa, was not available. The genus is discussed by Setchell & Christophersen (1935) and by Danvin (1979), the latter also publishing scanning electron micrographs of pollen grains. The Iarge genus Lasiarithiis was included by Verdcourt (1976) in Morindeae, but most authors have not supported his opinion. In the present study the following 10 genera are recognized and investigated: Appirttia Hooker fil. (incl. Bellyttkxia Miiller Arg.), Coelosperrmrtt Blume (incl. Olosrylu DC.), Damriacotithiis Gaertn. fil. (incl. Tetraplusia Rehder), Didyttioeciutti Bremek., Gytiodfhodes Blume (incl. Tetralopha Hooker fil.), Moririda L. (ittcl. Cuttertbergia & Mor., Itnariritia Hooker fil., Pogotiantliiis Montr. and Sphaerophora Blume), hlofleyia J. T. Johansson, Pogonolobirs F. v. Muell., Pristtiatotiieris Thw. (incl. Zertxartthe Ridl.) and Rettttclliu Korth. (incl. Tribrachyu Korth.). MATERIAL AND METHODS The investigation is based on specimens obtained from the following herbaria (abbreviations according to Holmgren, Keuken & Schofield 1981): BO, BRI, DNA, L, hllch, NSW. NY, P, S, SING, UC and Z. 45 specimens from 32 species in 10 genera have been investigated. Measurements of polar and equatorial diameters have been made on unacetolysed pollen grains from anthers softened in boiling water for 1-2 minutes. The pollen grains have been measured under the light microscope at a magnification of X400 using a Leitz Wetzlar Dialux 22 microscope equipped with an ocular micrometer. About 20 pollen grains per specimen have been measured. Apocolpium diameter, dimensions of colpi and ora, and thickness of exine have been measured on acetolysed pollen grains under oil immersion at a magnification of x Acetolysis follows Erdtman s standard method (Erdtman 1960). The measurements of apocolpium diameter are approximate, due to the curvature of the poles of the pollen grains. Exine thickness has been measured at the centre of mesocolpia. Diameter of lumina, width of muri, number of lumina per 100 pm2 as well as number of luminal processes have been measured on scanning electron micrographs. Acetolysed pollen grains for scanning electron microscopy have been suspended in 99.5 % ethanol, air dried on brass stubs and coated with gold palladium using a Jeol Fine Coat Ion Sputter JFC The pollen grains have been photographed with a Jeol JShl-25s-11 microscope using Ilford FP4 film. Unacetolysed pollen grains for transmission electron microscopy have been treated in a Na-cacodylate buffer at ph 7.4, post-fixed in 0.2% OsO,, dehydrated in an acetone series, embedded in Epon araldite and heat treated at 70 C. Ultra-thin sections of pollen \rails have been cut, using an LKB Ultrotome, and post-stained with uranyl acetate and lead citrate. The transmission electron micrographs have been taken with a Zeiss 10 a microscope. Terminology is basically according the Erdtman (1966, 1969) and Erdtman et al. (1961). The terminology of Fagri & Iversen (1975) is used shape to describe the shape of the amb. The terms reticulate, microreticulate and semitectate are used in the sense of Praglowski & Punt (1973). All LM-pictures are taken at a magnification of x DESCRIPTION OF POLLEN TYPES Getieral featiires.-pollen grains 3- to 6-colporate, radially symmetrical, isopolar, semitectate. Colpi long, straight or sometimes curved, with tapering ends. Sexine reticulate or microreticulate, usually slightly thicker at the equator than at the poles. Key to polleti types Pollen grains with elevated apocolpia, adjacent mesocolpia depressed; luminal processes with spinules Type 1 Pollen grains without elevated apocolpia, adjacent mesocolpia not depressed; luminal processes without.spinules or absent 2 Lumina 3-30 per 100 iim2 3 Apertures narrow (less than 3 pm wide) 4 Pollen grains usually small; lumina 7-9 per 100 pm2 Type 2 4 Pollen grains medium-sized; lumina usually more than 12 per 100 pm2 Type 3 3 Apertures wide (more than 3 Iim wide) 5 Largest lumina at least 10 pm in diameter; lumina 3-7 per 100 pm2; luminal processes usually abundant Type 4

4 136 J. T. Jolinrissor~ Fig. 1. A-C. Mofleyiu borneensis (Hose 87, UC). (A) Pollen grain in polar view. (B) The same, optical crosssection. (C) Pollen grain in equatorial view, showing narrow apertures (nrrows), and reticulate sexine with large lumina and numerous luminal processes. SEhl ~2600. D, E. Apprinin niirntifincn (Ule 7709, L). (D) Pollen grain in polar view, showing raised apocolpium and reticulate sexine. SEhl x (E) Part of sexine, showing muri with smooth upper surface and luminal processes having numerous apical, pointed spinules (nrrow). SEhl x Largest lumina less than 5 pm in diameter; lumina c per 100 pmz; luminal processes absent Type 5 2 Lumina more than 50 per 100 I'm2 6 Pollen grains usually suboblate to spheroidal; apertures always straight; exine usually reticulate Type 6 6 Pollen grains spheroidal to prolate; apertures very often curved; sexine microreticulate Type 7 Type I (Fig. ld, E) Pollen grains 3-colporate, oblate to suboblate. P=46-53 prn; E=59-69 pm. Amb semi-angular. Apocolpium diam. c pm. Apocolpia elevated and the adjacent mesocolpial areas depressed. Colpi 33 pm wide in the middle, straight. Ora lolongate, 4-5x33 pm. Sexine 2-3 pm thick, reticulate; nexine pm thich. Lumina less than I to 8 pm in diam.. largest at apocolpia and gradually diminishing towards equator, irregular in shape, 3 to c. 20 per 100 pm2. hluri rim wide, straight to sinuate, smooth on top and with spinules

5 Polleti of Aloritidme, Riibincene 137 on the sides. Luminal processes of varying length, with pointed spinules, few to abundant. Taxon included: Appirtiin Hooker fil. Type 2 (Fig. 1 A-C) Pollen grains 3-colporate, spheroidal. P=20-28 pm: E=20-28 pn. Amb circular. Apocolpium diam pm. Colpi 1-2 prn wide in the middle, straight. Ora lolongate, 2x1 pm. Sexine 2-3 pm thick, reticulate; nexine Iim thick. Lumina 1-7 Iim in diam., irregular in shape, 7-9 per 100 pm2. hluri [im wide, straight to sinuate, smooth. Luminal processes of varying length, smooth. few to abundant. Taxon included: Motleyin bortzeetzsis J. T. Johansson. Type 3 (Figs. 2, 3) Pollen grains 3- to 5-colporate, spheroidal. P=2i?-49 ~im; E=2849 rim. Amb circular to sometimes nearly hexagonal or semi-angular. Apocolpium diam. c pm. Colpi 1-3 Iim wide in the middle, straight. Ora lolongate, 3-7 x 1-3 pm. Sexine pm thick, reticulate; nexine 1-2 Iim thick. Lumina less than 1 to 6 pm in diam.. irregular in shape, 8-25 per 100 pm2. hlun pm wide, straight to sinuate, smooth on the uppermost part, wrinkled on the lower parts. Luminal processes of varying length, smooth, or with minute granules, few to abundant or absent. TEM (Retitiellin sp., Prirseglove P4311, Fig. 21). - Exine consisting of a comparatively thick ectexine (tectum, bacula, luminal processes, foot layer), and a thin endexine. Tectum as thick as or thicker than foot layer; tectal part of muri rounded in crosssection. Bacula long, narrower or thicker than or as thick as tecturn, usually tapering towards the base. Luminal processes of approximately the same width as bacula and usually narrower at the base and top. Foot layer continuous, often thin. Endexine thin, continuous, lamellated. Intine as thick as or thicker than foot layer at centre of mesocolpia, continuous. Taxa included: Didytnoeciirtti Bremek. (Fig. 3 A-C, G, H), Gynochthodes philippitierisis (Elmer) hlerr., Prismntonzeris Thw. (Fig. 3 D-F, I) and Retitiellin Korth. (Fig. 2). Type 4 (Fig. 4) Pollen grains 3-colporate, oblate to suboblate or sometimes spheroidal, rarely subprolate. P pm; E=34-40 Iim. Amb circular to semi-angular. Apocolpium diam pm. Colpi 3-5 pm wide in the middle, straight. Ora lolongate or rarely lalongate (hforinda snlottioniemis), x3-6 pm. Sexine 3-5 prn thick, reticulate; nexine 1-2 pm thick. Lumina 1-10 pm in diam., irregular in shape, 3-7 per 100 pm2. Muri pm wide, straight to sinuate, smooth or beset with scattered to abundant minute granules on the sides. Luminal processes of varying length, smooth, few to abundant or occasionally absent. TEA1 (Coelospertiiiitn balntzsacatiutti, Fig. 4 E). - Exine consisting of a comparatively thick ectexine (tectum, bacula, luminal processes, foot layer), and a thin endexine. Tectum as thick as or slightly thicker than foot layer; tectal part of muri more or less rounded in cross-section. Bacula long, narrower, thicker or as thick as tectum, usually tapering towards the base. Luminal processes of approximately the same width as bacula and often wider towards the base. Foot layer continuous. Endexine thin, continuous, lamellated. Intine approximately half as thick as foot layer at centre of rnesocolpia, continuous. Taxa included: Coelospernzzm B1. (Fig. 4 A-E), Alorindn uolirbilis (Blanco) hlerr. (Fig. 4 F), Al. rigidn Miq. and 111. snlar~zoriietzsis Engler (Fig. 4G-I). Type 5 (Fig. 5) Pollen grains 3-colporate, suboblate to spheroidal. P=2740 pm; E=3244 pm. Amb circular to semi-angular. Apocolpium diam. c iim. Colpi (2-)3-4 Iim wide in the middle, straight. Ora lolongate, 4-7x pm. Sexine 2.54 pm thick, reticulate; nexine pm thick. Lumina less than 0.5 lim to at least 4 pm in diam., irregular in shape, c per 100 pm2. hluri pm wide, straight to slightly sinuate, with minute granules on Fig. 2. A-D. Rentiellia elongnra (Yates 2642, hllch). (A) Pollen grain in polar view. (B) The same, optical crosssection. (C) Pollen grain in polar view, showing three narrow colpi, apocolpium and reticulate sexine. SEhl X1400. (D) Part of an aperture and adjacent parts of sexine, showing a narrow colpus, lolongate os, muri with smooth upper surface and lumina with numerous processes. SEhl X7500. E-I. Retitiellin sp. (Purseglove P. 4311, L). (E) Pollen grain in polar view. (F) The same, optical cross-section. (G) Pollen grain in polar view, showing three colpi, apocolpium and reticulate sexine. SEhl x ( I) Part of sexine, showing a lumen with numerous short to elongated processes and m um clearly differentiated into an upper homogeneous structure and a lower wrinkled part. SEhl X9600. (I) Section of exine: ectexine with tectum, bacula and thin foot layer; endexine thin lamellated (arrow); intine light-stained; interbacular areas partially filled with a dark-coloured, possibly lipidic material. TEhl X

6 Fig. 2.

7 Pollen of hforitideae, Riibiaceae 139 A D Fig. 3. AX, G, H. Didymoeciiini anzoetiiini (de Voogd 1178, BO). (A) Pollen grain in polar view. (B) The same, optical cross-section. (C) Pollen grain in equatorial view, showing aperture, mesocolpia and reticulate sexine. SEhI X (G) Part of aperture, showing a colpus with tapering ends and a lolongate 0s. SEM X5800. ( 1) Part of sexine, showing muri with smooth upper surface and a lower wrinkled part (cf. Fig. 2H), and lurnina with numerous luminal processes. SEM X D, E Prisnza- tonzeris tetrandrn (Sorensen et al. 3918, L). (D) Pollen grain in polar view. (E) The same, optical cross-section. F, I. Prisnzotonieris brachyps (Wenzel 669, NSW). (F) Pollen grain in equatorial view, showing narrow apertures, mesocolpia and reticulate sexine. SEM X (I) Part of sexine showing a colpus with a lolongate os, and adjacent structure; muri with smooth upper surface, and lumina with processes. SEhi ~3800.

8 140 J. T. Johntissnti top and particularly on the sides. Luminal processes absent. Taxon included: hloriridn reticiilata Benth. Type 6 (Figs. 6, 7) Pollen grains 3- or 4-colporate. suboblate to spheroidal, rarely oblate or prolate. P=25-63 pm; E=27-58 rim. Amb circular to semi-angular. Apocolpium diam. 640 pm. Colpi 2-6 rim wide in the middle, straight. Ora lolongate, 3-7 (-1O)x2-5 pm. Sexine Iim thick, reticulate or sometimes microreliculate; nexine prn thick. Lumina less than 0.1 Iirn to 3 pm in diam., rarely slightly larger, irregular to almost isodiametric in shape, c per 100 pmz. hluri prn wide, straight to more or less sinuate, smooth or usually beset with minute granules on top and on the sides. Luminal processes absent or occasionally few. TEhl (Gytiochfhodes sp., de Vogel3778, Fig. 6 E). - Exine consisting of a comparatively thick ectexine (tectum, bacula, foot layer), and a thin endexine. Tectum as thick as or thicker than foot layer; tectal part of muri rounded in cross-section. Bacula long, narrower than or as thick as tecturn, usually tapering towards base. Luminal processes absent. Foot layer continuous. Endexine thin, continuous, larnellated. Intine approximately as thick as foot layer at centre of rnesocolpia, continuous. Taxa included: Gynochrliodes B1. (excl. G. philippinetisis (Elmer) hlerr.) (Fig. 6A-E), hforitzdn nsferoscepa K. Schum., hl. cifrifolin L., hl. jnsriiitioides A. Cunn. (Fig. 7E-I), hl. lorigflora G. Don, hl. ririibellafa L. (Fig. 7A-D) and Pogoriolohiis F. v. hluell. (Fig. 6F-J). Type 7 (Fig. 8) Pollen grains 3- to 6-colporate, spheroidal to prolate. P=25-53 Iim; E=20-46 pm. Amb circular. Apocolpium dim. c pm. Colpi 1.54 pm wide in the middle, straight or irregularly curved, sometimes partially fused near the ends. Ora lolongate, 2 4x pm. Sexine pm thick, microreticulate; nexine pm thick. Lumina Iim in diam., irregular to isodiametric in shape, c. 80 to more than 100 per 100 pm2. hluri iim wide, straight or slightly sinuate, smooth or usually beset with minute granules on top and on the sides. Luminal processes absent. Taxon included: Dnnirincorifhiis Gaertn. fil. DISCUSSION Polletirriorphological variatioti Morindeae as commonly defined is an eurypalynous tribe. The general shape as well as the ornamentation of the sexine vary considerably. The pollen grains are usually 3-colporate, but occasionally 4-, 5- and 6-colporate grains have been found. They are all isopolar and radially symmetrical. hlost taxa have suboblate to spheroidal pollen grains. However, in Dnninncnnflrrrs most grains are subprolate or prolate, and in Aloritidn citrifolin prolate pollen grains have been observed. Appiiriin has oblate to suboblate grains. hiost of the investigated species have mediumsized (Erdtman 1966) pollen grains. The smallest grains occur in hfofleyia bortzeetisis, which has spheroidal pollen grains with a diameter ranging between 20 and 28 pm. Appiiriin, Coelospcrtriiini, Dnriitincntifhiis and Aforitidn have the largest pollen grains. The outline of the arnb varies from usually circular, as in Dattitincnrifliiis, hfofleyia, Pristiiaforiieris and Retinellin, to semi-angular, as in Appiiriin, Coelospertiiiim and species of hloritidn. The genera Gyiochfhodes and Pogotiolobiis are usually intermediate in this respect. The width of the colpi appears to be of some taxonomic significance. Didymoeciririi, Mofleyia, Prisriinfottieris and Reritiellin usually have 1-2 Itm wide colpi, while a width exceeding 3 p n predominates in most other taxa. The colpi of Dariirincarifkrts are often irregularly curved and sometimes nearly spiral-shaped (Fig. 8 D). The colpi may occasionally fuse at one or both ends. The 0s is practically always lolongate, although lalongate ora have been observed in hloritidn snlotriotiictisis. The sexine is reticulate in most species; rnicrore- Fig. 4. A-D. Coelosperniitrti sp. (Johansson 117, S). (A) Pollen grain in polar view. (B) The same, optical crosssection. (C) Pollen grain in polar view, showing apertures, small apocolpiurn and reticulate sexine. SEhl Xl300. (D) Part of sexine, showing muri with smooth upper surface and lumina with numerous luminal processes. SEhl x E. Coelosperniirm balnnsaeauion (Johansson 121, S). Section through exine: ectexine with tectum, long narrow bacula and foot layer; endexine thin lamellated (arrow); intine light-stained. TEM x9500. F. Morinda wlirbilis (Elmer 17789, S). Pollen grain in equatorial view, showing two colpi, rnesocolpiurn and reticulate sexine with large lumina containing numerous processes. SEhl x G I. M. salomoniensis (Gafui & coll. BSlP 8715, L). (G) Pollen gnin in polar view. (H) The same, optical cross-section. (I) Pollen grain in polar view, showing small apocolpium, reticulate sexine, muri with smooth upper surface, and large lumina lacking luminal processes. SEhl x Crana 26

9 Fig. 4. Polleti of hioritidcar, Riibiriceae 141

10 142 J. T. Johanssori Fig. 5. A-D. Morinda reficiilafa (Coveny 7106, NSW). (A) Pollen grain in polar view. (B) The same, optical cross-section. (C) Pollen grain in polar view, showing apertures, apocolpium and reticulate sexine. SEM x I 700. (D) Part of sexine, showing muri with granulate inner sides, bacula and lurnina. SEM ~8700. Fig. 6. A, B. Gjnochrhodes coriacea (Hochreutiner 2526, L). (A) Pollen grain in polar view. (B) The same, optical cross-section. C. G. oualifolia (A. C. Smith 9115, L). Pollen grain in polar view, showing three wide apertures, apocolpium and reticulate sexine. SEM ~1200. D, E. Gjnochfhodes sp. (de Vogel 3778, L). (D) Part of sexine, showing muri with granulate inner sides and lumina lacking processes. SEM X8600. (E) Section through exine: ectexine with tectum, long bacula and thin foot layer; endexine thin lamellated (arrow); intine light-stained. TEM x F-J. Pogonolobrts rericrtlafus (F-I: Scarth- Johnson 584 A, BRI; J: Specht & Salt W 333, BRI). (F) Pollen grain in polar view. (G) The same, optical crosssection. (H) Pollen grain in polar view, showing wide colpi, apocolpium and reticulate sexine. SEM X2000. (1) Pollen grain in equatorial view, showing two apertures. SEM ~2000. (5) Part of sexine. showing granulate muri and lumina with few or no processes. SEhI ~8600.

11 Polleti of Moritideae, Ritbiaceac 143 Fig. 6. Gram 26

12 144 J. T. Joharrssori I Fig. 7. A-D. Morindu irrnbellafu (T. & P L). (A) Pollen grain in polar view. (B) The same, optical crosssection. (C) Pollen grain in polar view, showing wide colpi, a small apocolpium and reticulate sexine. SEhI X (D) Pollen grain in equatorial view, showing a wide colpus with lolongate 0s. SEhl X E-I. Morinda jusminoides (E-G: IIubbard 4698, L; H. I: Roorman s.n.. L). (E) Pollen grain in polar view. (F) The same, optical cross-section. (G) Pollen grain in oblique polar view, showing two apertures, mesocolpium and reticulate sexine. SEM X1400. (H) Part of an aperture and adjacent sexine, showing a wide colpus and a lolongate 0s. SEhl X3200. (I) Part of sexine, showing granulate muri, bacula and small lumina. SEhl X7000. Fig. 8. A-F. Darnnocnnfhrts indicirs (Rokkakubashi & Kanagaux s.n., S). (A) Pollen grain in oblique polar view. (B) The same, optical cross-section. (C) Pollen grain in oblique polar view, showing five apertures, apocolpium and microreticulate sexine. SEhl ~1700. (D) Pollen grain in oblique equatorial view, showing cuned, partially fused colpi. SEhl x (E) Pollen grain in equatorial view, showing two apertures. SEhi x (F) Part of an aperture and adjacent sexine, showing B narrow colpus, a lolongate 0s and granulate muri. SEhl ~5500. Grona 26

13 Pollen of hloriiidene, Rubincene 145 A B Fig

14 ~~ ~ 146 J. T. Johnnsson Table I. Pollerir?iorpliologicnl clinrricrerisrics of llie getiera itt Moriridcnc The pollen type is given for each genus. Six main characteristics of pollen grains arc cornpared: (I) Size of pollen grains showing range for polar axis (P) and equatorial diarn. (E). (2) Shape in equatorial view. (3) Shape in polar view (amb.) (4) Width of colpi. (5) Number of lumina per 100 pm2. (6) Occurrence of lurninal processes. The general \miability of the characteristics is given for each genus. Abbreviations: 0, oblate; so, suboblate; sph, spheroidal; p, prolate; c, circular; sa, semiangular; pr, present; abs, absent; eury, eurypalynous: steno, stenopalynous Appunia Coelospermurn Damnacanthus Didyrnoeciurn Gynochthodes hlorinda hlotlcyia Pogonolobus Prismatomeris Rennellia Size Pollen P Shape in E equatorial Colpus No. of lumina Luminal Variatype ilrn I m view Amb width per 100 I m2 Processes bility I , 5, I & Sa c-sa C c-sa c-sa c-sa C c-sa C c-sa Wide Wide Narrow to wide Narrow Wide Wide Narrow Wide Narrow Narrow c. 80 to more than 100 c C c c c. IS Pr Pr abs Pr abs (pr) abs or pr Pr abs or pr Pr Pr? Steno Steno Steno Fairly eury Eury Steno Steno Steno Fairly steno ticulate sexine occurs in Dartiriocotirlirrs and sometimes in species of hloriridn. The sexine is always much thicker than the nexine. The size and number of lumina vary widely. Large lumina, up to at least 10 cim in diameter, 3-7 per 100 I d, occur frequently in Coelosperriiirrii and hforiridn volirbilis. In Dnriitincattfliirs the lumina are less than 1 Iim in diameter and often more than 100 per 100 Itrn2. Hoivever, most taxa have intermediate size and number of lumina. The muri are usually less than 1 Iim wide (often not more than 0.3 Itm wide). In many species, particularly of Dntiiriocntitlirrs, Gyriochhodcs and Moririrfn, the muri are provided with numerous minute granules on top and on the sides. The occurrence and number of luminal processes vary widely and appear to be of some taxonomic importance. There are numerous luminal processes in, e.g., Appritiin, Coclospertrirrrii, hlolleyia. Prisrtinrortieris and Retiriellia, while they are usually absent in the other genera. In Apprrriio, the luminal processes have numcrous pointed spinules resembling those on the pollen grains of e.g. Nerfern gratinderrsis (Robbrecht 1982, figs ). Tnxotioriiy The pollen morphology of the 10 genera investigated is discussed below and compared with other morphological features, in order to elucidate problems of generic delimitation. A number of pollen- morphological characteristics of the different genera are summarized in Table I. Apprrriia (Type l).-very limited material of this genus was available for the present study and the measurements are provisional. However, the investigated specimens have a uniform and characteristic type of pollen grains, which is not found in any other genus of the tribe. Distinguishing features are e.g. the elevated apocolpia and the spinules on the luminal processes and muri. Apprmin was included in llloriridn by Steyermark (l972), but appears to be distinguished by several characters. The sessile flowers are subtended by denticulate bracts and are collected in groups usually on axillary peduncles. The ovaries are not connate and the corolla, although puberulous outside, is glabrous inside. The corolla lobes are narrow and each is provided with an adaxial ridge. The anthers are included in the corolla tube and the stigma is usually club-shaped and only slightly divided at the apex, although A. tripliylln Ducke is provided with a 2-branched style, according to Steyermark (1972). There are ttvo ovules in each locule, separated by a secondary septum, and the fruit is a drupe. The pollenmorphological evidence supports the opinion that Apputiin should be kept as a distinct genus. The taxonomic relationships of Apprrtiin are still obscure and the genus is possibly not closely related to Aloririda.

15 Pollen of hloriiideiie, Rirbinceae 141 Coelosperriziini (Type 4).- 1he 3-colporate, usually oblate to suboblate pollen grains in this genus are medium-sized to sometimes (as in C. bolntzsnentiiiriz, C. niotiticoliiiiz and Coelospertiiiriii sp.) large. The colpi are fairly wide and the ora lolongate. The reticulate sexine has usually few, large lumina, which are up to 10 pm or more in diameter. The lurninal processes are usually abundant. Coelospertmtii has terete branches and the leaves of nearly all species are provided with domatia on the abaxial side. The corolla is white and has lobes flattened above and beset with long white hairs in the upper part of the tube. The exserted anthers are long and curved and the ovaries have two ovules in each locule. Coelospertiziitiz appears to be very closely related to hforitzdn. hf. voliibilis occupies an intermediate position with respect to inflorescence and the connate ovaries, although the pollen morphology fully agrees with that in Coelosperiniitiz. Dnriiiincaizfliiis (Type?).-The pollen grains are easily distinguished from those of the other genera by the microreticulate sexine. They are usually subprolate or prolate and the number of the usually narrow apertures varies from 3 to 6. The colpi are often irregularly curved, a feature which has not been observed in any other genus. hlinute granules are abundant on the muri and in this respect Dniiztincatifhiis agrees with most species of Gytzoclzdiodes and hforiizda. Dniiiizncarzrhris is further characterized by t\vo longitudinal ribs on the young branches and by narrow stipules, which develop into spines in D. iizdiciis Gaertn. fil. The axillary cymes are small and few-flowered. The corolla is provided with long hairs in the upper part of the tube and on the adaxial side of the lobes near the orifice. The stigma is composed of four lobes. Two ovules, separated by a secondary septum, are present in each locule and the fruit is a red drupe. The genus appears to be well-circumscribed and the generic affinities are obscure. The morphology of corolla and pollen grains resembles that in species of hforiiida. Longitudinal ribs occur also on the young branches in hfoflqia and Pristrznfoiiieris. Lo (1979) recombined Prisiizntoiiieris heizryi (LCveillC) Rehder (P. breuipes Hutch.) and P. labordci (LCveille) hlerr. ex Rehder (P. Iitiearis Hutch.) into Datmacntifhus and this opinion is supported by pollenmorphological evidence. Didytizoeciiiitz (Type 3).-The pollen grains in this monotypic genus are very similar to those in Prisiiznfotiieris and Retinellin. The tricolporate grains are spheroidal and medium-sized and have narrow colpi. The reticulate sexine has fairly large lumina (up to 5 pm or more in diameter), c per 100 Iim. The luminal processes are few to numerous. Didytlioecizrriz has many characters in common with Retitrellia. The inflorescence and flo\vers show the greatest similarities. Some of the pedicels are partially or completely connate in pairs. The corolla is glabrous inside and the lobes have a distal adaxial ridge. The anthers are included in the corolla tube and the bilobate stigma is more or less erect. There is only one ovule in each of the two locules. Fruits are lacking in the two known specimens of Didyttzoeciiitiz ntizoetziiiiz. The young branches are terete and the leaves lack domatia. Didytizoeciiiiiz is similar to some species of Retztzellia and these taxa may be congeneric. Gyzochfhodes (Types 3 and 6).--With a few exceptions the pollen grains of this genus are fairly uniform. The 3- or 4-colporate and usually suboblate to spheroidal grains are medium-sized and have fairly wide colpi. The sexine is reticulate with lumina of varying size and number. The lumina are usually not more than 3 Iim in diameter and occur in a number of 50 to 80 per 100 pm. Ho\vever, in at least one specimen from the Philippines (Ramos BS 22684, G. plzilippitreizsis. det. van Steenis) some of the lurnina are more than 5 Iim in diameter and occur in a number of per 100 pm. The pollen grains in this species are included in the Type 3. In Gytzoclirhodes the muri are usually provided with numerous granules. Luminal processes occur only exceptionally. Gytiochfhodes is also distinguished by stipules and bracts, which are provided with hairs along the margin, axillary short or elongate cymes with white flowers in whorls, recurved calyx tube and corolla with long hairs inside the tube and on adaxial side of the lobes. In several respects the genus is similar to e:g. Coelospertmiiz and hforiiida. Thus the leaves are provided with domatia, the corolla lobes are flattened above and each locule has t\vo ovules separated by a secondary septum. Moritzda (Types 4, 5, and 6).-This is the most eurypalynous genus of those discussed here. The 3- or 4-colporate pollen grains vary from suboblate or spheroidal in most species to sometimes oblate or Grona 26

16 148 J. T. Johnttssoii prolate (as in bf. citr$olin). In most of the investigated species of Moriiida the pollen grains are similar to those in Gyttochthodcs. The colpi are comparatively wide and often long. The lumina vary widely in size and number: from less than 3 Iim in diameter and up to c. 5@90 per 100 pm2 in most of the examined species to at least 10 Iim in diameter and only 3-5 per 100 pmz in hf. volrrbilis. The muri may be smooth or provided with few to numerous granules and vary in width between 0.3 Iim and at least 1.1 iim. Luminal processes are absent in most species, but they are abundant in M. uoliibilis and occur occasionaliy in some of the other species. Moriiida uoliibilis and hi. snloitiotiiemis are intermediate between Coelosperttiiiin and Moriiida with respect to type of inflorescences. The ovaries are connate in groups and develop into syncarps and the terminal inflorescence are corymb-shaped rather than umbel-shaped as in 111. wttbellnta. The flowers as well as the pollen grains are very similar to those in Coelosperitiritti and the generic affinities of hi. snlonto&visis and Af. volitbilis may be questioned. hi. rigidn has also pollen morphology similar to that in Coelosperttitiiti, but in other respects the species resembles fairly well most species of hforitida. hforitidn refictilntn Benth., which has fairly large lumina and muri beset with numerous granules, is included in the Type 5. This specics was described as Coclosperttiriiii clecipietis by Baillon (1879). However, the species differs from Coelospernirittt in many important characters including shape of stipules and bracts, type of inflorescence and morphology of flowers and pollen grains. It is here provisionally included in Moriitdn. There is no common feature uniting all species of hforittdn, although connate ovaries have been regarded as a taxonomically important character of this genus. Its generic delimitation is provisional and several species should probably bc excluded. hfotlqia (Type 2).-This monotypic genus has been described recently (Johansson 1987, in press). Only two flowering collections are known, but the pollen grains are very uniform. The spheroidal grains, which have narrow colpi and reticulate sexine with lumina up to 7 ttm or more in diameter and with abundant luminal processes, are fairly similar to those in Didyttioeciirtti. Pristtintottieris and Retttiellin. However, the pollen grains are smaller and have a characteristic morphology. dfoflqin appears to be closely related to Prisittntoiiieris, which it resembles by the two longitudinal ribs and the peeling epidermis on the young branches, and by the shape of stipules, inflorescence and flowers. However, there are several distinguishing features. Apart from pollen morphology, there are differences in the flowers, stipules and leaves. Pogotiolobtis (Type 6).-The pollen grains of this monotypic genus are similar to those in most species of Gytiochthodes and Morindn. The pollen grains are 3- or 4-colporate, suboblate or spheroidal or sometimes subprolate and medium-sized (P=25-35 pm; E=27-35 pm). The colpi are comparatively wide and the sexine is reticulate with lumina usually less than 2 pn in diameter and occurring in a number of c. 70 to more than 90 per 100 pmz. The muri are usually Iirn wide and smooth or with scattered granules at least on the sides. The luminal processes are few or absent. Pogoriolobiis reticiilntiis was previously included in Coelosperttirittt as C. retictilatiitii (F. v. hluell.) Bentham (1867). However, it forms a distinct monotypic genus, characterized by, e.g., glabrous umbel-shaped cymes, stipules and bracts with characteristic shape and corolla provided with long hairs inside the tube and on the adaxial side of the lobes. Pogoriolobiis differs from Coelosperttiutti in many respects and in floral as well as pollen morphology it resembles some species of Gytzochtkodes. Pristiiatottteris (Type 3).-This is a stenopalynous genus. The pollen grains are 3- to 5-colporate and similar to those in Didyttioecititti and Reiitiellia. The lumina are usually fairly large, have a diameter up to 5 prn or more and occur in a number of per 100 pmz. The luminal processes are few to numerous. Prisiiiatottieris is similar to Didyinoeciiiiti and Retitiellin also in other features. The corolla is glabrous inside and the lobes have a distal adaxial ridge. The anthers are included in the corolla tube and the stigma is erect. Each of the two locules has one ovule and the fruit is a drupe or sometimes a syncarp composed of two or several connate ovaries. The leaves lack domatia. Unlike Didyi)ioecirrtn and Retinellia the young branches in Prisitintottieris are provided with two longitudinal ribs and the

17 Polleti of hforitidene. Rribinccae 149 epidermis of the branches is peeling in flakes. This feature is shared with Moflqia. The genus Zeu.ratifhe, described by Ridley (1939), should be included in Prisniafottieris. The two genera are very similar in all important features and the pollen morphology of Zeii.rcitithe is identical with that of Prisninforneris. Connate ovaries, which have been used to distinguish Zeii.rntif/ir, are also met with in several species of Prisrrinfottieris. Retinellin (Type 3).-The pollen grains of this genus are similar to those in Didyrnoeciritii and Prisniafomeris. They are 3-colporate in the investigated specimens and the reticulate sexine has comparatively large lumina. The size and number of the lumina vary between the species. In R. elotignfn (King & Gamble) Ridl. the lumina rarely exceed 4 pm in diameter and occur in a number of c per 100 pm'. In other species the lumina may reach a size of at least 6 prn in diameter and occur in a number of 8-10 per 100 pm2. Luminal processes are usually abundant. The similarities between Didyttioeciiun and Retinelliu were discussed above. The inflorescence in Rentiellia is characteristic. The ovaries are connate, usually three or several together, and form syncarps. These are arranged in spikes, racemes, panicles or umbels of varying size and shape. Retiriellia was included in Moririda by e.g. Schumann (1891). but is distinct from this genus. More studies have to be camed out, before the generic delimitations and taxonomic relationships are clarified. Detailed analyses of the variation in microscopical characters, particularly in Moritidn, are needed. The delimitation of hlorindeae in relation to other tribes, especially Psathureae and Coussareeae, is obscure. Comprehensive investigations of the genera in these groups would probably result in a largely revised classification. ACKNOWLEDGEMENTS I am greatly indebted to the Directors and Curators of the herbaria for providing material for loan. Special thanks are due to Dr S. Nilsson and Dr B. Raj, the Palynological Laboratory, Stockholm, for all their advice and kind guidance during the work and for their critical reading of the manuscript. I also wish to express my sincere thanks to Miss M. Dahlberg, Miss E. Grafstrom. hlr hl. Hellbom and Mr J Pacull, the Palynological Laboratory, for their skilful technical assistance and kind advice. Financial support has been provided by grants from the Royal Academy of Sciences, Stockholm. TAXA INVESTIGATED Appirnin Hooker fit. A. artrunlinca (K. Krause) Sandtvith. BRAZIL. Ule 7709 (L). A. sirrinantensis. (Bremek.) Steyerm. SURI- NAhlE. Kappler 1453 (S). Coelospertnrrni Blume. C. bn/unsoeanirni Baillon. NEW CA1,EIIONIA. Johansson 43 (S); Johansson 121 (S). C. n~onricolrtni Baillon ex Guilt. NEW CALEDONIA. Johansson 59 (S). C. paniculurrrni F. v. hluell. AUSTRALIA. Sharpc 2471 (BRI). C. rritncurirrn (Wall.) King & Gamble. CHINA. Lau 1563 (P). Coelosprrmiinz SP. NEW CALEDONIA. Johansson 107 (S); Johansson I17 (S). Dan~nacanrRiis Gaertn. fit. D. henryi (Leveillk) H. S. Lo. CHINA. Henry 9MOE (NY). D. indicrcs Gaertn. fil. BURhlA. hfalaise 230 (S); JAPAN. Rokkakubashi & Kanagwa s.n. (S). Didjwoeciirtn Bremek. D. amoenirm Bremek. INDONESIA. Sumatra, dt Voogd 1178 (BO). Gyiochrltodes Blume. G. coriacea BI. INDONESIA. Riau Islands, Biinnemeyer 6387 (L); INDONESIA. Java, Hochreutiner 2526 (L). G. omlifoliu (Val.) Kanehira. FIJI. A. C. Smith 9377 (L); A. C. Smith 9415 (L). G. philippitiensis (Elmer) hlerr. PHILIPPINES. Ramos BS (L). Gjnochrhodes sp. INDONESIA. hloluccas, de Vogel 3778 (L). G~nochrhodes sp. AUSTRALIA. Jones 1556 (DNA); A. S. & hl. G. Thorsborne 337 (BRI). hforinda L. hf. asreroscepa K. Schum. TANZANIA. Flock s.n. (S). hf. cirrifolia L. PAPUA, NEW GUINEA. Brass (S); hlarshall ISLANDS. Taylor ). hf. jasminoides A. Cunn. AUSTRALIA. Boorman s.n. (L); Clemens s.n. (S); Hubbard 4698 (L). hf. long~nra G. Don GABON. Comtet s.n. (herb. d'alleizette 3269) (L). Af. rericirlata Benth. AUSTRALIA. Coveny 7106 (NSW); Gittins 1081 (NSW). hf. rigida hliq. INDONESIA. Borneo, Hallier 1048 (L). hf. salonioniensis Engler. SOLOhlON ISLANDS. Gafui &'coll. BSIP 8715 (L). M. mbdlain L. hlalaysia. Peninsular hlalaysia, T. & F. 351 (L). hf. wlrrbilis (Blanco) hlerr. PHILIPPINES. Elmer (S). hiorlqia J. T. Johansson. hf. borrieensis J. T. Johansson. hlalaysia. Saratmk. Hose 87 (UC). Pogonolobirs F. v. hluell. P. reticularus F. v. hluell, AUSTRALIA. ScarthJohnson 584 A (BRI); Specht & Salt W. 333 (BRI). Prisniaromeris Thw. P. beccnriana (Baillon) J. T. Johansson. h.i ALAYSIA. SaraNak, Fuchs (A). P. brachypiis Ridl. PHILIP- PINES. Wenzel 669 (NSW). P. sirbsessilis King & Gamble. MALAYSIA. Peninsular hlalaysia, Kunstler 8071 (Z). P. rerrandra (Roxb.) K. Schum. THAILAND. SOrensen et al (L). Rennellia Korth. R. elongatn (King & Gamble) Ridl. INDONESIA. SUmatra, Yates 2642 (hlich). Rennellia sp. hlalaysia. Peninsular hlalaysia, Comer (SING). Rennellia Sp. MALAYSIA. Peninsular hlalaysia, Purseglove P (L) Rennellio sp. MALAYSIA. Peninsular hlalaysia,

18 150 J. T. Jolirrtissotr Shah & Shukor hls 2307 (L). Retinellin sp. THAILAND. Sorensen et al. 823 (L). REFERENCES Baillon, H. E Sur les genres australiens de la famille des RubiacCes. - Bull. SOC. Linn. Paris 1: Bentham, G Flora australiensis pp. Lovell Reeve RC Co., London. Bremekamp, C. E. B Remarks on the position, the delimitation and the subdivision of the Rubiaceae. - Acta Bot. Neerl. IS: Chinnappa, C. C. R: Adams, K. J Pollen morphology in the genus Cogen. I. Scanning electron microscopy. - J. Coffee Res. 4: Chinnappa, C. C. & Warner, B. G Pollen morpho- logy in the genus Coffin (Rubiaceae) and its taxonomic significance. - Bot. J. Linn. SOC. 83: Chinnappa, C. C. & Warner, B. G Pollen morphology in the genus Cogen (Rubiaceae). 11. Pollen polymorphism. - Grana 21: Danvin, S. P A synopsis of the indigenous genera of Pacific Rubiaceae. - Allertonia 2 (I): 144. Danvin, S. P Notes on Airospentin (Rubiaceae), with a new species from Fiji. - J. Arnold Arbor. 61: Erdtman, G The aeetolysis method. A revised description. - Sven. Bot. Tidskr. 54: Erdtman, G Pollen morphology and plant taxonomy. Angiosperms. An introduction to palynology pp. Hafner Publ. Co., New York and London. Erdtman, G Handbook of palynology. An introduc- tion to the study of pollen grains and spores pp. hlunksgaard, Copenhagen. Erdtman, G., Berglund, B. & Praglowski, J An introduction to a Scandinavian pollen flora. - Gram Palyn. 2: Fzgri, K. & Iversen, J Textbook of pollen analysis, 3rd ed pp. hlunksgaard. Copenhagen. Holmgren. P. K., Keuken, W. & Schofield, E. K Index Herbariorum. I. The Herbaria of the world, 7th ed pp. Bohn, Scheltema & Holkema, Utrecht. Hooker, J. D Rubiaceae. - In: Bentham, G. 8: Hooker, J. D.: Genera plantarum, vol. 11. Pars I, pp Lovell Reeve &r Co.. London. Huang, T.-C Pollen flora of Taiwan pp. National Taiwn Univ., Botany Dept. Press. Keraudren-Aymonin, hl.. Straka. H. 6; Simon, A Palynologia hladagassica et hlascarenica. Family 184. Rubiaceae. - Pollen Spores II: Lewis, W. H Pollen morphology and evolution in Iledjoris subgenus Edrisio (Rubiaceae). - Am. J. Bot. 52: Lo, H A revision of the genus Duninnconhis Gaertn. f. from China. - Acta Phytotax. Sin. 17: Lobreau-Callen, D. & Leroy, J.-F Quelques donnees palynologiques sur le genre Coffeu e! autres genres du cercle des Cafiiers. - ASIC, 9' Colloque, Londres: , hlalplanche, hi Etude palynologique de trois genres de Rubiacees-GardCnikes d'afrique. - Adansonia, ser. 2, 11: hlathew, P. hi. & Philip, Studies in the pollen morphology of South Indian Rubiaceae. - Adv. Pollen Spore Res. 10: hlkdus, J. & Sanokho. A Description palynologique de quelques especes des genres norreria G. F. W. hley (Rubiaceae) et IIjgrophilo R. Hr. (Acanthaceae). - Bull. I.F.A.N. 36, scr. A: hlelhem, T. S., Bianco Rossi, C. L. del R: Silvestre, hl. S. F Pollen morphological studies in Rubiaceae. - Hoehnea 4: hlemll, E. D An enumeration of Philippine flotvering plants pp. Bureau of Printing, hlanila. hliquel, F. A. W Flora van Nederlandsch Indie pp. Amsterdam, Utrecht, Leipzig. hlitra, K Pollen morphology and identification of Gardenieae. - J. Sen. hlem. Vol.: Praglowski, J. & Punt, W An elucidation of the microreticulate structure of the exine. - Grana 13: Ridley, H. N Notes on some hlalayan Rubiaceae. - Kew Bull. 1939: Robbrecht, E Pollen morphology of the tribes Anthospermeae and Paederieae (Rubiaceae) in relation to taxonomy. - Bull. Jard. Bot. Natl. Belg. 52: Robbrecht, E The delimitation and taxonomic position of the tropical African genera Lepfncfitrn and Dicrjondrn (Rubiaceae). - PI. Syst. Evol. 145: Schumann, K. hl Rubiaceae. -In: Die natiirlichen Pflanzenfamilien (eds. A. Engler & K. Prantl) 4. w. Engelmann, Leipzig. Setchell, W. A. & Christophersen, E Preliminary notes on Snrcopygnie, a new rubiaceous genus from Samoa. - Occas. Pap. Bernice Pauahi Bishop hlus. 11~3-5. Steyermark. J. A Rubiaceae. - In: hlaguire, B. el al., The botany of the Guayana Highland 9. - hlem. N.Y. Bot. Card. 23: Verdcourt, B Remarks on the classification of the Rubiaceae. - Bull. Jard. Bot. Eta!, BNX. 28: Verdcourt, B Rubiaceae I. - In: Flora of Tropical East Africa (ed. R. hl. Polhill), 414 pp. Crown Agents for Oversea Governments and Administrations, London. Wang, F Pollen grains of China pp. (in Chinese). Willis, J. C A dictionary of the flowering plants and ferns (revised by H. K. Airy Shaw). - 8th.ed pp. Cambridge University Press, Cambridge.

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