SMITHSONIAN CONTRIBUTIONS TO BOTANY NUMBER 50 

Pollen Morphology and 

Phylogenetic Relationships 

of the Berberidaceae 

Joan W. Nowicke 

andJohn J. Skvarla 

SMITHSONIAN INSTITUTION PRESS 

City of Washington 

1981 
ABSTRACT 

Nowicke, Joan W., and John J. Skvarla. Pollen Morphology and Phylogenetic 

Relationships of the Berberidaceae. Smithsonian Contributions to Botany, number 

50, 83 pages, 215 figures, 3 tables, 1981.-Pollen from 68 collections representing 14 genera and 40 species of the family Berberidaceae was examined 

by light microscopy, SEM, and TEM. In part, the pollen data reinforce the 

traditional view of closely related pairs or small groups of genera. In Berberis 

and Mahonia the pollen morphology would support separate family status as 

well as congeneric treatment. The unusual exine structure in Nandina would 

reinforce its treatment as a monotypic family, Nandinaceae. The distinction 

of Bongardia from Leontice and of Dysosma from Podophyllum is confirmed by 

pollen data. The presence of a fundamentally similar tectum in Achlys, 

Dysosma, Epimedium,Jeffsonia, Podophyllum peltatum, P. hispidun, and Vancouveria 

suggests closer relationship among these genera than has been previously 

thought. The _close similarity of the polle-n in Jeffersonia and Plagiorhegma confirms their congeneric treatment, Palynologically, Bongardia, Caulophyllum, and Leontice are more closely related to each other than to any 

remaining genera. In three taxa, Diphylleia, Podophyllum hexandrum, and Rantania, certain characteristic(s) of the pollen render it unique and for the most 

part nullify any systematic value within the family. The pollen morphology 

of the Berberidaceae s. 1. is not similar to that of the Ranunculaceae, Hydrastis 

excepted, nor to Lardizabalaceae. There appear to be unusual examples of 

parallelism between the Berberidaceae and Cistaceae, and between Podophyllum 

and Croton. 

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded 

in the Institution’s annual report, Srnithsonian Year. SERIES COVER DESIGN: Leaf clearing from the 

katsura tree Cercidiphyllurn japonicurn Siebold and Zuccarini. 

Library of Congress Cataloging in Publication Data 

Nowicke, Joan W 

Pollen morphology and phylogenetic relationships of the Berberidaceae. 

(Smithsonian contributions to botany ; no. 50) 

Bibliography: p. 

1. Berberidaceae. 2. Palynotaxonomy. I. Skvarla, John J., joint author. 11. Title. 111. 

QKl.S2747 no. 50 [QK495.B45] 581s [583’.117] 80-21960 

Series: Srnithsonian Institution. Srnithsonian contributions to botany ; no. 50. 
Contents 

Page 

Introduction 1 

Acknowledgments ............................................... 2 

Previous Treatments of the Family ................................... 2 

Materials and Methods 6 

Results and Discussion of Pollen Analyses ............................ 7 

Ektexine Relationships .......................................... 19 

General Discussion .................................................. 21 

Literature Cited ..................................................... 28 

Tables and Figures ................................................... 31 

......................................................... 

.............................................. 

Summary ..................... ................................... 26 

... 

111 

Pollen Morphology and 

Phylogenet ic Relationships 

of the Berberidaceae 

Joan W. Nowicke 

and John J. Skuarla 

Introduction 

The geographical distribution of the flowering 

plants presents some perplexing problems, but 

none more so than that of disjunct or discontinuous genera that, by definition, occupy widely 

separated regions. If these taxa are regarded as 

monophyletic, then it follows, largely by assumption, that either at one time their range must 

have included intervening areas or the taxa have 

fruits and/or seeds with adaptations for long 

distance dispersal. There are, in fact, floristic 

relationships based upon two regions (rarely 

three) having a high number of disjunct genera 

common to both, and it is more logical and 

probable that the high number is an indication 

of a previously more continuous range. The floras 

of eastern North America and eastern Asia are 

one of the classic examples, with as many as 80 

genera having species in both regions. These genera are not randomly spread among the dicots or 

monocots, but tend to be concentrated in the 

more primitive families, one of which is the Berberidaceae. Even in the widest sense this is a small 

family, consisting of 10 to 12 genera and about 

Joan W. "dowzcke, Department of Botany, .Vatzonal ,2luseum oj 

Natural Histoy, Smithsonian Institution, Washington, 

D.C. 20560. John J. Skuarla, Department of Botany and Microbiology, C'niuersib of Oklahoma, Norman, Oklahoma 730l.Q. 

600 species, with as many as 500 of these belonging to Berberis L. 

The genera most commonly regarded as belonging to the Berberidaceae are the following. 

Achlys De Candolle, Berberis L., Bongardia C. A. 

Meyer, Caulophyllum Michaux, Diphylleia Michaux, Dysosma R. E. Woodson, Epimedium L., 

Jeffersonia Barton (Plagiorhegma Maximowicz) , 

Leontice L., Mahonia Nuttall, Nandina Thunberg, 

Podophyllum L., Ranzania Ito, and Vancouveria C. 

Morren and Decaisne. These genera are not considered to be a single closely related group, and 

this is reflected in the fact that few systematists 

have included all in one family. 

Most modern generalists consider the genera as 

primitive or at least unspecialized and place them 

with the Rannuculaceae, Menispermaceae, Lardizabalaceae, and several very small families as 

the Order Ranunculales or even Berberidales. 

This study of pollen morphology in the Berberidaceae is part of an extensive and continuing 

research project on the phylogenetic relationships 

of the Order Centrospermae. This unusual group 

of families with the unique nitrogen-containing 

pigments, the betalains, and distinctive sieve tube 

plastids (Behnke, 1976) has pollen with an ektexine characterized as spinulose and punctate/ 

tubuliferous. This particular surface pattern, 

1 
2 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

found in 85% of the taxa examined, is the predominant type in each of the betalain families as 

well as the two anthocyanin families, Caryophyllaceae and Molluginaceae. Both authors have 

regarded this ektexine type as unspecialized and 

consider that the significance attached to it resides mainly in its high frequency. These results 

have been published in two papers, one based on 

light microscopy and SEM (Nowicke, 1975) and 

the other emphasizing TEM (Skvarla and Nowicke, 1976). 

In the first investigation of families outside the 

Centrospermae, the pollen of the Plumbaginaceae, Polygonaceae, and Primulaceae was examined in a study that combined and integrated 

results from light microsocpy, SEM, and TEM 

(Nowicke and Skvarla, 1977). Examination of 136 

taxa in these families, considered to be related to 

the Centrospermae by various authors, revealed 

a wide range of variation in the ektexines, but not 

the common one in the Centrospermae. The 

Polygonaceae may be one of the most palynologically diverse families in the angiosperms, with 

variation in shape, apertures, tecta, and exine 

structure. 

The Order Ranunculales is the second group 

of families to be investigated palynologically for 

evidence of relationships to Centrospermae. At 

this writing almost 150 species have been examined in the Ranunculaceae, 40 species in the 

Berberidaceae s. l., 14 in the Lardizabalaceae, 

seven in the Coriariaceae, four in the Sabiaceae, 

and three in the Corynocarpaceae. Due to the 

large number of taxa and the general conclusions 

that the palynological data do not support a close 

relationship among any of the above families, the 

decision was made to treat each family in a 

separate publication. 

For purposes of comparison and the reader’s 

convenience, we have included electron micrographs of the common pollen type in the Centrospermae (Figures 1-6) as well as the predominant 

type in the Ranunculaceae (Figures 7-12). 

AcKNowLEDGMENTS.-The authors wish to acknowledge the fine technical assistance of J. L. 

Bittner at the Smithsonian Institution and W. F. 

Chissoe at the University of Oklahoma. The scanning electron micrographs were taken at the 

Scanning Electron Microscope Laboratory at the 

National Museum of Natural History. We thank 

Aaron Goldberg and Harold Robinson for their 

critical review and helpful comments. 

This research was supported in part by a grant 

from the Smithsonian Institution Fluid Research 

Fund to J. W. Nowicke and in part by National 

Science Foundation Grant DEB 75-19846 and 

DEB 80-02585 to J. J. Skvarla. 

Previous Treatments of the Family 

The Japanese botanist Masao Kumazawa 

worked on both the Ranunculaceae and Berberidaceae for a number of years (1930a, 1930b, 

1932a, 1932b, 1935, 1936a, 1936b, 1937a, 1937b, 

1937c, 1938a) and published a paper in 1938 

(193813) in which he reviewed and discussed the 

relationship within and between the families. Kumazawa (1938a:g) regarded both families as including “extremely heterogeneous types” with the 

systematic affinities of some genera still undecided. The Berberidaceae and Ranunculaceae 

have peculiar anatomical features not commonly 

found in dicots: fused cotyledons, trimerous parts, 

V-shaped xylem. The developmental mode of the 

pollen grains and endosperm are more characteristic of the monocots than dicots. 

Although numerous authors have considered 

that the connecting links between the Ranunculaceae and Berberidaceae were to be found in the 

transitional genera Glaucidium-Hydrastis and Podophyllum-Diphylleia, Kumazawa (1 938a) regarded 

the above generic pairs as widely separated, citing 

differences in vegetative structures and anther 

dehiscence, as well as the results from his most 

recent investigation of ovular structures in the 

two families (1938b). 

Kumazawa (1938a: 12) considered Nandina as 

the “farthest deviated” genus in the Berberidaceae; in fact, he would support family status 

based on the combination of vegetative and ovular characteristics as well as a type of anther 

dehiscence not found in any other berberidaceous 
NUMBER 50 3 

genera. He no longer regarded Diphylleia as closely 

related to Podophyllum, the two differing in dehiscence of the anthers, the pollen, and the type of 

vernation. He segregated Podophyllum as a monogeneric family, but left the fate of Diphylleia “for 

consideration” (1938a: 13). For the remaining 

genera, Kumazawa established a Berberidaceae 

consisting of two subfamilies: Berberidoideae 

with only Berberis and Mahonia; and Epimedioideae with three tribes, Epimedeae with Epimedium 

(Vancouveria?) , Leontice (Bongardia?), Caulophyllum, 

Jeffersonia, and Plagiorhegma, Achylieae with Achlys, and Ranzanieae with Ranzania. He cited the 

pollen of Berberis and Mahonia as the most striking 

distinction between the two subfamilies, possibly 

indicating a large phylogenetic gap between 

them. 

Buchheim (1964) maintained the relationship 

of Diphylleia and Podophyllum by segregating the 

two genera in a subfamily, the Podophylloideae. 

The second and much larger subfamily, Berberidoideae, has the remaining genera, but their similarities and distinctions are maintained by the 

establishment of three tribes: Nandineae with 

only Nandina; Berberideae with Berberis, Mahonia, 

and Ranzania; and the Epimedieae with Aceranthus, Achlys, Bongardia, Caulophyllum, Epimedium, Jeffersonia, Leontice, Plagiorhegma, and Vancouveria. His 

concept of the Order Ranunculales, which he 

described for the Syllabus der Pflanzenfamilien, includes the following families: Ranunculaceae, 

Berberidaceae, Lardizabalaceae, Menispermaceae, Nympheaceae, Ceratophyllaceae, and Sargentodoxaceae (only Sargentodoxa) . 

Buchheim’s (1964) interpretations of the relationships of the above families are of significance 

because he also described the Magnoliales, considered, at least by Hutchinson (1959), to be the 

woody counterpart of the Ranunculales. Undoubtedly his treatment of each order benefited 

from the knowledge and perspective provided by 

the treatment of the other. 

Cronquist (1968) placed the Berberidaceae in 

the Order Ranunculales, consisting of Ranunculaceae, Circaeasteraceae, Lardizabalaceae, Menispermaceae, Coriariaceae, Corynocarpaceae, 

and Sabiaceae. In his list (1968:365) of orders and 

families, Podophyllaceae are indicated as belonging to the Ranunculaceae, but no genera are 

listed; Nandinaceae are a part of the Berberidaceae. 

Takhtajan (1969:208) separated Podophyllum 

and Diphylleia as the Podophyllaceae and also 

gave Nandina family status. The remaining genera 

are assumed to be in the Berberidaceae since they 

do not appear elsewhere in his scheme as families. 

In addition to the above families, he regarded 

Lardizabalaceae, Sargentodoxaceae, Menispermaceae, Ranunculaceae, Glaucidiaceae, Hydrastidaceae, and Circaeasteraceae as belonging to 

the Order Ranunculales. 

Hutchinson (1959) designated the second order 

in his division Herbaceae as Berberidales, but the 

Berberidaceae are very reduced, consisting of only 

Berberis and Mahonia; Nandina is placed in a separate family in this order. The remaining berberidaceous genera are united as the Podophyllaceae, 

but placed in the first order, the Ranales (Ranunculales). 

Thorne (1974) designated the first superorder 

in the dicotyledons as the Annoniflorae, which he 

segregated into three orders: the Annonales, the 

largest with about 23 families; the Berberidales 

with six families; and the Nymphaeales with only 

four families. The significant difference between 

Thorne’s concept of the Berberidales and that of 

most other generalists is the addition of the Papaveraceae whose distinction is partially acknowledged by treating it as a suborder. The other 

suborder, the Berberidineae, includes Lardizabalaceae, Sargentodoxaceae, Menispermaceae, Berberidaceae, and Ranunculaceae. Thorne maintained a wide family concept, preferring to recognize the traditional generic alliances as subfamilies or tribes. 

In a more recent study utilizing comparative 

serology, Jensen (1974) concluded: that Berberis 

and Mahonia are very closely related, even congeneric; that Podophyllum and Diphylleia are similar in serological aspect; and that Nandina is very 

similar to the above four genera, but closer to 

Berberis and Mahonia. He also suggested that these 
4 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

five genera be segregated as a unit such as 

subfamily, and the distinction between the above 

be maintained by establishing three tribes. In 

comparing the reactions of other genera to the 

Berberis vulgaris antiserum and to the Podophyllum 

emodi (= P. hexandrum) antiserum, Jensen found 

that Vancouveria and Jeffersonia indicated at least 

some similarities to each system, but Caulophyllum 

and Epimedium had only a very weak reaction to 

each. Jensen also noted that Caulophyllum and 

Leontice are very similar in serological respects. 

But pending further studies, he would place the 

remaining genera of the Berberidaceae, Achlys, 

Bongardia, Caulophy llum, Epimedium, Jeffersonia, 

Leontice, and Vancouveria, in a second subfamily. 

Chapman (1936), in a study of carpel morphology in the Berberidaceae, used serial sections 

to trace the distribution of the vascular bundles 

and proposed that only an original condition of 

three separate, spirally arranged carpels from 

which two distinct lines evolved would satisfactorily explain the present variation. The two lines 

that Chapman suggested would require a fusion 

of the carpels with the loss or suppression of one 

or two. For Berberis, Mahonia, Leontice, and Caulophyllum the distribution of the vascular bundles 

could be the result of suppression of the upper 

two carpels and an expansion of the lowest one. 

In the other line, the two fused carpels found in 

Epimedium, Vancouveria, Nandina, Achlys, Jeffersonia, 

Diphylleia, and Podophyllum could be derived by 

the loss of one carpel in the process of fusion. She 

concluded that the separation of Berberis and 

Mahonia with their independent evolution occurred very early; that the lack of a close relationship of Nandina to the other genera would also 

indicate an early separation; that Jeffersonia and 

Achlys are more closely related to Epimedium than 

to each other; and that the carpel morphology of 

Diphylleia and Podophyllum does not support a close 

relationship to each other. 

According to Kumazawa’s developmental 

studies (1938a) the basilary placentation accorded to Berberis, Mahonia, Caulophyllum, and Achlys is in fact a modification of the parietal placentation found in Epimedium, Nandina, and Plagiorhegma (Jeffersonia), differing only in the area of 

elongation at a later stage. Furthermore, the 

ovules of the basilary types are in reality slightly 

dislocated towards the lateral walls, which also 

supports Kumazawa’s view that parietal placentation is the original type. 

Not all of Kumazawa’s results (1938a) are relevant here, but those on Nandina are significant 

in the later discussion. It was the only genus 

investigated in which the funiculus was absent; 

in the other genera it ranged from very short to 

prominent. Nandina had an atypical micropyle in 

which the outer integument did not project at the 

point of closure. 

The following review of the size and distribution of the berberidaceous genera is essential to 

the discussion of the results of this study. If a 

genus has been the subject of a separate study, 

the pertinent conclusion or observations are included. Closely related genera are discussed together. 

Achlys De Candolle has two species, A. triphylla 

(Smith) De Candolle in Pacific North America, 

and A. japonica Maximowicz from Asia. This is 

the only disjunct genus in the family with a 

Pacific North America and Asia distribution. 

Berberis L. is the largest genus in the family 

with as many as 500 species widely distributed in 

both the Old World and the New World. The 

closely related Mahonia Nuttall, with approximately 75 species, is the second largest genus. 

Although Ahrendt (1961) published an exhaustive study of these two genera, it is unfortunate 

that he did not discuss the relationships of Berberis 

and Mahonia to the remaining berberidaceous 

genera. 

Bongardia C. A. Meyer has a single species, B. 

chrysogonum (L.) Grisebach, found along the Afghanistan-Iran-U.S.S.R. border. It was first described as a species of Leontice by Linnaeus (1 753). 

Caulophyllum Michaux is a disjunct genus of two 

very similar species, C. thalictroides (L.) Michaux 

in eastern North America as far west as Nebraska 

and Missouri, and C. robustum Maximowicz from 

China, Japan, and Korea. The latter sometimes 

has been treated as a variety of the former. 
NUMBER 50 5 

Diphylleia Michaux has three species, one in 

eastern North America, D. cymosa Michaux, and 

two in Asia, D. grayii R. Schmidt in Japan and D. 

sinensis Li from China, and is a disjunct genus. 

Dysosma R. E. Woodson was established as a 

monotypic genus based on Podophyllum pleianthum 

Hance. At that time (1928), Woodson regarded 

all the following taxa as variations of Dysosma 

pleiantha (Hance) Woodson: Podophyllum versipelle 

Hance, P. veitchii Hemsley and E. H. Wilson, P. 

difforme Hemsley and E. H. Wilson, P. esquirolii 

Leveille, and P. ontoi Hayata. Later: Hu (1937) 

transferred two species of Podophyllum: P. delavayi 

Franchet, now Dysosma delavayi (Franchet) Hu 

and P. aurantiocaule Handel-Mazzetti, now 

Dysosma aurantiocaule (Handel-Mazzetti) Hu. 

Epimedium L. and the closely related Vancouveria 

C. Morren and Decaisne were treated by Stearn 

in a monograph published in 1938. He reduced 

two monotypic genera, Aceranthus C. Morren and 

Decaisne, and Vindicta Rafinesque, to Epimedium 

since the type species for each was E. diphyllum 

Loddiges; but he maintained the generic status 

of Vancouveria, citing a group of morphological 

distinctions that occur only individually in various species of Epimedium. 

Stearn (1938) recognized 21 species of Epimedium, all with an Old World distribution, but 

remarked on the difficulty of assessing their relationships to each other, the characteristics seeming to be either on a generic level and applicable 

to all, or on a species level and applicable to one. 

He did segregate the 21 species into eight small 

groups which he then placed in two sections 

defined by the origin or position of the leaves: 

section Rhizophyllum in which all leaves are 

basal with only one “group” of two species; and 

section Phyllocaulon in which all leaves are attached to the flowering stem, with the remaining 

seven “groups” and 19 species. Stearn (1938:428) 

based the four subsections, some of which include 

more than one “group,” on the number of leaves 

on the floral stem, but noted that “this is liable to 

some variation.” After attempting to verify the 

identification of some voucher specimens, the 

authors would agree. 

For Vancouveria, Stearn (1938) recognized three 

species: V. hexandra (Hooker) C. Morren and Decaisne, the most common and the most widely 

distributed (California, Oregon, and Washington), and V. chrysantha Greene and V. planipetala 

Calloni, both found in California and Oregon. 

The report of V. hexandra from Vancouver Island 

or continental Canada is apparently erroneous; 

Stearn did not see any collections from these 

regions. 

Jeffersonia Barton has two species, J. diphylla 

(L.) Persoon from eastern North America, and J. 

dubia (Maximowicz) Bentham and Hooker, which 

occurs in southeastern Manchuria, adjacent Korea, and eastern Siberia. The disjunct status of 

Jeffersonia depends on the validity of the reduction 

of Plagiorhegma dubia Maximowicz; most authors 

follow Bentham and Hooker in this, Hutchinson 

excepted (1959). 

Leontice L., an Old World genus of eight to 10 

species, is sometimes given separate family status, 

the Leonticaceae (Airy-Shaw, 1966), including 

Bongardia and Cau lop hy llum. 

Nandina Thunberg is a monotypic genus from 

China whose distinctions have been acknowledged by Chapman (1936), Ernst (1964), Kumazawa (1938a), and most generalists. 

Podophyllum L. is a disjunct genus with one 

species, P. peltatum L., very common in the eastern 

half of North America, and an uncertain number, 

but not more than four or five species, distributed 

in eastern Asia. The present authors follow Soejarto, Faden, and Farnsworth (1979) in the use of 

Podophyllum hexandrum Royale rather than P. emodi 

Wallich for the most common .4sian species. 

Rantania Ito is a monotypic genus with the 

single species, R. japonica (Ito) Ito, restricted to the 

northern part of Honshu, the largest of the Japanese Islands. Kumazawa (1937~) concluded 

after a detailed study that this species did bear 

some resemblance to Caulophyllum and Epimedium, 

but that it also had in the stamens, petals, and 

fruit some of the restricted or peculiar characteristics found in Berberis and Mahonia. He proposed 

that R. japonica represented an intermediate type 
6 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

and was not as closely related to the Epimedieae 

as he had previously thought. 

The cytological data on the genera of the Berberidaceae are almost complete and are of significance to “General Discussion” herein. The following reports were taken from Darlington and 

Wylie (1956): Achlys 2n = 12; Berberis x = 14, 2n 

= 28, 56; Bongardia x = 6, 2n = 14; Caulophyllum 

x = 8, 2n = 16; Dzphylleia x = 6, 2n = 12; 

Epimedium x = 6, 2n = 12; Jeffsonia x = 6, 2n = 

12; Mahonia x = 14, 2n = 28; Nandina x = 10, 2n 

= 20; Podophyllum x = 6, 2n = 12; Rantania x = 7, 

2n = 14; Vancouveria x = 6, 2n = 12. Leontice 

armeniaca with 2n = 14, and L. leontopetalum with 

n = 8 + lB, and 2n = 16, were taken from 

Ornduff (1968). Six genera, Achlys, Dzphylleia, 

Epimedium, Jeffersonia, Podophyllum, and Vancouveria, have chromosome number of 2n = 12. 

There are two monotypic genera, Glaucidium 

Siebold and Zuccarini and Hydrastis Ellis ex L., 

that are always included in the Order Ranunculales and are associated with Berberidaceae and 

Ranunculaceae but at different levels of recognition. Wettstein (1935) placed both genera in the 

Berberidaceae; Cronquist (1 968) included both 

in the Ranunculaceae; Hutchinson (1959) divided the Ranunculaceae s. 1. into the Ranunculaceae S.S. and Helleboraceae with both genera in 

the latter family; Takhtajan (1969) acknowledged 

their distinction from the Ranunculaceae, from 

the Berberidaceae, and from each other by separate family status, Glaucidiaceae and Hydrastidaceae. Thorne (1974: 187) summarized their 

characteristics and relationships as follows. 

Hydrastrs and Glaucidium, sometimes placed with the Berbericadeae or as a distinct family, do have the berberidaceous 

rhizomatous habit of growth and Gluuczdium frequently has 

only one carpel. However, their flowers have numerous 

stamens, many to two carpels or one carpel, no petals or 

nectaries. and their leaves are simple and palmately lobed. 

They are distinguishable from the other Ranunculaceae by 

the absence of nectaries, ovules with longer outer integument. rather fleshy fruit, and distinctive haploid chromosome numbers of n = 10 and 13. Their chemistry is very 

similar to that of the other Ranunculaceae (Hammond, 

1955: Jensen, 1968) but they possess several alkaloids in 

common also with the Berberidaceae (Willaman and Schubert, 1961). They seem better treated as an intermediate 

group but close enough to the other ranunculads to warrant 

subfamily treatment in the Ranunculaceae (Kumazawa, 

1938; Buchheim, 1964). 

The most comprehensive study of the pollen of 

the Berberidaceae to date may well be a paper 

published in 1936 which also included the Ranunculaceae and Lardizabalaceae. Kumazawa 

(1936a) provided descriptions and discussions for 

46 genera and 230 species with 72 illustrated by 

line drawings. Although his terminology differs 

somewhat from those currently in vogue, there is 

no problem in translation, e.g., expansion furrow 

being the equivalent of colpus. He recognized 

four pollen types based on apertures: Type 0, 

inaperturate; Type I, 3-zonocolpate, rarely 6-8- 

zonocolpate; Type 11, pantocolpate; and Type 

111, pantoporate. Shce Kumazawa (1936a) regarded Diphylleia as pantoporate, and Berberis and 

Mohonia as inaperturate, the Berberidaceae, in his 

estimation, had all four types. 

In a more recent contribution, Roland-Heydacker (1974) described the pollen of Berberis 

vulgaris L. and Mahonia aquifolium Nuttall as having unique helicoid colpi as well as a compacted 

ektexine, a granular endexine, and a persistent 

intine that reacted positively to tests for polysaccharides. 

Materials and Methods 

The pollen of 40 species assigned to 14 genera 

in the Berberidaceae (Table 1) has been examined 

in light microscopy (LM) and in scanning electron microscopy (SEM) and a limited number in 

transmission electron microscopy (TEM) . The 

pollen of three species from the Order Centrospermae (Table 2) and seven from the Ranunculaceae (Table 3) have also been included. Anthers were removed from herbarium specimens 

and all material acetolyzed according to procedures outlined in Erdtman (1966). Samples for 

SEM were vacuum coated with gold and examined with a Cambridge Stereoscan MK IIa, and 

S410, or a Coates and Welter 106B Field Emission 

Microscope. 
NUMBER 50 7 

Samples for the TEM were incorporated into 

agar, dehydrated through increased concentrations of ethyl alcohol, and subsequently embedded in araldite-epon resins (Skvarla, 1973). Pollen 

samples were stained in 0.125% OsO4 in 0.1 M 

sodium cacodylate buffer for two hours prior to 

agar incorporation. Thin sections were made with 

diamond knives, collected on uncoated grids and 

stained with uranyl acetate and then lead citrate. 

Electron microscope observations were made with 

a Philips model 200 transmission electron microscope. 

Light slides of all samples are deposited at the 

Palynological Laboratory, Department of Botany, Smithsonian Institution. 

The species examined, the collector and number, and country or U.S. state, as well as figure 

number(s) if illustrated, are given in Tables 1, 2, 

and 3. For the most part the names used are 

taken from the herbarium label or the most recent 

annotation; each collection sampled was similar 

to those remaining of a particular species as identified. For most of the disjunct berberidaceous 

genera, the geographical location, North America 

as opposed to Asia, provided sufficient identification for the purposes of this study. 

The investigation of the Berberidaceae is part 

of a study comparing pollen morphology of the 

Ranunculales with that in the Centrospermae 

and detailed measurements and/or descriptions 

are usually not included. However, within the 

Berberidaceae s. 1. a significant difference in size, 

as indicated by polar length, does distinguish two 

groups of genera from each other. Size could have 

been a factor in the transfer of Hydrastis L. from 

the Ranunculaceae to the Berberidaceae. For this 

reason the longest dimensions of ten grains in 

collections of Berberidaceae and Ranunculaceae 

were recorded. The high, low, and the mean are 

given in Tables 1 and 3, respectively; these figures 

should be treated with reserve in view of the small 

sample size. 

The results from the pollen investigation of 

each genus are presented first, along with a discussion of the generic relationships as indicated 

by palynology. A general discussion follows and 

attempts to evaluate and integrate the pollen 

data with those from vegetative and floral morphology (Kumazawa 1930a, 1930b, 1932a, 1932b, 

1935, 1936a, 1936b, 1937a, 193713, 1938a, 1938b; 

Takeda, 1915; Terabayashi, 1977, 1978), carpel 

morphology (Chapman, 1936), serology Uensen, 

1974), and cytology as reported by Darlington 

and Wylie (1956) and Ornduff (1968). 

Results and Discussion of Pollen Analyses 

Pollen from three families in the Centrospermae is illustrated in Figures 1-6: Anacampseros 

fifamentosa Sims (Portulacaceae), Figures 1, 2, has 

an aperture condition that can be described as 

pantocolpate but the configuration and the shape 

of the individual "colpi" are not always uniform, 

the tectum is spinulose and perforate: Tunica 

stricta (Bunge) Fischer and Meyer (Caryophyllaceae), Figures 3, 4, has a pantoporate aperture 

type and a tectum that is spinulose and sparsely 

punctate; Acrodon bellidiflorus N. E. Brown (Aizoaceae), Figures 5, 6, is 3-colpate with a tectum 

that has been described as reticulate (Radulescu, 

1974), but the size of the perforations varies 

within a sample and those illustrated in the high 

magnification micrographs are, in fact, unusually 

large. 

The possibility of a close relationship between 

the Berberidaceae and any families in the Centrospermae is unlikely, but most taxonomists consider the Berberidaceae and Ranunculaceae to be 

closely related and for this reason the latter family 

is illustrated by seven species: in SEM, Figures 

7-18, in TEM, Figures 115-123, and in the data 

of Table 3. It should be noted that the following 

discussion of Ranunculaceae pollen is based on 

the examination of almost 150 species (Nowicke 

and Skvarla, unpublished data). 

Ranunculus oreophytus Delile (Figures 7, 8) and 

Hepatica transsilvanica Fuss (Figures 15, 16) have a 

pantocolpate aperture condition: Clematis heracleifolia De Candolle (Figures 9, 10) has apertures 

best described as pores but neither their shape 

nor their distribution over the surface of the grain 

is uniform; Glaucidium palmatum Siebold and Zuc- 
8 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

carini (Figures 1 1, 12), Batrachium aquatile Dumortier (Figures 13, 14), and Hamadryas magellanica 

Lamarck (Figures 17, 18) have a 3-colpate condition. All six species have, in a general sense, a 

spinulose and punctate/perforate tectum. 

Many of the Ranunculaceae taxa examined in 

thin section have prominent or very large columellae, e.g., Ranunculus oreophytus (Figure 115), 

Batrachium aquatile (Figure 1 19), Hamadryas magellanica (Figure 121), and to a lesser extent in 

Clematis heracleifolia (Figure 1 17) and in Hepatica 

transsilvanica (Figure 120). Glaucidium palmatum 

(Figure 118) illustrates reduced columellae, a condition that is found in Aconitum (Nowicke and 

Skvarla, unpublished data) and Adonis (Nowicke 

and Skvarla, 1980, fig. 158). For the most part 

the pollen in this family has a well developed 

endexine layer (Figures 115, 116, 118, 120, 121). 

The perforations of the tectum, obscure in SEM 

(Figures 8, 10, 12, 14, 16, 18), are more conspicuous in thin section. Hydrastis canadensis L. (Figures 122, 123), will be discussed with the tribe 

Epimedieae. 

There is an unusual characteristic, demonstrated only in transmission microscopy, that is 

common to some Berberidaceae and to some 

Ranunculaceae: columellae-shaped ektexine 

units penetrate the endexine in the apertures 

(hereafter referred to as aperture columellae) . 

This condition has been found in all species of 

Ranunculus examined in TEM, illustrated here by 

R. oreophytus (Figure 116), in Batrachium aquatile 

(Figure 119), and in Hepatica transsilvanica (Figure 

120). It is also present in some species of Anemone 

and some species of Clematis (Nowicke and 

Skvarla, 1980, figs. 155, 156). In the Berberidaceae s. l., it is most conspicuous in the two closely 

related genera Epimedium and Vancouveria (Figures 

149, 154, 155, 159, 160, 161; see discussion of 

these genera). 

Santisuk (1979) investigated the pollen of 124 

taxa in the tribe Ranunculeae using light and 

scanning electron microscopy and established 10 

pollen types “based on the types of columellae 

and aperture and on the nature of the tectum” 

(Santisuk, 1979:3). For the same taxa his data 

and ours do not conflict (Nowicke and Skvarla, 

unpublished data). 

In addition to the Ranunculaceae all modern 

generalists (see “Introduction”) consider the Lardizabalaceae to be closely related to the Berberidaceae. The results from pollen studies do not 

support this contention. For the most part the 14 

species examined in the Lardizabalaceae have 

similar pollen: 3-colpate, the tectum can be psilate with punctae, or indentations, or finely punctate-striate; in thin section the tectum is the most 

conspicuous unit of the ektexine, the columellae 

are diminutive in size and sparsely distributed, 

the foot layer is very thin, the endexine is well 

developed in the region of the colpus but very 

reduced in the mesocolpus (Skvarla and Nowicke, 

unpublished data). 

We are of the opinion that most of the taxonomic difficulty associated with the Berberidaceae s.1. can be attributed to exceptional and 

restricted sporophytic characteristics: the perianth absent in Achlys, multiseriate in Nandina; 

petals spurred and/or retroflexed in Epimedium 

and Vancouveria; stamens tactile in Berberis, Mahonia, and Rantania; filaments connivent in Vancouveria; the fruits bladder-like in Bongardia and 

Leontice, follicle-like in Epimedium and Vancouveria, 

horizontally cleft in Jeffersonia; seeds large, fleshy, 

and glaucous in Caulophyllum; the habit woody in 

Berberis, Mahonia, and Nandina, and semisucculent 

in Bongardia and Leontice. 

Close scrutiny of the entire sections “Results 

and Discussion of Pollen Analyses” and “General 

Discussion” will reveal that the authors have not 

been consistent, from genus to genus, on the 

degree of importance attached to the same palynological characteristics. The endexine layer is a 

case in point: it is taxonomically significant in 

Nandina, but insignificant in all remaining genera; 

another, the condition in which the pollen is shed 

(monads versus tetrads) is significant in only one 

species and insignificant in all the remaining ones. 

The above statements are not intended to justify 

or validate any or all of the generic realignments 

proposed here, but to point out that we have been 

forced to evaluate irregular pollen data against 
NUMBER 50 9 

an already uneven background of floral and vegetative morphology. 

Within the Berberidaceae the following range 

of variation was found in apertures, tectum, and 

exine structure. There are three types of apertures, irregular or spiral found in Berberis and 

Mahonia, 6-pantocolpate in Ranzania, and 3-colpate, found in all the remaining genera examined. 

The tectum can be psilate, punctate, punctatestriate, finely reticulate, striate, striate-reticulate, 

two layers of striae, “random” rods (small, variously distinct rods with one end projecting outward), spinose, or gemmate, with some of the 

categories grading into another. The structure of 

the exine is typical of angiosperms: foot layer, 

columellae, and tectum for all genera except Berberis, Mahonia, and Rantania, which have an unstratified exine. 

Berberis L. (Figures 19-24, 124-132), and Mahonia Nuttall (Figures 25-30, 133-138) are considered to be closely related by generalists and specialists alike (see “Introduction”). The pollen of 

all species examined (Table 1) in these two genera 

is very similar (Figures 19-30, 124-138) and cannot be distinguished from each ,other using LM, 

SEM, or TEM. Of far greater significance than 

the expected similarity of the pollen is the fact 

that the unifying characteristics are unmistakably 

primitive and serve to emphasize the extent of 

the separation of Berberis and Mahonia from the 

remaining genera. 

Within the taxa examined in Berberis and Mahonia the shape and extent of formation of the 

apertures, i.e., some grains appear inaperturate, 

is highly variable but could be classified as either 

irregular or spiral. The irregular category applies 

to grains with cracks or breaks, e.g., Berberis fendleri 

A. Gray (Figures 2 1, 22), B. grandflora Turczaninow (Figure 24), Mahoniafremontii (Torrey) Fedde 

(Figures 25, 26), M. oiwakensis Hayata (Figure 

29), and M. haematocarpa (Wooton) Fedde (Figure 

30). Occasionally the “furrows” delimit the surface of the grain into plate-like areas, e.g., M. 

fremontii (Figure 25) or M. oiwakensis (Figure 29). 

More rarely some grains have areas with pebbleshaped pieces of exine, e.g., B. ilicfolia Forster 

(Figure 19). The spiral apertures could be designated as preformed but the configuration of the 

furrows is not uniform, e.g., Berberis vulgaris L. 

(Figure 23) and Mahonia nervosa (Pursh) Nuttall 

(Figures 27, 28). 

Kumazawa, who examined four species of Berberis and two of Mahonia, made the following 

points about their germinating apparatus (1936a: 

35). 

(1) The margin of the furrow expanded is irregularly 

denticulated in surface view, suggesting the breaking of the 

exine. 

(2) In some cases no furrows are found on the surface of 

the shrunken and swollen pollens. 

(3) There is no rule concerning the position of the furrow. 

(4) The shrunken pollens with furrows may represent the 

reshrunken form of the swollen pollens. 

The surface of the exine is unspecialized and 

randomly variable: punctate, psilate and punctate, psilate, or punctate-striate occur within a 

species or even within a sample, e.g., Mahonia 

fremontii (Figures 25, 26). 

In thin section the exine structure of Berberis 

(Figures 124- 132) and Mahonia (Figures 133- 138) 

are indistinguishable from each other. The ektexine is nearly amorphous and not organized into 

typical foot layer, columellae, and tectum units. 

Because of this lack of structural organization the 

pollen of Berberis and Mahonia was examined in 

both the acetolyzed and unacetolyzed conditions. 

Following acetolysis, the ektexine contains numerous channels and cavities of a highly pleomorphic nature, which for purposes of this discussion are classified as follows: (1) some completely bisect the ektexine (Figures 128, 130, 136), 

(2) some partially bisect the exine and occur with 

sufficient frequency as to resemble highly irregular columellae (Figures 125, 126, 128, 131-133), 

and (3) some channels appear as irregular, isolated, open holes in the ektexine (Figures 125, 

126, 128, 129, 131, 133). Without acetolysis there 

appears to be a fourth category of channels: 

extremely short, abundant, randomly oriented 

and “closed” or filled with electron-dense material (Figure 124). 

The primary difference between the examination of acetolyzed and unacetolyzed ektexine im- 
10 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

ages is that of stain density: the images from 

acetolyzed grains have considerably greater density than those from unacetolyzed grains. This no 

doubt explains the appearance or visibility of the 

fourth category of channels. Whether or not the 

lack of staining of unacetolyzed pollen was due 

to the dried (i.e., herbarium) nature of the pollen 

before processing is not known and certainly it 

would be useful in future work to collect pollen 

directly from the field and immediately process 

for TEM. This might clarify the nature of the 

thin electron-translucent layer or membrane(?) 

found on the ektexine of unacetolyzed Berberis 

(Figure 124) pollen. The extent of such a layer or 

specificity (it was not observed in Mahonia, Figure 

138) as well as its equivalence to the fibrousgranular extra-ektexinous layer as indicated in 

the acetolyzed preparation of Berberis ilicifo lia 

(Figure 13 1) is not clearly understood at this time. 

In the aperture regions the ektexine is represented as knobs or isolated fragments (Figures 

127, 132, 134-136). It appears identical in acetolyzed and unacetolyzed preparations. 

The endexine in Berberis (Figures 124- 127, 130- 

132) and Mahonia (Figures 133-137) is prominent 

and consists of a fibrous-granular layer; the inner 

surface is smooth and/or uniform but at the 

interface with the ektexine the endexine appears 

to partially fill or encroach upon the cavities and 

channels. It is present in the apertures and appears to support the ektexine fragments. The 

endexine is not noticeably altered by acetolysis. 

The presence of irregular cavities (Figures 124- 

132) and the concomitant segregation of material 

suggest an early stage of columellae development. 

In the six species of Berberis, the mean diameter 

ranges from a low of 38.4 pm in B. uulgaris to a 

high of 50.6 pm in B. grandiflora; in the four species 

of Mahonia, the low is 34.1 pm in M. haematocarpa 

and 33.8 pm in M. oiwakensis and the high is 51.2 

pm in M. neruosa. This degree of size variation is 

not unexpected since Berberis is known to have 

tetraploid entities as well as diploid; Mahonia has 

not, to our knowledge, been reported as having 

either a haploid number of 28 or a diploid number of 56; this does not deny the existence of 

polyploidy in Mahonia. 

Our results agree with those of Roland-Heydacker (1974), except for her characterization of 

all(?) apertures as spiral. 

The presence of irregular apertures, a surface 

that is psilate or nearly so, and above all the 

unstratified exine, are primitive characteristics 

and are in agreement with the phylogenetic position accorded Berberis and Mahonia by most systematists. 

Ranzania japonica (Ito) Ito (Figures 139- 148), 

although widely cultivated in the United States, 

has a very restricted distribution, northern Honshu, Japan. Kumazawa (1936a) described the 

pollen and illustrated it with line drawings 

(1936a:fig. 67,, 671, 672), but for purposes of 

comparison the authors preferred to examine the 

pollen of Ranrania in SEM and TEM. 

Despite its appeal as an ornamental plant, none 

of the major U.S. herbaria had specimens identified as such. The material finally obtained (Table 1) consisted of one pollen sample sent from 

Japan by Terabayashi; one flowering specimen, 

partially dried, from the garden of a private 

individual in New York State, Epstein s.n.; and 

all material at the Royal Botanic Gardens, Kew, 

only two collections, one from a cultivated plant, 

the other a sterile specimen collected by Tukeda 

s.n., 27 August 1905 in the vicinity of Mount 

Shirouma, in Honshu. 

The sample from Japan (Terabayashi 154 KYO) 

was examined in LM and SEM and is illustrated 

in Figures 139 and 140. Although the grains were 

not numerous, they were uniform in size, shape, 

aperture type, and the surface of the exine, and 

the two in Figure 139 are representative. They 

also appear to be a dyad (see TEM discussion of 

Figure 147). The configuration of the six colpi is 

such that there are four threefold axes delineating 

the surface of the grain into four triangular areas. 

Most of the colpi have rounded ends and the 

resulting uniform width gives the impression of a 

precise aperture formation. The opening is frequently blocked by a protruding wedge of exine. 

The surface of the grain is psilate. 
NUMBER 50 11 

The cultivated specimen from New York was 

examined in LM, SEM, and TEM, but illustrated 

here only in TEM, Figures 142, 143, and 146. In 

the SEM preparation about one-third of the 

grains appear to be sterile, based on the much 

smaller size. The remaining material, frequently 

collapsed or ruptured, etc., is also variable in size, 

but intact grains measure 25-35 pm in diameter. 

The apertures are 6-pantocolpate, and almost all 

grains, including the smaller ones, manifest this 

condition to some extent, i.e., less than six furrows, the furrows extended so that some grains 

have a wide angle L-shaped opening but even in 

collapsed and ruptured material the furrows are 

straight and not irregular cracks or breaks as in 

Berberis and Mahonia, Figures 19-30. 

Most of the minimal pollen sample from the 

cultivated collection (K) was prepared for TEM 

(Figures 141, 144, 145, 147, 148) but a small 

fraction was acetolyzed and examined in SEM. 

This material consists of a single expanded grain, 

ca 19 pm in diameter, and a half dozen clusters 

of collapsed grains, with as few as three and as 

many as ten. None of the grains had any evidence 

of apertures, neither the irregular cracks of Berberis 

and Mahonia, Figures 19-30, nor the 6-pantocolpate type as illustrated in Figure 139. The surface 

of the collapsed grains has a remarkably uniform 

texture, similar to small pebbles with no space 

between adjacent ones. 

The pollen morphology in the collections of 

Terabayashi and the cultivated one from New 

York agrees with that described and illustrated 

by Kumazawa (1936a). 

The pollen morphology found in the cultivated 

collection from Kew is perplexing due to the 

apparently complete absence of apertures. None 

of the grains split or ruptured, nor did the pattern 

of collapse suggest internal lines of weakness. If 

the pollen is considered to be anomalous or abnormal, the lack of any other aberrations (in the 

limited material examined in SEM), such as small 

grains, is in itself peculiar. 

The two collections of Rantania examined by 

TEM are basically similar in that both show a 

nearly amorphous ektexine and fibrous-granular 

endexine. The ektexines in the New York State 

collection (Figures 142- 143) are highly channeled 

and virtually indistinguishable from sections of 

acetolyzed pollen from Berberis and Mahonia (Figures 125- 136). The endexine, however, in contrast 

to Berberis and Mahonia, is proportionately thicker 

and contains fragments of the ektexine (Figures 

142-143). Further, the outer (i.e., distal) surface 

of the endexine appears lamellate in some sections 

(Figures 142-143). The New York State collection 

apparently contained some heteromorphic or 

anomalous pollen: the oblique section represented 

by Figure 146 is of a whole pollen grain and 

indicates an ektexine that appears more gemmate 

or nodular than the amorphous structures illustrated in Figures 142-143. The ektexine from 

pollen of the Kew collection (Figures 141, 144- 

145) differs from the New York State collection 

in that it appears to contain extremely short, 

narrow to broad, irregular columellae and a thin 

but distinguishable foot layer (see particularly 

Figure 145). The sections represented by Figures 

147 and 148 include dyad representatives in this 

collection and indicate that binding of adjacent 

grains is by fusion of their ektexine surfaces. Since 

pollen samples of Rantania were so limited we 

were unable to prepare any samples without acetolysis. 

Both Kumazawa (1938a) and Buchheim (1964) 

had very similar concepts of a tribe Epimedieae. 

The former placed Epimedium with Leontice, Caulophyllum, Jeffersonia, and Plagiorhegma as the tribe 

Epimedieae, but it is unclear whether Vancouueria 

is reduced to Epimedium, and whether Bongardia is 

reduced to Leontice, since neither genus is listed 

under any other subfamily or tribe. The latter 

author included Achlys, Bongardia, Caulophyllum, 

Epimedium, Jeffersonia, Leontice, and Vancouveria in 

the tribe Epimedieae. The only difference is that 

Kumazawa placed Achlys in its own tribe, Achly ieae. 

All of the above genera have grains that are 3- 

colpate, the colpi long and narrow, and have an 

incomplete tectum. The structure of the exine in 

all of these genera conforms with the common 

type in the angiosperms: foot layer, columellae, 
12 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

and tectum, with the endexine present in varying 

amounts and distribution. 

The present authors’ use of the tribe Epimedieae is more restricted and includes Achlys, Epimedium, Jeffsonia, and Vancouveria. 

Epimedium L. (Figures 31-36, 94, 99, 104, 105, 

110, 112, 114, 149-156), the largest genus in the 

Epimedieae with at least 25 species distributed in 

the Old World, has a range of variation in the 

tectum with phylogenetic implications since it 

links various entities of the family. For the most 

part we follow Stearn’s (1938) treatment of Epimedium and Vancouveria. 

It should be emphasized that the designation 

applied to the tectum in each of the following 

species is based on the most common form. Almost all samples had sufficient variation to indicate a link to other species. 

Epimedium diphyllum (Morren & Decaisne) Loddiges (Figures 31, 32, 149), E. cremeum Nakai 

(Figures 1 14, 15 1 - 154), E. grandiflorum Morren 

(Figures 11 2, 155, 156), and E. sempervirens Nakai 

(Figures 33, 34, 110) all have a tectum consisting 

of small rods with one end projecting as a very 

small tip. These rods are illustrated best in the 

high magnification SEMs (Figures 32, 34, 110, 

112, 114). Although the distribution of the rods 

appears to be random, there are some grains in 

which the free tips are arranged like the vanes of 

a pinwheel. This configuration is also found in 

Podophyllum peltatum (Figures 77, 78, 109, 11 1, 

113). The similarity of the pinwheel tectum to 

the crotonoid one (Lynch and Webster, 1975) is 

discussed under “Ektexine Relationships” at the 

end of the palynological section. 

Epirnedium alpinum L. (Figures 36, 104), classified here as having a striate-reticulate tectum, 

nonetheless has lost some of the distinction of the 

individual striae. 

The tectum of Epimedium brevicornu Maximowicz (Figures 35, 105, 150) is also classified as 

striate-reticulate, but, of the species of Epirnedium 

examined, it has, at least in some grains, the 

longest and most distinct striae. A predominantly 

striate condition such as that found in Achlys 

DeCandolle (Figures 49-5 1, 96, 175- 179), Jeffersonia Barton (Figures 43-48, 93, 95, 98, 107, 170- 

174), and Vancouveria planipetala Calloni (Figures 

37, 38, 101, 102, 165-169) very likely exists in 

Epimedium, but not in the specimens available for 

this study. 

Epimedium membranaceum K. Meyer (Figure 94) 

and E. sagittatum (Siebold & Zuccarini) Maximowicz (Figure 99) have a perforate tectum in 

which only the angular shape of the perforations 

and occasional long ridge (muri or striae?) indicate that it is a modification of the striate-reticulate type, 

Four species, Epimedium brevicornu (Figures 35, 

105, 150), E. cremeum (Figures 114, 151-154), E. 

diphyllum (Figures 3 1, 32, 149), and E. grandifllorum 

(Figures 112, 155, 156) were examined in thin 

section, and found to be almost indistinguishable 

from each other. The endexine is present only in 

the apertures and is penetrated by aperture columellae (see previous discussion of Ranunculaceae). This condition is illustrated in Figure 149 

of Epimedium diphyllum and in the higher magnification sections in Figure 154 (E. cremeum) and 

especially in Figure 155 (E. grandzjorum). The foot 

layer is thin, irregular and with notable radial 

channels (Figures 150, 153, 156). Columellae are 

short and fairly regular. The structure of the 

tectum in Figures 149, 153, 154, and 155 is consistent with that depicted in SEM (Figures 3 1-34, 

110, 112, 114); the gaps reflect the loose packing 

of the rods, and the small peaks reflect their free 

tips. In Figures 150, 151, and 152 the unattached 

dots or circles represent a cross section of the free 

tip. 

The mean polar length calculated for each of 

the eleven collections of Epimedium (Table 1) 

ranges from 28.2 pm for E. diphyllum to 33.9 pm 

for E. brevicornu and E. sagittatum. 

In Epimedium and closely allied genera-Achlys 

(Figure 177), Jeffersonia, Vancouveria (Figures 157- 

160, 163)-and in all material of Bongardia (Figure 193), Caulophyllum (Figures 184, 188, 189), and 

of Leontice (Figures 180-183) that was examined 

in thin section, the foot layer has radially oriented 

channels. These channels separate the foot layer 

into units that appear to be the result of colu- 
NUMBER 50 13 

mellae expanding laterally at the base. Since the 

foot layer is formed developmentally in this manner, it seems more likely that these channels 

should be interpreted as evidence of incomplete 

fusion as opposed to the idea that they have 

formed in an already solid wall. 

The three species of Vancouveria Morren and 

Decaisne (Figures 37-42, 97, 100-102, 157- 169) 

have ektexines in which the variation illustrates 

a near perfect continuum in the degree of distinction of the individual striae: V. hexandra Morren 

and Decaisne (Figures 39, 40, 100, 160-164) is 

finely striate-reticulate; V. chrysantha Greene (Figures 41, 42, 97, 157-159) is striate-reticulate with 

the striae more prominent than V. hexandra; and 

I.’. planipetala Calloni (Figures 37, 38, 102, 165- 

169) has a & striate ektexine. 

Each species was examined in thin section: 

Vancouveria chrysantha, Figures 157- 159; I.’. hexandra, Figures 160-164; and V. planzpetala, Figures 

165-169. ,411 are similar to Epimedzum, Figures 

149- 156: the endexine is restricted to the aperture 

regions and has aperture columellae, and there 

are channels in the foot layer. Differences in the 

structure of the tectum among the three species 

are in agreement with the differences illustrated 

by SEM: the more open striate-reticulate pattern 

of V. chrysantha, Figure 97, is reflected in the 

irregularity and gaps of the tectum, Figures 157- 

159; the finely striate-reticulate pattern of V. 

hexandra, Figures 40 and 100, is reflected in the 

more continuous tectum illustrated in Figures 160 

and 163: the mostly striate pattern of V. planipetala, Figures 38, 101, and 102, reflects this condition in Figure 166 and in the lower grain in 

Figure 169 in which the tectum appears to consist 

of a “string of beads” due to the mostly parallel 

striae being cut at right angle. 

Within Vancouveria the difference between the 

mean polar length of the two collections of V. 

hexandra, 34.6 pm for Allen 66 and 39.4 pm for 

Ebert s.n., was greater than differences among the 

three species; however, both collections were cited 

as V. hexandra by Stearn (1938). 

The American species of Jeffersonia Barton, 

(Figures 43-48, 93, 95, 98, 107, 170-174),J. diphylla (L.) Persoon (Figures 46-48, 98, 107, 170, 

17 1) and the Asian representative,]. dubza (Maximowicz) Bentham and Hooker (Figures 43-45, 

93, 95, 172-174), have grains that are 3-colpate 

with a striate ektexine. 

In each of five collections examined (Table 1) 

there are some grains in which the individual 

stria appears to consist of an outer or surface 

section and an inner or subsurface section. In the 

high magnification SEMs of both species (Figures 

45,48, 93, 95, 98, 107), at least some of the surface 

striae are branched and can be traced to the point 

where they sink, alter direction, and become part 

of the inner layer. 

One logical interpretation of such exine structure is that it provides a strong wall by the 

lamellation of cross grained layers since the long 

axis of the striae in the outer layer is at right 

angle or less to the long axis of the striae in the 

inner layer. 

In Figure 45 ofJeffersonia dubia and especially 

in Figure 48 of J. diphylla the wider spacing of the 

striae in both layers produces the effect of one 

layer of slats upon another. In the Pennsylvania 

collection of J. diphylla (Figures 47, 48, 98), the 

surface striae are shorter, are not closely packed 

and are deposited in a patchwork design, whereas 

in the New York collection (Figures 46, 107) the 

surface striae are longer, more densely packed, 

and with a nondescript or interwoven pattern. 

Most of the grains in each collection of]. dubia 

(Figures 43-45, 93, 95) have tecta in which the 

surface striae are parallel; in Figure 93 of the 

Korean collection some of the distinction of the 

individual striae has been lost. 

This particular tectum type, designated here as 

“two layers of striae,” is widely distributed in the 

dicots: Aceraceae (Clarke and Jones, 1978; Biesboer, 1975), Cneoraceae (Lobreau-Callen et al., 

1978), Cistaceae (Saenz de Rivas, 1979; Nowicke 

and Skvarla, unpublished data), Gentianaceae 

(Jonsson, 1973), Leguminosae (Graham and Barker, in press; Larsen, 1975). 

In TEM, the pollen ofJe&sonia (Figures 170- 

174) has a narrow, smooth to fragmented endex- 
14 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

ine, the foot layer appears very uneven, irregular, 

and has occasional channels, and the columellae 

are not well formed. In J. diphylla (Figure 171) the 

oblique angle of section has somewhat distorted 

the characteristics of the various layers but the 

endexine is present in non-apertural regions. In 

Figure 172 of J. dubia, the median section (at right 

angle to the long axis) depicts the endexine as 

thin and fragmented except near the apertures. 

The foot layer is not uniform and has channels, 

and the tectum consists of almost touching circular units, which is how the mostly parallel striae 

of J. dubia would appear in cross section (see also 

Vancouveria planipetala, Figure 169). In Figures 173 

and 174 the endexine is more uniform than in 

Figure 172. In Figure 174 there are small units of 

3, 4, 5, or even 6 circles connected below by a 

solid line. This probably represents a cut that is 

at right angle to the outer striae and parallel with 

part or all of an inner stria. 

The striate tectum of Jeflersonia pollen (Figures 

43-48, 93, 95, 98, 107) is similar to that of Vancouveria planipetala (Figure 102), Achlys triphylla 

(Figures 49-51, 96) and especially to that of 

Hydrastis (Figures 52-54). Comparison of the high 

magnification SEMs of J. dubia (Figure 45) and J. 

diphylla (Figure 48) with some whole grains of 

Hydrastzs (Figures 53 and 54) reveals the same 

type of structure: two layers of striae. The size of 

the Jeffersonia pollen (the mean of the five collections, reported in Table 1, varies from 29.3 pm to 

33.9 pm), would support a closer relationship to 

Achlys, Epimedium, Vancouveria, and even Hydrastis 

t han to Bongardia , Caulop hy llum , and Leont ice. 

None of the sections of Jeffsonia (Figures 171- 

173) have apertures with ektexinous material that 

could be designated, with confidence, as aperture 

columellae (see discussion of Ranunculaceae, 

Epimedium, and Vancouveria) . 

The pollen morphology of Jeflersonia is taxonomically significant in the following ways: the 

distinction of J. diphylla (Figures 46-48, 98, 170, 

17 1) from Podophyllum (Figures 73-78, 8 1-84, 9 1, 

106, 109, 11 1, 113, 198-202) supports the separate 

generic status accorded by Barton (1 793); the 

similarity of the pollen in the American (Figures 

46-48, 107) and Asian (Figures 43-45, 93, 95) 

taxa supports the congeneric status of Jeffersonia 

and Plagiorhegma. This does not, however, deny 

any palynological relationship between Jeffsonia 

diphylla and Podophyllum peltatum: there are occasional grains in J. diphylla (Figure 107) with a 

tectum that is similar to some grains of P. peltatum 

in which one of the pinwheel vanes (small rods) 

is predominant (Figure 108). 

The genus Achlys De Candolle is represented 

by numerous collections of A. triphylla (Smith) De 

Candolle (Figures 49-51, 96, 175-177), but only 

by a depauperate type collection of A. japonica 

Maximowicz (Figures 178, 179). The two collections examined of the American species have 

grains that are 3-colpate and have a striate tectum. The only pollen sample of A. japonica, Terabayashi 209 (KYO), was unsatisfactory due to a 

paucity of material and evidence of sterility. 

Some of the grains, however, are 3-colpate with 

a tectum similar to that of A. triphylla (Figure 49), 

i.e., coarse striae mostly parallel to each other. 

In TEM (Figures 175-179), the endexine is 

thin in the mesocolpal regions and thicker near 

the apertures (Figure 175), the foot layer uneven 

with occasional channels and is much thicker 

than the endexine. The columellae are narrow 

and short, the tectum is thick and the striae 

appear to be closely packed. As in Jeffirsonia 

(Figures 170- 174) none of the sections of Achlys 

have clearly defined aperture columellae. 

In comparing the striate grains of Achlys, JefferSonia, and Vancouveria planipetala, the striae in Achlys and in V. planipetala are usually parallel and 

more compacted than in either species of JefferSonia. All of the above have the same fundamental 

ektexine structure but modifications in the deposition of the striae produce variation in the 

tectum. There are, in fact, grains in each of the 

collections examined that have striae similar to 

that in Figure 43, and are indistinguishable from 

each other (Calder and Savile 8323 and Terabayashi 

209 of Achlys excepted). 

Although the two collections of Achlys triphylla 

had a high incidence of sterility, which could 

negate a size characteristic, the longest grains in 
NUMBER 50 15 

the Evert sample are 28.6 pm and in the Calder and 

Savile sample, 33.0 pm. 

The pollen morphology of Hydrastis canadensis 

L. (Figures 52-54, 103, 122, 123) has considerable 

taxonomic significance: the striate-reticulate tectum (Figures 52-54, 103, 122 and 123) distinguishes this species from all other Ranunculaceae 

examined, 1 50 species and 44 genera (illustrated 

here by Figures 7-18, 115-121), including Glaucidium (Figures 11, 12, 118), with which it is 

frequently paired. 

The two collections (Table 3) examined in 

SEM have grains that are slightly different, but 

this type of variation is not uncommon in the 

Berberidaceae (nor Ranunculaceae) . The collection from Arkansas (Figures 52 and 103) is similar 

to some grains of Epimedium alpinum (Figure 104), 

E. breuicornu (Figure 105), and Jeffersonia diphylla 

(Figure 107). The collection from Ohio, illustrated by a polar and equatorial view (Figures 53 

and 54), has a tectum that closely resembles that 

found in many grains of Jeffersonia diphylla (Figure 

48), in which two layers of striae can be seen. 

In thin section (Figures 122, 123), the structure 

of the exine in Hydrastis is also different from that 

in the Ranunculaceae (Figures 115-121). The 

prominent columellae and more or less continuous tectum that characterize many Ranunculaceae examined in thin section (Skvarla and Nowicke, unpublished data) are not found in Hydrastis. 

This conforms with impressions based on SEM 

micrographs. 

Achlys, Epimedium, Hydrastis, Jeffersonia, and Vancouueria have pollen with 3-colpate apertures, a 

tectum that is striate or striate-reticulate with 

overlapping variation, an endexine (mostly) in 

the region of the aperture, channeled foot layer, 

and a thin tectum. 

On the basis of all taxa examined to date in 

the Order Ranunculales, more than 250 collections in Ranunculaceae, Berberidaceae, and Lardizabalaceae, only five genera, Achlys, Epimedium, 

Hydrastis, Jeffsonia, and Vancouveria (four of which 

have three species or less), have the pollen morphology described above. As such the palynological data challenge the inclusion of Hydrastis in 

the Ranunculaceae, as well as the close relationship with Glaucidium. 

In Leontice L. (Figures 61-66, 69-72, 180-183), 

an Old World genus with as many as 10 species, 

the pollen of L. altaica Pallas (Figures 61, 62), L. 

armeniaca Boivin (Figures 65, 66, 180-182), L. 

eversmannii Bunge (Figures 7 1, 72), L. leontopetalum 

L. (Figures 69, 70, 183), and L. odessana Fischer 

(Figures 63, 64) were examined. All have similar 

grains: the colpi are very long, almost to the poles 

(Figures 61-63,65,69, 71, 72); the margins sometimes undulate (Figure 61); the tectum is almost 

continuous in L. altaica (Figures 6 1 , 62) and in L. 

odessana (Figures 63, 64), but in L. armeniaca (Figures 65, 66), L. leontopetalum (Figures 69, 70), and 

in L. eversmannii (Figures 71, 72), the tectum is 

incomplete and the lumina are smaller near the 

colpi, and/or larger in the mesocolpus. 

In thin section Leontice armeniaca (Figures 180- 

182) and L. leontopetalum (Figure 183) have a welldeveloped endexine, a foot layer with radial channels, small irregular columellae, and a thick, perfor ate t ec t um . 

In the disjunct genus Caulophyllum Michaux 

(Figures 55-60, 184-189), two collections of each 

of the two entities have been examined (Table 1). 

The results are ambiguous with reference to the 

status of the Asian taxon, either as a species, C. 

robustum Maximowicz (Figures 55, 56, 59, 184), or 

as a variety of the American species, C. thalzctroides 

(L.) Michaux (Figures 57, 58, 60, 185-189). 

All four collections (Figures 55-60) have very 

similar pollen, long narrow colpi (Figures 55, 57) 

with an incomplete or reticulate tectum (Figures 

55-60), and would be difficult to distinguish from 

each other using light microscopy. 

In TEM (Figures 184-189), both species of 

Caulophyllum have a consistent endexine, readily 

defined in the mesocolpal regions (Figures 184, 

189) as well as in the colpus (Figures 184, 188), 

an irregular foot layer, short columellae, and an 

incomplete tectum. Channels (Figure 184) or 

even gaps (Figure 189) are present in the foot 

layer. 

The pollen of Caulophyllum closely resembles 

that of Leontice. The tecta of C. robustum (Figure 
16 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

55) and C. thalictroides (Figure 57) are almost 

indistinguishable from L. leontopetalum (Figure 69) 

and L. euersamannii (Figure 71). The exine structure of C. robustum (Figure 184) is almost indistinguishable from that of L. leontopetalum (Figure 

183). Both genera have larger pollen, the mean 

polar lengths of the five species of Leontice as listed 

in Table 1 are 48.8 pm, 54.7 pm, 43.7 pm, 55.1 

pm, and 46.5 pm, and in the two collections of 

each species of Caulophyllum, 51.5 pm, 50.2 pm, 

48.9 pm, and 45.1 pm. 

The pollen of the monotypic genus Bongardia 

C.A. Meyer (Figures 67, 68, 190-197) has grains 

that are 3-colpate with an incomplete tectum of 

an apparently reticulate configuration. The high 

magnification (X 7500) SEM of the surface (Figure 68) and the tangential thin section (Figure 

195) illustrate lumina or perforations (?), angular 

in shape and not noticeably larger in the mesocolpal region, and “muri,” without small perforations, all of which could indicate a modification 

of an originally striate-reticulate tectum. 

Bongardia chysogonum (L.) Grisebach (Figures 

67, 68, 190-197) was first described as a species 

of Leontice and in SEM the tectum of Bongardia is 

remarkably similar to that found in some grains 

of at least one species of Leontice, L. altaica. The 

larger size (the two collections recorded in Table 

1 have a mean of 48.9 pm and 54.5 pm) would 

align Bongardia with Leontice and Caulophyllum. 

However, in thin section in TEM (Figures 190- 

193, 195-197) and fracture in SEM (Figure 194), 

the pollen of Bongardia can be distinguished from 

all other taxa examined in the family, including 

L. altaica, by the presence of long columellae 

(Figures 190, 193, 194, 196). which may account 

for 75% of the thickness of the ektexine, whereas 

in Leontice (Figures 180, 183) or in Caulophyllum 

(Figures 184, 188, 189) the columellae are very 

short, making up less than 20% of the total thickness. The magnitude of the difference is such that 

Bongardia could be identified in LM alone, but it 

is transmission microscopy that reveals the different structure under a very similar surface. The 

foot layer, with radial channels (Figure 193), is 

thicker and more prominent than the tectum. 

Typically, the endexine is prominent in the region 

of the colpus (Figures 190, 192, 196), and much 

thinner, almost absent, in the mesocolpus. 

Certain characteristics of the pollen support a 

relationship among Bongardia, Caulophyllum, and 

Leontice. All three have large grains (relative to 

Achlys, Epimedium, Hydrastis, Jeffersonia, and Vancouveria) and a tectum that is reticulate. The 

difference between the tectum of Bongardia-angular-shaped lumina and uniformly thin “muri” 

without small perforations (Figure 68)-and that 

found in Caulophyllum and in Leontice-circular 

lumina and “muri” that are variable in size but 

frequently larger than the lumina (Figures 56, 

58-60, 70, and 72)-suggests different origins. 

The variation in the size of the lumina in Caulophyllum and Leontice indicates derivation from a 

tectum that was continuous, whereas in Bongardia 

the restriction of a tectum to the distal fusion of 

long, narrow, and evenly distributed columellae 

indicates that this condition was original, or if it 

has evolved from a continuous tectum, then a 

very long period of time must have occurred. 

However subtle the above distinctions (long columellae, angular lumina, thin muri) may appear 

to nonpalynologists, the data reinforce the separate generic status accorded Bongardia on other 

bases. 

None of the material examined in Bongardia, 

Caulophyllum, and Leontice (two, four, and five 

collections, respectively) have any grains that 

might indicate a relationship to the tectum in the 

tribe Epimedieae, and Podophyllum peltatum. Achlys, 

Epimedium, Jeffersonia, Vancouveria, Bongardia, CauLophyLlum, and Leontice do have in common the 

channeled foot layer. 

There are a number of generic pairs in the 

Berberidaceae that undoubtedly are closely related, Berberis (Figures 19-24) and Mahonia (Figures 25-30), Epimedium (Figures 3 1-36) and Vancouueria (Figures 37-42), Caulophyllum (Figures 55- 

60) and Leontice (Figures 61-66, 69-72), and the 

pollen morphology supports these traditional 

views. But the distinction of the pollen found in 

Dzphylleia (Figures 85-88, 203-205) from that of 

Podophyllum (Figures 73-78, 81-84, 91, 106, 108, 
NUMBER 50 17 

109, 11 1, 113, 198-202) appears to challenge their 

common association by almost all modern generalists. Buchheim (1964) acknowledged the supposed relationship by treating the two genera as 

the only members of a subfamily Podophylloideae. Hutchinson (1959), while not assigning 

genera to subfamily categories, did have Podophyllum and Diphylleia key out as the first and 

second genus. Takhtajan (1969) gave separate 

family status to these two genera. 

Our investigation of the genus Podophyllum L. 

(Figures 73-78,81-84,91, 106, 108, 109, 111, 113, 

198-202) reveals an unusual range of variation in 

the pollen morphology, but the significance of the 

variability remains obscure due to a paucity of 

material. The following discussion is based on 

one collection of P. hispidum Hao (Figures 8 1, 9 I), 

eight of P. peltatum L. (Figures 73-78, 106, 108, 

109, 11 1, 113, 200-202), and two of P. hexandrum 

Royale (Figures 82-84, 198- 199). 

The variation in the tectum of Podophyllum 

peltatum (Figures 109, 11 1, 113) overlaps with that 

of some species of Epimedium (Figures 110, 112, 

114). 

The pollen (Figures 73-'78, 106, 108, 109, 11 1, 

113, 200-202) of the widespread and common 

May Apple, Podophyllum peltatum L., is shed as a 

monad, 3-colpate, the colpi long, the membrane 

covered with flecks of exinous material. The tectum could be described as consisting of short, 

flattened "rods" with one end projecting. There 

is considerable variation in the distinction of the 

rods or striae and the degree to which one end is 

free and projecting. Figures 74, 76, and 78 illustrate this variation. In each of the eight collections 

there are some grains in which the free tips are 

arranged like the vanes of a pinwheel, as shown 

in Figures 77, 78, 109, 11 I, and 113. 

Podophyllum peltatum (Figures 200-202) is as 

variable in TEM as in SEM. For the most part, 

all material sectioned has a thin foot layer, short 

slender columellae, and a predominant tectum. 

However, in each collection there is some evidence of radial channels in the foot layer as well 

as aperture columellae. The difference within the 

Nunan collection of the thickness of the tectum 

(Figures 200, 201) illustrates the problem. 

Although the pinwheel configuration is more 

precise in Podophyllum peltatum (Figures 77, 78, 

109, 1 1 1, and 113) than in Epimedium diphyllum 

(Figures 3 1, 32), E. cremeum (Figure 114), E. grandijlorum (Figure 1 12), or E. sempervirens (Figures 

33, 34, 110), the similarity is undeniable. However, all species of Epimedium examined in thin 

section (Figures 149, 150, 153-156) have a well 

defined foot layer with channels, while P. peltatum 

has perhaps the most reduced foot layer of all 

species examined in the family. 

The mean polar lengths in the nine collections 

of Podophyllum peltatum (Table l), 37.3 pm, 36.0 

pm,35.4pm,33.9pm,36.5pm,35.3pm,35.4~m, 

38.5 pm, and 37.7 pm respectively, overlap with 

some species of Epimedium, of Jeffersonia, and of 

Vancouveria. While the mean length of P. hispidum, 

38.9 pm, is slightly larger than any of P. peltatum, 

the high for each of the nine would include the 

low, 36.4 pm, for P. hispidum. 

Podophyllum hexandrum (Figures 82-84, 198, 199) 

is the only taxon examined in all the Order 

Ranunculales that has the pollen shed as tetrads, 

with the members arranged in either tetrahedral 

or rhomboidal configuration. The elongate apertures (Figures 82, 83) can be regarded as colpi 

and their distribution, while not irregular, is not 

necessarily consistent from one tetrad to the next. 

The surface is covered with gemmae of variable 

size that in turn have a ripplelike surface (Figures 

84, 198, 199). 

The tetrad mechanism is fusion of the gemmaeproducing layer along the common wall (Figure 

198) and the cytoplasm of each tetrad member 

would be discrete. Both the endexine and foot 

layer are thin and fairly uniform, and delicate 

columellae support gemmae of widely disparate 

sizes (Figures 198, 199). It should be noted that 

Figure 199 is somewhat oblique. Sections through 

the larger gemmae illustrate the undulate surface 

characteristic. The tectum is probably represented by a fusion of the small gemmae. 

Pollen of the above two species of Podophyllum 

Figures 73-78, 82-84, 106, 108, 109, 111, 113, 
18 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

198-202) examined in this study could scarcely 

appear more different. In P. hexandrum it is shed 

as tetrads and thin section confirms fusion by the 

gemmae-producing layer between adjacent 

grains. The apertures are furrow-like and not 

always in the same position from tetrad to tetrad, 

and the tectum consists of gemmae of variable 

sizes. In contrast, the pollen of P. peltatum is shed 

as a monad, is 3-colpate, and the ektexine or 

tectum has a “pinwheel” configuration or modifications thereof. 

A minimal pollen sample from an Arnold Arboretum collection identified as Podophyllum hispidum (Figures 81, 91) has 3-colpate grains, the 

colpi long and narrow with flecks of exine material on the membrane. The SEMs depict an 

almost complete or continuous tectum with faint 

lines (Figure 91), indicating that it might be a 

modification of the striate-reticulate type found 

elsewhere in the genus and family. These results 

should be treated with reserve. 

The only material available for the genus Dysosma R. E. Woodson was that of D. pleiantha 

(Hance) Woodson (Figures 79, 80, 92, 206), the 

type species. The 3-colpate grains (Figures 79, 

80), in which the tectum is again regarded as a 

modification of the striate-reticulate type, contribute little new information regarding the extent of Dysosma’s relationship with Podophyllum. 

The monad condition and the surface of the 

tectum appear much closer to Podophyllum peltatum 

than to P. hexandrum. 

In thin section (Figure 206), however, Dysosma 

could be distinguished from all remaining genera 

by a prominent tectum and foot layer that has a 

complementary, undulating interface bridged by 

delicate, uniform columellae. The endexine is 

thin and uniform in the mesocolpal regions and 

noticeably thickened in the colpus. 

Diphylleia Michaux (Figures 85-88, 203-205) 

has at least three species and an eastern North 

America and eastern Asia type of disjunction. 

The pollen of the North American species, D. 

cymosa Michaux (Figures 85, 86, 203, 204) and 

that of an Asian one, D. sinensis Li (Figures 87, 

88, 205), are 3-colpate and have a tectum composed of irregularly placed rods that form the 

base of stout, blunt spines. The sparse distribution 

of the rods makes the tectum appear punctate 

(Figures 85, 88). 

In TEM (Figures 203-205) the most striking 

feature is the delicate structure that supports 

massive spines. The tectum in each species appears irregular and broken, but it is consistent 

with the surface depicted in SEM; small sparsely 

distributed columellae connect the tectum with 

an equally irregular foot layer. The endexine is 

thin and fragmented. 

Like the other disjuncts, the two species of 

Diphylleia have subtle differences in the pollen, 

i.e., the Asian taxon (Figures 87, 88, 205) has 

more numerous and more slender spines than the 

North American one (Figures 85, 86, 203, 204), 

but this distinction might not be maintained if 

additional collections were examined. 

Podophyllum has two strikingly different pollen 

types, the tetrads of P. hexandrum (Figures 82-84, 

198, 199) and the monads of P. hispidum (Figures 

81, 91) and P. peltatum (Figures 73-78, 106, 108, 

109, 11 1, 113, 200-202) and the pollen of Diphyfleia has to be compared with each. But the tectum 

found in Diphylleia, stout blunt spines, has no 

counterpart in any of the other taxa examined in 

the family. 

Nandina domestica (Figures 89, 90, 207-21 1) was 

described by Thunberg (1 78 1) ostensibly from a 

Chinese collection, but the origin of this subshrub 

remains a matter of conjecture since the plant has 

a long history of cultivation and can be found in 

many parts of Asia as an escape. 

The distinction of this monotypic genus has 

been acknowledged by segregating it as a tribe or 

even as a family, Nandinaceae. The pollen morphology (Figures 89, 90, 207-21 1) supports Kumazawa’s (1938a:12) opinion that it is the “farthest deviated” if it is included in the Berberidaceae. 

As demonstrated in SEM (Figures 89 and go), 

the pollen morphology is among the most common types in the dicotyledons: the apertures are 

3-colpate and the tectum is deeply punctate with 

the punctae evenly distributed. 
NUMBER 50 19 

In thin section (Figures 207-21 l), the exine of 

Nandina can be distinguished from all members of 

the Berberidaceae s.1. by the presence of a massive endexine. Compared with most members of 

the family, the tectum is thick and almost complete (Figure 207), except for the punctae (Figure 

208), and it is uniform in the sense that it is the 

same thickness in the mesocolpal regions as well 

as near the colpi; the columellae are diminutive 

(Figures 207, 209), the foot layer is much thinner 

than the tectum but recognizable and consistent. 

The massive endexine is lamellar at the interface 

with the foot layer, and uneven and less electron 

dense on the inner surface (Figure 21 1). The 

continuity of this layer is disrupted by small gaps 

where the colpus and mesocolpus meet. 

This study is concerned with generic relationships within the Berberidaceae s. 1 ., and no other 

taxa examined had a thick punctate tectum similar to that of Nandina. Dysosma pleiantha (Hance) 

Woodson (Figure 206) had a thick tectum but 

this is the only characteristic that these two species have in common. 

The remarkable development of the endexine 

layer of Nandina as revealed in thin section (Figure 

207) is unique and has not been found in any 

taxa examined to date in the Centrospermae 

(Skvarla and Nowicke, 1976), or in Plumbaginaceae, Polygonaceae, or Primulaceae (Nowicke 

and Skvarla, 1977). Moreover, the distinction of 

the pollen of Nandina applies to the Order Ranunculales as well. Considering each of the various 

families as a whole, the Ranunculaceae does have 

the most consistent and well developed endexine 

(Figures 1 15- 12 1), but at least to date none rivals 

the one found in Nandina. Palynologically this 

species may be more closely related to certain 

taxa in the Lardizabalaceae, Akebia trifoliata 

(Thunberg) Koidzumi and Decaisnea fargesii Franchet, in that all three have at least the components of the ektexine represented in the same 

proportions, thick tectum, diminutive columellae, 

and thin foot layer (Skvarla and Nowicke, unpublished data). 

Just as there are exceptional and restricted 

sporoph yt ic characteristics, e. g., periant h absent 

in Achlys (see page 8), there are palynological 

distinctions that occur in only one or two genera: 

tetrads only in Podophyllum hexandrum, 6-pantocolpate aperture type only in Ranzania, a massive 

endexine only in Nandina, very long columellae 

only in Bongardia, spinose tectum only in Diphylleia, gemmate tectum only in P. hexandrum, and 

aperture columellae only in Epimedium and Vancouveria. An unstratified exine is found in three 

genera, Berberis, Mahonia, and Razania. 

EKTEXINE RELATIONSHIPS.-The 24 high magnification SEMs, Figures 91-114, of tecta found 

in Achlys, Epimedium, Dysosma, Hydrastis, Jeffirsonia, 

Podophyllum hispidium, P. peltatum, and Vancouveria 

have been arranged to demonstrate a continuum 

in variation and the existence of a relationship 

among these taxa. The relationships exist within 

and between groubs of figures so that the series 

should be viewed as a foldout. While the discussion could start with any one group, that of 

Figures 103- 108, representing four genera, Hydrastis, Figure 103, Epimedium brevicornu, Figure 

105, E. alpinum, Figure 104, Jeffersonia diphylla, 

Figure 107, and Podophyllum peltatum, Figures 106 

and 108, might serve this purpose best. Palynologically, Hydrastis, Figure 103, is more closely 

related to the Epimedium species, Figures 104 and 

105, and to Jeffersonia, Figure 107, than to any 

member of the Ranunculaceae (Nowicke and 

Skvarla, unpublished data). The similarity of the 

striae configuration in Jeffersonia, Figure 107, with 

that in the collection of Podophyllum peltatum in 

Figure 108 could suggest a relationship. The difference between the two collections of P. peltatum, 

Figures 106 and 108, is a loss of some of the 

distinction of individual rods and the fact that 

the free tip is no longer free. The difference 

between the tectum of Hydrastis, Figure 103, and 

that of Epimedium alpinum, Figure 104, can also be 

considered as a loss of some distinction. 

There is a hypothetical series, Figures 98, 97, 

92, 91, in which the tectum from one taxon could 

be derived from the preceding one by a loss of 

some distinction of either rods or striae. The 

tectum found in Vancouveria chrysantha, Figure 97, 

could be derived from Jeffsonia diphylla, Figure 
20 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

98; the tectum of Dysosma, Figure 92, could be 

derived from Vancouveria chrysantha, Figure 97; and 

Podophyllum hispidum, Figure 91, could be derived 

from Dysosma, Figure 92, by the loss of all distinction of the striae or rods. 

A second similar series, consisting of Figures 

106, 105, 100, 99, 94, 93, illustrates a continuum 

in variation from a striate-reticulate tectum to 

one that is almost complete, and could link Podophyllum peltatum, Epimedium brevicornu, Vancouveria 

hexandra, E. sagittatum, E. membranaceum, and Jeffersonia dubia, respectively. 

A third series, Figures 108, 107, 102, 101, 96, 

95, illustrates the possible stages of the transition 

from a striate-reticulate tectum to ones that are 

striate, the striae being mostly parallel to each 

other. The taxa linked include Podophyllum peltatum, Jeffesonia diphylla, Vancouveria planipetala, Achlys triphyla, and J. dubia. 

The group consisting of Figures 109-1 14, illustrates a tectum condition found in some species 

of Epimedium, Figures 110, 112, and 114, and in 

certain collections of Podophyllum peltatum, Figures 

109, 11 1, and 113. All six micrographs have at 

least some areas where the free tips are arranged 

like the vanes of a pinwheel. 

In a review paper (Nowicke and Skvarla, 1980) 

the authors documented the existence of similar 

tectum patterns (as illustrated by SEM) in families or genera that are widely separated on the 

basis of other characters. This phenomenon as 

well as the existence of very diverse (apparently) 

morphologies in closely related species raises the 

fundamental question of the origin and persistence of such forms. 

One possible interpretation of these results is 

that there are a limited number of structurally 

defined tectal types, each with a potential variation that may or may not be manifested. The two 

layers of striae tectum, known to occur in at least 

half a dozen families, could serve as an illustration 

of such a tectal type. 

Jeffsonia may be an example in which the 

potential variation is, at least in part, realized: in 

Figure 48 the tectum consists of two layers of 

striae, in Figure 95 the tectum is striate, in Figure 

45 the tectum appears intermediate between that 

in Figures 48 and 95, in Figure 107 the tectum is 

irregularly striate. 

Hydrastis canadensis may be another example: in 

the collection illustrated in Figures 53 and 54 the 

tectum consists of two layers of striae, while in a 

second collection, illustrated in Figures 52 and 

103, the tectum is striate-reticulate. 

Another tectal type may be that found in the 

euphorbiaceous genera Croton (Nowicke and 

Skvarla, unpublished data) and Manihot (Lynch 

and Webster, 1975, figs. 1-8; Nowicke and 

Skvarla, unpublished data), in the icacinaceous 

genus Platea (Lobreau-Callen, 1973, pl. 3: figs. 1- 

3), in the cistaceous genera Fumana (Saenz de 

Rivas, 1979, figs. 3.4-3C; Nowicke and Skvarla, 

unpubished data) and Lechea (Nowicke and 

Skvarla, unpubished data), in the Myristicaceae 

(Walker and Walker, 1980), in the Buxaceae 

(Nowicke and Skvarla, unpublished data), in 

Aquilaria, Cryptadenza, Lachnaea, Lophostoma, Phaleria, and Wikstroemia, all members of the Thymelaeaceae (Erdtman, 1966; Nowicke and Skvarla, 

unpublished data), in Podophyllum peltatum (Figures 77, 78, 109, 11 1, 113), and in some species of 

Epimedzum (Figures 110, 112, 114). These tecta 

could be classified as a continuous triangular 

array. In Scyphocephalium (Walker and Walker, 

1980, figs. 20, 2 l), Aquilaria, Croton, Lachnaea, Manihot (Lynch and Webster, 1975, fig. 7), and 

Wikstroemia the configuration of the triangular or 

prism-shaped subunit is very precise, whereas in 

Fumana, Podophyllum, and Epimedium it is identifiable only in some grains, sometimes only in certain 

areas, e.g., along the colpus. 

Most species of Croton have a tectum as defined 

above-a continuous triangular array-however, 

C. californicus (Solomon et al., 1973, figs. 46a-46c; 

Nowicke and Skvarla, unpublished data) represents a variation in this type by having the subunits rounded or gemmate and with a ripple 

surface. This is more or less paralleled in Podophyllum: those grains of P. peltatum that have a 

tectum of uniform “pinwheels” (Figure 78), 

would be equivalent to most species of Croton, 

with the “vanes” of the pinwheel equivalent to 

the traingular subunits; P. hexandrum (Figures 82- 
NUMBER 50 21 

84), with a tectum of ripple-surfaced gemmae 

would be equivalent to C. californicus. 

Of far greater interest is the remarkable parallelism of the pollen morphology in the family 

Cistaceae with that of the Berberidaceae. Saenz 

de Rivas (1979) examined 36 species representing 

five of the eight genera in the Cistaceae. He 

classified the exine sculpturing (1979, table 1) 

into five types, rugulose, retipilate, reticulate, 

striate, and reticulate-granular, all of which were 

documented by SEM micrographs, and most of 

which have a close counterpart in the Berberidaceae s. 1. 

The close similarity between Saenz de Rivas’ 

rugulose type (1979, figs lE, IF), and the reduced 

striae distinction type in the Berberidaceae, as 

illustrated by Vancouveria chrysantha (Figure 97) 

and Dysosma (Figures 79, 80, 92), would be difficult to refute. 

The retipilate exine in some species of Fumana 

(Saenz de Rivas, 1979, figs 3A-3C), in another 

cistaceous genus Lechea (Nowicke and Skvarla, 

unpublished data), and the pinwheel pattern 

found in Podophyllum peltaturn (Figures 77, 78, 109, 

11 1, 113) and some species of Epimedium (Figures 

110, 112, 114) are probably derivations of a continuous triangular array as discussed above. 

The striate type in the Cistaceae as illustrated 

by Halimium atriplicfolium (Saenz de Rivas, 1979, 

fig. 2A) is very similar to the striate-reticulate 

type in some species of Epimedium: E. alpinum 

(Figure 104) and E. brevicornu (Figure 105). Other 

examples of striate types in the Cistaceae (Saenz 

de Rivas, 1979, figs. 2B-2F) are equivalent to the 

two layers of striae as illustrated in Jeffersonia 

(Figures 45, 48), and in Hydrastis (Figures 53, 54). 

The reticulate-granular type in the Cistaceae 

(Saenz de Rivas, 1979, figs. 1A-1D) has its counterpart in the Berberidaceae in those species of 

Epimedium (Figures 31-34, 110, 112, 114) that 

have a tectum of small rods with one tip projecting. 

The parallel pollen morphology in the Berberidaceae and Cistaceae suggests that the tecta 

described by the present authors as two layers of 

striae, “randomly” placed small rods, and a continuous triangular array are closely related and 

may be variants of, or derived from, a major 

structural type. 

General Discussion 

The following discussion considers data from 

other sources-gross morphology, carpel morphology, serology, and cytology-together with 

the implications of pollen analyses. 

That Berberis and Mahonia are closely related is 

beyond question. Of more fundamental interest 

is the extent of their separation or isolation from 

the remaining genera traditionally aligned as the 

Berberidaceae. To regard the woody habit of 

Berberis and Mahonia as secondarily derived from 

a herbaceous one is a situation where Occam’s 

Law should be applied: there is no reason to 

assume that Berberis and Mahonia were ever anything but woody in habit. Certainly the distinguishing characteristics of their pollen are unequivocally primitive. Carpel morphology (Chapman, 1936) indicates the Berberis-Mahonia line 

separated very early from the ancestral stock. 

Both genera have tactile stamens, chromosome 

numbers of 2n = 28 or 56 and their interfertility 

as well as their mutual susceptibility as the alternate host for wheat rust clearly supports Jensen’s 

(1974) proposal that they are congeneric. All 

available evidence indicates that Berberis and Mahonia are primitive, isolated genera, and the present authors would agree with Hutchinson’s (1959) 

restricted view of the Berberidaceae as consisting 

of only Berberis and Mahonia. 

In a family that is said to consist of groups of 

genera not closely related to each other, the degree to which Ranzania is separated from the 

remaining genera may be exceeded only by Nandina. Ranzania japonica, found in an area of three 

degrees of latitude on northern Honshu, has one 

of the more restricted distributions in all of the 

dicots. This species possesses floral characteristics 

that align it with Berberis-Mahonia: petals with 

fleshy nectaries at the base, sensitive stamens, an 

unstratified exine, and baccate fruit. Certain vegetative characteristics, however, align it with Caulophyllum-Leontice: the habit, rhizome, leaf and 
22 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

petiole morphology. The type of aperture, 6-pantocolpate (Figure 139), is unique in the family 

s. l., a status that Kumazawa (1937~) also applied 

to the anther dehiscence. Kumazawa recognized 

four modes of dehiscence in the Berberidaceae: 

three were monogeneric, Nandina, Podophyllum, 

and Ramania, and the fourth included all remaining genera. However, the distinctions of the four 

types as illustrated by Kumazawa (1937c:59, fig. 

3) do not, at least to the present authors, seem 

very great. 

Terabayashi’s first publication in his studies of 

floral morphology of the Berberidaceae was on 

Ranzania (1977) and the second one on Berberis 

and Mahonia (1978). If the flower parts of Ranzania 

as depicted in line drawings by Terabayashi 

(1977, fig. 1) are compared with those of Berberis 

and Mahonia by the same author (1978, figs. 1, 2), 

the close similarity would make it difficult to 

deny a relationship between the three genera. 

Certainly the presence of an unstratified exine in 

both the Berberis-Mahonia alliance (Figures 124- 

138) and in Ranzania (Figures 141-145) supports 

this contention. 

Herbarium specimens of Ranzania, consisting of 

the only two collections at Kew, were obtained in 

April 1979. Unfortunately, one was cultivated, 

the other sterile. Nevertheless when these two 

collections (Figures 2 12,2 13) were compared with 

a Japanese species of Berberis, B. amurensis Ruprecht (Figure 2 14) and one of Mahonia, M. japonica (Thunberg) De Candolle (Figure 215), the 

contrast was striking: Ranzania is a slender, delicate herb with a single stem arising from a small 

rhizome, and at a height of six to eight inches the 

stem divides producing two petioles and the peduncle, which supports a single flower (the cultivated, partially dried New York State specimen 

is f identical). 

The difference in aperture type may be more 

significant than the similarity in exine structure. 

An unstratified exine is a generalized condition 

found in many primitive angiosperms, and in 

Berberis, Mahonia, and Ranzania it most likely represents an original, unchanged state. However, 

the 6-pantocolpate aperture of Ranzania is an 

advanced type, especially in regard to the irregular type found in Berberis and Mahonia. 

The similar floral morphology and exine structure would support the view that Ranzania, Berberzs, and Mahonia are monophyletic, but the great 

disparity in vegetative morphology and aperture 

type strongly suggests that the ancestral stock of 

Ranzania separated very early in time from that 

which produced Berberis and Mahonia. The present 

authors would maintain Rantania as a taxon incertae. 

The almost complete agreement on the close 

relationship of Epimedium and Vancouveria is not 

surprising since the latter genus has been treated 

as a section of the former (Baillon, 1871). The 

range of variation found in the tectum of Epimedium and Vancouveria would indicate that Stearn’s 

(1938) treatment as closely allied but separate 

genera is the most valid. Both genera have a 

chromosome number of 2n = 12, the basic one 

for the Berberidaceae. Chapman (1936) placed 

Epimedium and Vancouveria with the other predominantly two-carpellate genera (Achhs, Diphylleia, 

Epimedium , Jeffersonia , Nandina , Podop hy llum) , bu t 

emphasized their special relationship by her statement (1936:344), “The structure of the ovaries of 

the species commonly placed in the genus Vancouveria helps clarify the interpretation of conditions 

in Epimedium.” Comparison of herbarium specimens leaves little doubt as to their close association. 

Comparison of Bongardia, Caulophyllum, and 

Leontice collections, unfortunately, leaves considerable doubt as to the extent of their affinities to 

each other. Vegetatively, Bongardia and Leontice 

are almost succulent, a sharp contrast to the thin 

leaves and slender stems of Caulophyllum. All three 

genera have fruits described as bladder-like; but 

Caulophyllum has this condition only in the earliest 

stage of fruit development, and the large (ca. 1 

cm in diameter), exposed seeds with a dark blue, 

glaucous coat are “easily mistaken for fruits” 

(Ernst 1964: 19). Moreover, each of the two seeds 

is attached to an erect, conspicuous funiculus, as 

much as 7 mm long and 2 mm in diameter, a 

structure lacking in the other two genera. It could 
NUMBER 50 23 

be argued that the fundamental difference between the fruits of Caulophyllum and those of Leontice and Bongardia is the rapid and extensive 

growth of the seeds in the former genus. But the 

disparity of the mature fruits and/or seeds as well 

as the unusual funiculus would scarcely support 

a close relationship. 

Results from carpel morphology (Chapman, 

1936) and serology (Jensen, 1974) support AiryShaw’s (1966) viewpoint of a close relationship 

between Caulophyllum, Leontice, and Bongardia, but 

not necessarily separate family status since the 

same results also indicate some affinity to other 

berberidaceous genera. 

The palynological data alone are paradoxical: 

of all the 3-colpate taxa, Bongardia, Caulophyllum, 

and Leontice have the largest individual grains, 

averaging 49-35 pm long; all three have an incomplete tectum, and in eleven collections there 

were no variants that indicated a relationship to 

the tectum found in the tribe Epimedieae and 

Podophyllum peltatum. The type of tectal perforation in Bongardia differs sufficiently from that of 

Caulophyllum and Leontice to suggest different 

origins of the “incomplete” characteristic. In thin 

section and LM, the pollen of Bongardia can be 

distinguished from that of Caulophyllum, Leontice, 

and all remaining genera by the predominance 

of the columellae, which account for 80% of the 

exine. 

In a discussion following Jensen’s presentation 

of the serological results (1974), A. Takhtajan 

refers to his study of seed coat characteristics in 

Bongardia, Caulophyllum, and Leontice, and the fact 

that Bongardia differs considerably from the other 

All three genera have been reported as having 

chromosome numbers other than, or in addition 

to, the basic x = 6: Bongardia n = 6, 7, 2n = 12; 

Leontice n = 7, 8, 2n = 14, 16; Caulophyllum has to 

our knowledge only been reported as 2n = 16. 

Cltimately any statement regarding their relationship depends on the value attached to each 

of the above characteristics: habit, fruit, seeds, 

carpel morphology, serology, pollen morphology, 

and cytology. The paradoxical results indicate an 

two. 

early separation or a differential rate of evolution 

among the characteristics investigated. Nevertheless, Caulophyllum, Leontice, and Bongardia appear 

to be more closely related to each other than to 

any remaining genera and could be segregated as 

the tribe Leon ticeae. 

The similarity of pollen morphology in Achlys 

and Jeffersonia, a more or less striate tectum, consistent endexine, and small size range, prompted 

a comparison of the two genera on other characteristics. There are, however, differences of such 

magnitude as to preclude the possibility of any 

close relationship: the compact, spicate inflorescence of Achlys with numerous, small flowers which 

lack a perianth contrasts sharply with the scapose 

inflorescence of Jeffersonia with a single, showy 

flower. The fruit of Jeffersonia is as unusual as the 

inflorescence of Achlys: the oblong capsule opens 

by a horizontal cleft to release the numerous 

seeds. The fruit of Achlys is small, one-seeded, and 

either dehiscent (Hutchinson, 1959) or indehiscent (Rickett, 1971). 

According to Chapman (1936:346), “The frequent coupling of the genera Achlys andJeffersonia 

does not seem to be especially justified when the 

carpel morphology of the two is considered.” She 

regarded them as no more related to each other 

than each is to Epimedium. 

In a morphological and systematic study of 

Achlys, Takeda (1915) also dismissed the possibility of a close relationship to Jeffersonia, citing the 

much greater specialization of the latter genus. 

He regarded Achlys as being related to Epimedium 

and Leontice, and in fact characterized Achlys as a 

much reduced form of the latter genus. 

Both genera have a chromosome number of 2n 

= 12, the basic one for the Berberidaceae, which 

contributes little to the clarification of the relationships of Achlys and Jeffersonia to each other or 

to any of the remaining genera. 

Any discussion of the relationships and placement of Podophyllum must first attempt to resolve 

the vague circumscription of this genus. 

Woodson (1 928) elevated Podophyllum pleianthum 

Hance to separate generic status as Dysosma based 

primarily on the following characteristics: very 
SMITHSONIAN CONTRIBUTIONS TO BOTANY 

large leaves with regular, equal lobes and a finely 

dentate margin, as opposed to smaller leaves with 

irregular lobes and an entire or uneven margin in 

Podophyllum; an inflorescence of four to 19 flowers, 

as opposed to one; and introrse anthers as opposed to extrorse in Podophyllum and all the rest of 

the Berberidaceae. He also cited differences in the 

pollen, that of Dysosma being spherical and relatively small, while that of Podophyllum is lobed and 

relatively large. The latter description can only 

mean that Woodson used P. hexandrum pollen as 

representative of Podophyllum and interpreted the 

tetrad as a large, lobed grain. 

Kumazawa (1 935: 274) re-examined Podophyllum plelanthum in view of Woodson’s elevation and 

concluded that “the anthers are quite laterally 

situated on the connective and the dehiscence is 

extrorse.” He also commented that “the size of 

the pollen grain is larger in P. pleianthum than in 

P. peltatum, and this is quite contrary to his 

[Woodson’s] description.” Our data in Table 1 

confirm this, although the difference is not very 

great: Dysosma has a mean length of 42.9 pm, and 

in eight collections of P. peltatum, the means are 

37.3 pm, 36.0 pm, 35.4 pm, 33.9 pm, 36.5 pm, 

35.4 pm, 35.3 pm, 38.5 pm, and 37.6 pm. 

Woodson (1928) did not, in the opinion of the 

present authors, need a pollen difference to confirm the validity of Dysosma. However, the pollen 

of Dysosma (Figures 79, 80, 92) appears to be 

much closer to that of Podophyllum peltatum and P. 

hispidurn than that of P. hexandrum is to these two 

species. Examination of the collections (US) seem 

to justify his treatment. Hu (1937) apparently 

agreed with Woodson since he transferred at least 

three other species of Podophyllum to Dysosma. 

If the genus Dysosma and Hu’s (1937) subsequent transfers (see page 5) are accepted as valid, 

Podophyllum S.S. still includes two very dissimilar 

entities regarding pollen morphology: the 

common and widely distributed P. peltatum L. in 

North America and, judging from the material at 

US, a similarly common and widely distributed 

P. hexandrum Royale from Asia. The tetrads of P. 

hexandrum, in which the tectum is covered with 

ripple surfaced gemmae, are radically distinct 

from the monads of P. peltatum or any other 

member of the Berberidaceae. However difficult 

it may be to reconcile the distinction of the pollen 

in these two species, they are very similar in 

vegetative and floral morphology and the present 

authors would maintain Podophyllum as including 

both species until samples and/or other data from 

other species of Podophyllum or Dysosma become 

available. 

The pollen found in the two species of Diphylleia 

(Figures 85-88, 203-205), D. cymosa from North 

America and D. sinensis from Asia, is unique and 

reinforces their close relationship to each other 

and distinguishes them from all other members 

of Berberidaceae, s. 1. 

According to Chapman (1936:347), “the taxonomic association of Diphylleia and Podophyllum is 

one which the study of carpel structure does not 

confirm.” Furthermore, “it seems likely that the 

two may be derived from the complex which gave 

rise to the two carpel forms, but the separation 

between them can probably be extended back to 

an early representative in that evolution.” Her 

views of a remote connection between Diphylleia 

and Podophyllum agree with those of Kumazawa 

(1938a). 

Li (1947) recognized three species of Diphylleia, 

mostly on the basis of the origin of the inflorescence and the extent of the lobing in the leaves: D. 

cymosa Michaux from eastern North America, D. 

sinensis Li from China, and D. grayi R. Schmidt 

from Japan. Examination of the collections at the 

US indicates that Diphylleia can be separated into 

three entities using Li’s criteria. 

Diphylleia and Podophyllum have a chromosome 

number of 2n = 12, basic in the family and 

therefore of limited value as an indicator of relationships. 

According to Jensen (1974:223), Diphylleia and 

Podophyllum have “the possibility of great serological similarity,” but the two genera have the 

reality of widely divergent (apparently) pollen 

morphologies (Figures 73-78, 8 1-88, 198-205). 

In considering the variation in pollen morphology of the Berberidaceae s. l., the distinction 

of the grains in Diphylleia relative to the remaining 
NUMBER 50 25 

members of the family is surpassed only by that 

of the tetrads in Podophyllum hexandrum. 

Nandina domestica Thunberg is one of the few 

berberidaceous genera that has a woody habit 

and in this respect, as well as articulated leaves, 

it is similar to Berberis and Mahonia. Chapman 

(1936) placed Nandina with the 2-carpellate genera, but cited earlier work that recorded some 3- 

carpellate specimens among the predominantly 

2-carpellate ones. She (1936:346) considered the 

variation in Nandina “as an index to the history of 

the forms in the other genera rather than indicating the genus as ancestral in the evolution of 

the family.” 

Kumazawa (1938b: 12) made a strong case for 

elevating Nandina to separate family status. 

The outer integument of Nundznu is strongly developed and 

the micropyle is not observed from outside; moreover, the 

nucellus is absorbed before the flower comes into bloom and 

the external epidermis and the internal one change into the 

thin walled columnar tissue. These vegetative and ovular 

characters, as well as the dehiscing type of anther described 

before (Kumazawa, 1937c), are quite unique among the 

berberidaceous genera. 

The pollen of Nandina can be easily distinguished from all remaining members of the family 

by the massive endexine. 

Nandina has a chromosome number of 2n = 20, 

unique in the Berberidaceae. 

Jensen’s (1974:225) serological study of the 

Berberidaceae does not support the separation of 

Nandina since “it features serological similarities 

of a high degree with Berberis and Mahonia and 

with Podophyllum and Diphylleia.” He drew a parallel of the distinctive characteristics of Nandina 

relative to the Berberidaceae with certain groups 

in the Ranunculaceae relative to that family 

(1974:225): “The fact that the deviating chromosome number (n = 10) is by no means decisive 

is proved by the related family of Ranunculaceae, 

in which the Thalictreae and Coptideae also 

exhibit a completely different karyotypus.” The 

present authors are of the opinion that variation 

in a family as large as the Ranunculaceae is to be 

expected; but in a family of 12 genera, such 

variation may indicate a lack of relationship. 

In considering the disparity of the palynological results with Jensen’s (1974) preliminary data 

from serology (see page 3), it should be noted that 

conclusions from the latter source are restricted to comparisons among the taxa investigated. While pollen morphology also relies heavily on comparison, this discipline has reached a 

stage where a number of characteristics have 

values attached, primitive or unspecialized, and 

advanced or specialized. Most palynologists 

would designate the unstratified exine, irregular 

apertures, and undifferentiated surfaces found in 

Berberis and Mahonia as primitive without any 

knowledge of the rest of the family‘s pollen morphology. 

Reference has been made in the Introduction 

that the Berberidaceae have an unusually high 

number of disjunct or discontinuous genera, five 

of the 12 have species that are widely separated 

geographically. Achlys is the only one with a 

Pacific North America and eastern Asia distribution. Unfortunately, the paucity of material of 

the Asian taxon as well as the high incidence of 

sterility in both taxa compromises any statement 

about their relationships. 

Caulophyllum, Diphylleia, andJeffersonia have the 

more common eastern North America and eastern Asia type of disjunction. In each of these three 

genera, the pollen of the American species and 

that of the Asian species are fundamentally similar with only subtle differences in the tectum. 

The range of variation found within a sample 

and between collections of some species makes 

such differences suspect, and the paucity of Asian 

specimens curtailed any further investigation 

Podophyllum is another disjunct genus with a 

distribution similar to that of Caulophyllum, Diphylleia, and Jeffersonia, but if the pollen of P. 

hexandrum is arbitrarily dismissed due to unparalleled distinction (in all of the Order Ranunculales), and if the treatment of P. pleianthum as 

Dysosma pleiantha is considered valid, then for 

purposes of comparison the Asian possibilities are 

reduced to one pollen sample from a collection 

identified as Podophyllum hispidum at Gray Herbarium. The differences in the tectum between P. 
26 SMITHSONIAN CONTRIBUTIOKS TO BOTANY 

hispidum and P. peltatum are more pronounced 

than in the other disjuncts, but the type found in 

Dysosma pleianthum could be interpreted as intermediate and link the two entities. 

Summary 

The pollen diversity in the Berberidaceae confirms, for the most part, previous characterization 

as “groups of genera” not closely related to each 

other, especially regarding the distinction of Berberis and Mahonia, and of Nandina. Howevx, the 

pollen would suggest greater conformity or closer 

relationship among Achlys, Dysosma, Epimedium, 

Jeffersonia, Podophyllum species, and Vancouveria, 

than has been previously thought. 

For Berberis and Mahonia the characteristics of 

the pollen, an unstratified exine with a random 

or unspecialized surface, irregular and/or spiral 

apertures, as well as their woody habit, indicate 

that they are primitive genera, additionally distinguished by a chromosome number of n = 14 

(28 for some species of Berberis), susceptibility to 

Puccinia graminis, and articulated leaves. Hutchinson’s (1959) concept of the Berberidaceae as 

consisting of only Berberis and Mahonia could be 

justified. 

The pollen of the monotypic genus Nandina can 

be distinguished from those of all other taxa 

examined, which in combination with evidence 

from floral morphology (carpel morphology, development, anther dehiscence) and, above all, the 

unique chromosome number of 2n = 20, support 

the case for separate family status. 

Palynologically, Hydrastis is more closely related to Achlys, Epimedium, Jeffersonia, and Vancouueria than to any genus examined thus far in the 

Ranunculaceae. 

Pollen morphology reinforces the special relationship between Epimedium and Vancouveria: species assigned to these two genera were the only 

members of the Berberidaceae s. 1. to have aperture columellae. They are additionally distinguished by the presence of saccate petals or nectar 

spurs, a follicle-like fruit, and seeds with a conspicuous aril. Both have a chromosome number 

of x = 6. 

The close similarity of the pollen in the American Jeffersonia diphylla and the Asian Plagiorhegma 

dubia supports their congeneric treatment as Jef 

fersonia and allies them with Achlys, Epimedium, 

Podophyllum peltatum, and Vancouveria. While Jeffersonia has the typical chromosome number of x = 

6, and an anther dehiscence by narrow valves 

attached at the apex found in at least six other 

berberidaceous genera, no one genus seems to be 

especially allied with this Asian-American disjunct. Certainly the fruit, which resembles a moss 

capsule, is unique within the taxa examined. 

Achlys has pollen similar to Epimedium, Jeffersonia, Podophyllum peltatum, and Vancouueria, and a 

chromosome number of x = 6. The highly reduced flower (sepals and petals are absent) suggest no other generic relationships. 

Achlys, Epimedium, Jeffersonia, and Vancouueria 

are similar in pollen morphology, chromosome 

number, anther dehiscence, and habit, and could 

be segregated as a tribe. 

Palynologically the Old World genus Leontice, 

the monotypic Bongardia (based on L. chrysogonum), 

and the Asian-American disjunct Caulophyllum, 

are more closely related to each other than to any 

remaining taxa examined. Although the unifying 

characteristics are quantitative (larger size and 

thicker walled), the fact that their tecta are not 

related to the type found in Achlys, Epimedium, 

Jeffersonia, Podophyllum peltatum, and Vancouveria 

may be more significant. All three have chromosome numbers other than, or in addition to, n = 

6: Bongardia n = 6, 2n = 14, Caulophyllum 2n = 16, 

and Leontice 2n = 14, 16. Caulophyllum and Leontice 

have very similar stamen morphology, and all 

three have anthers opening by valves. Their distinction could be acknowledged by treating them 

as a tribe, Leonticeae. 

The structure of the exine supports the separate 

generic status of Podophyllum pleianthum as Dysosma 

Woodson, accorded on other bases. The tectum, 

aperture type, and size are similar to P. peltaturn, 

and Achlys,Jeffersonia, Epimedium, and Vancouveria. 

The pollen of Podophyllum hispidum and P. pel- 
NUMBER 50 

tatum is similar in the tectum, apertures, and size 

to that found in Achlys, Epimedium, Jeffersonia, and 

Vancouueria. Podophyllum peltatum has a 2n = 12, 

characteristic of the above genera, but this species 

has longitudinal anther dehiscence as opposed to 

valves. The pollen morphology of Podophyllum 

hexandrum is unique within the Order Ranunculales: tetrads with a tectum supporting ripplesurfaced gemmae. In leaf and floral morphology 

P. hexandrum is closely related to P. peltatum. The 

boundaries of Podophyllum have yet to be established. 

The characteristics of the pollen of Rantania are 

ambiguous: the 6-pantocolpate aperture type is 

unique within the Berberidaceae s. l., but the 

unstratified exine is similar to that in Berberis and 

27 

Mahonia. The chromosome number of 2n = 14 

has been reported only from Bongardia and one 

species of Leontice. 

The pollen found in two species of the disjunct 

genus Diphylleia is unique, so much so that no 

clear relationships within the Berberidaceae are 

suggested, while the chromosome number, 2n = 

12, is found in at least six other genera of the 

family. Evidence from floral morphology is inconclusive except to deny a close relationship with 

Podophyllum. Of all taxa examined in this study, 

Diphylleia is indeed a genus of uncertain affinities. 

Pollen morphology does not support a close 

relationship between the Berberidaceae and Ranunculaceae nor between the Berberidaceae and 

Lardizabalaceae. 
Literature Cited 

Ahrendt, L.W.A. 

1961. Berberis and Mahonia: A Taxonomic Revision. Journal of the Linnaean Society of London, Botany, 57: 1- 

410. 

A Dictionary of the Flowering Plants and Ferns. 7th 

edition, xxii + 1214 + liii pages. Cambridge: 

University Press. 

Monographie des menispermacees et des berberidacees. Histoire des Plantes, 3: 1-76, 

A Botanical Description of the Podophyllum Diphyllum of Linnaeus, in a Letter to Charles Peter 

Thunberg . . . . Transactions of the American Philosophical Societ).., 3 : 334-347. 

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Tables 

and 

Figures 
TABLE 1 .-Berberidaceae specimens examined, alphabetically by genus (grain size in pn; 

asterisk indicates longest dimension for tetrad member) 

Species 

Achlys japonica Maximowicz 

A. triphylla (Smith) De Candolle 

BerberiJ. fendleri A. Gray 

B. grandtflora Turczan i now 

B. ilicifolia Forster 

B. lischleri C. K. Schneider 

B. uulgaris L. 

Bongardia chrysogonum (L.) Spach 

Caulophyllum robustum Maximowicz 

C. thalictroides (L.) Michaux 

Diphylleia cymosa Michaux 

D. sinensis Li 

Dysosma pleianthu (Hance) R. E. Woodson 

Epimedium alptnum L. 

E. breuicornu Maximowicz 

E. cremeum Nakai 

E. diphyllum (Morren & Decaisne) Loddiges 

E. grandiflorum Morren 

E. membranaceum K. Meyer 

E. sagittatum (Siebold & Zuccarini) Maximowicz 

E. sempervirens Nakai 

Jeffersoniu diphylla (L.) Persoon 

Collect ion Location 

Terabayashi 209 KYO 

Calder & Savile 8323 US 

Evert s.n. 1920 US 

Eastwood 5272 US 

Arbelaez & Cuatrecasas 5908 US 

Mexia 7628 US 

Goodall 834 US 

Rock 17544 US 

Soper & Dale 3950 US 

Balls 776 US 

Sintenis 35 US 

Kirino 713 US 

Moran 5204 US 

Harper3864 US 

Henry 571 US 

Braun s.n. 25 Apr 27 US 

Pollard s.n. 16 May 01 US 

Rock 4230 US 

Steward & Cheo 210 GH 

Wilson 3203 GH 

Porta s.n. Jun 1894 US 

Rock 12302 US 

Togasi 1281 US 

Kirino 618 US 

Anon. 1314887 US 

Togasi 1031 US 

Forrest 25471 US 

Anon. 1314880 US 

Masayuki Oue 33 US 

Baxter s.n. 15 Apr 11 US 

Chandler s.n. 30 Apr 16 US 

Shafer & Miller 180a US 

Japan 

Canada 

Washington 

Colorado 

Colombia 

Colombia 

Argentina 

China 

Canada 

Turkey 

U.S.S.R. 

Japan 

Korea 

Alabama 

Pennsylvania 

Tennessee 

North Carolina 

China 

China 

China 

Italy 

China 

Japan 

Japan 

Japan 

Japan 

China 

Japan 

Japan 

New York 

Michigan 

Pennsylvania 

Longest dimension of 

ten grains 

Low Mean High 

22.1 24.3 26.0 

27.3 30.2 33.0 

24.7 26.3 28.6 

37.7 39.9 42.9 

39.0 43.2 45.5 

48.1 50.6 53.3 

45.5 49.9 53.3 

36.4 41.9 49.4 

32.5 38.4 41.6 

44.2 48.9 54.6 

50.7 54.5 58.5 

49.4 51.5 54.6 

46.8 50.2 53.3 

44.2 48.9 52.0 

42.9 45.1 48.1 

32.5 36.4 39.0 

36.4 40.4 44.2 

35.1 39.5 44.2 

39.0 42.9 50.7 

29.9 31.5 33.8 

29.9 33.9 37.7 

32.5 33.2 33.8 

26.0 28.7 31.2 

26.0 28.2 29.9 

28.6 3.1.3 33.8 

29.9 33.2 35.1 

32.5 34.1 36.4 

31.2 33.1 36.4 

29.9 32.9 36.4 

28.6 31.9 33.8 

31.2 33.9 36.4 

178

49, 

50,

21, 

24 

126

19, 

23 

194 

67,

55, 

59, 

60, 

57, 

86 

85,

87,

79, 

206 

36, 

35, 

151

114 

31, 

112

94 

99 

33, 

46. 
Table 1.-Continued 

Species 

J. dubia (Maximowicz) Bentham & Hooker 

Leontice altaica Pallas 

L. armenaica Boivin 

L. euersmannii Bunge 

L. leontopetalum L. 

L. odessana Rogowicz 

Mahonia fremontii (Torrey) Fedde 

M. haematocarpa (Wooton) Fedde 

M. neruosa (Pursh) Nuttall 

M. oiwakensis Hayata 

Nandina domestica Thunberg 

Podophyllum hexandrum Royale 

P. hispidum Hao 

P. peltatum L. 

Ranzania japonica (Ito) Ito 

Vancouueria chrysantha Greene 

V. hexandra Morren & Decaisne 

V. planipetala Calloni 

Collection Localion 

Longest dimension qf 

ten grains 

Low Mean Hiph 

Palczevsky 3616 US U.S.S.R. 

Mrs.R. K. Smith s.n. 30 May 38 US Korea 

Anon. 597803 US 

Koelz 14701 US 

Sintenis 121 MO 

Zillett & Rawi 10275 US 

4. Dojcz s.n. 5 Apr 08 MO 

Hope 9396 US 

McKelvey 1225 US 

Belton s.n. 26 May 43 US 

Wilson 10844 US 

zheng 2098 US 

rai & Class 4034 US 

Wilson 2379 US 

Rock 12259 US 

Rock 12259 GH 

Rock 12424 GkI 

Braun 391 1 US 

Zrampton 76 US 

lones s.n. 21 Mar 62 US 

McDougall 1231 US 

\Tease 3 10 US 

Vurian 1914 US 

Ricksecker s.n. 20 May 95 US 

Rowell, York & Tharp 47 I7 1 US 

rhieret 10356 US 

Zult. 12 Apr 47 K 

Epstein s.n. Cult. US 

rakeda s.n. 27 Aug 05 K 

rerabayashi 154 KYO 

rhompson 4605 US 

illen 66 US 

Ebert s.n. Aug lY20 US 

;onstance 2514 US 

Yoover 5046 US 

r. T. yu, 15977 A 

U.S.S.R. 

Iran 

U.S.S.R. 

Iraq 

U.S.S.R. 

Arizona 

Arizona 

Oregon 

Formosa 

China 

China 

China 

China 

China 

China 

China 

Kentucky 

Illinois 

Alabama 

Mississippi 

Tennessee 

Georgia 

Ohio 

Texas 

Louisiana 

England 

New York 

Japan 

Japan 

Oregon 

Washington 

Washington 

California 

California 

27.3 29.3 31.2 43, 

29.9 32.5 35.1 44, 

42.9 48.8 53.3 61, 

52.0 54.7 57.2 65, 

39.0 43.7 48.1 71, 

52.0 55.1 58.5 69, 

42.9 46.5 49.4 63, 

31.2 35.2 41.6 25, 

31.6 34.1 39.0 30 

49.4 51.2 53.3 27, 

29.9 33.8 37.7 29, 

41.6 44.2 48.1 207-

35.1 39.4 42.9 89, 

35.1 38.9 41.6 

31.5* 33.3* 35.8* 83, 

32.5* 33.3* 34.2* 198

27.3* 28.9* 31.3* 82 

36.4 38.9 41.6 81, 9

33.8 37.3 40.3 109

29.9 36.0 40.3 77, 7

32.5 35.4 39.0 

31.2 33.9 36.4 75, 7

32.5 36.5 41.6 

32.5 35.3 39.0 200, 

32.5 35.4 39.0 

35.1 38.5 41.6 73, 7

35.1 37.7 41.6 

141, 

213 

36.0 38.0 142, 

30.0 32.6 35.0 139, 

32.5 34.7 37.7 41, 4

32.5 34.6 35.4 

33.8 39.4 41.6 39, 4

33.8 36.5 40.3 101 

35.1 38.1 41.6 37, 3
TABLE 2.-Centrospermae specimens examined, alphabetically by family (grain size in pm) 

~ 

Species 

AIZOACEAE 

Acrodon bellidijlorus N. E. Brown 

CARYOPHYLLACEAE 

Tunica stricta (Runge) Fischer & Meyer 

PORTULACACEAE 

Anacampseros jilamentosa Sims 

Species 

Longest dimension of 

ten grains 

Collection Location Low Mean Hi,gh 

Van der Bijl 33 K S. Africa 26.9 27.0 28.6 

Goloskokov s.n. 20 Jun 59 US U.S.S.K. 22.1 23.1 24.7 

Rose & Stewart s.n. 1912 US S. Africa 51.0 54.3 58.5 

TABLE 3.-Ranunculaceae specimens examined, alphabetically by genus (grain size in pm) 

~ 

Batrachium aquatile Dumortier 

Clematis heracleifolia De Candolle 

Glaucidium palmalum Siebold & Zuccarini 

Hamadryas magellanica Lamarck 

Hepatica transsiluanica Fuss 

Hydrastis canadensis L. 

Kanunculus oreophytus Delile 

Collection 

Larsen & Pedersen s.n. 12 Jun 67 US 

Mrs. R. K. Smith s.n. 11 Aug 34 US 

Takeda s.n. 23 May 07 US 

Goodall 1073 US 

Richter s.n. 2 Apr 02 US 

Hardin 610 US 

Ricksecker s.n. 12 May 95 US 

Mearns 1402 US 

Location 

Denmark 

Korea 

Japan 

Argentina 

Hungary 

Arkansas 

Ohio 

Kenya 

Longest dimension of 

Low 

29.9 

22.1 

24.7 

26.0 

33.8 

19.5 

19.5 

36.4 

_____ 

ten grains 

Mean 

33.4 

24.7 

26.3 

28.7 

38.0 

22.8 

22.6 

37.8 

____

High 

36.4 

26.0 

27.3 

29.9 

41.6 

26.0 

26.0 

39.0 

FIGIJRES 7 12.-Ranunculaceae pollen, SEM: 7, Rununcu1u.r orrophytus Delile, pantocolpate, polar 

view, X 2260 (Mearns I402 US, Kenya); 8, K. orrophytus, ektexine surface, X 7560 (same 

collection); 9, Clemutzs heruclezjdzu De Candolle, irregularly (panto)poratq X 3000 (Mrs. R. K. 

Sniilh s.11. 11 Aug 34 US, Korea); 10, C. heruclez~?liu, cktexirie surface, X 7.500 (same collection); 

11, G'luuczdiumpulmu~um Siebold & Zuccarini, 3-colpate, polar view, X 4500 (Takeda s.11. 23 May 

07 US, Japan); 12, G. palmatum, ektexine surface, X 10,000 (same collection). (Micrographs 

reduced to 76'%).) 
FICIJRES 15 III.-Ranunculaceae pollen, SEM: 13, Batruchium aqua/zk Dumortier, kolpate

cquatorial view, X 242.5 (1,arseri c(r Pederseri s.n. 12 Jun 67 US, Denmark); 14, B. aquatilt-

ektexirie surface, X 7500 (same collection); 1.5, Hqmcn trcln.r.riluanicu Fuss, pantocolpate, polar 

view, X 2220 (liichter s.n. 2 Apr 02 US, Hungary); 16, H. ~mns.riluanicu, ektcxine surfacc

X 7500 (same collection); 17, Hamadryas rnagellanzca Lairiarck, :3-colpate, equatorial view, X 3300 

(Goodall 1073 US, Argentina); 18, H. ma.yellanica, ektexine surface, X 7500 (same collection)

(Microsraphs reducrd to 7.5%.) 
FIGURES 19 24.-Berberidaceae, Berberis pollen, SEM: 19, H. iliczjiiliu Forster, irregular apertures, 

X 1700 (Goodall 83.1- US, Argentina); 20, B. zlic@liu, ektexirie surface, X 3000 (same collection); 

2 I, B.,fundlrri A. Gray, irregular apertures, X 2000 (Eastwooti ,5272 US, Colorado); 22, B. fendlerz, 

five grains (onc at upper left may be sterile) illustrating variation in size and apertures, X 9.1-0 

(sanir collection); 23, H. uu(yuris Id., spiral apertures, X 2050 (Soper Kr Dale 3950 US, Ontario); 

24, H. grrmu’zflora Turczaninow, four grains illustrating variation in apertures, X 790 (Arbelaez 

8r Cuatrecasas 5908 US, Colombia). (Micrographs reduced to 7 l%.) 

FIGURES 3 I 36. -Berberidaceae, Epirnedium pollen, SEM: 3 I, Epirnedium dipilyllurn (Morren & 

Ikcaisrre) Loddiges, :%-colpate, polar view, X 3400 (Anon. 13 1.2887 US, .Japan); 32, E. dzphyllurn, 

ektexine surface, X 7.500 (same collection); 33, E. sernperuirens Nakai, 3-colpate, equatorial view, 

X 3000 (Masayuki Oue 33 US, Japan); E. .~m~i~ruirms, ektexine surface, X 7480 (same 

collection); 35, E. hreozcurnu Maximowicz, 3-colpate, equatorial view, X 2700 (Rock I2302 US, 

China); 36, 1;. nlpinurn L., kolpate, equatorial view, X 2.500 (Porta s.n. Jim 18!)4 US, Italy). 

(Micrographs reduced to 75'%.) 
FIGURES 37~42.~--Berberidaccac, Vuncouveria pollen, SEM: 37, V. plunipetulu Calloni, :$-colpate, 

equatorial view, X 2400 (Hoover 5046 US, California); 38, I:. plr~rizpetulu, ektexine surface, 

X 7500 (same collection); 39, V. hexundru Morren & Decaisne, :l-colpate, equatorial view, 

X 2320 (Ebert s.11. Aug 1920 US, Washington); 40, V. hexundru, ektcxine surface, X 7.500 (same 

collection); 4 1, I:. chrysunhi Greene, 3-colpate, equatorial view, X 2700 (Thonlpson 4605 US, 

Oregon); 42, C'. chrysnnthu, 3-colpate, polar view, X 3000 (same collect ion). (Micrographs 

reduced to 77'%,.) 
FrcirRes 43 48.~ . Bcrberidaccae, JeffPrJonzn pollen, SEM: 43, ,/pfler.ronza duhiu (Maxiniowicz) 

I~c111ham 8 I looker, 3-colpate, equatorial view, X 3000 (I’alczevsky 3616 US, U.S.S.K.); 44,J. 

dub, kolpatc, equatorial view, X 2880 (Mrs. K. K. Sriiith s.11. 30 May 38 CIS, Korea); 4.5, J. 

dubru, ektexirir surface, X 7470 (same collection); Mi,,/. di,thy//a (I,.) Persoori. 3-colpatr, equatorial 

view, X 2.500 (Raxtcr s.11. 1.5 Apr 11 US, Ncw York); 47, J. diphyllu, :$-colpatc, polar view, 

X 3200 (Sharer Kr Miller 180a US, Pennsylvania); 48,J. dip/!y/ln, ektexirie surface, X 5280 (smie 

collcctioii). (Micrographs reduced to 75‘X~) 
FI(;~IKES .4!) 54.-Herberidacrae, Ach1v.r and tfydrnmrli\ pollen, SEM. 49, Arhlyc trzphyllu (Smith) 

1k Ca~~tl(ill~~., kolpate, equatorial view, x :5400 (Chldrr & Savile 8 

.50, A. trzphyNa, :kolpate, polar view, X 2800 ( rt s.11. 1920 US, Washington); 51, A. trzphyllu, 

rktexirrr surf;ice, X 6300 (Caldcr & Savile 8 CJS, Chnadaj; 52, Ilydru.\/l.~ canadensk L., 3 

colptr, eqIIatorial virw, X 4000 (Hardirr 610 US, Arkansas); 53. 11. canndmsis, 3-colpate, polar 

virw. X 4750 (Kicksecker s.11. 12 May 9.5 US, Ohio); 54, H. cnnadtn.rz.\, :kolpate, equatorial 

view, X ,5000 (simie collection). (Micrographs rrducctl to 7 1'% .j 
FIGIIRES 55--60.-Berberidaceae, Cuulophyllurn pollen, SEM: 55, C. robusturn Maximowicz, 3- 

colpate, equatorial view, X 1700 (Kirino 713 IJS, Japan); 56, C’. robmtum, ektexine stirface, 

X 5000 (same collection); 57, C. thalictrozdes (I,.) Michaux, ?-colpate, equatorial view, X 1900 

(€ienry 57 I US, Pennsylvania); 58, C. thaliclroida, ektexine surface, X 7500 (same collection); 

59, 0’. robusturn, ektexine surface, X 5000 (Moran 5204 US, Korea); 60, C. thulictroides, ektexine 

surface, X 10,000 (I tarper 3864 [JS, Alabama). (Micrographs reduced to 77%) 
FIGURES 6 1-66.--Herberidaceae, Leontzce pollen, SEM: 61, L. allazcu I'allas, holpate, equatorial 

view, X 1920 (Anon. 597803 US, U.S.S.R.); 62, I.. allazca, cktexirrr siirfacc, X 7.500 (same 

collection); 63, I,. odessana Kogowici, 3-colpate, equatorial view, X 2000 (A. I)c?jcz s.n. 5 Apr 08 

MO, [J.S.S.R.); 64, L. odestnna, ektexine surface, X 7.500 (same collection); 65, L. ur~nmaicu 

Roivin, ?-colpate, equatorial view, X 1700 (Koelz 14701 US, Iran); 66, L. urrnenaim, ektexine 

surface, X 7480 (same collection). (Micrographs redi~ced to 77Y .) 
FIGURES 67~72.-Rerberidaceae, Bongardia and Leontice pollen, SEM: 67, Bongardiu chrysogonum 

(L.) Spach, kolpate, equatorial view, X 1670 (Sintenis 35 US, U.S.S.R.); 68, B. chrysogonum

ektexine surface, X 7.500 (same collection); 69, Leontice leonlofietalurn I>., kolpate, equatoria

view, X 1800 (Gillett Pr Rawi 1027.5 US, Iraq); 70, L. /eontopelalzrm, ektexine surface, X 750

(sanic collection); 7 1, L. euersmannii Bunge, 3-colpate, equatorial view, X 2300 (Sintenis 12

MO, U.S.S.K.); 72, I,. evrrsamannii, ektexine surface, x 7500 (same collection). (Micrograph

reduced to 77'h.) 
F~c:riws 73~78.~Herberidaceae, I’orfophyllurn pellakun pollen, SEM: 73, 3-colpate, equatorial 

view, X 2500 (Kowell, York & ‘l’harp 47171 CIS, ‘Iexas); 74, cktcxiric surface, X 7530 (same 

collection); 7.5, :kolpate, rquatorial view, X 2910 (Mcl)ougaII 1231 US, Mississippi); 

76. rktexiric surface, X 7.500 (sanic collection); 77, 3-colpate, equatorial view, X 2600 (Crampton 

76 US, Illinois); 78, ektexine surface, X 7500 (same collection). (Micrographs reduced to 79‘X .) 
FIGIJRES 79-84.-Berberidaceae, Dysosma arid Podophyllum pollen, SEM: 79, Dysosmu pleianthu 

(Hance) R. E. Woodson, kolpate, polar view, X 2000 (Steward & Cheo 210 GII, China); 

80, I). pleiaritha, 5-colpate, equatorial view, X 2000 (same collection); 8 1, I’odophyllurn hz,\/lzdurri 

Hao, :kolpate, equatorial view, X 2000 (T. T. Yu 15977 A, China); 82, f’. hexundrum Royale, 

rhomboidal tetrad, X 1500 (Rock 12424 GH, China); 83, 1’. hexandrum, tetrahedral tetrad, 

X 141.5 (Rock 122.59 US, China); 84, f’. hexandrum, ektexirie surface, X 7.500 (same collectiori). 

(Microzraptis rc:duced to 74‘%.) 
Fic:rrues t(,~~!)O.~Berberidaceac, Diphylleiu arid Nundinu pollen, SEM: 8.5, II$il$h cymosu 

Michaux, S-colpatc, equatorial view, X 2200 (Pollard s.n. 16 May 01 US, North Carolina)

86, I). cymo.\a, ektexine surface, X 5000 (Brauri s.11. 25 Apr 27 US, Teiinessee); 87, I). .rznun~ir Li

kolpate, equatorial view, X 2250 (Rock 4230 US, China); 88, D. .sinmsz.v, cktexirie surface

x 5300 (same collection). 89; Nundznu domestzcu Thuriberg, 3-colpate, equatorial view, X 2500 

(Tai I(r Class 4034 US, China); 90, N. domeJtzcu, ektexine surfacc, X 8400 (same collection)

(Micrographs reduced to 73'K.) 
E'IcuREs 9lp96.--Berberidaceae pollen, view of ektexine surface, SEM: 91, Podophyllurn hispidurn 

Hao, X 5000 (T. T. Yu 15977 A, China); 92, Dysosmuplezunlhu (Hance) R. E. Woodson, X 5000 

(Steward & Cheo 210 GH, China); 93, JeSfersoniu dubzu (Maximowicz) Bentharn & Hooker, 

X 7520 (Mrs. R. K. Smith s.n. 30 May 38 US, Korea); 94, Epimediurn membranuceurn K. Meyer, 

x 7500 (Forrest 25471 US, China); 95, JeJfersonzu dubzu (Maxirnowicz) Bentham & Hooker, 

x 7500 (Palczevsky 3616 US, U.S.S.R.); 96, Achlys lriphyllu (Smith) De Candolle, x 7500 (Evert 

s.n. 1920 US, Washington). (Micrographs reduced to 75%.) 
I;IC;~IRES 07 102. -1krl)eritlace;re pollcri, view ofektexine surface, SEM: 97, Vuncouvrriu chry.\arithu 

(irwnr. X 7500 (’I‘honipsoii 460.5 IJS, Orcgon); 98, Jrflrrtonru dipliyllu (L.) I’t.rsoon, X 7500 

(Shafrr Kr Millcr 180a US, l’erinsylvania); 99, E/~i,lmrdium cqi//ulum (Siebold Kr Zuccaririi) 

Maxiriiowicz, X 7500 (Anon. 13 148180 US, Japan); 100, Vunrouueriu hexundru Morreii Kr Decaisne, 

X 7.500 (t<hert s.11. Aug l!UO US, Washington); 101, I’. pluni/~e/alu Callorii. X 7.500 (Chistarice 

25 14 LJS, California); 102, C’. plunzpelulu. X 7.520 (Hoover ,5046 US, California). (Mici-ogi-aphs 

reduced to 77% .) 
FIGURES 103 108.- Berberidaceae and flydrustzs pollen, view of ektexine surface, SEM: 103, 

1lydra.rlz.c cunudenszs Id., X 10,000 (Hardin 610 US, Arkansas); 104, Epirnedzurn ulpinum L., X 7500 

(Porta s.11. Jun 1894 US, Italy); 105, E. hrevzcornu Maximowicz, X 7.500 (Rock 12302 US, 

China); 106, Podophyllurn pellutum L., X 7530 (Rowell, York 8r Tharp 47171 US, Texas); 107, 

~JefJkrsoniu diphyllu (L.) Persoon, X 7500 (Baxter s.n. 1.5 Apr 11 US, Ncw York); 108, 1’. peltaturn 

I,., X 7.510 (McUougall 1231 US, Mississippi). (Micrographs reduced to 77‘%.) 
FIGIJRES 109 1 14. ---Rerberidaceae pollen, view of ektexine surface, SEM: IO!], I’odo/,/y//um 

/w/t/~t/m L.. X 7.500 (Braun 391 1 US, Kentucky); 1 10, Epzrnrdiurn ~ernpr~vrert.~ Nakai, X 10,000 

(Masayriki Orre 33 US, .Japan); 11 1, f’. peltaturn, X 7:i60 (Mc1)ougall 1231 CJS, Mississippi); 

1 12, E. grartd!florurrr Morreri, X 14,920 (Togasi I03 1 lJS, .Japan); 113, f’. p~//a/urn, X 7490 

((hnipron 76 IJS, Illinois); 114, E. rremeiirn Nakai, X 10,000 (Kit-ino 618 US. Japan). 

(Micr-ographs rrdirced to 79‘XB.) 
54 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FIG~JRICS 115 123.-Ranunculaceae and 1IydruJtz.s pollen, TLM. Most of the taxa in the 

Kaniinculacae were similar in thin section: an endcxinc wcll developed in aperture regions and 

disriiptrd but still conspicuous in non-aperture regions; foot layer rclatively unifomr in the 

sense that none of the taxa examined had very thin or vc:ry thick foot layers; prominent 

colnnrellac, which in sonie taxa appear to penetrate the endexine in the apertures (see discussion 

in text as wcll as Figure 149 of E/~zmedzum dzphyllum, Figure 1.54 of E. crrmrum, Figurc 15.5 of E. 

,qrandIflorum, Figure 159 of Vancouruerza, Figure 161 of V. hrxuridra arid Figure 169 of V. planlprtala); 

tectunr uniform or average in thickness, but with perforations and spines, the latter sometimes 

large. 11.5, Ranunculus orro/ihytu.v, the massive colurnellae appear to be continuous with foot laycr 

and tectum, the endexine is well represented but somewhat disrupted, note acetolysis-resistant 

spongy material in the area between foot layer arid tectunr, X 12,760; 116, I<. O~~O/I/$US, section 

through the colpus showing highly lamellate endexine and aperture columellae, which appear 

to penetrate the endexine, X 12,760; 1 17, C’lernutiJ herackz/blzu, section through mesopore, note 

acctolysis resistant material between foot layer and tectum as shown in Figure 11.5, X 16,240; 

I 18, C:lnuczdiurn palmalurn, an example of this family with reduced columellae, X 12,650; 

1 19, .!latrachziini ciquatilr, typical Ranunculaceae structure, X !)!)00; 120, Hepulicei trc~n.~.duanzca

the tecturn is commonly channeled-perforate, a portion of the colpus (at thc right) contains 

aperture colunrellae as described in Figure 116 (see also right sidc of Figure 119). X 6120; 121, 

Hamadrycis mayllanzcci, typical Ranunculaccar structure (conrlxirc with Figures 1 1.5, 1 19), 

X 9570; 122, flyd7USlzs rrinadrnszs, low niagnification, nredian section more or Icss, as discussed in 

text notc thc: lack of similarity to other Kanunculaccae pollen grains (Iigures 11.5- 121) and 

general over-all similarity to JdjkrJonza dubza, ligure 173, and Vuncouumu hexandru, Figurc 163, 

X 1100; 123, 11. ranndrnszs, see legend comments to Figure 122, X (i120. (Scales equal 1 pi.) 
SMITHSONIAN CONTRIBUTIONS TO BOTANY 
I;ICURES 124- 127. He7h~ri.r pollen, ’I‘EM: 121, H. fendlerz, section of illen en prepared by rehydration in glutaraldehydc followed by stainirig in 0sOq, the outer part of ttic exirir (viz., 

cktexirie) is surrounded or encased by electron-translucent layer which is indicated in part by 

t hr arrows; the ektexine (ek) contains c:lectroIi-densc material as well as cavities of variou 

at thr interface with eridexirie (en), the ektexine is very irregular arid contains deep chaririels 

that at least in some instances appear to extend to ttic surface; the endexine is granular, slightly 

more electron dense than the ektexine, and has a smooth iririer wall; the intiric. (in) is thick (see 

portion of cytoplasm at lower right just beneath scalr), contains nunierous, electron-dense, large 

granules (possibly resulting from OsO4 staining), X 12,120; 12.5, B. ,findk72, a section of an 

acetolyzed grain from the same collection as above, in contrast to Figurr 124, all of the ektexine 

is very electron dense arid the heterogeneity is obscured, and it appears that acetolysis removed 

the thin laycr encasing the grain, X 21,280; 126, H. ,qrundtfZoru, section of acetolyzed grain, the 

orpnizatiori of the iririer half of the ektexirie suggests “~~rot~~e~~luinellae,” thc more or less solid 

outer half suggests a massive “tectum,” the protocoliirriellae terminate individually on the 

granular rridexiric, thus the exirie lacks a honiolog of the foot layer, X 16,720; 127, LL ,przd!fluru, 

aperture view, thc ektexine is less “structured” in the aprrturc and is represented by “nodules” 

or “islarids” above the granular cndexine, X 11,890. (Scales cqual I pi.) 
58 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FINJKES 128-1 32.-Rerberzs zlzczfulza pollen, TEM: 128, low magnification of entire grain, median 

section, X 2590; 129, low magnification of very oblique section enhancing a massive ektexine 

arid a consistent endexine, X 2000; 130, in this radial section, the ektexine is not continuous 

and consists of large, irregular blocks separated from each other by channels partially filled 

with an endexinc-like substance, X 21,460; 131, section more oblique than in previous figure 

and showing granular acetolysis-resistant material above ektexine surface, X 13,340 (this 

contrasts with Figure 125 in which the layer was removed by acetolysis); 132, aperture view 

showing “nodules” of ektcxine on arid partly embedded in, granular endexine (compare with 

IkrbrrzJ ,qrundij7ora, Figure 127), X 9180. (Scales equal 1 pm.) 
60 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FICUKES 133 138. -Mahonza pollen, TEM: 133, M. neruosa, acetolyzed grain, the ektexine is very 

irregular at the interface with thc endexine but does suggest “~~rotocolumellae” separated by 

cavities filled with an endexine-like material; the endexine proper is granular, uniform in 

electron density (relative to that in the cavities), and very smooth on the inner wall, X 35,340; 

134 arid 13.5, M. neriiosa, views of apertures showing granular endexirie supporting “islands” of 

ektexine (comparc with Figure 127 of Berherz~r grandZ/loru, Figure 132 of H. ilzczjdta, and Figure 

141 of h’unzania japonzw), 134: X 16,740, 135: X 10,620; 136, M. ozzuakeri.\z.r, the ektexine is 

comrrronly fragmcnted by channels (compare with Figure 130 of Rerbrrzs zlzcz/ulzu), short, 

irregularly shapcd “protocolumellae” are evident at base of ektexine (see legend to Figure 133), 

X 15,580; 137 arid 138, M. ozuiakens?s, rehydrated pollen grains (as described for Berberzs,findlerz 

in legend to Figure 124), in Figure 137 the “protocolumellae” (arrows), while less clearly 

differentiated than after acetolysis treatment (compare with 1:igure 136), are nearly identical to 

section of M. neruosa (Figure 133), Berberzs ilzcfilzu (Figure 130), R. /i~f/er? (Figure 125), and 

h‘an~arizu~aponlca (Figures 142, l43), X 3800; 138, low magnification near median view prepared 

as discussed imnrediately above, it is noteworthy that the combination of low magnification 

anti lack of acctolysis imparts a nearly amorphous appearance to the exine, X 4900. (Scales 

equal 1 pm.) 
62 SMITHSONIAN CONTRIBUTIOKS TO BOTANY 
FK;IJRICS I39 148.-Karizania yi/ionicu pollen, SEM arid TEM: 139, (7iwhnyu.h 1.74 KYU, 

Japan), SEM showing two pollen grains that appear attached (arrows) as dyads, X 14.50; 

140, (Trmbuycishr /.74 KYO, .Japan), SEM showing psilate-puiictate cxinr surface, X 7.500; 

141, (Cult. 12 Apr 47 K, England), TEM in colpus showing threc grariiilcs of ektexiiie above 

a disrupted endexine, X 13,650; 142, (Epstein s.n. Cult. [JS, New York), TEM through colpub 

arid adjaccnt mc:socolpus, the endexine in the colpus is both more larirrllate aiid reduced than 

in thc rnesocolpal areas, where it is smooth and regular, the ektexine is very similar in structure 

to that of Uerbrn\ (Figures 124- 132) and Muhonm (Figures 133 IM), foot layer, colunicllac, and 

tecturri are not clearly differentiated, the arrow indicates an extension of the ektexine through 

the endexinc, note that a “foot layer equivalent” appears lamellate or sheet-like in the 

mesocolpal areas, X 13,630; 143 (same collrction), section through niesocolpus, thc arrow 

indicates a free exine globule embedded in the endexine, free exiiie globules were frequently 

observed in ‘IEM of Knrizuniu and although not further illustrated in this group uf ligurcs they 

commonly occurred in clusters on the surface of the exine, to left of globule (arrow) is an 

cktexinc extension as discussed in legend to Figure 142, X 21,280; 144, (Cult. K), the massive 

cktexine arid endcxine may be, at least in part, the result of an oblique anglc of section, 

X 18,620; 145, (sanic collection), the ektexine has a very narrow “foot layer,” short, thick 

“coliiniellac” arid massive “tectrrm,” X 27,950; 146, (Epstcin IJS), tangential section, illustrating 

granular riatiire of exinc as well as thick endcxirre (cytoplasmic remains arc also present in the 

center of the exine), X 10,640; 147, (Cult. K), section ih through adjacent exincs of a dyad (see 

Figure 139) and shows a bridgelike connection (arrow) in the distal region (equivalent to region 

of arrows in Figure 139), tiotc the free exirics show a morphology similar to that descrilxxl lor 

Figure 14.5, X 9280; 118, (same collection), section of opposed internal walls of dyad indicating 

a fusion of ektexirie surfaces, X 13,6.50. (Scales equal 1 pm.) 
64 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
I;ICIJRES 149- I56-Epzrnedium pollen, 1EM: 149, R dzphyllum, low magnification of section near 

mcdian, rriesocolpus shows foot layer with channels arid without an endexinc whilc the colpus 

shows a lamellate eridexirie penetrated by columellae (ser also Vancouuerzu chrymntha, Figure 

159, V. hexandra, Figures 160, 161, and V. planzpetulu, Figure lW), X 1400; 

150, E. hrruzcornu, section through mesocolpus illustrating highly channeled foot layer, X 3800; 

151, E. cremeum, tangential section at and slightly beneath exinc surface, the arrows indicate 

cross sections of free tips of tectal rods illustrated by SEM (see Figure 114), X 4930; 1.52, E. 

crrmeum, oblique section including eridexirie in rriesocolpal region, X 3060; 153, E. cremeum, 

radial section through mesocolpus, small peak in tectuni probably represents longitudinal 

section through a free tip of a rod, X 12,880: 154, E. cremeum, colpus showing lamellate endexine 

perforated by columellae, X 10,080; 155, E. cqrandzflorum, colpiis similar to Figure 1.54, X 13J1.0; 

156, E. grandz/lorum, section of mesocolpus with samc: structiirr as in Figures 1.50 arid 1.53, 

X 36,400. (Scales equal 1 pni.) 
66 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FI(;llRk:S 1.57- 164.- Vanouuena pollen, M: 1.57, V. chrysunlha, low magnification oblique 

section near median showing endexine development in colpal regions and absence in mesocolpal 

regions as well as abundant channels in the thick irregular foot layer, X 7380; 158, V. chrysanlhu, 

angle of section is less oblique than in Figure 157, and illustrates foot layer channels and 

paucity of endexinc characteristic of the rrir:socolpus, X 9430; 159, V. chrysunthu, lower graiii 

shows thick endexinc with columellae (arrows) in colpus, upper grain shows an oblique section 

of a mesocolpus, X 9430; 160, V. hrxandru, low magnification cross section at median showing 

similar niorphology as V. chrysuntha (Figure 157), foot layer channels are abundant but less 

conspicuous because of low magnification, X 4000; 161, V. hexandru, radial section through 

colpus showing lamellar nature of endexine arid apparent penetration by colurnellae (also sec 

Figure 159), X 15,580; 162, V. hpxandrn, oblique view showing cross sections of foot layer 

channels and endexinc accumulation in colpr~s, X 4.500; 163, V. hexandru, section parallel with 

colpus showing reduced columellae, foot layer channels arid eridexine, X 11,890; 161, V. 

hrxnndra, tangrntial section illustrating reticulate arid sonirwhat striatc nature of exine surface, 

X 5.510. (Scales equal 1 pi.) 
68 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
Fic:rrwics 165 169.- Vanconueria pianipetala pollen, M: 16.5, view of mesocolpus, eridexine 

absent, the foot layer is thick, irregular and with nunierous channels, the inconsistent and 

uneven tecrum is the result of both section plane and striate pattern, the circular or club-like 

appearance of the distal ends of the columellac represent cross sections of these striae, X 26,650; 

166, oblique sectioii clearly showing endexine development in the colpus and absence in 

niesocolpns; the foot layer channels are present bul low magnification and dark printing tend 

to obscure them, X ,5460; 167 and 168, tangential sections at and slightly beneath exirie surface, 

Figure 167 agrees with thc mostly parallel exine striae depicted in SEM, Figures 37, 38, 101, 

arid 102, just as the tangential section of V. iiuxandru (1:igure 164 ) agrees with the tectiim 

deipictcd in SLM, (Figures 39, 40, and loo), X 5760, in Figure 168 cross sections of columellae 

arc ~urrounded by exine striae, x 5290; 169, upper grain highly oblique section erriphasizing 

striate exine surface and foot layer with barely visible cross sections of channels; lower grain 

shows a colpus wir h thickened endexine and colurriellae, as described previously (see V. 

~h~.tu~ilh~~, Figure 159, and V. hexandra, Figiirc Ifl), X ,5460. (Scales equal 1 pin.) 
70 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FI(XJRI~S 170 179. JeJersoniu arid Achlys pollen, TEM: 170, J. dzphyllu, rnesocolpal view, note 

the well dcvrhped arid essentially uniform endexine which contrasts with the highly irregular 

foot layer, X 10,080 (Shafer Nr Miller 180a US, Pennsylvania); 171,J. diphyllu, low magnification 

view including portions of each mesocolpal region, X 5000 (same collection); 172, J. dubiu, low 

magnification, median section, the endexirie is present in rnesocolpus but is irregular; the 

beaded appearance of the tecturri is due to the mostly parallel striae being cut perpendicular to 

the long axis, X 3780 (I’alczevsky 3616 US, U.S.S.R.); 173,,/. dubia, section in colpus region 

indicates cktexirie elernents do not penetrate endexine as is commonly noted for Epimpdzum and 

Vuncouuerzu, X 6200 (same collection); 174, J. dubzu, mc:socolpal-colpal (at bottom) view, arrow 

indicates “inner” striae, note the regular and consistent foot layer arid eridexine, X 9120 (same 

collection); 175, Achlys lrzphyllu, low magnification median section, the endexine is very narrow 

in the mesocolpus and thicker in the colpirs, the foot layer is thicker than the endexine and 

highly irregular, X 4300 (Calder Kr Savile 8 US, Canada); 176, A. lriphyllu, mesocolpal 

section, the numerous openings in the tectum, reflect packing of striae as discussed in text, 

X 4600 (same collection); 177, A. triphyllu, section in colpus showing reduced ektexine over 

endexine (see corririierits to Figure 173 above), X 8410 (same collection); 178, A. juponicu, low 

rnagnificat ion of a near equatorial section (approximately perpendicular to section in Figure 

175), X 4000 (Terabayashi 209 KYO, Japan); 179, A. pponzcu, in this tangential view the 

openings (see legend to Figure 176) are abundant in the ektexine, X 4060 (same collection). 

(Scales equal I p.) 
72 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
E’IGIJRES 180- 189.- Leonticr and Caulophylhm pollen, TEM: 180, L,. nrmeniaca, section of niesocolpus showing a thick, uniform, and lamellate endexine, irregular foot layer with ctiannrls. 

short columellae and thick, irregular, incomplete tectum, X 10,120; 181, L,. armenzacci, at rriargirr 

of colpus emphasizing channeled foot layer and thickening of endexirir (to the left), X 5880; 

182, L. urrncnzucu, section includes colpus arid shows ektexine fragments on surface of endexine, 

these fragments appear joined by a narrow foot layer, X 5880; 183, L. lPO7llO/Jdfhm, low 

magnification, median section, the endexirie is well developed in non-apertural regions as well 

as in the colpus, X 3010; 184, Chulophyllurn robusturn, low niagriification median section illustrating 

same basic structure as in Figure 183: incomplete tectiim, short columellae, channels in foot 

layer, endexirre present in [ion-aperture arid apcrt lire regions, note trace of foot layer across 

colpus as suggested in Figure 182, X 2800; 18.5, C. thalictrotd~.r, tangential scction illlistrating 

circular lumina of exine surface as shown in SEM (see ligure 60), X 2990; 186, C. thalzchzh, 

tangential view but including cross sections of columrllae, X 2990; 187, C. thalzctrozd~s, oblique 

cross section indicating iiriiforni endexine, X 1400; 188, C’. thnlictrozdes, colpal view showing 

thickened lanrellate endcxirie supporting fragments of ektexine, X 6480; 189, C. thalictrozdur, 

nicsocolpal view similar to I,. urmenzuca in ligurr 180. I.. lron~oprtalurn in Figure 189 arid C 

robusturn iri Figure 181, X 11,310. (Scales equal I pi.) 
74 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FIC~JRES 190- 197.--Hnn~ardin chrysogonum pollen, TEM arid SEM: 190, low niagnification 

median section showing portions of the three apertures, note that the endexine is only developed 

in the colpal rcgions (arrows), X 2730; 191, tangential section just beneath tectum and showing 

cross sections of coluniellae, X 1400; 192, section of colpus emphasizing thinning of foot layer 

and presence of endexine, X 4370; 193, mesocolpal view showing thick irregular foot layer 

containing numerous channels, an endexine is not present in this area of the exine, X 15,960; 

194, SEM of fractured grain, the long, slender coluniellae in the mesocolpus and thick, irregular 

foot layer correlate well with TEM (Figures 190 and 193), X 6060; 195, tangential section 

showing reticulate exine surface, note identical correlation with SEM surface in fractured grain 

(Figurc 194, exine fragment to the left of the scale), X 2.530; 196, section parallel with the 

colpus showing well developed and uniform endexine, although not clearly shown the foot 

layer has channels (see Figure I%), note that in the coipus the columellae are reduced (as in 

Figures 190 and 194 which show both colpal and mesocolpal regions), X 11,310; 197, highly 

oblique section that includes a substantial area of a colpus (bottom half of TEM), X 3700. 

(Scales equal 1 pm.) 
76 SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FIMJRE~ 198-206.-- I’odophyllum, Diphylleza arid Dywsmu polleri, M: 198, l’od~ip~~llurn hexundrum, 

portion of two members of mature tetrad, some gemmac on thc distal or free exine surfaces 

confirrii the ripple-likc morphology depicted in SEM (see Figure 84), note thickened, undulatc. 

structure of the foot layer in the oblique section of distal surfacc of tetrad member at the right 

(arrow), the tectum between tetrad members is shared, resulting in a solid layer that is attached 

to each individual grain by it’s columellae, the endexine is uniform, riarrow and disrupted (at 

left), X 3800; 199, P. hexandrum, view of external or distal surface, which, in contrast to Figure 

198, shows a slightly thicker endexine, X ,5320; 200, P. pvl/ulurn (Nunan /9/4 US, Georgia), the 

obliquc angle of section has enhanced the thickness and irregularity of the tectuni produced by 

ttie “flattened rods” (see SEM Figures 109, 11 1, 1 13), the foot layer is thin and irregular and 

decreases toward the colpus (at the right), the endexine is fairly iinifornm, slightly thicker than 

the foot layer and increases in the colpus, X 12,180; 201, 1’. peltutum (same collection), in 

contrast to Figure 200 this section is less oblique and more parallel to the colpus, the eridexine 

is smooth, uniforrn arid considerably thicker than thc narrow, somewhat intermittent foot layer, 

thc colurnellae are short and well developed, the tectiim is thick and fairly regular, the 

protrusions from [he tecturri probably represent sections through free tips of rods, X 12,180; 

202, 1’. pellaturn (Hruun .39// US, Kentucky), section includes colpus, note that exine area to the 

left of the colpus resembles Figure 201 while exine to ttie right of thc colpus resembles Figure 

200, in thc colpus flecks of exine appear to be supported by a narrow foot layer, the endexirie 

is not clearly differcritiated from the foot layer but is thickened, lamellate and somewhat 

disrupted, X 9430; the pleomorphic nature of the exirie of 1’. peltalum as shown in Figures 200 

202 supports results from SEM (see text discussion); 203, Dzphyllezu cymosa, radial section through 

niesocolpus, the cndexine is narrow, uniforrn and about equal to the irregular foot layer; the 

short, regular columellae support a thin tectum interrupted by massive spines, X 11,020; 

204, I). rymoui, section through colpus illustrating endexine thickening, X 9660; 205, D. sznensis, 

slightly oblique section through mesocolpus, X 8050; 206, I)ysoJrna plezuntha, ripper grain shows 

slightly obliqiic section through mesocolpus and lower one shows section through colpus, note 

that undulating outer surface of foot layer corresponds with undulating inner surface of tectum, 

the two layers are separated by narrow colurnellae, the colpus shows thickened, highly lamellate 

ciidexirie. X 6300. (Scales equal 1 pm.) 
7% SMITHSONIAN CONTRIBUTIONS TO BOTANY 
FIGURES 207 21 I.-Nundznn dompstzm pollen, TEM: 207, the most striking aspcct of the central 

grain and parts of three surrounding grains is the remarkably developed endcxinc, which in 

most of thcse sections is thicker than the entirc cktcxinc, a condition unparalleled for Berberidaceae pollen; the tecturii is considered to be thick, hiit thc columcllae are very reduced and 

the foot layer thin; note traces of ektexirie in the aperture as well as the gap between nieso and 

colpial endexine (arrows), X 4200; 208 and 20!), tarigential sections. in Figure 208 the section 

is at the cxinc surface and shows the punctate morphology illustrated by SLM (Figures 89, YO), 

X 6670, in Figure 209 part of the section (i.c., thc surrounding margins) shows the punctate 

surface morphology (as seen in Figure 208) whilc the ccntral arca represents the region beneath 

the tecturn surface and distinguishes the narrow coluniellae depicted in Figure 207, X 4620; 

210 and 21 1, oblique sections that include the three apertures, in Figure 210. which is highly 

oblique and close to a pole, the massiveness of thc cndcxinc is cxaggerated, X 6300, in Figure 

21 I, which is less oblique, the thick cndexine is again emphasized arid may also be sorncwhat 

lamellar (arrows), x 4900. (Scales equal 1 pm.) 
80 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

FIGURE 2 12.-Herbarium specimen, Ranranza pponzca (Ito) Ito, cultivated, Royal Botanic 

Gardens at Kew, 12 April 1947 (K). 
NUMBER 50 

FIGURE 2 13.-Herbarium specimen. Ranzaniu japnoica (Ito) Ito, Takedu s.n., 27 .4ugust 190.5 

(K), Japan. 

81 
82 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

FIGURE 2 14.-Herbarium specimen, Berbens arnu~ensis Ruprecht, Korshznsky s.n., 22 May 1891 

(US), U.S.S.R. 
NGMBER 50 

FIGURE 2 15 -Herbarium specimen, Mohonia japontca De Candolle Mtrushtma s.n, 22 March 

1954 (US), Japan. 

83