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Pollen morphology of some species of the genus Euphorbia L.
Review of Palaeobotanyand Palynology,78 (1993): 293-319
293
Elsevier SciencePublishers B.V., Amsterdam
Pollen morphology of some species of the genus
Euphorbia L. G a m a l A. E1-Ghazaly a a n d R a m C h a u d h a r y b
aSwedish Museum of Natural History, PalynologicalLaboratory, S-10405 Stockholm, Sweden bDepartment of Botany, Tribhuvan University, Kathmandu, Nepal (Received October 9, 1992; revised and accepted April 7, 1993)
ABSTRACT E1-Ghazaly, G.A. and Chaudhary, R., 1993. Pollen morphologyof some species of the genus EuphorbiaL. Rev. Palaeobot. Palynol., 78: 293-319. The pollen morphologyof sixtyspeciesof the genus Euphorbiahas been examinedwith LM and SEM. The genus has been found to be remarkablyeurypalynous.Seven pollen types have been distinguished.A detailed diagnosis of each pollen type is given.The geographicaldistributionof the pollen types is presented, and a putativeevolutionaryrelationshipbetweenpollen types is suggested.
Introduction
Euphorbia have been published (e.g. Kuzmanov,
Euphorbiaceae is a distinctly eurypalynous family. Various pollen-morphological studies have shown the great diversity of pollen types in this family (Punt, 1962, 1972, 1987; K6hler, 1965, 1967; Khan, 1968; Bor, 1979; Park and Lee, 1988; Saad and E1-Ghazaly, 1988). The genus Euphorbia belongs to the subfamily Euphorbioideae and comprises ca. 2000 species, mainly distributed in subtropical and warm temperate regions (Heywood, 1979). So far, the pollen morphology of this genus has not been examined extensively. Only a few species of Euphorbia were described by Punt (1962), Nair (1961) and Schill (1973). Hesse (1980) examined the pollen wall ultrastructure and pollenkitts of two species of Euphorbia and Frean (1983) described sporoderm morphogenesis in E. obesa. Weber-El Ghobary (1985) did a detailed LM and SEM study on the pollen morphology of four succulent species of Euphorbia and recently E1Ghazaly (1989) investigated in detail the morphology of pollen and orbicules of nine species of Euphorbia by LM and SEM. Several taxonomic investigations on the genus
1963; Khan, 1964; EI-Hadidi, 1978). Moreover, several new names and new combinations in the genus Euphorbia were estated in the floras of different parts of the world, e.g. Flora of Iraq (Radcliffe-Smith, 1980), Flora of Turkey (RadcliffeSmith, 1982), Flora of Tropical East Africa (Carter, 1988), and Flora Europaea (Smith and Tutin, 1968). Recently, Oudejans (1989) published new names and combinations in the genus Euphorbia, followed in 1990 by a comprehensive list of over 10,000 names belonging to the tribe Euphorbieae, including changes, synonyms and misspellings (Oudejans, 1990). In the present study, sixty species of Euphorbia representing different sections according to the classification of Pax (1896) were examined by LM and SEM. The new names and synonyms reported by Oudejans (1989, 1990) were taken into consideration. This study demonstrates the variability within the species of Euphorbia. In addition, the phylogenetic relationships between the types are discussed and taxonomic suggestions based on pollen morphology are presented.
0034-6667/93/$06.00
© 1993 -- Elsevier SciencePublishers B.V. All rights reserved.
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Materials and methods This study is based on polliniferous material of sixty species collected from the herbarium of the Swedish Museum of Natural History, Stockholm [S], acetolysed using Erdtman's (1960) standard acetolysis method. The LM studies were made using a Leitz Wetzlar Dialux microscope with apochromatic oil immersion objective (× 100, N.A.I.32) and periplan eyepieces (G.F., x 10). Measurements were made with oil immersion, and are based on 20 or more pollen grains per species. Exine thickness has been measured in the centre of mesocolpia of pollen grains lying in equatorial view. For SEM, acetolysed pollen grains were suspended in a drop of absolute alcohol, transferred to brass stubs and coated with gold-palladium for 7 min using a Fine Coat ION Sputter JFC 1100. Scanning micrographs were taken with a Jeol JSM 25S-II microscope using Ilford FP4 film. The morphological characteristics of pollen are summarised in Table I. The terminology of pollen grains mainly follows that of Erdtman (1969) and Praglowski and Punt (1973).
Results General description
G . A E L - G H A Z A L Y A N D R. C H A U D H A R Y
than nexine, or equally thick except at the apertures, tectate perforate, rugulose, foveolate, microreticulate and reticulate. Scanning electron microscopy Most pollen grains are pertectate with minute perforations which are single or fuse in groups of 2, 3 or 4; or with broadly elliptic to linear oblong perforations, surface smooth, rarely beset with minute granules or masked with a thin layer. Some taxa have microreticulate to reticulate sexine with tetragonal to hexagonal lumina, with or without minute perforations; rugulose sexine consisting of elongated elements (rugulae), smooth or granular. In some taxa (E. bicolor, E. marginata) the sexine pattern is differentiated into perforate to foveolate or perforate to microreticulate.
Descriptions of the pollen types Type 1 - E. villosa Pollen grains 3-colporate, subprolate to prolate spheroidal, rarely oblate spheroidal and prolate. Outline in polar view rounded, 3-lobed. Sexine smooth, continuous, tectate-perforate to discontinuous +_rugulose. Colpi with usually broad margins and protruding well-developed sexine. Apocolpium diameter 6-11.3.
Light microscopy Subtype la- E. villosa (Plates I,II) Pollen grains generally isopolar, only in some specimens of E. caputmedusae heteropolar, radially symmetrical, rounded to 3-lobed in polar view. P=22.4-59.0 and E = 16.3-47.0 l a m , Subspheroidal to prolate, 3-colporate. Colpi long (17.6-47.2 lam), narrow to wide, sometimes constricted at the equator due to sexine overlappings, and with acute to obtuse ends; margines smooth, straight to wavy. Ora lalongate (2.5 × 4-9.1 x 11.2 txm) to lolongate (6.6 × 5.614.6x 10.3 txm), rarely elliptic or "H"-shaped. Apocolpium diameter varying, 2.9-11.1 (12.5) lam, rarely absent (tendency to syncolpate) or left intact (parasyncolpate?) in E. caputmedusae. Exine 2-5 (5.3) Jam thick at the centre of mesocolpia, thickness decreases towards poles. Sexine usually thicker
LM: pollen grains 3-colporate. Outline in polar view 3-lobed, rarely rounded, 30-45 × 20.2-41.2 Ixm. Colpi 22.6-33.4 lam long with + obtuse ends. Ora lalongate to lolongate, rarely circular, 2.4 × 5.2-9.8 x 7.7 ~tm. Apocolpium diameter 4.6-9.9 Ixm. Exine 2 4.1 tam thick at the centre of mesocolpium. Sexine perforate. SEM: Colpi with broad, sparsely granular, perforate margins. Colpus membrane rarely coarsely granulated. Ora encircled by thick margin. Sexine perforated at apocolpium, very rarely _+nonperforate smooth (E. cheirolepis). Sexine perforations are single or fuse in groups of 2, 3 or 4. Some pollen grains have perforations with granules.
POLLEN MORPHOLOGY
295
O F S O M E S P E C I E S O F T H E G E N U S E U P H O R B I A L.
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POLLEN
MORPHOLOGY
OF SOME SPECIES OF THE GENUS
297
EUPHORBIA L.
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PLATE I
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIAL.
Taxa included." E. atropurpurea, E. balsamifera, E. burmannii, E. cheirolep&, E. hieronymi, E. lata, E. petiolata, E. phylloclada, E. prolifera, E. retusa, E. sopina, E. tirucalli, E. tuberosa, E. villosa, E. virosa.
Subtype lb - E. monteiri (Plates Ill,IV) LM: Pollen grains 3-colporate, subprolate to prolate spheroidal 31.6-57x27.8-46.3 ttm. Outline in polar view rounded to 3-lobed. Colpi 25-47.2 lxm long with _ obtuse ends. Ora lalongate to lolongate, rarely 'H"-shaped, 3 x 5.9-14.6 x 10.3 ~tm. Apocolpium diameter 7.7-11.3 lxm. Exine 3.0-4.1 lam thick at the centre of mesocolpium. Sexine indistinctly perforate. SEM: Colpi relatively narrow with usually smooth margins, thickened at the os region. Colpus membrane granular. Sexine partly consists of elongated elements (rugulae) separated by single or fused perforations in groups located in deep narrow irregular slits. Typical rugulose pattern is mainly found in the central part of mesocolpia; in others sexine areas and at apocolpia usually microreticulate to perforate. Taxa included: E. akenocarpa, E. bourgaeuna, E. cassia, E. densa, E. dracunculoides, E. engleri, E. eremophila, E. esula, E. inundata, E. monteiri, E. polyantha, E. rigida, E. scheffleri, E. trichdenia, E. wallichii.
Type 2 - E. nutans (Plate V) LM: Pollen grains 3-colporate, usually prolate, sometimes subprolate and rarely prolate spheroidal, 23.2 x 16.8-31.7 x 17.0 ttm. Outline in polar view 3-lobed. Sexine tectate perforate to _microreticulate. Colpi 17.6-25.0 ttm long with
299
acute ends, margin narrow, constricted usually at the equitorial region around os. Ora predominantly lalongate, 2.2 x 5.0-2.8 x 5.9 ttm. Apocolpium diameter small, 2.9-5.4 Ixm. Exine 2.0-2.7 ttm thick at the centre of mesocolpium. SEM: Colpi sunken lacking clearly protruding sexine at the os, margin +wavy, membrane smooth, becoming narrow and indistinct towards the poles. Sexine with circular to slit like perforations, rarely +microreticulate with indistinct (masked) lumina, occasionally with a ring (valve) like marginal structure and minute granules. Taxa included: E. atoto, E. chamaesyce, E. hirta, E. humifusa, E. hypericifolia, E. macropus, E. mesembryanthemifolia, E. nutans, E. peplis, E. prostrata, E. thymifolia, E. vestita. Type 3 - E. caputmedusae (Plate VI) LM: Pollen grains 3-colporate, subprolate, 49.2-54.6 x 42.7-46.9 ttm. Outline in polar view rounded to 3-lobed. Sexine rugulose. Colpi 39-43.3 lam long with obtuse ends. Ora lalongate to lolongate, 9 x 11 ~tm. Apocolpium diameter in isopolar pollen grains 7.9-9.7 ~tm. Heteropolar pollen grains are parasyncolpate only at one pole leaving an intact polar area of varying size and shapes. Exine 3.7-4.4 ttm thick at the centre of mesocolpium. SEM: Colpi extended in E. caputmedusae to one pole (parasyncolpate grains) with rather thick margin beset with scattered minute granules and markedly thickened at os region. Colpus membrane densely granular. Sexine rugulose, occasionally microreticulate at apocolpia particularly in heteropolar pollen grains. Rugulae of variable shape, appears cerebroid with granules of different
PLATE I Type 1-6. 1. 2. 3. 4. 5. 6. 7.
1, subtype la. Euphorbia villosa. LM, polar view, ornamentation at high focus ( x 1000). LM, polar view, optical cross-section ( x 1000). LM, Equatorial view, optical cross-section ( x 1000). SEM, polar view ( x 1700). SEM, equatorial view ( x 1700). SEM, magnified part of the exine and an aperture, showing perforate exine and thickened margin at sides of the os ( x 5400). E. petiolata. SEM, perforate exine and colpus with thick margin ( x 4500).
300
size and irregular distribution, often filling the grooves. Taxa included: E. caputmedusae, E. tuberculata.
Type 4 - E. peplus (Plate VII) LM: Pollen grains 3-colporate, prolate spheroidal, 24.1-24.9 x 10 24.0-24.1 jam. Outline in polar view rounded to 3-lobed. Sexine basically microreticulate, becoming reticulate along the colpal margin, especially towards the os. Colpi 16.9-19.1 jam long with +pointed ends. Ora variable in shape, generally lalongate to lolongate, elliptic, rarely "H"-shaped, 3.2 x 3.6-5.4 x 6.8 jam. Apocolpium diameter 6.2-7.4 jam. Exine 2.5-2.7 jam thick at the centre of mesocolpium. SEM: Colpus margin generally narrow, thickened and protruding at the os, with few scattered perforations. Colpus membrane granular. Sexine microreticulate to + irregularly reticulate, rarely perforate, bottom of lumina minutely perforate. Taxa included: E. peplus, E. schimperiana.
G.A. EL-GHAZALYAND E. CHAUDHARY
Type 5- E. bicolor (Plate VIII) LM: Pollen grains 3-colporate, prolate spheroidal, 34.3-39.9 x 30.6-35.3 jam. Outline in polar view rounded to 3-lobed. Sexine varies from tectate perforate to microreticulate. Colpi 24.4-30.9 jam long with + obtuse ends. Ora talongate, 3.2 x 6.64.3 x 8.2 jam. Apocolpium diameter 8.2-9.6 jam. Exine 4.2 jam thick at the centre of mesocolpium, becoming thin near the poles. SEM: Colpus margin wavy, broad with few scattered perforations, wavy. Colpus membrane beset with few scattered granules. Sexine, heterogenous, perforate at apocolpia and centre of mesocolpia, changing gradually to a foveolate, microreticulate or reticulate zone bounded by a sparsely perforate colpus margin. Taxa included: E. bicolor, E. rnarginata.
Type 6 - E. corollata (Plate IX) LM: Pollen grains 3-colporate, generally subpro-
late,
rarely
prolate
spheroidal
and
prolate,
PLATE II Type I, subtype la. 8. E. supina. SEM, magnified part showing a colpus and exine perforation with minute granules ( x 5500). 9, 10. E. cheirolepis. 9. SEM, equatorial view ( x 2000). 10. SEM, polar view, showing small polar area with few perforations ( × 4000). 11. E. tuberosa. SEM, perforate exine and thick colpus margin at sides of the os ( × 3500). 12. E. virosa. SEM, equatorial view, showing perforated exine and thick colpus margin. Note colpus membrane and margin beset with granules ( × 5500). 13. E. atropurpurea. SEM, polar view ( x 2300). PLATE III (see p. 302) Type 1, subtype lb. E. monteiri. 14. LM, polar view, ornamentation at high focus ( × 1000). 15. LM, polar view, optical cross-section (× 1000). 16. LM, equatorial view, optical cross-section ( x 1000). 17. SEM, sub-polar view (× 1500). 18. SEM, equatorial view (x 1500). 19. SEM, magnified part of exine showing fused perforations located in narrow irregular concavities ( × 6500). PLATE IV (see p. 303) Type 1, subtype lb. 20. E. akenocarpa. SEM, polar view ( x 2000). 21. E. polyantha. SEM, detail of exine ornamentation ( x 4000). 22. E. rigida. SEM, ornamentation and colpus with thick margin ( x 4000). 23. E. engleri. SEM, ornamentation and colpus ( x 4000). 24. E. esula. SEM, note thick colpus margin at sides of the os and granular colpus membrane ( x 4000). 25. E. scheffteri. SEM, magnified part showing perforate exine and thick colpus margin ( x 4000).
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
P L A T E II
301
302
G.A. EL-GHAZALYAND R. CHAUDHARY PLATE
III
(for description see p. 300)
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE IV
(for description see p. 300)
303
304
G.A. EL-GHAZALYAND R. CHAUDHARY
25.8-31.3 × 19.3-26.7 tam. Outline in polar view rounded to 3-lobed. Sexine microreticulate. Colpi 17.8-23.8 tam long with +pointed ends. Ora distinctly lalongate, 2 x 6.3-3 x 7.2 tam. Apocolpium diameter 5.3-7.7 tam. Exine 2.4-3.0 tam thick at the centre of mesocolpium. SEM: Colpus margin narrow, slightly wavy, increasing in thickness towards the os. Colpus membrane faintly granular. Sexine microreticulate with slitlike perforations along the colpus margins which are beset with few granules. Taxa included: E. curtisii, E. corollata, E. hexagona, E. ocymoidea, E. polyphylla, E. xanti.
Type 7 - E. fulgens (Plate X) LM: Pollen grains 3-colporate, subprolate to prolate spheroidal, 30.8-40.7 x 25.1-38.5 tam. Outline in polar view rounded to 3-lobed, Sexine clearly reticulate. Colpi 21.2-29.8 tam long. Ora lalongate, 4.4 x 8.2-7.0 x 10.1 lam (indistinct in E. ariensis). Apocolpium diameter relatively large, 8.4-11.1 tam. Exine 3.9-5.3 tam thick at the centre of mesocolpium. SEM: Colpi margin undulate, thin and indistinct. Colpus membrane + barren smooth. Sexine reticulate, sometimes coarsely reticulate, lumina pentagonal, hexagonal or elliptic.
PLATE V Type 2. 26-30. E. nulans. LM, optical section in polar view ( x 1000). 26. LM, equatorial view, ornamentation at high focus ( × 1000). 27. LM, optical cross-section in equatorial view ( x I000). 28. SEM, sub-polar view ( x 4000). 29. SEM, equatorial view ( x 4000). 30. E. chamaesyce. SEM, magnified part of exine and colpus ( x 5800). 31. E. nutans. SEM, magnified part of exine and colpus ( x 9500). 32. 33, 34. E. hirta. 33. SEM, part of exine showing indistinct lumina ( × 6000). 34. SEM, part of exine showing distinct perforations ( x 5500). PLATE VI (see p. 306) Type 3. E. caputmedusae. 35. LM, polar view, ornamentation at high focus ( x 1000). 36. LM, polar view of the previous pollen grain, note parasyncolpate at this pole ( x 1000). 37. LM, equatorial view, optical cross-section ( x 1000). 38. SEM, polar view (parasyncolpate at this pole, x 1 I00). 39. SEM, equatorial view ( x 1100). 40. SEM, magnified part of apocolpium, note rugulose exine, beset with dense granules ( x 3800). PLATE VII (see p. 307) Type 4. 41-47. 41. 42. 43. 44. 45. 46. 47. 48.
E. peplus. LM, polar view, ornamentation at high focus ( x I000). LM, polar view, optical cross-section ( x 1000). LM, equatorial view, high focus ( x 1000). LM, equatorial view, optical cross-section ( x 1000). SEM, polar view ( x 2500). SEM, equatorial view ( x 2500). SEM, magnified part of exine showing minute perforations at the bottom of the lumina and thick colpus margin at sides of the os ( x 8500). E. schimperiana. SEM, part of the exine showing microreticulate ornamentation beset with granules and perforation at the bottom of lumina ( x 6400).
305 POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE V
306 PLATE
G.A. EL-GHAZALY AND R. CHAUDHARY VI
(for description see p. 304)
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE VII
( f o r d e s c r i p t i o n see p. 304)
307
GA. EL-GHAZALYAND R. CHAUDHARY
308
Taxa included: E. ariensis var. villicaulis, E. fulgens, E. heterophylla, E. radians.
(3) Sexine not perforated throughout (4) Sexine mainly rugulose
Key to pollen types
(4) Sexine not mainly rugulose (5) Sexine mainly coarsely reticulate
...................................
E. c a p u t m e d u s a e
(type 3) (type 2)
(6) Sexine microreticulate (7) With luminal perforations
....................................... E. bicolor (type 5)
(1) Pollen isopolar (2) Ora with thin margin .......................................
E. n u t a n s
(2) Ora with thick margin (3) Sexine perforated throughout
........................................
...................................
PLATE VIII Type 5. 49-55. E. bicolor. LM, polar view, high focus ( x 1000). 49. LM, polar view, optical cross-section ( x 1000). 50. LM, equatorial view, high focus ( x 1000). 51. LM, equatorial view, optical cross-section ( × 1000). 52. SEM, sub-polar view ( x 2000). 53. SEM, equatorial view ( x 1500). 54. SEM, magnified part of the exine and colpus ( x 4000). 55. E. marginata. SEM, details of exine ornamentation and a colpus ( x 4500). 56. PLATE IX (see p. 310)
E. corollata. LM, polar view, high focus ( x 1000). LM, polar view, optical cross-section ( x 1000). LM, equatorial view, high focus ( × 1000). LM, equatorial view, optical cross-section ( x 1000). SEM, polar view (× 2500). SEM, equatorial view ( x 2500). E. xanti. SEM, details of exine ornamentation ( × 8000). E. corollata. SEM, details of exine ornamentation, arrow shows Ubisch body ( x 10,000).
PLATE X (see p. 311) Type 7. 65-70. 65. 66. 67. 68. 69. 70. 71, 72. 71. 72.
E. p e p l u s
(type 4)
(7) Without luminal perforations
...................................... E. villosa (type l a)
Type 6. 57 62. 57. 58. 59. 60. 61. 62. 63. 64.
(type l b)
...................................... E. f u l g e n s (type 7) (5) Sexine finely reticulate (6) Sexine heterogenous, reticulate to foveolate
(1) Pollen heteropolar ............................
E. m o n t e i r i
E. fulgens.
LM, polar view, optical cross- section ( × 1000). LM, equatorial view, high focus showing ornamentation (× 1000). LM, equatorial view, optical cross-section ( × 1000). SEM, sub-polar view ( × 1700). SEM, equatorial view (× 1700). SEM, details of exine and a colpus ( × 5000). E. heterophylla. SEM, face view at low right corner and sub-polar view ( × 800). SEM, details of exine ornamentation and oral area ( × 4000).
E. c o r o l l a t a
(type 6)
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE
VIII
309
310
G.A. E L - G H A Z A L Y A N D R. C H A U D H A R Y
PLATE IX
57
(for description see p. 308)
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,,
311
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE
X
65
(for d e s c r i p t i o n see p. 308)
66
.
312
Discussion Distinct pollen-morphological diversity in the genus Euphorbia is evident from the seven pollen types recognized in the present study. The exine of examined taxa has an interesting ornamentation, which warrants the creation of the seven pollen types in this genus. Besides, it permits a suggestion of evolutionary relationship between the examined taxa. The pollen grains of Euphorbia caputmedusae and E. tuberculata (type 3) resemble each other closely. Both exhibit a rugulose sexine with granules of different size and they are heteropolar, being parasyncolpate at one pole. These characteristics not only distinguish them from the other species but also point at their close relationship. Another group of closely related taxa are included under the E. fulgens pollen type 7, on the basis of their coarsely reticulate sexine. Similarly, E. peplus and E. schimperiana (type 4), because of their pollen-morphological affinity, seem to be closely related. From the previous examples it is obvious that pollen-morphological characters are extremely useful in the systematics of Euphorbia, in suggesting relationships among the species investigated. Pollen morphology and taxonomy The pollen morphology of some subsections is homogeneous and easily distinguishable; thus, they support the delimitation of the section, e.g. section Poinsettia with coarsely reticulate pollen, and subsection Medusea with heteropolar pollen. However, in other subsections more than one pollen type is observed, e.g. in subsection Esulae three pollen types were described (cf. Table I). The E. villosa pollen type 1 occurrs in species of different subsections and pollen morphology does not fully support the delimitation of any of these subsections. Pollen types will be discussed here by comparing the pollen data with the system of Pax and Hoffmann (1931). Section 1 - Anisophyllum Hooker (1885) considered this section as "a group indefinitely multiplied...". Later, Pax and
G.A. E L - G H A Z A L ¥ A N D R. C H A U D H A R Y
Hoffmann (1931) revised the section and added more subsections. The pollen grains of species in this section (types l a and 2) are generally characterized by a perforate to microreticulate sexine pattern. Occasionally some variations with regard to shape of apertures and sexine pattern are observed that might support the heterogeneity in this section. Clear variation is noticed in E. hirta, particularly in the characteristics of sexine pattern. This species is widely distributed throughout the tropics (Hooker, 1885; Brown et al., 1925), and shows considerable morphological variations that might reflect the variations within pollen morphology. The subsection Chamaesyce was raised to the status of subgenus by Wheeler (1941). In spite of the acceptance of this status by authors today, the pollen morphology of this subsection (E. chamaesyce, E. peplis, E. prostrata, E. thymifolia, and E. humifusa) provides evidence to retain this subsection within section Anisophyllum (Pax and Hoffann, 1931). Both E. sopina (syn. E. maculata) subsection Chamaesyce and E. lata subsection Acutae are placed in section Anisophyllum. However, their pollen morphology differs from those of other species in this section by the presence of ora with thick margin, and suggests their placement in another section with a similar pollen type for example section Rhizanthium. Section 2 - Adenopetalum This section includes three pollen types (5, 6, and 7). The sexine pattern of these types varies from perforate, foveolate, microreticulate to reticulate. This section includes 11 subsections (Pax and Hoffmann, 1931) that indicate heterogeneity in the morphology of the species within the section which is expressed by different pollen types. However, the pollen grains of the species within each subsection are very similar and belong to one pollen type, except in subsection Cyttarospermum, where two pollen types, 6 and 7, are distinguished. This may indicate the homogeneity between the species within each subsection. The pollen grains of subsection Tithymalopsis, pollen type 6, are similar to
313
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
E. xanti of subsection Alectoroctonum, E. ocymoidea of subsection Cyttarospermum and E. hexagona of subsection Zygophyllidium (Table I). However, those of subsection Petaloma (type 5) and subsection Tricherostigma (type 7) are quite different from each other and from other subsections in the section Adenopetalum. Generally, the species of this section are of limited distribution mainly in North America and the northern region of South America. Section 3 - Poinsettia The pollen grains of this section are homogenous, i.e. belonging to one pollen type (type 7) which is characterized by coarsely reticulate sexine. Two species from this section were investigated by us, and E. pulcherrima by Nair (1961). These species show very similar pollen characteristics, and they are native to Mexico. Pollen grains of species belonging to sections 2 and 3 show clear overlapping by the presence of three pollen types (Table I). E. ariensis and E. fulgens of section 2 possess a distinct pollen type 7, which suggests their placement within section 3 to form a natural section with one pollen type. Section 4 - Eremophyton Our study includes three subsections out of the four subsections of this section, i.e. subsection Eueremophyton, subsection Cheirolepidium and subsection Pseudocalypha. The pollen morphology belongs to type 1, in which the sexine is perforate. However, the details of pollen morphology of E. cheirolepis show distinct differences from the other species in the pollen type. A characteristic feature of the pollen of this species is the presence of relatively small apocolpia that are devoid of perforations. Besides, the ora are surrounded by conspicuously thick margine (labia). Such variations are in favor of separating E. cheirolepis from section Eremophyton (Prokhanov, 1949). Section 5 - Lyciopsis The pollen grains of E. polyantha (type lb) from this section are characterized by more or less
rugulose sexine and thick labia. Carter (1985) removed this species to the subgenus Eremophyton, which is not in agreement with the pollen morphology data obtained from our study, mainly because rugulose pollen grains are not observed in section Eremophyton. Section 6 - Pseudeuphorbium This section is not divided into subsections and is characterized by a clearly rugulose sexine and large lolongate ora. These pollen characteristics indicate a close correlation between this section and the previous one. Section 7 - Euphorbia Out of 11 subsections that are included by Pax and Hoffmann (1931) in this section, five species from 4 subsections were investigated. The species E. burmanii, E. tirucalli, and E. virosa have similar pollen type l a that is distinguished by perforate sexine. E. caputmedusae, and E. tuberculata are very distinguished from the other species in this section and may form a separate section (Carter, 1988). In addition the pollen morphology proved that these two species are unsatisfactory placed in section Euphorbia. They belong to pollen type 3, which is observed only in these two species. It is characterized by rugulose, coarsely granulate sexine. In E. caputmedusae ca. 75% of the pollen grains are isopolar and 3-colporate while the rest are heteropolar. In the heteropolar pollen grains the colpi meet just before reaching to one of the poles and form a continuous aperture area similar to the case of parasyncolpate described by Erdtman (1986). On the other pole, the aperture ends do not meet and the apocolpium is generally small. Section 8 - Rhizanthium According to Pax and Hoffmann (1931), this section is not divisible in to subsections. E. tuberosa from this section shows perforate pollen type la which is similar to that observed in many Euphorbia species in this study.
314
G.A. EL-GHAZALY AND R. C H A U D H A R ' t
Section 9 - Tithymalus Out of 22 species described in this section 21 species belong to the two subtypes of pollen type 1. The pollen grains are generally perforate in subtype la with a tendency to-rugulose in subtype lb. Only pollen grains of E. peplus are clearly different from other species of this section. They form a separate pollen type 4, which is distinguished by reticulate, perforate sexine, that characterized them even from all species of Euphorbia examined in this study. E. schimperiana is a widespread species with almost all combinations of variability in its characteristics found throughout its distribution (Carter, 1985). Several characteristics were used to distinguish numerous taxa which have since been placed in synonymy. Similar pollen grains to those of E. peplus pollen type are encountered in many species of Phyllanthus (cf. Bor, 1979) and Andrachne (E1-Ghazaly and Raj, 1986), thus pointing to their natural relationship. E. petiolata, perhaps better known by its syn-
onym E. lanata (Radcliffe-Smith, 1974), is included by Boissier (1862) in a special subsection, Crotonopsideae, of his section Tithymalus. The pollen morphology of E. petiolata (type la) is similar to that of E. cheirolepis of section Eremophyton. This close similarity in pollen morphology, beside other general morphological similarities, supports Radcliffe-Smith (1974) placement of E. petiolata under subgenus Cystidospermum (Prokhanov) Prokhanov (section cheirolepidium Boissier) along with E. cheirolepis.
Geographical distribution of pollen types The geographical distribution of each pollen type found in Euphorbia is summarized in Fig. 1. An attempt is made to consider the native distribution of the species becayse many species of this genus are introduced, cultivated and naturalized. The species belonging to pollen type 1, are widely distributed in Africa, Asia, and South America. They are characterized by a perforate
"4...°
--¢"-x
.-':" ""
[] [It]
"-..
2
. . . .
CY
z; Fig. 1. Map showinggeographicaldistributionof differentpollen types of Euphorbiaspecies. • =Type la; A =Type Ib; [] =Type 2; -* =Type 3; O =Type 4; • =Type 5; -k=Type 6; • =Type 7.
POLLENMORPHOLOGYOF SOMESPECIESOF THE GENUSEUPHORBIAL.
exine that may indicate that the perforate exine type is a basic one. The species of pollen type lb are also widely distributed in Asia, Australia, North Africa, Europe and North America and the southern part of Canada. This type shows a clear transition between the perforate and ___rugulose one. Different shapes of perforations and amalgamation between the perforations are observed. This observation might reflect an intermediate evolutionary step of this species. The species of pollen type 4 are distributed in East Africa and Middle Europe. It shows a characteristic reticulate pattern with perforate lumina which could be a derived case through arrangement and amalgamation of perforations. The distribution of species of pollen belonging to type 3 is even more restricted than the previous one; they are mainly native to the northern part of North America. This type is characterized by perforate, foveolate to clear reticulate patterns in the pollen grains. It shows a clear tendency towards reticulate exine. Such a tendency has been established in pollen type 5 where the species are distributed in the coastal and northern parts of North America. Moreover, a homogeneous reticulate exine is demonstrated in pollen type 6 where the species are native only to Mexico and its adjacent regions. This might indicate the end of an evolutionary trend from a perforate to reticulate pattern. The evolutionary trend towards a reticulate pattern has been presented by Punt (1967) and Meewis and Punt (1983) in the genus Phyllanthus. A particular pollen type is observed in E. caputmedusae and E. tuberculata that are distributed to south Africa. The exine of their pollen is clearly rugulose and beset with coarse granules. In additon, a peculiar aperture type is observed which is a case between tricolporate and parasyncolpate pollen grains.
Putative evolutionary relationship between pollen types Pollen morphology is considered to be a conservative feature of a species. Consequently it provides significant insight into evolutionary relationships and could have a critical role in establishing different taxonomic groupings (Hebda
315
and Chinnappa, 1990). In the present study, an outline of the putative evolutionary relationship between the various pollen types in Euphorbia is shown in Fig. 2 and Plate XI. Pollen type la with pertectate perforate sexine might be the ancestral type. Species belong to this pollen type, e.g.E, tirucalli and E. virosa, display several characters considered primitive, e.g. the frequently 4-5-celled capsules and the more commonly dioecious habit (Leach, 1973). From this ancestral pollen type it seems that two separate evolutionary lines have evolved. On one line the pertectate pollen grains with minute perforations fuse in groups of 2, 3 or 4 and finally differentiate into rugulae of various shape and grooves (type l b). The grooves become very narrow and the rugulae thickened, irregularly oriented and form a cerebroid structure (type 3). The development of pollen type 4 from pollen type l b seems to have taken place as divergence from the rugulose pattern by widening the area of grooves which give general reticulate pattern with perforate lumina. Pollen type 7 may have been derived from the ancestral type (type l a) by gradual change from minute perforations to broadly elliptic and linear oblong perforations (type 5), microreticulate (type 6) and finally reticulate (type 7). Appendix 1. Specimens investigated Euphorbia akenocarpa Gussone, Italy, Sicily, No collector, Herb. No. 8010 [S] E. ariensis Kunth, var. villicaulis Fernald, USA, OK, Corn, Mexiano and Pringle 10116 [S] E. atoto Forster, Papua New Guinea, Woodlark Ist. L.J. Brass 28750 [S] E. atropurpurea Broussonet, Spain, Canary Islands, A. Stork, Herb. No. 8015 [S] E. balsamifera Aiton, Spain, Gran Canaria, Hulten, Herb. No. 8017 [S] E. bicolor Engelmann and Gray, USA, TX, C.L., Lundell 11783 [S] E. bourgaeana J. Gay ex Bossier, Spain, Tenerife, O. Burchard, Herb. No. 8021 [S] E. burmannii Meyer ex Krauss, S. Africa, Cape Province, Clanvilliam, B. Wagine 1051 [S] E. caputmedusae L., S. Africa, Cape Town, Wall, 195 IS] E. cassia Boissier, Syria, Chonchour, Wall, Herb. No. 8024 [S] E. chamaesyce L., Bulgaria, Shumen, B. Kuzmanov, Herb.
No. 8025 [S]
G.A. EL-GHAZALY AND R. CHAUDHARY
316
PLATE XI
317
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
I Type7
E. fulge,ns I
I Type4
Type 6
E. heterophylla L., USA, FL, P.O. Schallert 13207 [S] E. hexagona Nuttall, USA, KS, W.H. Horr and L.H. Franklin
E 276 [S] E. hieronymi Subils, syn. dioica Hieronymus, Mexico, Durango,
I.M. Johnston 7780 [S] E. hirta L., Tanzania, Kibaha, O.Flock 606 [S]; Madagascar,
Marie De Marovoay, W. Kaudern, Herb. No. 8065 [S] Russia, Prov. Primorje, T, Neczaeva 2574 [S] E. hypericifolia L., USA, VA, A.H. Curtiss Herb. No. 19802 [S] E. inundataTorrey ex Chapman, USA, FL, R.K. Godfrey 68487 [S] E. lata Engelmann, USA, TX, B.H. Warnock 46186 [S] E. macropus (Klotzsch and Garcke ex Klotzsch) Boissier, Mexico, Hidalgo, C.G. Pringle, Herb. No. 8043 IS] E. marginata Pursh, USA, KS, W.H. Horr E 36 [S] E. mesembryanthemifolia Jacquin, syn. buxifolia Lamarck, USA, FL, H.N. Moldenke 402 [S] E. monteiri Hooker, Namibia, Karibib, K. Dinter, Herb. No. 8046 [S] E. nutans Lagasca, USA, TX, Gertrude Heller, Herb. No. 8047 [S] E. ocymoidea L., Mexico, Mina, Y. Mexiano 9031 IS] E. peplis L., Italy, Lido, B. Pampanini, Herb. No. 8049 IS] E. peplus L., Algeria, Oran, A. Faure, Herb. No. 8055 [S]; Poland, Sanniki, Drymmer, Herb. No. 8067 [S]; Czechoslovakia, Moravia, G. Sirjaev, Herb. No. 8071 [S] E. petiolata Banks and Solander, syn. lanata Sieber ex Sprengel, Iran, No collector, Herb. No. 8040 [S] E. phylloclada Boissier, S. Africa, Welwitschia, L.E. Kers l l l 3 [S] E. polyantha Pax, Kenya, P.G. Greenway 9765 [S] E. polyphylla Engelmann, USA, FL, T.K. Small, Herb. No. 8053 [S] E. prolifera Hamilton ex Don, India, Punjab, R.R. Stewart 1483 [S] E. prostrata Aiton, Tanzania, H.J. Schliebenn 3840 [S] E. radians Bentham, Mexico, Saltillo, Palmer 53 [S] E. retusa Forsk~tl, syn. cornuta Persson, Iran, E.WalI, Herb. No. 8027 [S] E. rigida Marschall von Bieberstein, syn. biglandulosa Desfontaines, Italy, Sicily, I. Segelberg, Herb. No. 8019 [S] E. scheJ~eri Pax, Kenya, R. Polhill and S. Paulo 933 IS] E. humifusa Willdenow ex Schlechtendal,
t
I
Tvpe3
Types
•caput-medusaeI
t I E.Type lb monteiri I
E. bicolor l
[ E. nutnns [
1
I
Type2
1
Typela E. villosa
I
Fig. 2. Scheme of putative evolutionary relationship between pollen types of Euphorbia. E. cheirolepis Fischer and Meyer, Uzbekistan, Bukhara, N.V.
Androsov, Herb. No. 8026 [S] E. corollata L., syn. apocynifolia Small, USA, GA, No collector,
Herb. No. 8011 IS] E. corollata L., Canada, P. Pierron and V.C. Penn, Herb.
No. 8028 [S] E. curtisii Engelmann, USA, GA, A.H. Curtiss 6822 [S] E. densa Schrenk, lran, Khorassan, E. Wall 4307 [S] E. dracunculoides Lamarck, India, Punjab. No collector, Herb.
No. 8051 [S] E. engleri Pax, Uganda, Motondwe Hill, Drummond and
Hemsley 2908 [S] E. eremophila Cunningham ex Mitchell, Australia, Qld., T.
Mauritzon, Herb. No. 8138 [S] E. esula L., USA, MI, V.A. Dieterle, 1963 IS] E. fulgens Karwinsky ex Klotzsch, Mexico, H. Mohlins, Herb.
No. 8033 IS]
PLATE XI SEM showing magnified parts of exine and aperture to indicate putative evolutionary relationships between the pollen types presented in this study (cf. Fig. 2) 73. A primitive pollen type (la) E. tirucalli ( x 5500) is placed at the base. Two evolutionary parallel lines are suggested: (l) Type la, at the base leads to type lb, e.g. 74. E. polyantha ( x 5000), which developed to type 3, e.g. 74a. E. tuberculata ( x 4000), or to type 4, e.g. 74b. E. peplus ( x 6000). (2) Type la leads to type 2, e.g. 75. E. chamaesyce (x 6000), which developed to type 5, e.g. 75a. E. bicolor ( x 5000), then to type 6, e.g. 75b. E. corollata ( x 4000), which is followed by type 7, e.g. 75c. E. fulgens ( × 5000).
318
E. schimperiana Scheele, Burundi, Muromvya, Reekmanss 10915 [S] E. supina Rafinesque, syn. maculata L., USA, N J, H.N. Moldenke 1303 [S] E. thymifolia L., Japan, Chichi-Jima, Fusure and Nagasawa 7501 IS] E. tirucalli L., Ethiopia, Harar, W. Burger 2598 [S] E. trichadenia Pax, S. Africa, Cape Province, No collector, Herb. No. 8076 [S] E. tuberculata Jacquin, S. Africa, Cape Province, A. Penther, Herb. No. 8073 [S] E. tuberosa L., S. Africa, Bottelary, J.P.H. Acock 434 [S] E. vestita Boissier, Mexico, Hacienda, F. Lyle Wynd and C.H. Mueller 37 [S] E. villosa Waldstein and Kitaibel ex Willdenow, Bulgaria, Ljulia, Kuzmanov, Herb. No. 8084 [S] E. villosa Waldstein and Kitaibel ex Willdenow, ssp. austriaca Steiermark, syn. austriaca Kerner, Austria, Stiria, Rechinger, Herb. No. 8016 [S] E. virosa Willdenow, Namibia, Hanam Plateau, K. Dinter 791 [S] E. wallichii Hooker, Nepal, Lauribinayak, R.P. Chaudhary 598 (TU BOT) E. xanti Engelmann ex Bossier, USA, CA, Palmer 792 [S]
Acknowledgements We are thankful to the Director, Swedish Museum of Natural History, Stockholm for allowing us to collect polliniferous material from the herbarium. The second author is grateful to the Swedish Institute for the support which enabled him to work at the palynological Laboratory, Stockholm. Finally we wish to thank all members of the Palynological laboratory for helping us in many ways, and particularly Mrs Anita Norrthon for typing the manuscript.
References Boissier, E., 1862. Euphorbiaceae. In: A.P. De Candolle (Editor), Prodromus systematis naturalis regni vegetabilis 15(2.1). Masson, Paris, pp. 3-188. Bor, J., 1979. Pollen morphology and the bi-reticulate exine of the Phyllanthus species (Euphorbiaceae) from Mauritius and Rrunion. Rev. Palaeobot. Palynol., 27: 149-172. Brown, N.-E., Hutchinson, J. and Prain, D., 1925. Euphorbiaceae. In: W.T. Thiselton-Dyez (Editor), Flora Capensis, Vol. 5(2). Reese, London, pp. 216-377. Carter, S., 1985. New species and taxonomic changes in Euphorbia from East and Northeast tropical Africa and a new species from Oman. Kew Bull., 40(4): 809-825 Carter, S., 1988. Tribe Euphorbieae, Euphorbia. In: R.M. Polhill (Editor), Flora of Tropical East Africa. Euphorbiaceae 2. Balkema, Rotterdam, pp. 409-531. E1-Ghazaly, G. and Raj, B., 1986. A contribution to the pollen
G.A. E L - G H A Z A L Y A N D R. C H A U D H A R Y
morphology of Andrachne (Euphorbiaceae). Pollen Spores, 28(3/4): 297-310. E1-Ghazaly, G., 1989. Pollen and orbicule morphology of some Euphorbia species. Grana, 28: 243-259. EI-Hadidi, M.N. and Fayed, A.A., 1978. Studies on the genus Euphorbia L. in Egypt. II. Systematic treatment. Taeckholmia, 9: 9-57. Erdtman, G., 1960. The acetolysis method. A revised description. Sven. Bot. Tidskr., 54: 561-564. Erdtman, G., 1969. Handbook of Palynology. Munksgaard, Copenhagen, 486 pp. Erdtman, G., 1986. Pollen Morphology and Plant Taxonomy (Angiosperms). Brill, Leiden, 553 pp. Frean, M., 1983. Sporoderm morphogenesis in Euphorbia obesa and Croton gratissimus. Bothalia, 14:849-856 Hebda, R.J. and Chinnappa, C.C., 1990. Studies on pollen morphology of Rosaceae in Canada. Rev. Palaeobot. Palynol., 64: 103-108. Hesse, M., 1980. Ultrastrukture und Entwicklungsgeschichte des Pollenkitts von Euphorbia cyparissias, E. palustris, und Mercurialis perennis (Euphorbiaceae). Plant Syst. Evol.. 135: 253-263. Heywood, V.H., 1979. Flowering Plants of the World. Oxford Univ. Press, Oxford, 336 pp. Hooker, J.D., 1885. Euphorbiaceae. Flora Br. Ind., 5: 239-477. Khan, M.S., 1964. Taxonomic revision of Euphorbia in Turkey. Notes R. Bot. Gard. Edinburgh, 25(2): 71-161. Khan, R., 1968. Contributions to the pollen morphology of the Euphorbiaceae. J. Palynol., 4: 21-35. Kuzmanov, B., 1963. A taxonomic study of the species of the genus Euphorbia widespread in Bulgaria. IZV. Bot. Inst. Bulg. Akad. Nauk., 12: 121-186. K6hler, E., 1965. Die Pollenmorphologie der biovulaten Euphorbiaceae und ihre bedeutung fiir die Taxonomic. Grana Palynol. 6: 26-120. 33 K6hler, E., 1967. t0ber Beziehungen zwischen Pollenmorphologie und Polyploidiestufen im Verwandschaftsbereich der Gattung Phyllanthus (Euphorbiaceae). Feddes Repert., 74: 159-165. Leach, L.C., 1973. Euphorbia tirucaUi L.; its typification, synonymy and relationships with notes on "Almeidina" and "Cassoneira". Kirkia, 9(1): 69-89. Meewis, B. and Punt, W., 1983. Pollen morphology and taxonomy of the subgenus Kirganelia (Jussieu) Webster (genus Phyllanthus, Euphorbiaceae) from Africa. Rev. Palaeobot. Palynol., 39: 131-160. Nair, P.K.K., 1961. Pollen grains of cultivated plants. II. Bougainvillaea Comm., Hibiscus medik, and Euphorbia pulcherima Willd. J. Indian Bot. Soc., 40:365-381. Oudejans, R.C.H.M., 1989. New names and new combinations in the genus Euphorbia L. (Euphorbiaceae). Phytologia, 67: 43-49. Oudejans, R.C.H.M., 1990. World Catalogue of Species Names Published in the Tribe Euphorbieae (Euphorbiaceae) with their Geographical Distribution. Oudejans, Utrecht, 444 pp. Park, K. and Lee, S., 1988. A palynotaxonomic study of the Korean Euphorbiaceae. Korean J. Plant Tax., 18(2): 69-94. Pax, F. and Hoffmann, K., 1931. Euphorbia. In: A. Engler and K. Prantl (Editors), Die Natiirlichen Pflanzenfamilien, 19C. Engelsmann, Leipzig, 2nd ed., pp. 208-221
POLLENMORPHOLOGYOF SOMESPECIESOF THE GENUSEUPHORBIAL. Pax, F., 1896. Euphorbiaceae. In: A. Engler and K. Prantl (Editors), Die natiirlichen Pflanzenfamilien. 111, 5 Abt. Engelmann, Leipzig, pp. 1-119. Praglowski, J. and Punt, W., 1973. An elucidation of the microreticulate structure of the exine. Grana, 13: 45-50. Prokhanov, J., 1949. Euphorbia. In: B. Schischkin and E. Bobrov (Editors), Flora URSS, 14. Acad. Sci. USSR, Moscow, pp. 304-495. Punt. W., 1962. Pollen morphology of the Euphorbiaceae with special reference to taxonomy. Wenria, 7: 1-I 16. Punt., W., 1967. Pollen morphology of the genus Phyllanthus (Euphorbiaceae). Rev. Palaeobot. Palynol., 3: 141-150. Punt, W., 1972. Pollen morphology and taxonomy of section Ceramanthus s.1. of the genus Phyllanthus (Euphorbiaceae). Rev. Palaeobot. Palynol., 13: 213-228. Punt, W., 1987. A survey of pollen morphology in Euphorbiaceae with special reference to Phyllanthus. Bot. J. Linn. Soc., 94: 127-142. Radcliffe-Smith, A., 1974. The taxonomic position of Euphorbia petiolata and the reduction of E. postff (Euphorbiaceae). Kew Bull., 29(3): 503-505. Radcliffe-Smith, A., 1980. Euphorbiaceae, Euphorbia. In: C.C.
319 Townsend and Evan Guest (Editors), Flora of Iraq, 4(1). Baghdad, pp. 327-362. Radcliffe-Smith, A., 1982. Euphorbia. In: P.H. Davis (Editor), Flora of Turkey and the East Aegean Islands, 7. Univ. Press, Edinburgh, pp. 571-630. Saad, S.I. and El-Ghazaly, G., 1988. Pollen morphology of some species of Euphorbiaceae. Grana, 27: 165-175. Schill, R., 1973. Palynologische (lichtmikroskopische) Untersuchungen an sukkulenten Vertretern der Gattung Euphorbia L. aus Madagaskar. Akad. Wiss. Lit. Mainz Trop. Subtrop. Pflanzenwelt, 2: 151-165. Smith, A.R. and Turin, T.G., 1968. Euphorbia. In: T.G. Turin, V.H. Heywood, N.A. Burges, D.M. Moore, D.H. Valentine, S.M. Waiters and D.A. Webb (Editors), Flora Europaea, 2. Cambridge Univ. Press, Cambridge, pp. 213-226. Weber, E1-Ghobary, M.O., 1985. Pollen morphology of four succulent species of Euphorbia (Euphorbiaceae). An. Asoc. Palinol. Leng. Esp., 2: 75-86. Wheeler, L.C., 1941. Euphorbia subgenus Chamaesyce in Canada and the United States. Exclusive of South Florida. Rhodora, 43: 97-286, pl. 654-668.
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Elsevier SciencePublishers B.V., Amsterdam
Pollen morphology of some species of the genus
Euphorbia L. G a m a l A. E1-Ghazaly a a n d R a m C h a u d h a r y b
aSwedish Museum of Natural History, PalynologicalLaboratory, S-10405 Stockholm, Sweden bDepartment of Botany, Tribhuvan University, Kathmandu, Nepal (Received October 9, 1992; revised and accepted April 7, 1993)
ABSTRACT E1-Ghazaly, G.A. and Chaudhary, R., 1993. Pollen morphologyof some species of the genus EuphorbiaL. Rev. Palaeobot. Palynol., 78: 293-319. The pollen morphologyof sixtyspeciesof the genus Euphorbiahas been examinedwith LM and SEM. The genus has been found to be remarkablyeurypalynous.Seven pollen types have been distinguished.A detailed diagnosis of each pollen type is given.The geographicaldistributionof the pollen types is presented, and a putativeevolutionaryrelationshipbetweenpollen types is suggested.
Introduction
Euphorbia have been published (e.g. Kuzmanov,
Euphorbiaceae is a distinctly eurypalynous family. Various pollen-morphological studies have shown the great diversity of pollen types in this family (Punt, 1962, 1972, 1987; K6hler, 1965, 1967; Khan, 1968; Bor, 1979; Park and Lee, 1988; Saad and E1-Ghazaly, 1988). The genus Euphorbia belongs to the subfamily Euphorbioideae and comprises ca. 2000 species, mainly distributed in subtropical and warm temperate regions (Heywood, 1979). So far, the pollen morphology of this genus has not been examined extensively. Only a few species of Euphorbia were described by Punt (1962), Nair (1961) and Schill (1973). Hesse (1980) examined the pollen wall ultrastructure and pollenkitts of two species of Euphorbia and Frean (1983) described sporoderm morphogenesis in E. obesa. Weber-El Ghobary (1985) did a detailed LM and SEM study on the pollen morphology of four succulent species of Euphorbia and recently E1Ghazaly (1989) investigated in detail the morphology of pollen and orbicules of nine species of Euphorbia by LM and SEM. Several taxonomic investigations on the genus
1963; Khan, 1964; EI-Hadidi, 1978). Moreover, several new names and new combinations in the genus Euphorbia were estated in the floras of different parts of the world, e.g. Flora of Iraq (Radcliffe-Smith, 1980), Flora of Turkey (RadcliffeSmith, 1982), Flora of Tropical East Africa (Carter, 1988), and Flora Europaea (Smith and Tutin, 1968). Recently, Oudejans (1989) published new names and combinations in the genus Euphorbia, followed in 1990 by a comprehensive list of over 10,000 names belonging to the tribe Euphorbieae, including changes, synonyms and misspellings (Oudejans, 1990). In the present study, sixty species of Euphorbia representing different sections according to the classification of Pax (1896) were examined by LM and SEM. The new names and synonyms reported by Oudejans (1989, 1990) were taken into consideration. This study demonstrates the variability within the species of Euphorbia. In addition, the phylogenetic relationships between the types are discussed and taxonomic suggestions based on pollen morphology are presented.
0034-6667/93/$06.00
© 1993 -- Elsevier SciencePublishers B.V. All rights reserved.
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Materials and methods This study is based on polliniferous material of sixty species collected from the herbarium of the Swedish Museum of Natural History, Stockholm [S], acetolysed using Erdtman's (1960) standard acetolysis method. The LM studies were made using a Leitz Wetzlar Dialux microscope with apochromatic oil immersion objective (× 100, N.A.I.32) and periplan eyepieces (G.F., x 10). Measurements were made with oil immersion, and are based on 20 or more pollen grains per species. Exine thickness has been measured in the centre of mesocolpia of pollen grains lying in equatorial view. For SEM, acetolysed pollen grains were suspended in a drop of absolute alcohol, transferred to brass stubs and coated with gold-palladium for 7 min using a Fine Coat ION Sputter JFC 1100. Scanning micrographs were taken with a Jeol JSM 25S-II microscope using Ilford FP4 film. The morphological characteristics of pollen are summarised in Table I. The terminology of pollen grains mainly follows that of Erdtman (1969) and Praglowski and Punt (1973).
Results General description
G . A E L - G H A Z A L Y A N D R. C H A U D H A R Y
than nexine, or equally thick except at the apertures, tectate perforate, rugulose, foveolate, microreticulate and reticulate. Scanning electron microscopy Most pollen grains are pertectate with minute perforations which are single or fuse in groups of 2, 3 or 4; or with broadly elliptic to linear oblong perforations, surface smooth, rarely beset with minute granules or masked with a thin layer. Some taxa have microreticulate to reticulate sexine with tetragonal to hexagonal lumina, with or without minute perforations; rugulose sexine consisting of elongated elements (rugulae), smooth or granular. In some taxa (E. bicolor, E. marginata) the sexine pattern is differentiated into perforate to foveolate or perforate to microreticulate.
Descriptions of the pollen types Type 1 - E. villosa Pollen grains 3-colporate, subprolate to prolate spheroidal, rarely oblate spheroidal and prolate. Outline in polar view rounded, 3-lobed. Sexine smooth, continuous, tectate-perforate to discontinuous +_rugulose. Colpi with usually broad margins and protruding well-developed sexine. Apocolpium diameter 6-11.3.
Light microscopy Subtype la- E. villosa (Plates I,II) Pollen grains generally isopolar, only in some specimens of E. caputmedusae heteropolar, radially symmetrical, rounded to 3-lobed in polar view. P=22.4-59.0 and E = 16.3-47.0 l a m , Subspheroidal to prolate, 3-colporate. Colpi long (17.6-47.2 lam), narrow to wide, sometimes constricted at the equator due to sexine overlappings, and with acute to obtuse ends; margines smooth, straight to wavy. Ora lalongate (2.5 × 4-9.1 x 11.2 txm) to lolongate (6.6 × 5.614.6x 10.3 txm), rarely elliptic or "H"-shaped. Apocolpium diameter varying, 2.9-11.1 (12.5) lam, rarely absent (tendency to syncolpate) or left intact (parasyncolpate?) in E. caputmedusae. Exine 2-5 (5.3) Jam thick at the centre of mesocolpia, thickness decreases towards poles. Sexine usually thicker
LM: pollen grains 3-colporate. Outline in polar view 3-lobed, rarely rounded, 30-45 × 20.2-41.2 Ixm. Colpi 22.6-33.4 lam long with + obtuse ends. Ora lalongate to lolongate, rarely circular, 2.4 × 5.2-9.8 x 7.7 ~tm. Apocolpium diameter 4.6-9.9 Ixm. Exine 2 4.1 tam thick at the centre of mesocolpium. Sexine perforate. SEM: Colpi with broad, sparsely granular, perforate margins. Colpus membrane rarely coarsely granulated. Ora encircled by thick margin. Sexine perforated at apocolpium, very rarely _+nonperforate smooth (E. cheirolepis). Sexine perforations are single or fuse in groups of 2, 3 or 4. Some pollen grains have perforations with granules.
POLLEN MORPHOLOGY
295
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PLATE I
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIAL.
Taxa included." E. atropurpurea, E. balsamifera, E. burmannii, E. cheirolep&, E. hieronymi, E. lata, E. petiolata, E. phylloclada, E. prolifera, E. retusa, E. sopina, E. tirucalli, E. tuberosa, E. villosa, E. virosa.
Subtype lb - E. monteiri (Plates Ill,IV) LM: Pollen grains 3-colporate, subprolate to prolate spheroidal 31.6-57x27.8-46.3 ttm. Outline in polar view rounded to 3-lobed. Colpi 25-47.2 lxm long with _ obtuse ends. Ora lalongate to lolongate, rarely 'H"-shaped, 3 x 5.9-14.6 x 10.3 ~tm. Apocolpium diameter 7.7-11.3 lxm. Exine 3.0-4.1 lam thick at the centre of mesocolpium. Sexine indistinctly perforate. SEM: Colpi relatively narrow with usually smooth margins, thickened at the os region. Colpus membrane granular. Sexine partly consists of elongated elements (rugulae) separated by single or fused perforations in groups located in deep narrow irregular slits. Typical rugulose pattern is mainly found in the central part of mesocolpia; in others sexine areas and at apocolpia usually microreticulate to perforate. Taxa included: E. akenocarpa, E. bourgaeuna, E. cassia, E. densa, E. dracunculoides, E. engleri, E. eremophila, E. esula, E. inundata, E. monteiri, E. polyantha, E. rigida, E. scheffleri, E. trichdenia, E. wallichii.
Type 2 - E. nutans (Plate V) LM: Pollen grains 3-colporate, usually prolate, sometimes subprolate and rarely prolate spheroidal, 23.2 x 16.8-31.7 x 17.0 ttm. Outline in polar view 3-lobed. Sexine tectate perforate to _microreticulate. Colpi 17.6-25.0 ttm long with
299
acute ends, margin narrow, constricted usually at the equitorial region around os. Ora predominantly lalongate, 2.2 x 5.0-2.8 x 5.9 ttm. Apocolpium diameter small, 2.9-5.4 Ixm. Exine 2.0-2.7 ttm thick at the centre of mesocolpium. SEM: Colpi sunken lacking clearly protruding sexine at the os, margin +wavy, membrane smooth, becoming narrow and indistinct towards the poles. Sexine with circular to slit like perforations, rarely +microreticulate with indistinct (masked) lumina, occasionally with a ring (valve) like marginal structure and minute granules. Taxa included: E. atoto, E. chamaesyce, E. hirta, E. humifusa, E. hypericifolia, E. macropus, E. mesembryanthemifolia, E. nutans, E. peplis, E. prostrata, E. thymifolia, E. vestita. Type 3 - E. caputmedusae (Plate VI) LM: Pollen grains 3-colporate, subprolate, 49.2-54.6 x 42.7-46.9 ttm. Outline in polar view rounded to 3-lobed. Sexine rugulose. Colpi 39-43.3 lam long with obtuse ends. Ora lalongate to lolongate, 9 x 11 ~tm. Apocolpium diameter in isopolar pollen grains 7.9-9.7 ~tm. Heteropolar pollen grains are parasyncolpate only at one pole leaving an intact polar area of varying size and shapes. Exine 3.7-4.4 ttm thick at the centre of mesocolpium. SEM: Colpi extended in E. caputmedusae to one pole (parasyncolpate grains) with rather thick margin beset with scattered minute granules and markedly thickened at os region. Colpus membrane densely granular. Sexine rugulose, occasionally microreticulate at apocolpia particularly in heteropolar pollen grains. Rugulae of variable shape, appears cerebroid with granules of different
PLATE I Type 1-6. 1. 2. 3. 4. 5. 6. 7.
1, subtype la. Euphorbia villosa. LM, polar view, ornamentation at high focus ( x 1000). LM, polar view, optical cross-section ( x 1000). LM, Equatorial view, optical cross-section ( x 1000). SEM, polar view ( x 1700). SEM, equatorial view ( x 1700). SEM, magnified part of the exine and an aperture, showing perforate exine and thickened margin at sides of the os ( x 5400). E. petiolata. SEM, perforate exine and colpus with thick margin ( x 4500).
300
size and irregular distribution, often filling the grooves. Taxa included: E. caputmedusae, E. tuberculata.
Type 4 - E. peplus (Plate VII) LM: Pollen grains 3-colporate, prolate spheroidal, 24.1-24.9 x 10 24.0-24.1 jam. Outline in polar view rounded to 3-lobed. Sexine basically microreticulate, becoming reticulate along the colpal margin, especially towards the os. Colpi 16.9-19.1 jam long with +pointed ends. Ora variable in shape, generally lalongate to lolongate, elliptic, rarely "H"-shaped, 3.2 x 3.6-5.4 x 6.8 jam. Apocolpium diameter 6.2-7.4 jam. Exine 2.5-2.7 jam thick at the centre of mesocolpium. SEM: Colpus margin generally narrow, thickened and protruding at the os, with few scattered perforations. Colpus membrane granular. Sexine microreticulate to + irregularly reticulate, rarely perforate, bottom of lumina minutely perforate. Taxa included: E. peplus, E. schimperiana.
G.A. EL-GHAZALYAND E. CHAUDHARY
Type 5- E. bicolor (Plate VIII) LM: Pollen grains 3-colporate, prolate spheroidal, 34.3-39.9 x 30.6-35.3 jam. Outline in polar view rounded to 3-lobed. Sexine varies from tectate perforate to microreticulate. Colpi 24.4-30.9 jam long with + obtuse ends. Ora talongate, 3.2 x 6.64.3 x 8.2 jam. Apocolpium diameter 8.2-9.6 jam. Exine 4.2 jam thick at the centre of mesocolpium, becoming thin near the poles. SEM: Colpus margin wavy, broad with few scattered perforations, wavy. Colpus membrane beset with few scattered granules. Sexine, heterogenous, perforate at apocolpia and centre of mesocolpia, changing gradually to a foveolate, microreticulate or reticulate zone bounded by a sparsely perforate colpus margin. Taxa included: E. bicolor, E. rnarginata.
Type 6 - E. corollata (Plate IX) LM: Pollen grains 3-colporate, generally subpro-
late,
rarely
prolate
spheroidal
and
prolate,
PLATE II Type I, subtype la. 8. E. supina. SEM, magnified part showing a colpus and exine perforation with minute granules ( x 5500). 9, 10. E. cheirolepis. 9. SEM, equatorial view ( x 2000). 10. SEM, polar view, showing small polar area with few perforations ( × 4000). 11. E. tuberosa. SEM, perforate exine and thick colpus margin at sides of the os ( × 3500). 12. E. virosa. SEM, equatorial view, showing perforated exine and thick colpus margin. Note colpus membrane and margin beset with granules ( × 5500). 13. E. atropurpurea. SEM, polar view ( x 2300). PLATE III (see p. 302) Type 1, subtype lb. E. monteiri. 14. LM, polar view, ornamentation at high focus ( × 1000). 15. LM, polar view, optical cross-section (× 1000). 16. LM, equatorial view, optical cross-section ( x 1000). 17. SEM, sub-polar view (× 1500). 18. SEM, equatorial view (x 1500). 19. SEM, magnified part of exine showing fused perforations located in narrow irregular concavities ( × 6500). PLATE IV (see p. 303) Type 1, subtype lb. 20. E. akenocarpa. SEM, polar view ( x 2000). 21. E. polyantha. SEM, detail of exine ornamentation ( x 4000). 22. E. rigida. SEM, ornamentation and colpus with thick margin ( x 4000). 23. E. engleri. SEM, ornamentation and colpus ( x 4000). 24. E. esula. SEM, note thick colpus margin at sides of the os and granular colpus membrane ( x 4000). 25. E. scheffteri. SEM, magnified part showing perforate exine and thick colpus margin ( x 4000).
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
P L A T E II
301
302
G.A. EL-GHAZALYAND R. CHAUDHARY PLATE
III
(for description see p. 300)
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE IV
(for description see p. 300)
303
304
G.A. EL-GHAZALYAND R. CHAUDHARY
25.8-31.3 × 19.3-26.7 tam. Outline in polar view rounded to 3-lobed. Sexine microreticulate. Colpi 17.8-23.8 tam long with +pointed ends. Ora distinctly lalongate, 2 x 6.3-3 x 7.2 tam. Apocolpium diameter 5.3-7.7 tam. Exine 2.4-3.0 tam thick at the centre of mesocolpium. SEM: Colpus margin narrow, slightly wavy, increasing in thickness towards the os. Colpus membrane faintly granular. Sexine microreticulate with slitlike perforations along the colpus margins which are beset with few granules. Taxa included: E. curtisii, E. corollata, E. hexagona, E. ocymoidea, E. polyphylla, E. xanti.
Type 7 - E. fulgens (Plate X) LM: Pollen grains 3-colporate, subprolate to prolate spheroidal, 30.8-40.7 x 25.1-38.5 tam. Outline in polar view rounded to 3-lobed, Sexine clearly reticulate. Colpi 21.2-29.8 tam long. Ora lalongate, 4.4 x 8.2-7.0 x 10.1 lam (indistinct in E. ariensis). Apocolpium diameter relatively large, 8.4-11.1 tam. Exine 3.9-5.3 tam thick at the centre of mesocolpium. SEM: Colpi margin undulate, thin and indistinct. Colpus membrane + barren smooth. Sexine reticulate, sometimes coarsely reticulate, lumina pentagonal, hexagonal or elliptic.
PLATE V Type 2. 26-30. E. nulans. LM, optical section in polar view ( x 1000). 26. LM, equatorial view, ornamentation at high focus ( × 1000). 27. LM, optical cross-section in equatorial view ( x I000). 28. SEM, sub-polar view ( x 4000). 29. SEM, equatorial view ( x 4000). 30. E. chamaesyce. SEM, magnified part of exine and colpus ( x 5800). 31. E. nutans. SEM, magnified part of exine and colpus ( x 9500). 32. 33, 34. E. hirta. 33. SEM, part of exine showing indistinct lumina ( × 6000). 34. SEM, part of exine showing distinct perforations ( x 5500). PLATE VI (see p. 306) Type 3. E. caputmedusae. 35. LM, polar view, ornamentation at high focus ( x 1000). 36. LM, polar view of the previous pollen grain, note parasyncolpate at this pole ( x 1000). 37. LM, equatorial view, optical cross-section ( x 1000). 38. SEM, polar view (parasyncolpate at this pole, x 1 I00). 39. SEM, equatorial view ( x 1100). 40. SEM, magnified part of apocolpium, note rugulose exine, beset with dense granules ( x 3800). PLATE VII (see p. 307) Type 4. 41-47. 41. 42. 43. 44. 45. 46. 47. 48.
E. peplus. LM, polar view, ornamentation at high focus ( x I000). LM, polar view, optical cross-section ( x 1000). LM, equatorial view, high focus ( x 1000). LM, equatorial view, optical cross-section ( x 1000). SEM, polar view ( x 2500). SEM, equatorial view ( x 2500). SEM, magnified part of exine showing minute perforations at the bottom of the lumina and thick colpus margin at sides of the os ( x 8500). E. schimperiana. SEM, part of the exine showing microreticulate ornamentation beset with granules and perforation at the bottom of lumina ( x 6400).
305 POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE V
306 PLATE
G.A. EL-GHAZALY AND R. CHAUDHARY VI
(for description see p. 304)
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE VII
( f o r d e s c r i p t i o n see p. 304)
307
GA. EL-GHAZALYAND R. CHAUDHARY
308
Taxa included: E. ariensis var. villicaulis, E. fulgens, E. heterophylla, E. radians.
(3) Sexine not perforated throughout (4) Sexine mainly rugulose
Key to pollen types
(4) Sexine not mainly rugulose (5) Sexine mainly coarsely reticulate
...................................
E. c a p u t m e d u s a e
(type 3) (type 2)
(6) Sexine microreticulate (7) With luminal perforations
....................................... E. bicolor (type 5)
(1) Pollen isopolar (2) Ora with thin margin .......................................
E. n u t a n s
(2) Ora with thick margin (3) Sexine perforated throughout
........................................
...................................
PLATE VIII Type 5. 49-55. E. bicolor. LM, polar view, high focus ( x 1000). 49. LM, polar view, optical cross-section ( x 1000). 50. LM, equatorial view, high focus ( x 1000). 51. LM, equatorial view, optical cross-section ( × 1000). 52. SEM, sub-polar view ( x 2000). 53. SEM, equatorial view ( x 1500). 54. SEM, magnified part of the exine and colpus ( x 4000). 55. E. marginata. SEM, details of exine ornamentation and a colpus ( x 4500). 56. PLATE IX (see p. 310)
E. corollata. LM, polar view, high focus ( x 1000). LM, polar view, optical cross-section ( x 1000). LM, equatorial view, high focus ( × 1000). LM, equatorial view, optical cross-section ( x 1000). SEM, polar view (× 2500). SEM, equatorial view ( x 2500). E. xanti. SEM, details of exine ornamentation ( × 8000). E. corollata. SEM, details of exine ornamentation, arrow shows Ubisch body ( x 10,000).
PLATE X (see p. 311) Type 7. 65-70. 65. 66. 67. 68. 69. 70. 71, 72. 71. 72.
E. p e p l u s
(type 4)
(7) Without luminal perforations
...................................... E. villosa (type l a)
Type 6. 57 62. 57. 58. 59. 60. 61. 62. 63. 64.
(type l b)
...................................... E. f u l g e n s (type 7) (5) Sexine finely reticulate (6) Sexine heterogenous, reticulate to foveolate
(1) Pollen heteropolar ............................
E. m o n t e i r i
E. fulgens.
LM, polar view, optical cross- section ( × 1000). LM, equatorial view, high focus showing ornamentation (× 1000). LM, equatorial view, optical cross-section ( × 1000). SEM, sub-polar view ( × 1700). SEM, equatorial view (× 1700). SEM, details of exine and a colpus ( × 5000). E. heterophylla. SEM, face view at low right corner and sub-polar view ( × 800). SEM, details of exine ornamentation and oral area ( × 4000).
E. c o r o l l a t a
(type 6)
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE
VIII
309
310
G.A. E L - G H A Z A L Y A N D R. C H A U D H A R Y
PLATE IX
57
(for description see p. 308)
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,,
311
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
PLATE
X
65
(for d e s c r i p t i o n see p. 308)
66
.
312
Discussion Distinct pollen-morphological diversity in the genus Euphorbia is evident from the seven pollen types recognized in the present study. The exine of examined taxa has an interesting ornamentation, which warrants the creation of the seven pollen types in this genus. Besides, it permits a suggestion of evolutionary relationship between the examined taxa. The pollen grains of Euphorbia caputmedusae and E. tuberculata (type 3) resemble each other closely. Both exhibit a rugulose sexine with granules of different size and they are heteropolar, being parasyncolpate at one pole. These characteristics not only distinguish them from the other species but also point at their close relationship. Another group of closely related taxa are included under the E. fulgens pollen type 7, on the basis of their coarsely reticulate sexine. Similarly, E. peplus and E. schimperiana (type 4), because of their pollen-morphological affinity, seem to be closely related. From the previous examples it is obvious that pollen-morphological characters are extremely useful in the systematics of Euphorbia, in suggesting relationships among the species investigated. Pollen morphology and taxonomy The pollen morphology of some subsections is homogeneous and easily distinguishable; thus, they support the delimitation of the section, e.g. section Poinsettia with coarsely reticulate pollen, and subsection Medusea with heteropolar pollen. However, in other subsections more than one pollen type is observed, e.g. in subsection Esulae three pollen types were described (cf. Table I). The E. villosa pollen type 1 occurrs in species of different subsections and pollen morphology does not fully support the delimitation of any of these subsections. Pollen types will be discussed here by comparing the pollen data with the system of Pax and Hoffmann (1931). Section 1 - Anisophyllum Hooker (1885) considered this section as "a group indefinitely multiplied...". Later, Pax and
G.A. E L - G H A Z A L ¥ A N D R. C H A U D H A R Y
Hoffmann (1931) revised the section and added more subsections. The pollen grains of species in this section (types l a and 2) are generally characterized by a perforate to microreticulate sexine pattern. Occasionally some variations with regard to shape of apertures and sexine pattern are observed that might support the heterogeneity in this section. Clear variation is noticed in E. hirta, particularly in the characteristics of sexine pattern. This species is widely distributed throughout the tropics (Hooker, 1885; Brown et al., 1925), and shows considerable morphological variations that might reflect the variations within pollen morphology. The subsection Chamaesyce was raised to the status of subgenus by Wheeler (1941). In spite of the acceptance of this status by authors today, the pollen morphology of this subsection (E. chamaesyce, E. peplis, E. prostrata, E. thymifolia, and E. humifusa) provides evidence to retain this subsection within section Anisophyllum (Pax and Hoffann, 1931). Both E. sopina (syn. E. maculata) subsection Chamaesyce and E. lata subsection Acutae are placed in section Anisophyllum. However, their pollen morphology differs from those of other species in this section by the presence of ora with thick margin, and suggests their placement in another section with a similar pollen type for example section Rhizanthium. Section 2 - Adenopetalum This section includes three pollen types (5, 6, and 7). The sexine pattern of these types varies from perforate, foveolate, microreticulate to reticulate. This section includes 11 subsections (Pax and Hoffmann, 1931) that indicate heterogeneity in the morphology of the species within the section which is expressed by different pollen types. However, the pollen grains of the species within each subsection are very similar and belong to one pollen type, except in subsection Cyttarospermum, where two pollen types, 6 and 7, are distinguished. This may indicate the homogeneity between the species within each subsection. The pollen grains of subsection Tithymalopsis, pollen type 6, are similar to
313
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
E. xanti of subsection Alectoroctonum, E. ocymoidea of subsection Cyttarospermum and E. hexagona of subsection Zygophyllidium (Table I). However, those of subsection Petaloma (type 5) and subsection Tricherostigma (type 7) are quite different from each other and from other subsections in the section Adenopetalum. Generally, the species of this section are of limited distribution mainly in North America and the northern region of South America. Section 3 - Poinsettia The pollen grains of this section are homogenous, i.e. belonging to one pollen type (type 7) which is characterized by coarsely reticulate sexine. Two species from this section were investigated by us, and E. pulcherrima by Nair (1961). These species show very similar pollen characteristics, and they are native to Mexico. Pollen grains of species belonging to sections 2 and 3 show clear overlapping by the presence of three pollen types (Table I). E. ariensis and E. fulgens of section 2 possess a distinct pollen type 7, which suggests their placement within section 3 to form a natural section with one pollen type. Section 4 - Eremophyton Our study includes three subsections out of the four subsections of this section, i.e. subsection Eueremophyton, subsection Cheirolepidium and subsection Pseudocalypha. The pollen morphology belongs to type 1, in which the sexine is perforate. However, the details of pollen morphology of E. cheirolepis show distinct differences from the other species in the pollen type. A characteristic feature of the pollen of this species is the presence of relatively small apocolpia that are devoid of perforations. Besides, the ora are surrounded by conspicuously thick margine (labia). Such variations are in favor of separating E. cheirolepis from section Eremophyton (Prokhanov, 1949). Section 5 - Lyciopsis The pollen grains of E. polyantha (type lb) from this section are characterized by more or less
rugulose sexine and thick labia. Carter (1985) removed this species to the subgenus Eremophyton, which is not in agreement with the pollen morphology data obtained from our study, mainly because rugulose pollen grains are not observed in section Eremophyton. Section 6 - Pseudeuphorbium This section is not divided into subsections and is characterized by a clearly rugulose sexine and large lolongate ora. These pollen characteristics indicate a close correlation between this section and the previous one. Section 7 - Euphorbia Out of 11 subsections that are included by Pax and Hoffmann (1931) in this section, five species from 4 subsections were investigated. The species E. burmanii, E. tirucalli, and E. virosa have similar pollen type l a that is distinguished by perforate sexine. E. caputmedusae, and E. tuberculata are very distinguished from the other species in this section and may form a separate section (Carter, 1988). In addition the pollen morphology proved that these two species are unsatisfactory placed in section Euphorbia. They belong to pollen type 3, which is observed only in these two species. It is characterized by rugulose, coarsely granulate sexine. In E. caputmedusae ca. 75% of the pollen grains are isopolar and 3-colporate while the rest are heteropolar. In the heteropolar pollen grains the colpi meet just before reaching to one of the poles and form a continuous aperture area similar to the case of parasyncolpate described by Erdtman (1986). On the other pole, the aperture ends do not meet and the apocolpium is generally small. Section 8 - Rhizanthium According to Pax and Hoffmann (1931), this section is not divisible in to subsections. E. tuberosa from this section shows perforate pollen type la which is similar to that observed in many Euphorbia species in this study.
314
G.A. EL-GHAZALY AND R. C H A U D H A R ' t
Section 9 - Tithymalus Out of 22 species described in this section 21 species belong to the two subtypes of pollen type 1. The pollen grains are generally perforate in subtype la with a tendency to-rugulose in subtype lb. Only pollen grains of E. peplus are clearly different from other species of this section. They form a separate pollen type 4, which is distinguished by reticulate, perforate sexine, that characterized them even from all species of Euphorbia examined in this study. E. schimperiana is a widespread species with almost all combinations of variability in its characteristics found throughout its distribution (Carter, 1985). Several characteristics were used to distinguish numerous taxa which have since been placed in synonymy. Similar pollen grains to those of E. peplus pollen type are encountered in many species of Phyllanthus (cf. Bor, 1979) and Andrachne (E1-Ghazaly and Raj, 1986), thus pointing to their natural relationship. E. petiolata, perhaps better known by its syn-
onym E. lanata (Radcliffe-Smith, 1974), is included by Boissier (1862) in a special subsection, Crotonopsideae, of his section Tithymalus. The pollen morphology of E. petiolata (type la) is similar to that of E. cheirolepis of section Eremophyton. This close similarity in pollen morphology, beside other general morphological similarities, supports Radcliffe-Smith (1974) placement of E. petiolata under subgenus Cystidospermum (Prokhanov) Prokhanov (section cheirolepidium Boissier) along with E. cheirolepis.
Geographical distribution of pollen types The geographical distribution of each pollen type found in Euphorbia is summarized in Fig. 1. An attempt is made to consider the native distribution of the species becayse many species of this genus are introduced, cultivated and naturalized. The species belonging to pollen type 1, are widely distributed in Africa, Asia, and South America. They are characterized by a perforate
"4...°
--¢"-x
.-':" ""
[] [It]
"-..
2
. . . .
CY
z; Fig. 1. Map showinggeographicaldistributionof differentpollen types of Euphorbiaspecies. • =Type la; A =Type Ib; [] =Type 2; -* =Type 3; O =Type 4; • =Type 5; -k=Type 6; • =Type 7.
POLLENMORPHOLOGYOF SOMESPECIESOF THE GENUSEUPHORBIAL.
exine that may indicate that the perforate exine type is a basic one. The species of pollen type lb are also widely distributed in Asia, Australia, North Africa, Europe and North America and the southern part of Canada. This type shows a clear transition between the perforate and ___rugulose one. Different shapes of perforations and amalgamation between the perforations are observed. This observation might reflect an intermediate evolutionary step of this species. The species of pollen type 4 are distributed in East Africa and Middle Europe. It shows a characteristic reticulate pattern with perforate lumina which could be a derived case through arrangement and amalgamation of perforations. The distribution of species of pollen belonging to type 3 is even more restricted than the previous one; they are mainly native to the northern part of North America. This type is characterized by perforate, foveolate to clear reticulate patterns in the pollen grains. It shows a clear tendency towards reticulate exine. Such a tendency has been established in pollen type 5 where the species are distributed in the coastal and northern parts of North America. Moreover, a homogeneous reticulate exine is demonstrated in pollen type 6 where the species are native only to Mexico and its adjacent regions. This might indicate the end of an evolutionary trend from a perforate to reticulate pattern. The evolutionary trend towards a reticulate pattern has been presented by Punt (1967) and Meewis and Punt (1983) in the genus Phyllanthus. A particular pollen type is observed in E. caputmedusae and E. tuberculata that are distributed to south Africa. The exine of their pollen is clearly rugulose and beset with coarse granules. In additon, a peculiar aperture type is observed which is a case between tricolporate and parasyncolpate pollen grains.
Putative evolutionary relationship between pollen types Pollen morphology is considered to be a conservative feature of a species. Consequently it provides significant insight into evolutionary relationships and could have a critical role in establishing different taxonomic groupings (Hebda
315
and Chinnappa, 1990). In the present study, an outline of the putative evolutionary relationship between the various pollen types in Euphorbia is shown in Fig. 2 and Plate XI. Pollen type la with pertectate perforate sexine might be the ancestral type. Species belong to this pollen type, e.g.E, tirucalli and E. virosa, display several characters considered primitive, e.g. the frequently 4-5-celled capsules and the more commonly dioecious habit (Leach, 1973). From this ancestral pollen type it seems that two separate evolutionary lines have evolved. On one line the pertectate pollen grains with minute perforations fuse in groups of 2, 3 or 4 and finally differentiate into rugulae of various shape and grooves (type l b). The grooves become very narrow and the rugulae thickened, irregularly oriented and form a cerebroid structure (type 3). The development of pollen type 4 from pollen type l b seems to have taken place as divergence from the rugulose pattern by widening the area of grooves which give general reticulate pattern with perforate lumina. Pollen type 7 may have been derived from the ancestral type (type l a) by gradual change from minute perforations to broadly elliptic and linear oblong perforations (type 5), microreticulate (type 6) and finally reticulate (type 7). Appendix 1. Specimens investigated Euphorbia akenocarpa Gussone, Italy, Sicily, No collector, Herb. No. 8010 [S] E. ariensis Kunth, var. villicaulis Fernald, USA, OK, Corn, Mexiano and Pringle 10116 [S] E. atoto Forster, Papua New Guinea, Woodlark Ist. L.J. Brass 28750 [S] E. atropurpurea Broussonet, Spain, Canary Islands, A. Stork, Herb. No. 8015 [S] E. balsamifera Aiton, Spain, Gran Canaria, Hulten, Herb. No. 8017 [S] E. bicolor Engelmann and Gray, USA, TX, C.L., Lundell 11783 [S] E. bourgaeana J. Gay ex Bossier, Spain, Tenerife, O. Burchard, Herb. No. 8021 [S] E. burmannii Meyer ex Krauss, S. Africa, Cape Province, Clanvilliam, B. Wagine 1051 [S] E. caputmedusae L., S. Africa, Cape Town, Wall, 195 IS] E. cassia Boissier, Syria, Chonchour, Wall, Herb. No. 8024 [S] E. chamaesyce L., Bulgaria, Shumen, B. Kuzmanov, Herb.
No. 8025 [S]
G.A. EL-GHAZALY AND R. CHAUDHARY
316
PLATE XI
317
POLLEN MORPHOLOGY OF SOME SPECIES OF THE GENUS EUPHORBIA L.
I Type7
E. fulge,ns I
I Type4
Type 6
E. heterophylla L., USA, FL, P.O. Schallert 13207 [S] E. hexagona Nuttall, USA, KS, W.H. Horr and L.H. Franklin
E 276 [S] E. hieronymi Subils, syn. dioica Hieronymus, Mexico, Durango,
I.M. Johnston 7780 [S] E. hirta L., Tanzania, Kibaha, O.Flock 606 [S]; Madagascar,
Marie De Marovoay, W. Kaudern, Herb. No. 8065 [S] Russia, Prov. Primorje, T, Neczaeva 2574 [S] E. hypericifolia L., USA, VA, A.H. Curtiss Herb. No. 19802 [S] E. inundataTorrey ex Chapman, USA, FL, R.K. Godfrey 68487 [S] E. lata Engelmann, USA, TX, B.H. Warnock 46186 [S] E. macropus (Klotzsch and Garcke ex Klotzsch) Boissier, Mexico, Hidalgo, C.G. Pringle, Herb. No. 8043 IS] E. marginata Pursh, USA, KS, W.H. Horr E 36 [S] E. mesembryanthemifolia Jacquin, syn. buxifolia Lamarck, USA, FL, H.N. Moldenke 402 [S] E. monteiri Hooker, Namibia, Karibib, K. Dinter, Herb. No. 8046 [S] E. nutans Lagasca, USA, TX, Gertrude Heller, Herb. No. 8047 [S] E. ocymoidea L., Mexico, Mina, Y. Mexiano 9031 IS] E. peplis L., Italy, Lido, B. Pampanini, Herb. No. 8049 IS] E. peplus L., Algeria, Oran, A. Faure, Herb. No. 8055 [S]; Poland, Sanniki, Drymmer, Herb. No. 8067 [S]; Czechoslovakia, Moravia, G. Sirjaev, Herb. No. 8071 [S] E. petiolata Banks and Solander, syn. lanata Sieber ex Sprengel, Iran, No collector, Herb. No. 8040 [S] E. phylloclada Boissier, S. Africa, Welwitschia, L.E. Kers l l l 3 [S] E. polyantha Pax, Kenya, P.G. Greenway 9765 [S] E. polyphylla Engelmann, USA, FL, T.K. Small, Herb. No. 8053 [S] E. prolifera Hamilton ex Don, India, Punjab, R.R. Stewart 1483 [S] E. prostrata Aiton, Tanzania, H.J. Schliebenn 3840 [S] E. radians Bentham, Mexico, Saltillo, Palmer 53 [S] E. retusa Forsk~tl, syn. cornuta Persson, Iran, E.WalI, Herb. No. 8027 [S] E. rigida Marschall von Bieberstein, syn. biglandulosa Desfontaines, Italy, Sicily, I. Segelberg, Herb. No. 8019 [S] E. scheJ~eri Pax, Kenya, R. Polhill and S. Paulo 933 IS] E. humifusa Willdenow ex Schlechtendal,
t
I
Tvpe3
Types
•caput-medusaeI
t I E.Type lb monteiri I
E. bicolor l
[ E. nutnns [
1
I
Type2
1
Typela E. villosa
I
Fig. 2. Scheme of putative evolutionary relationship between pollen types of Euphorbia. E. cheirolepis Fischer and Meyer, Uzbekistan, Bukhara, N.V.
Androsov, Herb. No. 8026 [S] E. corollata L., syn. apocynifolia Small, USA, GA, No collector,
Herb. No. 8011 IS] E. corollata L., Canada, P. Pierron and V.C. Penn, Herb.
No. 8028 [S] E. curtisii Engelmann, USA, GA, A.H. Curtiss 6822 [S] E. densa Schrenk, lran, Khorassan, E. Wall 4307 [S] E. dracunculoides Lamarck, India, Punjab. No collector, Herb.
No. 8051 [S] E. engleri Pax, Uganda, Motondwe Hill, Drummond and
Hemsley 2908 [S] E. eremophila Cunningham ex Mitchell, Australia, Qld., T.
Mauritzon, Herb. No. 8138 [S] E. esula L., USA, MI, V.A. Dieterle, 1963 IS] E. fulgens Karwinsky ex Klotzsch, Mexico, H. Mohlins, Herb.
No. 8033 IS]
PLATE XI SEM showing magnified parts of exine and aperture to indicate putative evolutionary relationships between the pollen types presented in this study (cf. Fig. 2) 73. A primitive pollen type (la) E. tirucalli ( x 5500) is placed at the base. Two evolutionary parallel lines are suggested: (l) Type la, at the base leads to type lb, e.g. 74. E. polyantha ( x 5000), which developed to type 3, e.g. 74a. E. tuberculata ( x 4000), or to type 4, e.g. 74b. E. peplus ( x 6000). (2) Type la leads to type 2, e.g. 75. E. chamaesyce (x 6000), which developed to type 5, e.g. 75a. E. bicolor ( x 5000), then to type 6, e.g. 75b. E. corollata ( x 4000), which is followed by type 7, e.g. 75c. E. fulgens ( × 5000).
318
E. schimperiana Scheele, Burundi, Muromvya, Reekmanss 10915 [S] E. supina Rafinesque, syn. maculata L., USA, N J, H.N. Moldenke 1303 [S] E. thymifolia L., Japan, Chichi-Jima, Fusure and Nagasawa 7501 IS] E. tirucalli L., Ethiopia, Harar, W. Burger 2598 [S] E. trichadenia Pax, S. Africa, Cape Province, No collector, Herb. No. 8076 [S] E. tuberculata Jacquin, S. Africa, Cape Province, A. Penther, Herb. No. 8073 [S] E. tuberosa L., S. Africa, Bottelary, J.P.H. Acock 434 [S] E. vestita Boissier, Mexico, Hacienda, F. Lyle Wynd and C.H. Mueller 37 [S] E. villosa Waldstein and Kitaibel ex Willdenow, Bulgaria, Ljulia, Kuzmanov, Herb. No. 8084 [S] E. villosa Waldstein and Kitaibel ex Willdenow, ssp. austriaca Steiermark, syn. austriaca Kerner, Austria, Stiria, Rechinger, Herb. No. 8016 [S] E. virosa Willdenow, Namibia, Hanam Plateau, K. Dinter 791 [S] E. wallichii Hooker, Nepal, Lauribinayak, R.P. Chaudhary 598 (TU BOT) E. xanti Engelmann ex Bossier, USA, CA, Palmer 792 [S]
Acknowledgements We are thankful to the Director, Swedish Museum of Natural History, Stockholm for allowing us to collect polliniferous material from the herbarium. The second author is grateful to the Swedish Institute for the support which enabled him to work at the palynological Laboratory, Stockholm. Finally we wish to thank all members of the Palynological laboratory for helping us in many ways, and particularly Mrs Anita Norrthon for typing the manuscript.
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