J. Jpn. Bot. 91 Suppl.: 257–292 (2016)
Pollen Morphology and Taxonomy in Malesian Phyllanthus (Phyllanthaceae)
a, b c a Ming-Jou Wu *, Tseng-Chieng Huang , Chia-Chin Liu , Yeng-Juei Chen , a a a a Yung-Sheng Chang , Chia-Lun Hsu , Shin-Yi Wu , Ai-Yi Tseng , a a a Yin-Chen Chang , Cheng-Chuan Liu and Anusara Kaewmuan
aDepartment of Natural Resources and Environmental Studies, National Dong Hwa University, Shoufeng, Hualien 974, TAIWAN; bInstitute of Plant Biology, National Taiwan University, Taipei, 106 TAIWAN; cDepartment of Life Sciences, Tzu Chi University, Hualien, 970 TAIWAN *Corresponding author: [email protected]
(Accepted on January 9, 2016)
Pollen morphology in 89 of 127 Malesian Phyllanthus species (Phyllanthaceae) was investigated. Thirty-four pollen types are recognized. They are grouped into five pollen classes. These pollen classes are I. Colporate pollen, II. Incomplete synaperturate pollen, III. Synaperturate pollen, IV. Clypeate pollen, and V. Porate pollen. A key for the pollen classes and types is provided. Evolutionary trends in pollen morphology and infrageneric classification inPhyllanthus are discussed.
Key words: Euphorbiaceae, Malesia, Phyllanthaceae, Phyllanthus, pollen class, pollen type.
A total number of 110 Phyllanthus species Phyllanthus. Pollen morphology of 89 out of 127 in Malesia was estimated in 2001 (Malesian species was investigated. Previous palynological Euphorbiaceae Newsletter 11). Since studies on Malesian Phyllanthus species were then, several regional taxonomic revisions reported mainly by Punt (1980) and Chen et accompanying pollen studies of Malesian al. (2009). Punt examined 37 New Guinea Phyllanthus have been done by the authors Phyllanthus and reported nine pollen types, and including Peninsula Malaysia (Chang 2012), Chen et al. examined 21 Philippine Phyllanthus Borneo (Hsu 2011), Central Malesia (Wu and recognized eight pollen types. Many authors 2012), the Philippines (Chen 2009, Chen et al. have discussed pollen morphology, phylogeny 2009) and New Guinea (Chang 2010, Tseng and infrageneric classification inPhyllanthus and 2012). Based on these studies, 127 Malesian concordance with the value of palynological data Phyllanthus species are recognized. In this paper, in Phyllanthus taxonomy. Punt (1967) proposed palynological data of these studies and some evolutionary trends of seven pollen characters new data collected from Java (Liu 2015) and to discuss evolutionary trends in Phyllanthus Sumatra (Kaewmuan 2016) are compared and pollen types. Webster (1957) and Webster integrated for grouping pollen types and pollen and Carpenter (2002, 2008) discussed pollen classes to discuss evolutionary trends in pollen morphology and systematics of neotropical and morphology and infragenus classification in paleotropical Phyllanthus, and grouping sections
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Table 1. Voucher specimens of Malesian Phyllanthus pollen class and pollen type. The numbers in circle correspond to those in Map 1 Pollen class Pollen type Taxa Voucher specimens Locality Iα 1. P. amarus ① P. amarus Schumach. & Thonn. Idenburg 17 (L) Sumatra N. F. Stein 10 (SING) Peninsular Malaysia E. Kuswata Kartawinata 1063 (L); C. G. C. Reinwardt s.n. Java (L 0135108) F. H. Endert 2098 (L) Borneo D. R. Pleyte 172 (L) Moluccas M.-J. Wu 2951 (TAI) Palawan L. J. Brass 26029 (L) New Guinea ② P. debilis J. G. Klein ex Willd. W. J. C. Kooper 555 (L) Java J. W. Purseglove 4034 (L) Peninsular Malaysia H. Wiriadinata 1362a (L) Borneo J. Elbert 2903 (L) Sulawesi E. E. Henty NGF49173 (L) New Guinea 2. P. erythrotrichus ③ P. erythrotrichus C. B. Rob. C. B. Robinson BS29333 (L) Luzon, Rizal 3. P. maderaspatensis ④ P. maderaspatensis L. J. Jeswiet s.n. (L 0159955) Java C. W. Kooy 413 (L) Lesser Sunda Islands 4. P. microcarpus ⑤ P. microcarpus Müll. Arg. Hardial 486 (L) Peninsular Malaysia A. Hoogerwerf s.n. (L0135559) Java ⑥ P. novae-hollandiae Müll. Arg. R. Schodde 2425 (L) New Guinea 5. P. acinacifolius ⑦ P. acinacifolius Airy Shaw & G. L. Webster C. D. Sayers NGF19967 (L) New Guinea ⑧ P. flaviflorus (Lauterb. & K. Schum.) Airy Shaw R. D. Hoogland 5422 (L) New Guinea ⑨ P. kostermansii Airy Shaw A. J. G. H. Kostermans & W. Soegeng-Reksodihardjo New Guinea 656 (L) ⑩ P. poli-borealis Airy Shaw Sleumer BW14087 (LAE) New Guinea ⑪ P. stultitiae Airy Shaw L. J. Brass 11534 (L) New Guinea Iβ 6. P. urinaria ⑫ P. benguetensis C. B. Rob. E. D. Merrill 9684 (L) Luzon ⑬ P. chamaepeuce Ridl. R. Kiew RK2408 (SING) Peninsular Malaysia H. Winkler 3156 (L) Borneo ⑭ P. nozeranii Rossignol & Haicour J. Sinclari SF39526 (SING) Peninsular Malaysia K. Abdul A2889 (L) Borneo ⑮ P. urinaria L. subsp. urinaria C. G. G. J. van Steenis 24290 (L) Sumatra J. W. Purseglove P4034A (SING) Peninsular Malaysia J. P. Mousset 117 (L) Java P. Buwalda 5973 (L) Moluccas M.-J. Wu 2954 (TAI) Palawan J. W. Purseglove BSIP9864 (LAE) New Guinea December 2016 Wu et al.: Pollen in Malesian Phyllanthus 259
Table 1. Continued Pollen class Pollen type Taxa Voucher specimens Locality ⑯ P. urinaria L. subsp. nudicarpus Rossignol & Haicour Bakar s.n. (SING 0036094) Peninsular Malaysia J. W. F. Slik 2004-13 (L) Borneo A. Zippelius s.n. (L0136094) Lesser Sunda Islands M.-J. Wu 2952 (TAI) Palawan ⑰ P. submarginalis Airy Shaw E. Schmutz 2975 (L) Lesser Sunda Islands ⑱ P. aff. urinaria 1 E. Schmutz 3057 (L) Lesser Sunda Islands ⑲ P. aff. urinaria 2 L. L. Co 5993 (TAI) Luzon 7. P. roseus ⑳ P. ridleyanus Airy Shaw T. C. Whitmor KEP FRI4273 (L) Peninsular Malaysia ㉑ P. roseus (Craib & Hutch.) Beille C. Davidson 1344 (L) Peninsular Malaysia 8. P. tenellus ㉒ P. tenellus Roxb. V. F. Schiffner 2153 (L) Java 9. P. securinegioides ㉓ P. securinegioides Merr. M. D. Sulit PNH16268 (L) Palawan 10. P. glochidioides ㉔ P. glochidioides Elmer G. E. Edaño PNH40177 (L) Luzon ㉕ P. aff. glochidioides M. Q. Lagrimas PNH39954 (L) Luzon ㉖ P. pectinatus Hook. f. H. N. Ridley 5030 (SING) Peninsular Malaysia 11. P. collinsae ㉗ P. collinsae Craib E. Schmutz 850 (L) Lesser Sunda Islands J. A. J. Verheijen 3467 (L) Lesser Sunda Islands 12. P. triphlebius ㉘ P. triphlebius C. B. Rob. M.-J. Wu 3374, 3375 (TAI) Luzon 13. Pilate ㉙ P. aff. triphlebius M. Ramos BS43203 (L) Bohol Iγ 14. P. hookeri ㉚ P. hookeri Müll. Arg. J. H. Coert 521 (L) Java A. Hoogerwerf 252 (L) New Guinea 15. P. emblica ㉛ P. emblica L. F. W. Junghuhn s.n. (L 0159502) Sumatra S. Kiah SK613 (SING) Peninsular Malaysia F. W. Junghuh s.n. (L 0159536) Java P. W. Korthals s.n. (L 0159572) Borneo E. Demandt s.n. (L0159581) Lesser Sunda Islands 16. P. oxyphyllus ㉜ P. columnaris Müll. Arg. R. E. Holttum 15134 (SING) Peninsular Malaysia ㉝ P. oxyphyllus Miq. E. F. de Vogel 2986 (L) Sumatra J. W. Purseglove 4135 (L) Peninsular Malaysia C. Ploem s.n. (L 0230439) Java P. Hommel 111ZII (L) Java II 17. P. casticum ㉞ P. acidus (L.) Skeels S. M. Popta 613/97 (L) Java J. Elbert 2035 (L) Lesser Sunda Islands F. J. M. Gaerlan et al. PPI10249 (L) Luzon 260 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Table 1. Continued Pollen class Pollen type Taxa Voucher specimens Locality ㉟ P. ciccoides Müll. Arg. F. J. M. Gaerlan et al. PPI10249 (L) New Guinea ㊱ P. reticulatus Poir. T. S. Suppiah KEP FRI11438 (L) Peninsular Malaysia Koorders, S.H. 20576 (L) Java W. Giesen 19A (L) Borneo J. G. Hallier 1301 (L) Borneo H. Hallier 4117 (L) Luzon J. E. Teysmann HB11622 (L) Lesser Sunda Islands J. Elbert 5538 (L) Sulawesi 18. P. maritimus ㊲ P. caesius Airy Shaw & G. L. Webster C. Versteegh BW(Ind.) 4701. (L) New Guinea ㊳ P. maritimus J. J. Sm. L. J. Toxopeus 368 (L) Moluccas J. J. F. E. de Wilde 1205 (L) New Guinea ㊴ P. pullenii Airy Shaw & G. L. Webster P. van Royen 6288 (L) New Guinea ㊵ P. ramosii Quisumb. & Merr. C. Mabesa 853 (L) Luzon 19. P. aeneus ㊶ P. ardisianthus Airy Shaw & G. L. Webster L. J. Brass 11357 (LAE) New Guinea ㊷ P. cuscutiflorus S. Moore A. K. Nura NK261 (KEP) Peninsular Malaysia ㊸ P. finschii K. Schum. V. Novotny 9 (L) New Guinea ㊹ P. merinthopodus Diels P. F. Stevens LAE58638 (L) New Guinea ㊺ P. paniculatus Oliv. P. Katik LAE 56277 (L) New Guinea ㊻ P. praelongipes Airy Shaw & G. L. Webster R. D. Hoogland 4737 (L) New Guinea ㊼ P. tagulae Airy Shaw & G. L. Webster L. J. Brass 27986 (LAE) New Guinea 20. P. papuanus ㊽ P. bourgeoisii Baill. C. L. Ledermann 9740 (L) New Guinea ㊾ P. rheophilus Airy Shaw E. E. Henty NGF12403 (L) New Guinea ㊿ P. rosselensis Airy Shaw & G. L. Webster A. N. Gillison NGF25404 (L) New Guinea P. tenuirhachis J. J. Sm. W. H. de Vriese s.n. (L0135901) Sulawesi D. R. Pleyte 503 (L) New Guinea 21. P. ovatifolius P. clamboides (F. Muell.) Diels R. D. Hoogland 9044 (L) New Guinea P. effuses S. Moore R. D. Hoogland 3917 (L) New Guinea P. gjellerupii J. J. Sm. H. A. van der Sijde BW (Ind.) 4188 (L) New Guinea P. ovatifolius J. J. Sm. Jaheri s.n. (L0135238) Moluccas December 2016 Wu et al.: Pollen in Malesian Phyllanthus 261
Table 1. Continued Pollen class Pollen type Taxa Voucher specimens Locality P. papuanus Gage L. J. Brass 6960 (L) New Guinea III 22. P. aphanostylus P. aphanostylus Airy Shaw & G. L. Webster L. J. Brass 32430 (L) New Guinea 23. P. tabularis P. tabularis Airy Shaw J. F. Veldkamp 8359A (L), 11220 (LAE) New Guinea P. warburgii K.Schum. Atasrip 117 (L) New Guinea 24. P. rubriflorus P. rubriflorus J. J. Sm. H. J. Lam 7758 (L) New Guinea IV 25. P. aff. samarensis P. aff. samarensis C. E. Ridsdale 1479 (L) Luzon 26. P. tenuipes P. tenuipes C. B. Rob. C. E. Ridsdale ISU276 (L) Luzon 27. P. virgatus P. virgatus G. Forst. Asdat 197 (L) Sumatra Unknown (L0136230) Java P. W. Korthals s.n. (L0136233) Borneo J. Metzner 7 (L) Lesser Sunda Islands M.-J. Wu 2953 (TAI) Palawan B. J. Conn 1489 (L) New Guinea R. Pullen SN6696 (LAE) New Guinea P. womersleyi Airy Shaw & G. L. Webster J. S. Womersley NGF41245 (L) New Guinea 28. P. panayensis P. lanceifolius Merr. M. Ramos & G. Edano BS75281 (PUH) Catanduanes P. panayensis Merr. J. A. J. Verheijen 1366 (L) Lesser Sunda Islands P. samarensis Müll. Arg. E. J. Reynoso PPI7550 (L) Samar Vα 29. P. cochinchinensis P. albidiscus (Ridl.) Airy Shaw A. Latiff 1023 (L) Peninsular Malaysia J. E. Teysmann s.n. (L 0159164) Java Vβ 30. P. pulcher P. gomphocarpus Hook. f. W. J. J. O. de Wilde 12277, 18332 (L) Sumatra M. M. J. van Balgooy 7108 (L) Peninsular Malaysia G. Murata J-873 (L) Java C. N. A. de Voogd s.n. (L 0136564) Java P. aff. gracilipes R. Kiew RK3676 (L) Peninsular Malaysia P. pulcher (Baill.) Wall. ex Müll. Arg. J. van Borssum Waalkes 1681 (L) Sumatra Asdat 28 (L) Sumatra L. E. Teo KL3147 (L) Peninsular Malaysia H. Raap 76 (L), J. J. Afriastini 1239 (L) Java A. Dilmy 1052 (L) Lesser Sunda Islands P. aff. pulcher P. F. A. Colfs 211 (L) Lesser Sunda Islands P. aff. pulchroides J. A. J. Verheijen 3290 (L) Lesser Sunda Islands 262 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Table 1. Continued Pollen class Pollen type Taxa Voucher specimens Locality 31. P. filicifolius P. filicifoliusGage E. J. H. Corner s.n. (SING 0151346) Peninsular Malaysia P. aff. gomphocarpus R. E. Holttum SFN31287 (L) Peninsular Malaysia P. sikkimensis Müll. Arg. M. R. Henderson 22872 (SING) Peninsular Malaysia 32. P. kinabaluicus P. gracilipes Müll. Arg. E. P. Tay 145 (SING) Peninsular Malaysia J. van Borssum Waalkes 417 (L), J. E. Teysmann s.n. Java (L 0159782) H. P. Nooteboom 1396 (L) Borneo P. hullettii Ridl. H. G. Keith 9046 (L) Borneo P. kinabaluicus Airy Shaw J. Clemens 28615 (L) Borneo C. E. Ridsdalem SMHI241 (L) Palawan P. sibuyanensis Elmer A. D. E. Elmer 12113 (L) Sibuyan P. watsonii Airy Shaw P. F. Cockbrn, KEP FRI7988 (L) Peninsular Malaysia P. aff. winitii C. G. G. J. van Steenis 18027 (L) Lesser Sunda Islands 33. P. buxifolius P. acutissimus Miq. O. Posthumus 637 (L) Sumatra R. C. B. van den Brink Sr. 1702 (L); J. E. Teysmann s.n. Java L0158822 (L) P. W. Korthals s.n. (L) Borneo P. balgooyi Petra Hoffm. & A. J. M. Baker A. Gibot SAN 91613 (L) Borneo P. buxifolius (Blume) Mull. Arg. V. F. Schiffner 2134 (L) Java Polonio 3422 (L) Borneo J. J. Loeters 1337 (L) Lesser Sunda Islands M. Ramos BS43248 (L) Bohol P. lamprophyllus Mull. Arg. E. Schmutz 3563 (L0465604) Lesser Sunda Islands F. J. M. Gaerlan PPI13214 (L) Palawan D. R. Pleyte 502. (L) New Guinea P. megalanthus C. B. Rob. H. M. Curran FB17243 (L) Luzon P. mindorensis C. B. Rob. E. A. Forsten, s.n. (L 0135008) Sulawesi M. D. Sulit PNH 15718 (L) Luzon P. zollingeri Mull. Arg. J. E. Teysmann s.n. (L0136402), Unknown (L0136400) Java 34. P. aff. acutissimus P. aff. acutissimus J. E. Teysmann s.n. (L0158822) Java December 2016 Wu et al.: Pollen in Malesian Phyllanthus 263 five pollen classes. Class I. Red. Class II. Yellow. Class III. Green. Class IV. Blue. Class V. Purple. V. Class Blue. IV. Class Green. III. Class Yellow. II. Class Red. I. Class classes. pollen five Phyllanthus Map 1. Distribution (location) map of Malesian Malesian of map (location) Distribution 1. Map 264 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue under 10 subgenera in Phyllanthus. 100 % ethanol solutions and pipetted onto a Based on pollen units, aperture form filter membrane to be air dried. For Java and and location, or an extremely distinctive Sumatra samples, a Critical Point Dehydration ornamentation character, Hesse et al. (C. P. D.) process is added after an additional (2009) listed 16 pollen classes for grouping dehydration of 100 % acetone to prevent pollen palynological variations of the seed plants, i.e., grain collapse. Under a thin layer of gold polyads, tetrads, dyads, saccate, inaperturate, coating, the pollen grains were examined and sulcate, ulcerate, colpate, colporate, porate, photographed using a Hitachi S-800 or S-4500 synaperturate, spiraperturate, lophate, clypeate Scanning Electron Microscope. Pollen size was and plicate. Pollen classes of Malesian based on measuring (1–)2–4(–10) pollen grains Phyllanthus in this paper mainly followed the per species. above classification. The terminology used in this paper follows Diploporate colpi or multiporate colpi was Punt et al. (2007) and Hesse et al. (2009). reported in seven pollen types of Phyllanthus and other related genera (Sagun and van der Results Ham 2003). But a pollen grain with 2(–3) pori Pollen morphology in 89 of the 127 Malesian in a colpus is here proposed as a new pollen Phyllanthus species was examined, 34 pollen Class heteroporate (Huang 1972, p. 3, fig. 1: types are recognized and are grouped into 22). In addition, an incomplete synaperturate (or five pollen classes. These pollen classes are I. pseudo-synaperturate), also a new pollen class, Colporate pollen, II. Incomplete synaperturate is proposed and added as a special pollen class pollen, III. Syncolpate pollen, IV. Clypeate found in many Malesian Phyllanthus species. pollen, and V. Porate pollen. A key for the pollen Thus, Phyllanthus pollen can be classified into classes and types is also provided after the seven pollen classes, i.e., clypeate, colporate, detailed descriptions of the five pollen classes as heteroporate, inaperturate, porate, synaperturate below. and incomplete synaperturate. In this paper, thirty-four pollen types of the Malesian Class I. Colporate pollen (Figs. 1–16) Phyllanthus are grouped into five of the seven Sixteen pollen types in three subgenera of pollen classes, excluding Classes heteroporate Malesian Phyllanthus belong to the colporate and inaperturate pollen which have not been pollen class, which have 3- to 5- colporate examined in Malesia so far. The relationships pollen. Five pollen types with 3-colporate pollen among pollen class, pollen type and infrageneric and eight pollen types with 4-colporate pollen classification of Webster and Carpenter (2002, are constant in colporate number. No colporate 2008) are also discussed. number varied within species was observed in these pollen types. However, different colporate Materials and Methods numbers of 4- and 5-colporate pollen within Pollen samples were collected from an individual or a same species were observed specimens deposited in the following herbaria: in three pollen types, i.e., P. emblica type, P. KEP, L, LAE, PUH and SING (Table 1). Per hookeri type and P. oxyphyllus type (Figs. sample, anthers of 1–3 flowers were placed in 14–16). In P. emblica type, pollen grains of P. 1.5 ml centrifuge tubes, immersed in acetic acid emblica L. of Java and Central Malesia are 4- for 30 min until soft, crushed with a glass bar colporate, Peninsular Malaysia are 5-colporate, to release the pollen grains, and then acetolyzed but individuals with both 4- and 5-colporate (Erdtman 1952). The acetolyzed pollen was pollen were found in a Borneo population. In then dehydrated in a series of 70 %, 90 % and P. hookeri type of Malesia, 5-colporate pollen December 2016 Wu et al.: Pollen in Malesian Phyllanthus 265 was found in most of the P. hookeri Müll. Arg. and Cicca belonging to P. casticum type, and populations, 4-colporate pollen was only found 21 species of subgenus Gomphidium sections in a Java population, but individuals with both 4- Adenoglochidion, Gomphidium and Nymania and 5-colporate pollen were found in a Philippine belonging to the remain four pollen types. population. In P. oxyphyllus type, pollen grains of P. oxyphyllus Miq. of Sumatra and Peninsular Class III. Synaperturate pollen (Figs. 22–24) Malaysia are 5-colporate, but individuals with This pollen class contains four pollen both 4- and 5-colporate pollen were found in types. In synaperturate pollen class, both ends Java populations. The colporate pollen class is of the three colpi of the pollen completely then divided into three subgroups Iα, Iβ, and Iγ anastomosing at both poles were observed. Three subclasses by the different colporate numbers, Malesian Phyllanthus pollen types belonging such as, 3-, 4- and 4–5-colporate, respectively. to synaperturate pollen class, P. aphanostylus Exine ornamentation is varied in different pollen type, P. tabularis type and P. rubriflorus type, types of these three subclasses. Bireticulate or have rugulate-reticulate, rugulate, and rugulate tectate-perforate, microreticulate and reticulate and pilate exine ornamentation respectively. exine ornamentation were found in types of Three species of subgenus Gomphidium section all of these three subclasses. In contrast, striate Nymania belong to these three pollen types, was only found in subclass Iα, and pilate and respectively. reticulate rugulate were only found in subclass Iβ. Class IV. Clypeate pollen (Figs. 25–28) This pollen class contains four pollen types. Class II. Incomplete synaperturate pollen The term ‘areolate’ was commonly used to (Figs. 17–21) describe this pollen class in Phyllanthus (Punt The incomplete synaperturate pollen class 1987, Chen et al. 2009). Hesse et al. (2009) with five pollen types, is first coined here. Only suggested that this type of ornamentation is 3-colporate pollen was found having tendency better called clypeate, a pollen wall, in which the to unite its colporus ends at poles in this study. exine is subdived into shields. Four pollen types, In incomplete synaperturate pollen, at least one P. panayensis type, P. aff. samarensis type, P. end of the three colpori is not united or almost tenuipes type and P. virgatus type, with seven anastomosing, but not exactly touching, leaving species in subgenus Isocladus section Macraea a very small reticulate area in between the colpus represent the clypeate pollen class in Malesian ends (Figs. 17–21). Species with incomplete Phyllanthus. Shield-exine of P. aff. samarensis synaperture pollen grains may possess both type and P. virgatus type are microreticulate syncolporate and incomplete syncolporate while the others are rugulate-reticulate. Colpus characters simultaneously, different pollen in margins of P. aff. samarensis type and P. a same individual, or different poles in a same tenuipes type consist of two parallel muri (colpus pollen grain. Five Malesian Phyllanthus pollen membrane absent or obscure), while the others types belong to the incomplete synaperturate consist of four parallel muri. pollen class; P. casticum type, P. maritimus type, P. aeneus type, P. papuanus type and P. Class V. Porate pollen (Figs. 29–34) ovatifolius type, having exine ornamentation This pollen class has pantoporate grains varying from reticulate, microreticulate with including six pollen types in two pollen granules, rugulate-reticulate, rugulate to subclasses, one of which has elliptic or rugulate and pilate. There are three species reniform apertures as well as microreticulate of subgenus Kirganelia sections Anisonema ornamentation without granules, and the other 266 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 1. Scanning electron micrographs of the Phyllanthus amarus pollen (P. amarus type). Scale bar: A–C = 5 μm; D–F = 2 μm.
Fig. 2. Scanning electron micrographs of the Phyllanthus erythrotrichus pollen (P. erythrotrichus type). Scale bar: A–C = 5 μm; D–F = 2 μm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 267
Fig. 3. Scanning electron micrographs of the Phyllanthus maderaspatensis pollen (P. maderaspatensis type). Scale bar: A–C = 5 μm; D–F = 2 μm.
Fig. 4. Scanning electron micrographs of the Phyllanthus microcarpus pollen (P. microcarpus type). Scale bar: A–C = 5 µm; D–F = 2 µm. 268 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 5. Scanning electron micrographs of the Phyllanthus flaviflorus pollen (P. acinacifolius type). Scale bar: A–C = 5 μm; D–F = 2 μm.
Fig. 6. Scanning electron micrographs of the Phyllanthus chamaepeuce pollen (P. urinaria type). Scale bar: A–C = 5 µm; D–F = 2 µm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 269
Fig. 7. Scanning electron micrographs of the Phyllanthus roseus pollen (P. roseus type). Scale bar: A–C = 5 µm; D–F = 2 µm.
Fig. 8. Scanning electron micrographs of the Phyllanthus tenellus pollen (P. tenellus type). Scale bar: A–C = 5 μm, D–F = 2 μm. 270 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 9. Scanning electron micrographs of the Phyllanthus securinegoides pollen (P. securinegioides type). Scale bar: A–C = 5 µm; D–F = 2 µm. (from Blumea 54: 57; fig. 10).
Fig. 10. Scanning electron micrographs of the Phyllanthus pectinatus pollen (P. glochidioides type). Scale bar: A–C = 5 µm; D–F = 2 µm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 271
Fig. 11. Scanning electron micrographs of the Phyllanthus collinsae pollen (P. collinsae type). Scale bar: A– C = 5 μm; D–F = 2 μm.
Fig. 12. Scanning electron micrographs of the Phyllanthus triphlebius pollen (P. triphlebius type). Scale bar: A–C = 5 μm; D–F = 2 μm. 272 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 13. Scanning electron micrographs of the Phyllanthus aff. triphlebius pollen (Pilate type). Scale bar: A– C = 5 µm; D–F = 2 µm.
Fig. 14. Scanning electron micrographs of the Phyllanthus hookeri pollen (P. hookeri type). Scale bar: A–C = 5 μm; D–F = 2 μm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 273
Fig. 15. Scanning electron micrographs of the Phyllanthus emblica pollen (P. emblica type). Scale bar: A–C = 5 µm; D–F = 2 µm.
Fig. 16. Scanning electron micrographs of the Phyllanthus columnaris pollen (P. oxyphyllus type). Scale bar: A–C = 5 μm; D–F = 2 μm. 274 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 17. Scanning electron micrographs of the Phyllanthus ciccoides pollen (P. casticum type). Scale bar: A– C = 5µm; D–F = 2 µm.
Fig. 18. Scanning electron micrographs of the Phyllanthus cupuliformis (P. maritimus type). Scale bar: A–C = 5µm; D–F = 2 µm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 275
Fig. 19. Scanning electron micrographs of the Phyllanthus merinthopodus pollen (P. aeneus type). Scale bar: A–C = 5µm; D–F = 2 µm.
Fig. 20. Scanning electron micrographs of the Phyllanthus tenuirhachis pollen (P. papuanus type). Scale bar: A–C = 5μm; D–F = 2 μm. 276 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 21. Scanning electron micrographs of the Phyllanthus effuses pollen (P. ovatifolius type). Scale bar: A–C =5 μm; D–F = 2 μm.
Fig. 22. Scanning electron micrographs of the Phyllanthus aphanostylus pollen (P. aphanostylus type). Scale bar: A–C = 5 μm; D–F = 2 μm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 277
Fig. 23. Scanning electron micrographs of the Phyllanthus tabularis pollen (P. tabularis type). Scale bar: A– C = 5μm; D–F = 2 μm.
Fig. 24. Scanning electron micrographs of the Phyllanthus rubrifloruspollen (P. rubriflorus type). Scale bar: A–C = 5μm; D–F = 2 μm. 278 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 25. Scanning electron micrographs of the Phyllanthus aff. samarensis pollen (P. aff. samarensis type). Scale bar: A–C = 5μm; D–F = 2 μm. (from Blumea 54: 51; fig. 3g–l)
Fig. 26. Scanning electron micrographs of the Phyllanthus tenuipes pollen (P. tenuipes type). Scale bar: A–C = 5μm; D–F = 2 μm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 279
Fig. 27. Scanning electron micrographs of the Phyllanthus virgatus pollen (P. virgatus type). Scale bar: A–C = 5μm; D–F = 2 μm.
Fig. 28. Scanning electron micrographs of the Phyllanthus panayensis pollen (P. panayensis type). Scale bar: A–C = 5μm; D–F = 2 μm. 280 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 29. Scanning electron micrographs of the Phyllanthus albidiscus pollen (P. cochinchinensis type). Scale bar: A–C = 5 μm; D–F = 2 μm.
Fig. 30. Scanning electron micrographs of the Phyllanthus pulcher pollen (P. pulcher type). Scale bar: A–C = 5μm; D–F = 2μm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 281
Fig. 31. Scanning electron micrographs of the Phyllanthus aff. gomphocarpus pollen (P. filicifolius type). Scale bar: A–B = 5μm; C–D = 2μm.
Fig. 32. Scanning electron micrographs of the Phyllanthus hulettii pollen (P. kinabaluicus type). Scale bar: A–C = 5μm; D–F = 2μm. 282 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Fig. 33. Scanning electron micrographs of the Phyllanthus buxifolius pollen (P. buxifolius type). Scale bar: A–C = 5μm; D–F = 2μm.
Fig. 34. Scanning electron micrographs of the Phyllanthus aff. acutissimus pollen (P. aff. acutissimus type). Scale bar: A–C = 5μm; D–F = 2μm. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 283 has circular apertures as well as reticulate or 1 μm ...... 25. P. aff. samarensis type microreticulate ornamentation with granules 3. Shield-exine rugulate-reticulate; lumina more within the lumina. Phyllanthus cochinchinensis than 1 μm ...... 26. P. tenuipes type type is representative of the elliptic aperture 4. Shield-exine microreticulate; lumina less than subclass. Only one Malesian species, P. 1 μm ...... 27. P. virgatus type albidiscus (Ridl.) Airy Shaw, of subgenus 4. Shield-exine rugulate-reticulate; lumina more Isocladus section Ceramensis belongs to P. than 1 μm ...... 28. P. panayensis type cochinchinensis pollen type (Fig. 29). The other 5. Grains pantoporate (Class V. Porate pollen) ..... 6 five pollen types, Phyllanthus aff. acutissimus 5. Grains colporate or syncolporate ...... 11 type, P. buxifolius type, P. filicifolius type, P. 6. Pori elliptic; lumina without granules kinabaluicus type and P. pulcher type, represent (Subclass Vα.) .... 29. P. cochinchinensis type the circular aperture subclass (Figs. 30–34). 6. Pori circular; lumina enclosing granules Twenty-two Malesian species of subgenus (Subclass Vβ.) ...... 7 Erioccus belong to this pollen subclass, which 7. Murus discontinuous ...... are very similar in ornamentation and only ...... 34. P. aff. acutissimus type differ among each other in lumina size, shape 7. Murus continuous ...... 8 or murus nature. Phyllanthus pulcher type (Fig. 8. Exine microreticulate ...... 9 30) and P. filicifolius type (Fig. 31) both have 8. Exine reticulate ...... 10 micro-reticulate exine with lumina 0.5–1.0 μm 9. Lumen shape regular; muri not curved ...... wide, however, the former having more regular ...... 30. P. pulcher type lumen shape differs from the latter. Phyllanthus 9. Lumen shape irregular; muri strongly curved . kinabaluicus type (Fig. 32) and P. buxifolius ...... 31 P. filicifolius type type (Fig. 33) are common pollen types; each 10. Lumen shape regular; muri not curved ...... type includes seven Malesian species. These two ...... 32. P. kinabaluicus type pollen types have reticulate exine with lumina 10. Lumen shape irregular; muri strongly curved 1.0–3.0 μm wide, rarely mixed with few micro- ...... 33. P. buxifolius type reticulate lumina, however, the former having 11. Grains colporate (Class I. Colporate pollen) . more regular lumen shape differs from the latter...... 12 Phyllanthus aff. acutissimus type (Fig. 34) has 11. Grains syncolporate or incompletely reticulate exine similar to P. kinabaluicus type, syncolporate ...... 27 containing only one species, can be separated 12. Grains 3- colporate (Subclass Iα. 3-colporate from the other pollen types by its reduced exine pollen) ...... 13 with broken muri as well as fewer and smaller 12. Grains 4-, 5-, or 4–5-colporate ...... 17 free columellae within lumina. 13. Pollen wall with hole less than 0.1 μm wide (finely perforate or finely microsulcate)...... 14 Key to the pollen classes and pollen types 13. Pollen wall without perforations less than 0.1 1. Exine surface subdivided into shield-shape μm wide ...... 16 (Class IV. Clypeate pollen) ...... 2 14. Grains prolate; exine striate ...... 1. Exine surface not subdivided into shield- ...... 2. P. erythrotrichus type shaped ...... 5 14. Grains prolate spheroidal to subprolate; 2. Colpus margins consisting of 2 parallel muri.... exine more or less reticulate ...... 15 ...... 3 15. Exine bireticulate; perforations clustered in 2. Colpus margins consisting of 4 parallel muri..... lumina of the primary reticulum ...... 4 ...... 1. P. amarus type 3. Shield-exine microreticulate; lumina less than 15. Exine perforate to reticulate; perforations 284 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
dispersed in reticulate ornamentation ...... 27. Grains syncolporate (Class III. Synaperturate ...... 3. P. maderaspatensis type pollen) ...... 32 16. Amb semilobate; lumina 0.5–1 μm wide ...... 28. Exine reticulate ...... 29 ...... 4. P. microcarpus type 28. Exine more or less rugulate or pilate ...... 30 16. Amb circular; lumina 1–2 μm wide ...... 29. Lumina without pili ...... 17 P. casticum type ...... 5. P. acinacifolius type 29. Lumina enclosing with pili ...... 17. Grains 4-colporate (Subclass Iβ. 4-colporate ...... 18 P. maritimus type pollen) ...... 18 30. Exine rugulate-reticulate .... 19. P. aeneus type 17. Grains 4–5- or 5-colporate (Subclass Iγ. 30. Exine rugulate or rugulate and pilate ...... 31 5-colporate pollen) ...... 25 31. Exine regulate ...... 20. P. papuanus type 18. Pollen wall with holes or perforations less 31. Exine rugulate and pilate ...... than 0.2 μm wide (finely (micro-)perforate or ...... 21. P. ovatifolius type finely microsulcate)...... 19 32. Exine rugulate-reticulate ...... 18. Pollen wall without holes or perforations less ...... 22. P. aphanostylus type than 0.2 μm wide ...... 20 32. Exine rugulate or rugulate and pilate ...... 33 19. Grains prolate; exine bireticulate ...... 33. Exine regulate ...... 23. P. tabularis type ...... 6. P. urinaria type 33. Exine rugulate and pilate ...... 19. Grains spheroidal to subprolate; exine ...... 24. P. rubriflorustype perforate-reticulate with granules filled in the perforations ...... 7. P. roseus type Discussion 20. Exine reticulate ...... 21 The relationship between pollen characters 20. Exine pilate or rugulate-reticulate ...... 24 of 34 pollen types and the infrageneric taxa in 21. Lumina circular, subcircular or circle- Malesian Phyllanthus is summarized into the combined shaped ...... Table 2. Based on Table 2, the evolutionary ...... 8. P. securinegioides type trends of pollen characters among the 21. Lumina irregular shaped ...... 22 infrageneric taxa are discussed below. 22. Grains subprolate; lumina less than 1 μm Class I. Colporate pollen which grain wide ...... 9. P. tenellus type possess colporate aperture is the common 22. Grains spheroidal; lumina more than 1 μm feature in three Malesian subgenera (Emblica, wide ...... 23 Phylanthodendron and Phyllanthus), two 23. Amb semilobate; muri acute ridged ...... New Guinean subgenus Gomphidium (sect...... 10. P. glochidioides type Gomphidium) and subgenus Isocladus (sect. 23. Amb circular; muri round ridged ...... Paraphyllanthus), as well as heterogeneously ...... 11. P. collinsae type with pollen Class II. in subgenus Kirganelia 24. Amb rhomboidal; exine regulate-reticulate... section Anisonema. Even though homogenous ...... 12. P. triphlebius type within the same pollen class, different pollen 24. Amb circular; exine pilate ..... 13. Pilate type Subclasses Iβ and Iγ or Iα–Iγ occurred in 25. Exine bireticulate ...... 14. P. hookeri type subgenus Emblica and Phyllanthus, respectively; 25. Exine reticulate ...... 26 and different pollen Subclasses Iα and Iβ 26. Amb circular; lumina 0.5–1 μm wide ...... occurred in section Gomphidium and sect...... 15. P. emblica type Paraphyllanthus. Pollen subclasses of Class I. 26. Amb semilobate; lumina 1–2 μm wide ...... are grouped on the basis of colporate numbers, ...... 16. P. oxyphyllus type therefore, increasing colporate number shows a 27. Grains incompletely syncolporate (Class II. fast evolutionary rate in Phyllanthus speciation. Incomplete synaperturate pollen) ...... 28 Only colporate numbers of three to five are December 2016 Wu et al.: Pollen in Malesian Phyllanthus 285 found in Malesian Phyllanthus stepanocolporate In this study, two Malesian species pollen. High colporate numbers of 6–11 have of subgenus Phyllanthodendron sect. been reported in some African and American Phyllanthodendron were examined as P. roseus species, especially in neotropical species of type and compared with P. maderaspatensis subgenus Emblica section Microglochidion, type (Fig. 3) of subgenus Isocladus section but all having diploporate colpi (Sagun and van Paraphyllanthus. It was found that P. der Ham 2003, Webster and Carpenter 2002). maderaspatensis type has tricolporate pollen Since no heteroporate (diploporate colpi) pollen type, lalongate endoaperture and microreticulate grains were examined in Malesian Phyllanthus, to perforate exine and that therefore, they are the trend in doubling of the endoaperture more closely related than the species of subgenus (Punt 1967) might be not have occurred in the Emblica. Malesian Phyllanthus. In contrast to the rapid evolution in exine There is only one section Emblica with four ornamentation, Malesian subgenus Phyllanthus species, Phyllanthus emblica L., P. columnaris has evolved at a more conservative pace. Müll. Arg., P. oxyphyllus Miq. and P. pectinatus This subgenus in Malesia is composed of two Hook f., composed of the Malesian subgenus sections, Phyllanthus and Urinaria, with three Emblica. Pollen grains of the former three pollen subclasses. All Malesian species of species, P. emblica, P. columnaris and P. section Phyllanthus, P. amarus Schumach. & oxyphyllus, with colporate numbers 4–5 are Thonn. and P. debilis J. G. Klein ex Willd. are classified into Subclass Iγ, and the latter, P. of neotropical origin with tricolporate pollen pectinatus, with the same number of 4-colporate grains and species of section Urinaria are Asian are classified into Subclass Iβ. The Malaka origin with 3-, 4- or 5-colporate pollen grains. tree, P. emblica, and its closely related species Despite the difference in colporate number, P. pectinatus have similar morphology and all species of the subgenus have the same have long been confused (Ng 2000). However, tectate-perforate to bireticulate ornamentation, pollen grains of these two species are different except P. erythrotrichus C. B. Rob. which has in colporate numbers and exine ornamentation a slightly different, tectate-perforate to striate, and belong to different pollen subclasses and ornamentation. However, Bor (1979) noticed pollen types. Several couples of closely related ornamentation of P. amarus type resembles that species also show palynological variations in of the P. urinaria type in LM, but differs in SEM this study (discussed below). The results imply micrographs. He also found the presence of an that increasing both colporate number and exine outer-reticulum is not clear in P. urinaria type ornamentation variation might indicate rapid under SEM, and suggested that its ornamentation evolutionary rates in Phyllanthus speciation. is better classified as tectate perforate, not Webster and Carpenter (2008) compared bireticulate (Bor 1979). However, both tectate- the similarities of the pollen grains between perforate and bireticulate ornamentation are subgenus Phyllanthodendron and subgenus found in both pollen types and also within Emblica. It was found that they have different individuals in this study. In individual pollen aperture types. The former differs from the grains, polar areas usually having tectate- latter in having lalongate rather than circular perforate and intercolpate areas usually having endoapertures (Webster and Carpenter bireticulate ornamentation was observed. 2008). Also, The former differs in having Therefore, the resemblance of ornamentation microreticulate to perforate exine with regular between P. amarus type and P. urinaria type is lumina rather than microreticulate to rugulate accepted. exine with irregular lumina. Instead of exine ornamentation, colporate 286 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue December 2016 Wu et al.: Pollen in Malesian Phyllanthus 287 N N N N N N N N N N N 6 P P P P P P P P P P P P ugulate- r C C C C C C C C b b b B B B B B J J J J J J J Distribution areas Distribution m m m M M M M M M M M S S S 5 ugulate-microreticulate. R-r. R-r. ugulate-microreticulate. Pil Bir R-r R-r R-r R-r R-r R-r r Mic Mic Mic R-m tr + T-p + tr R-r, mr R-r, R-r, mr R-r, R-r, mr R-r, S Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Bir + T-p + Bir Mic + Per + Mic Mic + Per + G + Per + Mic Mic + Per + G + Per + Mic Ornamentation 4 c c c c c c c c c c c c c c c c c c c c c c c c c la la la la Pore Pore shape eticulate. R-m. R-m. eticulate. r - 7.0 7.0 9.5 9.5 10.2 10.2 12.1 12.1 7.8 ± 0.4 0.4 ± 7.8 9.4 ± 1.6 1.6 ± 9.4 diameter 4.3 ± 0.4 0.4 ± 4.3 5.9 ± 0.4 0.4 ± 5.9 3.8 ± 0.4 0.4 ± 3.8 5.1 ± 1.4 1.4 ± 5.1 9.6 ± 1.3 1.3 ± 9.6 6.9 ± 0.2 0.2 ± 6.9 7.8 ± 0.8 0.8 ± 7.8 8.0 ± 1.4 1.4 ± 8.0 4.2 ± 0.0 0.0 ± 4.2 5.7 ± 1.3 ± 5.7 4.7 ± 0.4 0.4 ± 4.7 4.5 ± 1.7 ± 4.5 6.2 ± 0.5 0.5 ± 6.2 2.4 ± 1.7 ± 2.4 3.3 ± 0.4 ± 3.3 1.9 ± 4.0 5.6 ± 0.9 0.9 ± 5.6 9.0 ± 0.6 0.6 ± 9.0 5.8 ± 0.7 0.7 ± 5.8 3.3 ± 0.9 ± 3.3 10.9 ± 0.6 0.6 ± 10.9 Polar area area Polar 12.5 ± 0.7 ± 12.5 ilate. Ret. Ret. ilate. p 3 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 3 4 3 4 3 3 3 3 3 3 3 3 3 No. Aperture Aperture ) 2 erforate. Pil. Pil. erforate. S p 10.2 P/E (L/ 1.23 ± 0.06 ± 1.23 1.06 ± 0.04 ± 1.06 0.05 ± 1.00 1.15 ± 0.03 ± 1.15 1.05 ± 0.08 ± 1.05 1.13 ± 0.05 ± 1.13 1.97 ± 0.04 ± 1.97 1.81 ± 0.19 ± 1.81 1.63 ± 0.07 ± 1.63 1.67 ± 0.10 ± 1.67 1.47 ± 0.27 ± 1.47 0.94 ± 0.03 ± 0.94 1.21 ± 0.01 ± 1.21 1.40 ± 0.14 ± 1.40 1.27 ± 0.17 ± 1.27 1.78 ± 0.04 ± 1.78 1.38 ± 0.17 ± 1.38 1.67 ± 0.04 ± 1.67 1.08 ± 0.14 ± 1.08 1.74 ± 0.10 ± 1.74 0.09 ± 1.37 0.92 ± 0.03 ± 0.92 0.99 ± 0.02 ± 0.99 0.86 ± 0.01 ± 0.86 1.03 ± 0.00 ± 1.03 0.02 ± 0.96 1.20 ± 0.07 ± 1.20 1.08 ± 0.06 ± 1.08 hort axis of pollen grains. The mean value and standard deviation are provided. are deviation standard and value mean The grains. pollen of axis hort s ) S E ( 19.2 19.2 uri ridged. Per. Per. ridged. uri 9.8 ± 1.3 ± 9.8 9.5 ± 0.2 ± 9.5 11.4 ± 0.4 0.4 ± 11.4 11.4 ± 1.6 1.6 ± 11.4 11.3 ± 0.5 0.5 ± 11.3 11.8 ± 2.2 2.2 ± 11.8 11.4 ± 0.1 0.1 ± 11.4 17.7 ± 0.6 0.6 ± 17.7 21.9 ± 0.5 0.5 ± 21.9 0.4 ± 12.8 12.6 ± 0.5 0.5 ± 12.6 17.0 ± 0.8 0.8 ± 17.0 18.8 ± 0.6 0.6 ± 18.8 12.1 ± 0.9 0.9 ± 12.1 15.6 ± 0.9 0.9 ± 15.6 16.6 ± 0.5 0.5 ± 16.6 13.4 ± 1.7 ± 13.4 10.1 ± 0.6 0.6 ± 10.1 14.0 ± 2.1 ± 14.0 12.8 ± 0.6 0.6 ± 12.8 16.2 ± 1.2 ± 16.2 18.4 ± 0.1 0.1 ± 18.4 19.7 ± 0.1 ± 19.7 17.6 ± 0.7 0.7 ± 17.6 10.8 ± 0.7 ± 10.8 0.2 ± 16.2 11.6 ± 0.1 0.1 ± 11.6 10.7 ± 0.5 0.5 ± 10.7 m P (L) 19.5 19.5 21.8 ± 0.3 0.3 ± 21.8 11.1 ± 0.7 ± 11.1 23.3 ± 0.7 0.7 ± 23.3 0.4 ± 12.8 14.4 ± 0.9 0.9 ± 14.4 17.8 ± 0.5 0.5 ± 17.8 21.3 ± 0.3 0.3 ± 21.3 22.4 ± 0.4 0.4 ± 22.4 20.5 ± 0.7 0.7 ± 20.5 19.6 ± 0.6 0.6 ± 19.6 18.9 ± 1.8 1.8 ± 18.9 14.7 ± 0.5 0.5 ± 14.7 16.9 ± 1.5 1.5 ± 16.9 20.0 ± 0.5 0.5 ± 20.0 15.9 ± 1.4 1.4 ± 15.9 17.2 ± 1.5 ± 17.2 17.9 ± 1.6 1.6 ± 17.9 19.0 ± 0.8 ± 19.0 21.3 ± 0.6 0.6 ± 21.3 10.7 ± 2.7 ± 10.7 16.4 ± 0.9 ± 16.4 2.7 ± 22.3 17.0 ± 0.7 0.7 ± 17.0 19.5 ± 0.5 0.5 ± 19.5 15.1 ± 0.7 0.7 ± 15.1 15.5 ± 0.1 ± 15.5 11.5 ± 1.1 1.1 ± 11.5 13.9 ± 0.8 0.8 ± 13.9 infrageneric taxa in Malesia in taxa infrageneric . 2 1 ata not available. not ata icroreticulate. mr. mr. icroreticulate. d m subsp urinaria urinaria triphlebius glochidioides Phyllanthus Phyllanthus aff. aff. aff. aff. aff. aff. pecies P. glochidioides P. P. securinegioides P. pectinatus P. P. tenellus P. P. ridleyanus P. P. roseus P. P. P. P. P. submarginalis P. P. urinaria P. nudicarpus P. collinsae P. triphlebius P. P. P. urinaria P. P. P. S P. nozeranii P. P. amarus P. P. chamaepeuce P. P. deblis P. P. benguetensis P. P. kostermansii P. P. microcarpus P. novae-hollandiae P. P. erythrotrichus P. maderaspatensis P. P. stultitiae P. P. poli-borealis P. P. flaviflorus P. P. acinacifolius P. yncolporate. ‘-‘. ‘-‘. yncolporate. s alongate. l umen with granules. Mic. Mic. granules. with umen l ectate-perforate. t ection Gomphidium Gomphidium Gomphidium Emblica Floribundi Phyllanthodendron Phyllanthodendron Urinaria Urinaria Urinaria Urinaria Paraphyllanthus Phyllanthus Phyllanthus Urinaria S Urinaria Phyllanthus Urinaria Phyllanthus Urinaria Gomphidium Anisonema Anisonema Urinaria Paraphyllanthus Gomphidium Gomphidium Gomphidium Gomphidium riate. T-p. T-p. riate. s ireticulate. G. G. ireticulate. b rregular elliptic. la. la. elliptic. rregular tr. tr. i S ncomplete syncolporate. syn. syn. syncolporate. ncomplete i umatra. M. Peninsular Malaysia. J. Java. B. Borneo. C. Central Malesia. P. The Philippines. N. New Guinea. Alphabets in italic lower case indicate pollen data not available. not data pollen indicate case lower italic in Alphabets Guinea. New N. Philippines. The P. Malesia. Central C. Borneo. B. Java. J. Malaysia. Peninsular M. umatra. S . . S ubgenus Gomphidium Gomphidium Gomphidium Emblica Kirganelia Phyllanthodendron Phyllanthodendron Phyllanthus Phyllanthus Phyllanthus Phyllanthus Isocladus Phyllanthus Phyllanthus S Phyllanthus Phyllanthus Phyllanthus Phyllanthus Phyllanthus Phyllanthus Gomphidium Kirganelia Kirganelia Phyllanthus Isocladus Gomphidium Gomphidium Gomphidium Gomphidium icular. ie. ie. icular. c 1 9 8 7 7 6 6 6 6 6 6 1 6 1 6 5 4 4 2 3 5 5 5 5 11 10 10 10 12 13 type Pollen Pollen 1 Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iβ Iα Iα Iα Iα Iα Iα Iα Iα Iα Iα Iα class Pollen Pollen See Table 1 and text for explanation in each pollen class and pollen type. S. pollen axis. and Long class L. pollen each polarity. in distinct explanation without for text pollen and for 1 ratio Table L/S See polarity. with grains pollen for ratio P/E isyn. number: Aperture c. shape: Pore Bir. ornamentation: Exine areas: Distribution Table 2. Pollen class, type, characters and distribution of distribution and characters type, class, Pollen 2. Table 6 1 2 3 4 5 reticulate. Rug. Rugulate. Rugulate. Rug. reticulate. 286 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue December 2016 Wu et al.: Pollen in Malesian Phyllanthus 287 N N N N N N N N N N N N N N N N N N N N N N N N N 6 p p P P P P P ugulate- r c c c C C C C C C C b b b B B B J J J J J J Distribution areas Distribution M M M M M M s s S S S 5 ugulate-microreticulate. R-r. R-r. ugulate-microreticulate. R-r R-r R-r R-r R-r R-r R-r R-r R-r R-r R-r R-r R-r Rug Rug Rug Rug Rug Rug r R-m, mr R-m, Mic + G + Mic Mic + G + Mic Mic + G + Mic Mic + G + Mic Bir + T-p + Bir Rug + Pil + Rug Rug + Pil + Rug Rug + Pil + Rug Pil + Rug Pil + Rug Rug + Pil + Rug Ornamentation 4 c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c Pore Pore shape eticulate. R-m. R-m. eticulate. r 0.3 0.3 0.0 0.0 0.0 0.0 0.0 0.9 0.9 0.0 0.0 0.7 0.7 0.4 0.4 0.9 0.9 0.9 0.9 1.0 0.8 0.8 2.0 0.8 0.8 diameter 0.6 ± 0.8 0.8 ± 0.6 0.7 ± 0.5 1.3 ± 1.0 0.2 ± 0.9 1.3 ± 0.5 0.5 ± 1.3 4.0 ± 0.3 0.3 ± 4.0 0.8 ± 0.4 0.4 ± 0.8 8.3 ± 3.1 3.1 ± 8.3 0.3 ± 0.4 0.4 ± 0.3 9.8 ± 2.0 2.0 ± 9.8 0.5 ± 0.3 0.3 ± 0.5 9.0 ± 2.0 2.0 ± 9.0 0.9 ± 0.1 0.1 ± 0.9 1.6 ± 0.4 0.4 ± 1.6 1.0 ± 0.9 0.9 ± 1.0 1.7 ± 0.9 ± 1.7 0.4 ± 0.5 0.5 ± 0.4 Polar area area Polar ilate. Ret. Ret. ilate. p 3 4–5 4–5 4–5 4–5 No. 3-syn 3-syn 3-syn 3-syn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn 3-isyn Aperture Aperture ) 2 erforate. Pil. Pil. erforate. S p 0.86 0.90 P/E (L/ 1.00 ± 0.1 ± 1.00 0.85 ± 0.12 ± 0.85 0.10 ± 0.85 0.04 ± 0.86 0.03 ± 0.85 0.04 ± 0.78 0.86 ± 0.05 ± 0.86 0.92 ± 0.03 ± 0.92 0.90 ± 0.02 ± 0.90 0.84 ± 0.05 ± 0.84 0.82 ± 0.02 ± 0.82 1.65 ± 0.05 ± 1.65 0.87 ± 0.05 ± 0.87 0.91 ± 0.09 ± 0.91 0.80 ± 0.02 ± 0.80 1.03 ± 0.03 ± 1.03 0.88 ± 0.02 ± 0.88 1.07 ± 0.02 ± 1.07 0.76 ± 0.05 ± 0.76 0.93 ± 0.01 ± 0.93 0.80 ± 0.07 ± 0.80 1.07 ± 0.17 ± 1.07 0.88 ± 0.04 ± 0.88 0.83 ± 0.06 ± 0.83 0.94 ± 0.02 ± 0.94 0.91 ± 0.03 ± 0.91 0.96 ± 0.01 ± 0.96 0.95 ± 0.03 ± 0.95 0.99 ± 0.03 ± 0.99 hort axis of pollen grains. The mean value and standard deviation are provided. are deviation standard and value mean The grains. pollen of axis hort s ) S E ( 15.2 15.2 15.8 15.8 uri ridged. Per. Per. ridged. uri 9.9 ± 0.8 0.8 ± 9.9 11.1 ± 0.8 0.8 ± 11.1 15.5 ± 0.9 0.9 ± 15.5 1.7 ± 20.1 0.5 ± 17.7 1.1 ± 20.8 0.4 ± 19.8 16.0 ± 0.2 0.2 ± 16.0 22.2 ± 1.1 1.1 ± 22.2 18.2 ± 1.3 1.3 ± 18.2 16.1 ± 0.9 0.9 ± 16.1 16.4 ± 0.4 0.4 ± 16.4 13.0 ± 1.8 1.8 ± 13.0 18.0 ± 0.2 0.2 ± 18.0 15.4 ± 0.3 0.3 ± 15.4 17.9 ± 0.4 0.4 ± 17.9 16.4 ± 1.6 1.6 ± 16.4 17.2 ± 0.1 0.1 ± 17.2 16.6 ± 1.9 1.9 ± 16.6 17.5 ± 0.1 0.1 ± 17.5 15.1 ± 0.8 0.8 ± 15.1 17.4 ± 0.4 0.4 ± 17.4 14.4 ± 1.3 1.3 ± 14.4 18.2 ± 1.2 1.2 ± 18.2 12.9 ± 1.1 1.1 ± 12.9 17.9 ± 1.0 1.0 ± 17.9 14.5 ± 1.7 1.7 ± 14.5 17.1 ± 0.1 0.1 ± 17.1 14.2 ± 1.9 1.9 ± 14.2 m P (L) 13.0 13.0 14.2 14.2 11.1 ± 1.6 1.6 ± 11.1 13.1 ± 1.1 1.1 ± 13.1 1.5 ± 17.0 0.4 ± 15.3 1.5 ± 17.7 1.1 ± 15.5 13.8 ± 0.6 0.6 ± 13.8 20.5 ± 1.0 1.0 ± 20.5 16.4 ± 1.4 1.4 ± 16.4 13.5 ± 0.0 0.0 ± 13.5 13.5 ± 0.3 0.3 ± 13.5 21.5 ± 2.9 2.9 ± 21.5 15.6 ± 1.0 1.0 ± 15.6 13.9 ± 1.2 1.2 ± 13.9 14.3 ± 0.7 0.7 ± 14.3 16.9 ± 1.4 1.4 ± 16.9 15.1 ± 0.4 0.4 ± 15.1 17.7 ± 2.4 2.4 ± 17.7 13.3 ± 0.8 0.8 ± 13.3 14.1 ± 0.6 0.6 ± 14.1 13.9 ± 0.9 0.9 ± 13.9 10.4 ± 1.0 1.0 ± 10.4 12.6 ± 0.8 0.8 ± 12.6 15.0 ± 0.7 0.7 ± 15.0 12.1 ± 0.8 0.8 ± 12.1 16.3 ± 1.3 1.3 ± 16.3 13.9 ± 1.6 ± 13.9 16.3 ± 0.5 0.5 ± 16.3 14.0 ± 1.8 1.8 ± 14.0 ata not available. not ata icroreticulate. mr. mr. icroreticulate. d m clamboides
pecies P. tenuirhachis P. P. effusus P. gjellerupii P. ovatifolius P. P. warburgii P. P. tabularis P. P. aphanostylus P. P. papuanus P. P. rosselensis P. P. hookeri P. P. rubriflorus P. S P. rheophilus P. P. bourgeoisii P. P. emblica P. P. tagulae P. P. praelongipes P. P. columnaris P. P. paniculatus P. P. oxyphyllus P. P. merinthopodus P. P. reticulatus P. P. ciccoides P. P. finschii P. P. cuscutiflorus P. P. acidus P. P. ardisianthus P. P. maritimus P. P. ramosii P. P. caesius P. P. pullenii P. yncolporate. ‘-‘. ‘-‘. yncolporate. s alongate. l umen with granules. Mic. Mic. granules. with umen l ectate-perforate. t ection Nymania Nymania Nymania Nymania Nymania Nymania Nymania Nymania Nymania S Nymania Urinaria Nymania Nymania Gomphidium Emblica Nymania Nymania Emblica Nymania Emblica Nymania Anisonema Anisonema Nymania Nymania Cicca Nymania Adenoglochidion Adenoglochidion Adenoglochidion Nymania riate. T-p. T-p. riate. s ireticulate. G. G. ireticulate. b rregular elliptic. la. la. elliptic. rregular tr. tr. i S ncomplete syncolporate. syn. syn. syncolporate. ncomplete umatra. M. Peninsular Malaysia. J. Java. B. Borneo. C. Central Malesia. P. The Philippines. N. New Guinea. Alphabets in italic lower case indicate pollen data not not data pollen indicate case lower in italic Alphabets Guinea. N. New Philippines. The P. Malesia. C. Central B. Borneo. J. Java. Malaysia. M. Peninsular umatra. i S . . S ubgenus icular. ie. ie. icular. S Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium Phyllanthus Gomphidium Gomphidium Gomphidium Emblica Gomphidium Gomphidium Emblica Gomphidium Emblica Gomphidium Kirganelia Kirganelia Gomphidium Gomphidium Kirganelia Gomphidium Gomphidium Gomphidium Gomphidium Gomphidium c 1 20 21 21 21 21 23 23 22 21 20 14 24 20 20 15 19 19 16 19 16 19 17 17 19 19 17 19 18 18 18 18 type Pollen Pollen 1 II II II II II II II II II II II II II II II II II II II II II II II Iγ Iγ Iγ Iγ III III III III Distribution areas: areas: Distribution See Table 1 and text for explanation in each pollen class and pollen type. S. pollen axis. and Long class L. pollen each polarity. in distinct explanation without for text pollen and for 1 ratio Table L/S See polarity. with grains pollen for ratio P/E isyn. number: Aperture c. shape: Pore Bir. ornamentation: Exine class Pollen Pollen reticulate. Rug. Rugulate. Rugulate. Rug. reticulate. 1 2 3 4 5 6 available. Table 2. Continued 2. Table 288 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue N N N N 6 p p P P P P P P P P P P P P ugulate- r C C C C C C C C C C C C b B B B B B B B B J J J J J J J J J J J Distribution areas Distribution M M M M M M M M M M s S S S S S S 5 ugulate-microreticulate. R-r. R-r. ugulate-microreticulate. R-r R-r R-r R-r r Mic Mic Mic R-m R-r + G + R-r R-r + G + R-r R-r + G + R-r R-r + G + R-r R-r + G + R-r R-r + G + R-r R-r + G + R-r R-r + G + R-r R-r + G + R-r Ret + G + Ret Ret + G + Ret Ret + G + Ret G + Ret Ret + G + Ret G + Ret Ret + G + Ret Mic + G + Mic Mic + G + Mic Mic + G + Mic Mic + G + Mic Mic + G + Mic R-m + G + R-m R-m + G + R-m R-m + G + R-m Ornamentation 4 c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c ie Pore Pore shape eticulate. R-m. R-m. eticulate. r ------diameter Polar area area Polar ilate. Ret. Ret. ilate. p 3 18 18 8 17 11 11 12 12 13 10 ------– – – – – – – – – – 6 No. 6 8 8 7 5 6 15 12 13 Aperture Aperture ) 2 erforate. Pil. Pil. erforate. S p 1.18 1.04 1.17 1.06 1.03 1.07 1.09 P/E (L/ 1.11 ± 0.03 ± 1.11 1.04 ± 0.00 ± 1.04 1.08 ± 0.01 ± 1.08 0.04 ± 1.01 1.04 ± 0.01 ± 1.04 1.07 ± 0.04 ± 1.07 1.07 ± 0.07 ± 1.07 1.03 ± 0.02 ± 1.03 1.02 ± 0.01 ± 1.02 1.05 ± 0.05 ± 1.05 1.03 ± 0.04 ± 1.03 1.05 ± 0.05 ± 1.05 1.04 ± 0.01 ± 1.04 1.05 ± 0.00 ± 1.05 1.03 ± 0.03 ± 1.03 1.02 ± 0.02 ± 1.02 1.01 ± 0.01 ± 1.01 1.01 ± 0.02 ± 1.01 1.03 ± 0.02 ± 1.03 1.13 ± 0.03 ± 1.13 1.02 ± 0.02 ± 1.02 1.09 ± 0.05 ± 1.09 1.05 ± 0.07 ± 1.05 1.01 ± 0.01 ± 1.01 1.08 ± 0.05 ± 1.08 hort axis of pollen grains. The mean value and standard deviation are provided. are deviation standard and value mean The grains. pollen of axis hort s ) S E ( 15.0 15.0 16.3 16.3 17.5 17.5 17.4 17.4 17.1 17.1 18.3 18.3 18.1 18.1 uri ridged. Per. Per. ridged. uri 21.6 ± 0.7 0.7 ± 21.6 15.9 ± 0.8 0.8 ± 15.9 1.4 ± 18.2 16.3 ± 0.6 0.6 ± 16.3 18.0 ± 0.6 0.6 ± 18.0 16.4 ± 1.7 1.7 ± 16.4 17.0 ± 1.7 ± 17.0 18.4 ± 0.6 0.6 ± 18.4 15.2 ± 0.8 0.8 ± 15.2 18.0 ± 0.7 0.7 ± 18.0 18.3 ± 1.5 1.5 ± 18.3 18.5 ± 0.5 0.5 ± 18.5 16.3 ± 2.1 2.1 ± 16.3 24.9 ± 0.2 ± 24.9 16.4 ± 1.3 1.3 ± 16.4 18.9 ± 1.9 1.9 ± 18.9 17.0 ± 1.5 1.5 ± 17.0 15.0 ± 0.2 0.2 ± 15.0 17.7 ± 0.1 0.1 ± 17.7 17.0 ± 0.4 0.4 ± 17.0 20.8 ± 2.0 2.0 ± 20.8 15.6 ± 4.9 4.9 ± 15.6 20.4 ± 0.8 0.8 ± 20.4 22.6 ± 1.8 1.8 ± 22.6 19.1 ± 1.7 1.7 ± 19.1 m P (L) 17.7 17.7 16.9 16.9 20.5 20.5 18.4 18.4 17.4 17.4 19.5 19.5 19.7 19.7 22.5 ± 0.8 0.8 ± 22.5 17.1 ± 1.0 1.0 ± 17.1 1.0 ± 18.5 17.0 ± 0.6 0.6 ± 17.0 19.3 ± 0.8 0.8 ± 19.3 17.5 ± 1.6 1.6 ± 17.5 17.6 ± 1.5 1.5 ± 17.6 18.7 ± 0.7 0.7 ± 18.7 16.1 ± 0.3 0.3 ± 16.1 18.5 ± 0.2 0.2 ± 18.5 19.3 ± 1.8 1.8 ± 19.3 19.5 ± 0.5 0.5 ± 19.5 16.8 ± 1.7 1.7 ± 16.8 25.5 ± 0.2 ± 25.5 16.6 ± 1.2 1.2 ± 16.6 19.1 ± 1.6 1.6 ± 19.1 17.6 ± 1.4 1.4 ± 17.6 17.0 ± 0.3 0.3 ± 17.0 18.1 ± 0.4 0.4 ± 18.1 18.8 ± 0.3 0.3 ± 18.8 22.6 ± 2.6 2.6 ± 22.6 16.2 ± 4.0 4.0 ± 16.2 20.5 ± 0.7 0.7 ± 20.5 24.3 ± 1.8 1.8 ± 24.3 19.8 ± 1.7 1.7 ± 19.8 ata not available. not ata icroreticulate. mr. mr. icroreticulate. d m gomphocarpus acutissimus gracilipes samarensis pulcher pulcheroides winitii . sikkimensis . aff. aff. aff aff. aff. aff. aff. aff. aff. aff. pecies P. albidiscus P. P. panayensis P. samarensis P. P. gomphocarpus P. P. lanceifolius P. P. virgatus P. P. P. pulcher P. P. womersleyi P. P. tenuipes P. P. acutissimus P. P. P. mindorensis P. P. megalanthus P. P. P. S P. P. P. P. P. zollingeri P. P. pulcheroides P. P. kinabaluicus P. P. gracilipes P. hullettii P. P. sikkimensis P. P. P. filicifolius P. P. buxifolius P. P. sibuyanensis P. P. P. balgooyi P. P. P. P. lamprophyllus P. P. watsonii P. yncolporate. ‘-‘. ‘-‘. yncolporate. s alongate. l umen with granules. Mic. Mic. granules. with umen l ectate-perforate. t ection Ceramanthus Macraea Macraea Eriococcus Macraea Macraea Eriococcus Eriococcus Macraea Macraea Eriococcodes Macraea S Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Scepasma Eriococcus Eriococcus Emblicastrum Eriococcodes Emblicastrum Emblicastrum riate. T-p. T-p. riate. s ireticulate. G. G. ireticulate. b rregular elliptic. la. la. elliptic. rregular tr. tr. i S ncomplete syncolporate. syn. syn. syncolporate. ncomplete i umatra. M. Peninsular Malaysia. J. Java. B. Borneo. C. Central Malesia. P. The Philippines. N. New Guinea. Alphabets in italic lower case indicate pollen data not available. not data pollen indicate case lower italic in Alphabets Guinea. New N. Philippines. The P. Malesia. Central C. Borneo. B. Java. J. Malaysia. Peninsular M. umatra. S . . S ubgenus Isocladus Isocladus Isocladus Eriococcus Isocladus Isocladus Eriococcus Eriococcus Isocladus Isocladus S Eriococcus Isocladus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus Eriococcus icular. ie. ie. icular. c 1 29 28 28 30 28 27 30 30 27 26 33 25 33 33 30 33 30 33 32 32 32 32 31 31 31 33 32 32 33 34 33 33 type Pollen Pollen 1 IV IV IV IV IV IV IV Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vβ Vα Vβ Vβ Vβ class Pollen Pollen See Table 1 and text for explanation in each pollen class and pollen type. S. pollen axis. and Long class L. pollen each polarity. in distinct explanation without for text pollen and for 1 ratio Table L/S See polarity. with grains pollen for ratio P/E isyn. number: Aperture c. shape: Pore Bir. ornamentation: Exine areas: Distribution 1 2 3 4 5 6 Table 2. Continued 2. Table reticulate. Rug. Rugulate. Rugulate. Rug. reticulate. December 2016 Wu et al.: Pollen in Malesian Phyllanthus 289 number becomes a key character to distinguish ramosii showed syncolporate character in SEM closely related species in subgenus Phyllanthus (Chen et al. 2009; fig. 8) but six pollen grains sect. Urinaria. Rossignol et al. (1987) found showed 50% incomplete syncolporate character the relationship between colporate number and examined under light microscope. Luo et al. chromosome polyploidy in subsection Urinaria: (2011) distinguished P. microcarpus Müll. Arg. species with 4-colporate pollen grains are from P. reticulatus Poir. with morphological diploid, whereas species with 5-colporate pollen data as well as ITS sequence analysis. The grains are tetraploid. The 5-colporate pollen difference of the colpate lengthening between grains of section Urinaria are classified as P. P. microcarpus and P. reticulatus also provides hookeri type and separate from the P. urinaria useful evidence for separating these two species. type. However, a Java P. hookeri population As a result, only four Malesian Phyllanthus having 4-colporate pollen and a Philippine species, i.e., P. aphanostylus Airy Shaw & population having 4- and 5-colporate were found Webster, P. tabularis Airy Shaw, P. warburgii and differ from all other 5-colporate populations K. Schum. and P. rubriflorus J. J. Sm. were in Malesia. These Philippine populations characterized as Class III. Synapeturate pollen. might be of hybrid origin or might simply be All of them were found to be in subgenus a misidentification. More chromosome data Gomphidium section Nymania. are needed to test this relationship between Class IV. Clypeate pollen was found in all colporate number and chromosome polyploidy Malesian species of subgenus Isocladus section in Malesian section Urinaria. Macraea. This pollen class was also found in Punt (1980) reported three pollen types, P. neotropical species of the subgenera Botryanthus aeneus type, P. casticum type and P. maritimus and Xylophylla, however, the endoapertures type, as synaperturate pollen for New Guinea situated in the middle of the colpus differ from Phyllanthus subgenera Gomphocarpus and the latters’ with endoapertures under the point of Kirganelia. He noticed that colpus ends often the three coalescence colpi (Punt 1987). anastomosed at the poles, sometimes not exactly Variations of colpus margin (Chen et al. touching, leaving a very small reticulate area 2009), lumen size and shape in the shields (Chen in between the colpus ends. In this study such and Wu 1997) of the clypeate pollen have been pollen types are classified as Class II. Incomplete noticed and are helpful for species identification synapeturate pollen. In the incomplete in section Macraea. Three additional pollen synapeturate pollen grains, three colpate ends types in Class IV. clypeate pollen are proposed meet at the pole and may be separated by two for facilitating species classification in Malesian attached muri less than 2 μm. This pollen class section Macraea. mainly occurs in subgenus Gomphidium sections Class V. Porate pollen Subclass Vα is the Adenoglochidion and Nymania, and subgenus solo representative for species of subgenus Kirganelia sections Anisonema and Cicca. The Isocladus section Ceramanthus; and Subclass colpate ends meet closely at the pole but are Vβ represents solely for species of subgenus separated by a distance of more than 2 μm in P. Eriococcus. The pollen grains of Subclass Vα microcarpus type of subgenus Kirganelia sect. mainly differ from Subclass Vβ by having Anisonema and are classified as pollen Class I. irregular elliptic or reniform apertures and no Nevertheless, colpate length of sect. Anisonema granules in lumina while the latter possesses the might have a lengthening tendency toward circular aperture and granules in lumina. As to syncolporate. Two or three colpate ends might the exine ornamentation in Subclass Vα, only completely meet at one pole or both poles in microreticulate ornamentation in P. albidiscus pollen Class II. For example, pollen grains of P. (Ridl.) Airy Shaw was found in this study; 290 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue however, both microreticulate and reticulate characters of section Phyllanthus, i.e., typical ornamentation in section Ceramanthus were phyllanthoid branching, the staminate flowers reported by Punt (1972), and therefore is similar with two or three stamens, and colporate pollen. to Subclass Vα. Although the pollen grains Therefore, they should belong to subgenus of section Ceramenthus have some similarity Phyllanthus. Moreover, P. aff. triphlebius having to subgenus Eriococcus, several vegetative the inordinate unique pilate ornamentation and reproductive characters are different which is similar to the pollen types reported in between these two taxa. The species of section Africa (P. dinklagei type) or in South America Ceramenthus lack phyllanthoid branching, (P. brasiiensis type and P. attenuates type), is have six entire tepals in male flowers, and most certainly convergence (Punt 1986, Webster urceolate disk in female flowers (Punt 1972), and Carpenter 2002, Chen et al. 2009). Whereas whereas the species in subgerera Eriococcus P. aff. triphlebius closely related to species have phyllanthoid branching, four lacerate P. triphlebius has a totally different rugulate- tepals in male flowers, and no urceolate disk reticulate ornamentation. This is another in female flowers (Webster 1957). Therefore, example of two closely related species having the relationship between section Ceramanthus the same pollen class but showing extremely and subgenus Eriococcus is distant. Especially varied exine ornamentation. Possibly there is a section Ceramanthus possessing the pollen rapid evolution in the exine ornamentation. Class V is different from pollen Classes IV and I Finally, the same pollen evolution trends of two other sections in subgenus Kirganelia so (Punt 1967; fig. 1) in colpate length, numbers of that the section Ceramanthus could be raised to colporus (pores), shape of the endoaperture and be an independent rank of subgenus. exine ornamentation are also observed in our Variation of lumen size and shape in work. reticulate exine ornamentation within subgenus Eriococcus has been noticed (Webster and We would like to express our sincere thanks Carpenter 2008). Based on lumen size and to the directors of the National Herbarium shape, five pollen types are classified for Nederland (L), Papua New Guinea Forest Malesian subgenus Eriococcus. As it might Research Institute, (LAE), Singapore Herbarium be useful for species identification, four new (SING), Forest Research Institute Malaysia pollen types, P. aff. acutissimus, P. filicifolius, P. Herbarium (KEP), and the Jose Vera Santos kinabaluicus and P. pulcher types, are proposed. Memorial Herbarium (PUH) for the loan of Phyllanthus triphlebius C. B. Rob. was specimens and providing pollen materials. published as a new species in section Eriococcus We appreciate the anonymous reviewers for (Robinson 1909), possibly due to having typical providing various advice. Thanks also to Ms Jin- phyllanthoid branching and the staminate Yen Lin, Ms Ya-Yun Yang, and Ms Ya-Jen Yang, flowers with two stamens. However, the pollen National Taiwan University, and Ms Mei-Jiun morphology of P. triphlebius (Fig. 13) and its Yang, Tzu Chi University for their assistance in closely related species P. aff. triphlebius (Fig. using the scanning electron microscope. Thanks 14) is Class I. colporate pollen, thoroughly also to Prof. Emeritus H. Ohashi of Tohoku different from Class V. porate pollen of subgenus University for encouraging us to prepare this Eriococcus. In addition, these two species have manuscript. This study was supported by the entire tepal margin in both male and female National Science Council (grant no. NSC 101- flowers, therefore, excluding these two species 2621-B259-001 & NSC102-2621-B-259-001), from section Eriococcus seems reasonable. Executive Yuan, Taiwan. Furthermore, these two herbaceous species bear December 2016 Wu et al.: Pollen in Malesian Phyllanthus 291
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吳 明洲 a，黃 增泉 b，劉 嘉卿 c，陳 彥叡 a，張 永 聖 a，許 家倫 a，吳 信毅 a，曾 艾翊 a，章 尹禎 a，劉 澄 a a 娟 ，A. Kaewmuan ：マレーシア地域のコミカンソウ 属（ミカンソウ科）の花粉形態と分類 2001 年にマレーシア地域には 110 種のコミカンソウ はマレー半島 (Chang 2012)，ボルネオ (Hsu 2011)，中 属（ミカンソウ科）が知られていた．その後，われわれ 部マレーシア地域 (Wu 2012)，フィリピン (Chen 2009, 292 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue
Chen et al. 2009)， お よ び ニ ュ ー ギ ニ ア (Chang 2010, pollen classes にまとめることができた (Table 2)．各花粉 Tseng 2012) のコミカンソウ属を花粉形態とともに分類 型と花粉群との区別点を検索表で示した．また，花粉型 学的研究を行ってきた．その結果，マレーシア地域に における進化方向とマレーシア地域のコミカンソウ属 127 種を認めることができた．本研究ではその内，89 の属内分類について論議した． 種の花粉形態を調べ，34 の花粉型を認めた．これらは （a台湾・National Dong Hwa University, I. 溝孔粒 Colporate pollen class，II. 不完全合流溝型花粉 Department of Natural Resources and Environmental Studies, Incomplete synaperturate pollen class，III. 合流溝型花粉 b台湾・National Taiwan University, Institute of Plant Biology, Synaperturate pollen class，IV. 楯型花粉 Clypeate pollen c台湾・Tzu Chi University, Department of Life Sciences） class，および V. 孔粒花粉 Porate pollen class の 5 花粉群