sign in sign up
<<
Home , Abronia (plant), Acantholimon, Achyronychia, Antigonon, Armeria maritima, Beta (plant)

SMITHSONIAN CONTRIBUTIONS TO BOTANY 0 NUMBER 37

Pollen Morphology and the Relationship of the , , and Prirnulaceae to the Centrospermae

Joan W. Nowicke and John 3. Skvnrln

SMITHSONIAN INSTITUTION PRESS City of M7ashington 1977 ABSTRACT Nowicke, Joan W., and John J. Sklarla. Morphology and the Relation- ship of the Plumbaginaceae, Polygonaceae, and to the Order Centro- spermae. Siiiz1hsoniun Contl-zbzitions to L’olany, number 37, 64 pages, 200 figures, 3 tables, 197’i.-Three families, Plumbaginaceae, Poljgonaceae, and Pi imulaceae, are consiclei ed to be related to or dei i\ ed from the 01der Centrospei mae by 1 ari- ous authors. These three families hai e pigments in contrast to the found in all but tu o families in the Centrospermae. In addition, all three are known to hale staich-tjpe sieie-tube plastids in contrast to the piotein type found in all centiospermous families. Examination of the pollen of 134 by SEN, TEN, and light micioscopy reiealed g.reat dii ersity, especially in the Polygonaceae, but not the spinulose and tubuliferous/punctate ektexine, which characterizes the iast majoritj of the centrospermous taxa. Recent ei idence argues against a close relationship of the Plumbaginaceae, Pol) gonaceae, and Primulaceae with the Centrospei mae, and the absence of any pollen tjpes com- mon to the three families further suggests that they are not closely related to each other.

OFFICIALPVBLICATIOS DATE is handstamped in a limited number of initial copies and is recorded in the Institution’s annual report, Smithsoninn Year. SERIFSCOVER DESIGN: clearing from the katsura Cercidiphylltcm japoniczcm Siebold and Zuccarini.

Library of Congress Cataloging in Publication Data Sorvicke, Joan LV. Pollen morphology and the relationship of the Plumbaginaceae, Polygonaceae, and Primulaceae to the order Centrosperrnae. (Smithsonian contributions to botany ; no. 37) Bibliography: p. 1. Plumbaginaceae. 2. Pol>-gonaceae. 3. Primulaceae. 4. Centrospermae. 5. Palynotaxonomy. 6. Pollen morpholorry. I. Sktarla, Tohn T., ioint author. 11. Title. 111. Series: Sinithsonian Institution. SkithsoGian contributioGs to 6ota”uy ; no. 37. QKl.S2747 no. 37 [QK495.A12] 581’.08s [583’.672] 77-608070 Contents

Page Introduction ...... 1 Materials and Methods ...... 3 Results of Pollen Analyses ...... 4 CENTROSPERMAE...... 4 PLUMBAGINACEAE...... 5 POLYGONACEAE...... 8 PRIMULACEAE...... 11 Discussion and Conclusions ...... 12 Literature Cited ...... 15 Tables ...... 16 Figures ...... 23

... 111

Pollen Morphology and the Relationship of the Plumbaginaceae, Polygonaceae, and Primulaceae to the Order Centrospermae

Joan W. Nowicke and John 3. Skvarla

Introduction Gyrostemonaceae as part of the , and Takhtajan separates it as a distinct . Takh- The Centrospermae () represents tajan recognizes the Tetragoniaceae as a separate one of the most controversial orders in the angio- family while Cronquist includes it in the . sperms. This group of at least 10 families, which in is treated as a member of the Chenopo- the past has been cited as one of the few natural diaceae by both authors; and finally Takhtajan also orders based mostly on morphological characteris- places the Hectorellaceae and the Bataceae in this tics, has unique N-containing pigments, the beta- order. lains, and a distinctive structure in the sieve-tube Thorne (1968) in a synopsis of angiosperm classi- plastids. Both Cronquist (1968) and Takhtajan fication has placed the families in a sub- (1969) unite the betalain families, Aizoaceae, Ama- order, Chenopodiinae, one of two constituting the ranthaceae, Basellaceae, Cactaceae, Chenopodiaceae, order Chenopodiales. He recognized the Gyrostemo- , , Phytolaccaceae, and naceae and the Halophytaceae as distinct families , as well as two anthocyanin families, and , in the order but treated the Molluginaceae as a in the Aizoaceae, the as a subfamily in Caryophyllales ( k Centrospermae). Both authors include Halophytum ameghinoi Spegazzini (a beta- the Phytolaccaceae, and Dysphania as a member of the Chenopodiaceae. The other suborder, Caryo- lain taxon) and the Gyrostemonaceae in this order: phyllinae, consists of two families, the Caryophylla- Cronquist (1968) treats Halophytum as a monotypic ceae and the Polygonaceae. The next order, Bati- in the Chenopodiaceae while Takhtajan (1969) gives it family status; Cronquist regards the dales, consists of only the Batidaceae, but Thorne apparently regards this family as somewhat related tithe Chenopodiales since both orders are united Joan W. Nowicke, Department of Botany, National Museum under a superorder, Chenopodiiflorae. of Natural History, Smithsonian Institution, Washington, D. C. 20560. John J. Skvarla, Department of Botany and Micro- Mabry, and Turner and Behnke biology, University of Oklahoma, Norman, Oklahoma 73019. and Turner (1971) have treated the betalain fami-

1 2 SMITHSONIAN CONTRIBUTIONS TO BOTANY

lies as a distinct group, separate from, yet closely from palynology, pigmentation, and plastid struc- allied to, the two anthocyanin families, Caryo- ture indicates that these three families are not phyllaceae and Molluginaceae. closely related to the Centrospermae. The relation- Evidence from ultrastructural research on sieve- ship of the Achatocarpaceae, a family unknown tube plastids (Behnke and Turner, 1971; Behnke, with regard to pigmentation, to the Centrospermae 1976) and pollen morphology (Nowicke, 1975; is more obscure-the pollen morphology does not, Skvarla and Nowicke, 1976) has reinforced the close in Nowicke’s opinion (1975) support a close tie, but tie between the betalain families and the Caryo- on the other hand the two genera that comprise the phyllaceae and the Molluginaceae. In an investiga- family, Achatocarpus and Phaulothamnus, do have tion of these plastids (colorless leucoplasts found in the P-type of plastid (Behnke, 1976). the sieve-tubes) of the above-mentioned families The Gyrostemonaceae have in fact been the sub- (Behnke and Turner, 1971) and the Magnoliidae ject of a multidisciplinary study (Goldblatt, et al., and Ranunculidae (Behnke, 1971), two main types 1976) in which all lines of evidence, including cyto- were found: plastids accumulating only starch and logical, argue strongly against any relationship of designated as the S-type; and plastids accumulating this family to the Centrospermae. at least some protein, variously deposited, and desig- Although there is almost universal agreement on nated as the P-type. The betalain families and the treating the betalain families as a closely related Caryophyllaceae and the Molluginaceae all had the group, the precise definition of the order Centro- P-type plastid in which proteinaceous filaments spermae, i.e., to include or exclude the Caryo- formed a peripheral ring usually around a crystal- phyllaceae and Molluginaceae, may never be re- loid. IVithin the above-mentioned families, Behnke solved to everyone’s satisfaction. Of more interest (1976) was able to distinguish three groups based on in view of the accumulating data on the Centro- the crystalloid: globular, the most common; polyg- spermae (sensu lato) is the question of the deriva- onal, found in the Caryophyllaceae and in two tion of the families Plumbaginaceae, Polygonaceae, other genera, Limeum (Molluginaceae) and Stegno- and Primulaceae from this order. sperma (Phytolaccaceae); and crystalloid-free, hav- ing only the ring, found in two families, the Takhtajan (1969) considers the Polygonales, con- and the Chenopodiaceae. taining only the Polygonaceae, as near the Caryo- Examination of the pollen of 177 species (No- phyllales, especially the Portulacaceae and Basella- wicke, 1975) by light microscopy and SEM revealed ceae, and probably derived from the same stock as that 85% had a similar type of ektexine pattern or the Caryophyllales (Centrospermae). His views on sculpture, which was described as spinulose and the the Plumbaginaceae are similar: nearest to Portula- tectum perforate, the openings described as tubules caceae and Basellaceae and probably derived from or punctae. This was the predominant ektexine pat- the same stock as Caryophyllales. He does admit tern in every betalain family and in the Caryo- that the pollen morphology of the Plumbaginaceae phyllaceae and the Molluginaceae; in some families, is different-apparently from that of Portulacaceae i.e., the Phytolaccaceae and the Molluginaceae, this and Basellaceae. pattern was the only one found. Examination of A4ccording to Cronquist (1968: 185), “both the selected taxa by TEM (Skvarla and Nowicke, 1976) Polygonaceae and Plumbaginaceae are pretty clearly revealed that the predominant pollen-type in the related to the Caryophyllales. Both have a single, betalain families and in the Caryophyllaceae has a , bitegmic, crassinucellate in a com- similar, sometimes identical, wall structure. pound, unilocular , and both have trinucleate Pollen of the Achatocarpaceae, Bataceae, Gyro- pollen. These characters are not known to occur in stemonaceae, and Theligonaceae was also examined, combination outside the subclass Caryophyllidae. but none of the species in these small families has The Polygonaceae are further bound to the Caryo- the spinulose and tubuliferous/punctate ektexine phyllales by similarities in the pollen and by a more described above. The Bataceae, Gyrostemonaceae, or less transitional group of genera which are vari- and Theligonaceae all have the starch-type plastid ously referred to the Caryophyllaceae or treated as and lack the betalain pigments. Thus the evidence a separate family, Illecebraceae. The Plumbagina- NUMBER 31 3

ceae are somewhat more isolated but may also be or another, but Janice Bittner at the Smithsonian derived from the Caryophyllaceae.” Institution and William Chissoe at the University In one respect the system of Thorne (1968) paral- of Oklahoma deserve special thanks for their fine lels those of Cronquist (1968) and Takhtajan (1969) technical assistance and helpful suggestions. The in that all three authors consider the Polygonaceae scanning electron photographs were prepared by as related to the Caryophyllaceae. Although Thorne the Scanning Electron Microscope Laboratory at the treats the Primulales and Plumbaginales as adjacent Smithsonian Institution. We also wish to thank orders indicative of some relationship, they are far Aaron Goldberg and Stanwyn G. Shetler for their removed from the Chenopodiales, at least in his critical review and Clara Ann Simmons for her linear sequence. assistance in the preparation of the manuscript. Philipson (1975) in a review paper on - This research was supported in part by BMS grant ary lines in the states that there is 75-19846 to John J. Skvarla. general agreement to exclude the Primulaceae from the subclass Caryophyllidae (sensu Cronquist, 1968). Materials and Methods “Almost as universal is the acceptance of the Poly- gonaceae as at least peripheral to the group. The Pollen of 20 species in the Plumbaginaceae position of the Plumbaginaceae remains more de- (Table 3), 85 in the Polygonaceae (Table 4) and 29 batable” (Philipson, 1975:74). in the Primulaceae (Table 5) was examined by light Hutchinson (1959: 117) regarded the Caryophyl- microscopy, scanning electron microscopy (SEM), lales (Elatinaceae, Molluginaceae, Caryophyllaceae, and transmission electron microscopy (TEM). Also Ficoidaceae, and Portulacaceae) as “a prolific herba- examined and included are 38 additional taxa from ceous group which has given rise to apetalous orders the centrospermous families (Table 2). Pollen sam- such as Polygonales, Chenopodiales, and perigynous ples were removed from herbarium material and petaliferous families as Lythrales, besides sympeta- acetolyzed according to procedure outlined in Erdt- lous groups as and Primulales.” The man (1966). Samples for the SEM were vacuum- Illecebraceae are given family status and included coated with gold, and examined and photographed as the only other family in the Polygonales. It is with a Cambridge Stereoscan MK IIA microscope. noteworthy that Hutchinson included Hemiayia, Samples for the TEM were incorporated into agar, , and , as well as rllecebrzirn, dehydrated through increased concentrations of among the genera listed at the end of the family ethyl alcohol, and subsequently embedded in description. He united the Primulaceae and Plum- araldite-epon resins (Skvarla, 1973). Some pollen baginaceae as the order Primulales, closely related samples were stained in 0.125y0 OsO, in 0.1 M so- to the Caryophyllaceae and perhaps the Saxifraga- dium cacodylate buffer for two hours prior to agar ceae. The Primulaceae, Polygonaceae, and Plumba- incorporation. Thin-sections were made with dia- ginaceae contain the anthocyanin pigments, and the mond knives, collected on uncoated grids and last two, at least, are known to have the starch-type stained with uranyl acetate and then lead citrate. of plastid (Behnke and Turner, 1971) and appar- Electron microscope observations were made with ently the Primulaceae also has this type (Behnke, a Philips model-200 transmission electron micro- pers. comm.). scope. Slides of all samples are deposited at the In an effort to resolve the limits and relationships Palynological Laboratory, Department of Botany, of the Centrospermae, pollen of Plumbaginaceae, Smithsonian Institution. Polygonaceae, and Primulaceae were examined by This study is a comparison of the pollen mor- light microscopy, SEM, and TEM. For purposes of phology of three families, Plumbaginaceae, Poly- comparison and the reader’s convenience, we have gonaceae, and Primulaceae, with the pollen of the included a brief discussion and a SEM and TEM Centrospermae, and detailed measurements and/or of a species from several betalain families, and from descriptions are not given. The species examined the Caryophyllaceae and Molluginaceae. are listed in Tables 2-5; the names were taken from ACKNOWLEDGMENTS.-In an extensive study like the herbarium labels or the most recent annota- this numerous persons have contributed in one way tions. The identifications would have to be mis- 4 SMITHSONIAN CONTRIBUTIONS TO BOTANY taken at the level of family to be significantly mis- The internal structure of the exine in various leading in this type of study, but all vouchers and centrospermous pollen types is illustrated in Fig- geographical locations are given in Tables 2-5. ures 19-28. Characteristically in the centrospermous taxa, the ektexine is well developed while the en- dexine, with few exceptions (e.g., Mesembryanthe- Results of Pollen Analyses mum variabile, Figure 19; glabra, Figure Pollen analysis of the Plumbaginaceae, Polygona- 24), is developed only in the region of the aperture. ceae, and Primulaceae revealed diverse forms within Apertures with spine-shaped flecks of ektexine are each family, especially the Polygonaceae, but no dis- common in the Centrospermae and in this study are tinctive pollen type(s) was common to all three illustrated by Opuntia (Figure 22), Limeuni (Fig- families. For this reason each family will be dis- ure 26), and (Figure 23). Representa- cussed separately following a review of the Centro- tive pollen from nine families of the Centrospermae spermae. were examined by TEM. Comparison of these data with those of earlier TEM work in the Centro- spermae (Skvarla and Nowicke, 1976) allows us to CENTROSPERMAE expand our knowledge of this order, and a brief FIGURES1-28 summary for each family is presented below. AIZoAcEAE.-Mesem bryanthemum variabile pol- The common pollen types in the Centrospermae len (Figure 19) is considerably different from that are illustrated in Figures 1-6: 3-colpate, pantopo- of M. crystallinum (Skvarla and Nowicke, 1976, fig. rate, and pantocolpate, all with a spinulose and tubuliferous/punctate ektexine. With the exception 13) in possessing a thinner tectum and columellae, of some taxa in the Caryophyllaceae which are as well as an extremely thick foot layer and a nar- row but consistent endexine. Mesembrganthemum, 3-colporoidate, the apertures in the Centrospermae pollen are simple. The most wriable class of aper- however, is a large and unsatisfactory genus and structural yariation is not unexpected. The exine tures is that of pantoporate. Anredera scandens stratification of M. varia bile bears a striking simi- (Figure 3) is usually 6-porate, with one pore on each larity to that of erecta of the Nyctagina- plane of the roughly cube-shaped grain. Gymnocar- ceae (Sklai-la and Nowicke, 1976, fig. 30). pos frziticosum pollen (Figure 4), with large, sunken pores in a geometric pattern, contrasts sharply AMARANTHACEAE.-The pollen of this family has with that of Chenopodizrm ambrosioides (Figure 5), been shown with SEhI and TEM to be highly pleo- which has numerous small pores. morphic (Nowicke, 1975; Skvarla and Nowicke, Figures 7 through 12 illustrate at high magnifica- 1976). The exine structure of Psilotrichurn amplum tion (X 7500) the ektexine surface, spinulose, and (Figure 20) extends this pleomorphism by indicat- ing a complete absence of endexine. tubuliferous/punctate, which characterizes the T ast majority (85%) of the centrospermous taxa. Hama- BASELLACEAE.-some pollen in this family is tocactus septispinus pollen (Figure 12) has the unique in having a cuboidal shape (Nowicke, 1975; largest perforations among the species examined Skvarla and Nowicke, 1976). The structure of by SEM. Anl-edera scandens pollen (Figure 21), is quite dif- Figures 13 through 18 illustrate specialized or un- ferent from that of Basella alba (Skvarla and usual forms, but at least one species, Cal-dioizerna Kowicke, 1976, fig. 19) but similar to that of ramosissima (Figure 16), has the typical ektexine. Bozissingniiltia gracilis (Roland, 1968, pl. 8: fig. 4), Two other taxa, Psilotrichtim amplum (Figure 13), a more typical member of the family. considered unusual because of the stellate aperture CACTACEAE.-Tlle structure of Opzintia Zindhei- plates, and (Figure 15), in which meri pollen (Figure 22) is consistent with other ex- the grains have a rare tetrahedral shape, also have amples of the Cactaceae. Comparison of this micro- the common ektexine pattern but a modified ~er- graph with one of Allztaz~clia(Skvarla and Nowicke, sion of it-the spines and perforations are much 1976, fig. 28) again underscores the close relation- reduced. ship of the Cactaceae and Didieriaceae. NUMBER 37 5

CARYOPHYLLACEAE.-The two taxa examined, since these types are of wide occurrence in the Gymnocarpos fruticosum (Figure 23) and Herniaria order. The evidence from plastid structure is more glabra (Figure 24), correspond in exine structure to definitive and supports the treatment of Hectorella that previously noted for the family (Skvarla and and presumably also Lyallia as a separate family, Nowicke, 1976, figs. 41-48). Additional comments or at least argues for their exclusion from the on H. glabra will be given later. Caryophyllaceae. Hectorella has the P-type plastid CHENOPGDIACEAE.-The exine structure Of Che- but lacks the polygonal central crystalloid that char- nopodium ambrosioides (Figure 25) agrees with acterizes the Caryophyllaceae (Behnke, 1975). other examples in the family: thick tectum with The pollen types in Figures 15 and 16 are rep- few spines and a thin foot layer. resentative of a small group of genera that have MoLLUGINACEAE.-The exine structure of this been treated as a subtribe, the Jllecebrinae, in the family has not been previously examined. Pollen of Caryophyllaceae (Pax and Hoffman, 1934) or given Limeum viscoszim (Figure 26) appears similar to the family status, the Illecebraceae (Hutchinson, 1959). pollen of Cometes surattensis of the Caryophyl- Pax and Hoffman regarded the subtribe as consist- laceae (Skvarla and Nowicke, 1976, fig. 41), as well ing of four genera, , Haya, , as to Mesembryanthemum crystallinurn of the and Chaetonychia, while Hutchinson's concept of Aizoaceae (Skvarla and Nowicke, 1976, fig. 13). the Illecebraceae includes several additional genera, These relationships are of interest in the context among them, Herniaria. Pax and Hoffman placed of the introductory remarks concerning the Mol- this particular genus in the first subtribe, Parony- luginaceae. chiinae, with the Illecebrinae as the second. Cron- NYCTAGINACEAE.-~bronia angzistifolia (Figure quist (1968:185) regards these genera as a transi- 27) pollen morphology differs from that of previous tional group between the Caryophyllaceae and the taxa examined by lacking an endexine. As indicated Polygonaceae. Figure 15 is a single grain of Her- earlier (Skvarla and Nowicke, 1976), however, the niaria glabra and is extremely similar to those of Nyctaginaceae display a spectrum of exine mor- Illecebrum verticillatum in scanning electron mi- phology. croscopy and light microscopy. Herniaria glabra is PORTL'LACACEAE.-The exine morphology Of illustrated because the material of Illecebrum was Naiocrene pal-vifolia (Figure 28) is similar to that insufficient for examination by TEM. Figure 16 is of other taxa examined in the family, most notably Cardionema ramosissima; material of Haya and umbellatum (Skvarla and Nowicke, Chaetonychia was not available. 1976, fig. 38). For a detailed discussion of pollen morphology Several taxa whose placement or affinities are in in the order Centrospermae the reader is advised to dispute were also examined. m inimzim consult Nowicke (1975) and Skvarla and Nowicke (Figure 9), the single species of this monotypic (1976). genus, has an ektexine pattern that is characteristic of the order Centrospermae, but the presence of PLUMBACIN ACEAE would seem to restrict the family placement to Caryophyllaceae or Molluginaceae. FIGURES29-81 Two more monotypic genera, Hectorella and Twenty species and one variety, representing Lyallia, have been united as a separate family, nine genera (Table 3), were examined by light Hectorellaceae (Philipson and Skipworth, 196l), or microscopy and SEM, and eleven of these species included in the Caryophyllaceae (Eckhardt, 1964). were sectioned and examined by TEM. In all Material of Hectorella was not available, and a taxa, the apertures appeared to be simple, mostly pollen sample of Lyallia kerguelensis yielded only 3-zonocolpate, rarely 4- (or 5-)zonocolpate, and in 10-12 grains, all of which were 3-colpate with a one collection of willmottianzim (Fig- spinulose and sparsely punctate ektexine. As with ure 59) the grains were pantocolpate. The ektexine Geocarpon, the pollen morphology of Lyallia ap- was either reticulate or verrucose, two sharply dis- pears characteristic of the Centrospermae, but in- tinct morphologies with no intermediate forms. conclusive with regard to status or family affinity These correspond to the two pollen types noted for 6 SMITHSONIAN CONTRIBUTIONS TO BOTANY the family by Erdtman (1966:325); the Baker (1948, 1966) regarded Ceratostigma and type, which is verrucose, and the Armeria type, Plumbago as having monomorphic pollen, but the which is reticulate. The Plumbago type (Figures similarity of the two forms makes them difficult to 2940, 59-64) has a well-defined foot layer, highly distinguish using only light microscopy. As a result irregular columellae and a continuous tectum. Ex- only those species examined also by SEAMhave been tending from the latter is another set of columellae, designated as having pointed verrucae or rounded designated as verrucae, thicker than those below the verrucae in Table 3. Collections having the pointed tectum, with the terminal sculpturing appearing as verrucae were found in Plum bag0 rosea (Figures 33, fine bristles in TEN. The Armeria type (T’g‘1 ures 34) and in Ceratostigma willmottianum (Figures 41-58) has a foot layer supporting straight, regular 59-62). A collection identified as Plumbago auri- columellae, which are fused distally into an incom- culata (Figures 39, 40) had the more rounded plete tectum of the reticulate configuration. verrucae. Heterostyly, frequently associated with dimorphic The above reservation does not apply to the stigmas and dimorphic pollen grains, is a well- Armeria type in which the two forms are strikingly documented phenomenon in the Plumbaginaceae distinct even in light microscopy. The Armeria (Baker, 1948, 1953, 1966; Dulberger, 1975; Philipp, forms can be illustrated by two collections each 1974). Although the collections at the US. h’ational of (Figures 43-46), Herbarium are too limited and valuable to permit uiilgare (Figures 51, 52), and Statice sinziata (Figures a study of heterostyly per se, and this is not our in- 55-58) and one collection of Statice tenella (Figures tention, the survey of the Plumbaginaceae revealed 47-50) with several unattached branches, presum- seemingly controversial results. Neither author ably from different . In each of the above claims taxonomic expertise in the Plumbaginaceae, species there is a prominently (or coarsely) reticu- but the collection sampled in each case was similar late form (Figures 45-48, 51, 55, 56) and a finely to or within the range of variation of the remaining reticulate form (Figures 43, 44, 49, 50, 52, 57, 58). collections of the particular species as identified. ilihile each form exhibits subtle interspecific differ- Few specimens had sufficient numbers of open ences, i.e., the coarsely reticulate grain of Armeria to permit a designation of short- or long- maritima may be slightly different from the coarsely styled with any degree of confidence, nor could we reticulate grain in Statice sinuata, the classification follow Baker’s (1966) scheme of labeling the two of grains as to coarsely or finely reticulate could Armeria forms “A” or “B” since this too is based have been made without knowledge of the alternate on style length. However, the results in two species form. The remaining Armeria types illustrated by with the Plumbago type reinforce each other, and SEN are Goniolinum collinum (Figures 53, 54) and the pollen forms found in four species with the Limonium viciosoi (Figures 41, 42). In both species Armeria type reinforce each other. The following the collection sampled had the coarsely reticulate discussions apply only to the particular collections form. listed in Table 3 for each species, and within each TEA1 observations corroborate the dimorphism major type the different grains are referred to as shown by SEM. The verrucose type is represented forms. by Ceratostigma grifithii (Figure 69): the fine What appears to be the two forms in the Plum- bristle-like columellae heads correspond to the bago type pollen can be illustrated by two collec- rounded verrucae illustrated in Figure 30 by SEM; tions of Ceratostigma grifithii from (Figures in Figure 70, the verrucae have thicker bristles, and 29-32) and two collections of Plum bag0 europaea those with perfect longitudinal section illustrate the (Figures 35-38). In each species there is a form with large blunt protrusion of the pointed verrucae pointed verrucae (Figures 32, 38) and a form with shown in Figure 32 by SEM. In Armeiia maritima more rounded verrucae (Figures 30, 36). TZ’hether (Figures 67, 68) and Statice sinziata (Figures 77-80), these two forms actually represent dimorphic pollen representative of the reticulate morphology, TEN and are associated with heterostyly remains to be reinforces the differences in diameter and length answered, but our results agree, for the most part, of the columellae between the finely and coarsely with those of Erdtman (1970). reticulate forms, and also the existence of a fine NUMBER 37 7 network of sporopollinen around the muri of the thers from each collection had been examined, the coarsely reticulate forms (Figure 67), which was not larger sample might have produced results more readily apparent in the finely reticulate forms. Our compatible with those of previous workers. In the observations of A. maritima agree with the TEM case of Limonium vuZgare, examination of four col- investigations of Erdtman and Dunbar (1966). lections (Table 3) revealed three with the coarsely These workers designated the coarsely reticulate reticulate form (Figure 51) and one with the finely exines as “A-line” and the more finely reticulate reticulate form (Figure 52). Our coarsely reticulate exines as “B-line.” Direct correlations in exine struc- form corresponds exactly with the “A” grain of ture between our TEMs (Figures 67, 68) and those Baker (1966, fig. I), but we did not find the form of Erdtman and Dunbar (1966, figs. 1, 2) are ob- which he illustrated as the alternate or “B” (1966, vious. fig. 2) and described as bearing a pattern of small In all samples examined the endexine pollen wall spines on the surface of the grain. In fact, the closest unit that characteristically occurs beneath the foot similarity to his “B” grain is Plumbago rosea (Fig- layer in the majority of angiosperm poIlen grains ures 33, 34). It seems unlikely that both major is highly reduced in the Plumbaginaceae. We have pollen types, which are morphologically and struc- noted its presence only in the aperture region, and, turally very different, would be found in one species, therefore, it is depicted in just a few of the trans- but our results do not exclude this possibility. mission electron micrographs included in this report Another problematical taxon is Armeria maritima (Figures 65, 66, 68, 71, 73, 74, 80). Internal foramina var. sibiricu (Turczaninow) Lawrence. This particu- in the columellae and foot-layer (Figures 65-67, 75) lar variety, sometimes treated as a subspecies or even are also found in the Plumbaginaceae. This feature as a species, has been investigated by a number of has been described in the large family Compositae workers, with differing, but not necessarily mutually by Skvarla and Larson (1965). These holes are of exclusive, results. Both Baker (1966:355-356) and sporadic distribution and are most commonly noted Philipp (1974:41) regard “sibirica” as monomorphic, in the Armeria pollen type. having the papillate and Type A pollen In Ceratostigma willmottianurn, a collection from (coarsely reticulate form). However, in a study of had 3-colpate grains (Figures 61, 62), and a collections made between longitudes 30°W and collection from China had pantocolpate grains (Fig- 60°E, Praglowski and Erdtman (1969) described six ures 59, 60). The pantocolpate grain has larger clus- pollen forms, and found as many as four in a single ters of verrucae, but at high magnification, x 7500 anther. These incIude an “A” and “B” that cor- (Figures 60, 62), the tips of the verrucae in both respond to our coarsely and finely reticulate forms. forms are very similar in the terminal structure. Of all the Plumbaginaceae examined in our study, These results do not correlate with those of Cera- 39 collections representing 20 species, only Armeria tostigma grifithii and , but di- maritima var. sibirica had both forms within a morphic pollen grains based on aperture structure single sample. The holdings of var. sibirica at are not unknown (Kohler, 1976). Additional sam- the National Herbarium are mostly ples are needed to confirm the alternate form as from Greenland and Canada, with only two from 3-colpate. Norway. Pollen was removed from a single inflores- As stated above, this study was not intended to cence on each of six collections (Table 3). The document or identify the species of Plurnbaginaceae SEhIs, taken at a range of low magnifications, illus- with dimorphic pollen. We are aware that a de- trate mixtures of the finely and coarsely reticulate tailed investigation of each of the species listed in Armeria forms. Unfortunately this variety was ex- Table 3 might well reveal that a majority of these amined late in the study and the micrographs could have dimorphic grains. Also, most pollen samples in not be included here. However, two observations this family consist of a single with the five seem worthy of note: the coarsely reticulate form anthers. This sampling technique limits damage to appears to be predominant, and, secondly, the dis- the specimen, but does not yield large numbers of tinction between the two forms is not as striking grains. as in the other dimorphic Armeria taxa. Philipp If, especially in the Armeria types, 15 or 20 an- (1974, fig. 1) illustrates grains from dimorphic a SMITHSONIAN CONTRIBUTIONS TO BOTANY

Danish Armeria maritima (1974, fig. IA,B) which this extensive variation may have great taxonomic agree very well with our Figures 4346, but more potential at all levels, particularly that of generic importantly the two SEWS from monomorphic definition. Greenland plants (1974, fig. Ic,D) also show a pos- The aperture structure is more complex and vari- sible dilution of the distinction: the mesh of what able than in the Primulaceae and much more so could be the finely reticulate form (fig. lc) is larger, than in the Centrospermae or Plumbaginaceae. and the mesh of what could be the coarsely reticu- IVhile the most common type in the Polygonaceae late form (fig. 1~)is slightly smaller. is 3- (rarely 4-) colporate, the endoaperture, readily Philipp (1974:49) also cites the existence of large delimited in light microscopy, is variable and in- and small pollen grains in the hybrids between cludes some zonorate types. Also found in the the dimorphic subspecies, A. maritima ssp. mari- family are taxa with pantoporate (Figures 113, 114, tima X ssp. elongata. The proportion of the grains 134) and pantocolpate (Figures 112, 118, 120, 133) varies widely; in one cyme the percentage of large apertures. Some collections of 3-colporate taxa had grains in open flowers ranged from 45 to 90. In one occasional grains that were syncolporate. the maximum variation between the cymes The surface of the ektexine varies widely and in- was from 24y0 to 90% large grains. The variation cludes tectate and nontectate (reticulate) forms. The in size is not exactly comparable to the structural tectate forms can be punctate (Figures 82-85); variation in the exine, but her results, those of punctate-striate (Figures 94-99): prominently spinu- Praglowski and Erdtman (1 969), and ours, indicate lose (Figures 133, 134); or perforate and small- that one plant, or even one , is capable spinulose (Figures 136, 138); and there are some of producing variable or dimorphic grains. unique types that are difficult to describe accurately To summarize the results of pollen analysis in in text (Figures 98, 106, 108, 110). The nontectate this family-the striking difference in the two types forms are finely to coarsely reticulate (Figures 112- designated as “Armeria” and “Plumbago,” the dis- 123). In some taxa the grains had one type of sur- tinction of the Plumbago type from all other pollen face outlining the colpi, and another on the poles examined to date in these studies, the existence of and mesocolpial ridges (Figures 130, 140). the two Armeria forms within a single inflorescence The most common surface pattern is punctate. raise more questions than they answer. The exist- The size and distribution alone of these punctae ence of heterostyly and dimorphic pollen grains in vary widely, but an additional characteristic is pres- the Plumbaginaceae, however, in no way detracts ent in many taxa-the punctae are connected by from the conclusion of this study: None of the grooves or striae which are also variable in depth, pollen examined in the Plumbaginaceae is simi- width, and placement (Figures 89, 91, 93, 95, 97, 99). lar or related to the common type found in the In laxiflora (Figure 106), the tectum be- Centrospermae. tween the striae is variously upraised, producing an uneven surface. In Ruprechtia ramiflora (Figures 108, log), the intergroove tectum is more promi- POLYCONACEAE nently upraised. In buxifolia (Figures 98, 99), the connecting striae are larger, tend to be FICURE~82-173 parallel, and result in, at least superficially, a striate- This is a much larger family than either the like surface pattern. These distinctions are not Plumbaginaceae or Primulaceae. The possibility of as conspicuous in TERI (Atraphaxis, Figure 143; a relationship with the Centrospermae is more Ruprechtia laxiflora, Figure 171; R. pallida, Figure widely held and thus was examined in greater 172), but this, of course, is frequently the case when depth. The 85 species (Table 4) representing 36 cross-sections are compared with surfaces having genera were examined by light microscopy and irregular variations. SERI; 32 of these species were sectioned and ex- Within the broad category of punctate ektexines, amined by TEM. the following six subtypes with some representative The Polygonaceae are one of the most palyno- species can be recognized: logically diverse families in the dicotyledons, and 1. Ektexine finely punctate: breweri, NUMBER 31 9

Eriogonum correllii, and denudata zanthe spp. (Figures 145, 146), parishii (Figure 82). (Figure 149), Nemacaulis (Figure 157), and 2. Ektexine with clustered punctae: trilobata (Figure 158) all had a tectum in which the thurberi, (Figure 84), C. pani- inner face was conspicuously granular. culata (Figure 85), , and E. race- Two of these 16 taxa examined by TEM, Mueh- mosum. Eenbeckia chilensis (Figure 153) and Podopterus 3. Ektexine punctate, the punctae connected by mexicanus (Figure 160), are distinguished from the small striae: , E. marifolium preceeding ones by a prominently developed foot (Figures 90, 91), E. thomasii, californica layer and an endexine well developed only in the (Figures 88, 89), Oxytheca trilobata (Figure 83). region of the aperture. (Figure 151) 4. Ektexine more prominently punctate-striate: and (Figure 173), with a thin foot-layer Antigonum guatemalense, comosum and endexine, appear intermediate between the (Figures 94, 95), Gymnopodium antigonoides (Fig- above groups. ures 92, 93), Harfordia macroptera (Figures 96, 97), The second most common surface pattern is a chilensis (Figures 102, 103), M. poly- reticulum formed by larger and fewer columellae, botryar, Neomillspaugh ia panicu Eata, and Triplaris arranged in a network and distally fused, thus pro- americana (Figure 86). ducing incomplete tectum. Differences in the size 5. Ektexine with prominent sunken punctae: and placement of the primary columellae and in esculentum (Figure 87), Muehlen beckia the surface of the lumina produce wide varieties tamnifolia (Figures 104, 105). and some recognizable pollen types. Grains with 6. Ektexine microreticulate: drege- this ektexine were 3-colpate (colporate?) (Figures anum, 0. zeyheri, and Podopterus mexicanus (Fig. 116, 122), pantocolpate (Figures 112, 118, 120), or ure 132). pantoporate (Figures 113, 114). In Polygonurn capi- The subtypes listed above should be treated with tatum (Figures 122, 123) and P. dielsii (Figures 116, reserve since the distinction between consecutive 117) the columellae are massive, and a high, con- ones is not very great, particularly between subtypes spicuous reticulum is the result. The lumina are 3 and 4. Also, variation within a sample made larger in P. dielsii, but in both species they are classification of some taxa arbitrary or impossible. almost free of any columella material. In Poly- Observations of exine wall with TEM indicate gonum acuminatum (Figure 113) and P. orientale that the six subtypes established by SEM have con- (Figures 114, 115), both pantoporate, the muri alter- siderable structural diversity as well. Sixteen of nate with large lumina filled with smaller, free these taxa were examined in sections: Chorizanthe columellae. In three pantocolpate taxa, breweri (Figure 145) and Nemacaulis denudata (Fig- coccinea (Figure 112), Polygonurn amphibium (Fig- ure 157) of subtype 1, Chorizanthe paniculata (Fig- ures 120, 121), and P. virginianum (Figures 118, ure 146) and Eriogonum parishii (Figure 149) of 119), the columellae which form the reticulum are subtype 2, (Figure 148) and smaller in length and diameter, closely placed, and Oxytheca trilobata (Figure 158) of subtype 3, a finer reticulum results. In all three the lumina A n tigon u m guatema lense (Figure 142), Ca 11igon um are filled with small, free columellae. comosum (Figure 144), Harfordia macroptera (Fig- Thin-sections of orientale (Figure ure 152) and Muehlenbeckia polybotryar (Figure 159), P. dielsii (Figure 166), P. amphibium (Figures 156) of subtype 4, and Muehlenbeckia tamnifolia 162, 163), and P. virginianum (Figure 169) empha- (Figure 154) and Fagopyrum esculentum (Figure size the SEM observations. 150) of subtype 5 are all essentially similar in pos- The formation of the reticulum in the above sessing a moderate to thick tectum, long, narrow Polygonaceae is unusual: the ridges or muri are columellae (Calligonum comosum, Figure 144, ex- formed by distal fusion along the midline of two cepted), a very reduced (absent?) foot-layer, and a rows of columellae, which are opposite or sometimes distinguishable endexine. The TEM’s of some of alternate, producing a “staggered” effect best illus- the above taxa revealed an unusual characteristic trated in a “planar” view (Figures 115, 117). that may be of phylogenetic significance: Chori- Four species of Polygonum, P. afine (Figure 124), SMITHSONIAN CONTRIBUTIONS TO BOTANY

P. (Figures 128, 129), P. vaccinifolium (Fig- paralled by that of Polygonella fimbriata (Figure ures 126, 127) and P. uiviparum (Figure 125), which 130) and closely related species (Horton, 1963. belong, among others, to the Bistorta complex 181-183): both groups have grains with similar (Hedberg, 1947), and an Australian species of apertures and a dimorphic ektexine in which the Muehlenbeckia, M. cunninghamii (Figures 100, two surface patterns have the same distribution. 101), have an ektexine pattern that could be de- Examination of P. convolvulus in TEM (Figure scribed as sparsely spinulose and sparsely punctate. 165) revealed a remarkably uniform tectum Grains of all five taxa were 3-colporate, the endo- (throughout the psilate area of the ektexine) and aperture well defined. In thin-section, Mziehlen- foot layer, underlain by a prominent endexine. beckia cunninghumii, (Figure 155) is very similar to This rare combination of well-developed foot layer the other species of Muehlenbeckia examined by and endexine was also found in Polygonella (Fig- TEN (Figures 153, 154, 156). ure 161), which reinforces the parallel exomor- It is difficult to reconcile the TEM of P. bistorta phologies. Polygonzim cilinode, P. czispidatum, and (Figure 164) with the sparsely spinulose and sparsely P. mzilfiporiim, which Hedberg lists as typical punctate ektexine depicted in SEM (Figures 128, Tiniaria, have 3-colporate grains and a uniform 129). The lack of a continuous tectum may be due ektexine, punctate-striate or prominently punctate. in part to an oblique section and perhaps to the Four species of were examined: R. densely packed columellae. The SEM’s of P. vac- aqziaticzis, R. acetosa (Figures 138, 139), R. aceto- cinifolium (Figures 126, 127), with the larger per- sella, and R. sczitafus, all of which had a perforate forations in the tectum, are more compatible with and very finely and evenly spinulose ektexine (Fig- the cross-section illustrated in TEM (Figure 168). ure 139). Two species of Emex had an ektexine islandica, Polygonum cyanandyium (Figure 136) similar to that of Rumex, but with a (Figures 134, 135), and P. forrestii (Figure 133) had distinctive aperture structure. The ectoaperture is grains that were either pantoporate or pantocolpate very reduced in length, and its polar margins with a prominently spinulose ektexine. Comparison almost coincide with those of the endoaperture. of these grains (Figures 133-135) with the common The close similarity of the ektexine in Emex and type in the Centrospermae (Figures 1-12) indicates Rzimex and its restricted occurrence reinforce Dam- that the above species could not be related paly- mer’s (1893) consecutive placement of the two nologically to that order. Polygonzim f orrestii (Fig- genera. Comparison of the ektexine of Rumex ure 167) was the most distinctive Polygonum of (Figure 139) with the common Centrospermae type those examined by TEM. The exine consists of a (Figures 7-12) indicates that there is not a close thin endexine and an ektexine containing abun- relationship between the two groups. The section dant holes or internal foramina. The surface of the of Riimex acetosn (Figure 170) reveals a thin exine tectum was composed of very large, solid spines in which the columellae and especially the foot- with numerous, small projections in between. layer-endexine unit are greatly reduced. Hedberg (1947), in a classic study of pollen The ektexine of seven species in the large New morphology in the genus Polygonum, sensu lato, TVorld genus illustrates a continuous recognized ten pollen types for which he gave variation. ,411 taxa are 3-colporate, and Coccoloba descriptions and listed species. He segregated Poly- cordafn (Figures 110, 111) has an ektexine best de- gonzim convolvultis (Figures 140, 141), P. cristatunz, scribed as columnar-pyramidal on a base of ran- and P. dumetorum as slightly aberrant forms of his domly oriented small rods; C. bm-beyuna has an Tiniaria type. These three species have almost ektexine similar to Riiprechtia ramifEora (Figures identical pollen grains: 3-colporate with a zonorate 108, 109); C. diven~ifolinis similar to Calligonzim endoaperture, the ektexine echinate near the colpi comosiim (Figures 94, 95); Coccoloba uenosa and and psilate at the poles and the mesocolpial re- C. obovata are prominently punctate; and C. @ri- gions. The above characteristics make the grains mensis has a microreticulate ektexine similar to distinct, not only from the more typical Tiniaria Podopfertis mexicanzis (Figure 132) and Polygonella pollen, but from the remaining species examined in polygama (Figure 131), but with slightly smaller the present study. This particular morphology is lumina. NUMBER 97 11

The internal morphology of Coccoloba cordata thickened at the margins; the ektexine -+ micro- pollen (Figure 147) also appears unique for the reticulate. family. The ektexine surface consists of prominent Comparison of the major subdivisions of the irregular protuberances supported by a moderateIy Polygonaceae (Dammer, 1893; Roberty and Vau- thick tectum underlain by notably reduced colu- tier, 1964; Reveal and Howell, 1976) with pollen mellae, greatly thickened foot-layer, and an ex- morphology reveals little correlation. This lack of tremely thin endexine, if any. correlation is due primarily to two complementary The genus has been regarded as con- phenomena: the wide distribution of the punctate- sisting of two endemic species, L. chilensis Remy in striate pollen type, which cuts across subfamily and Chile, and L. coriacea (Goodman) Hoover in Baja tribal lines, and the wide array of pollen types and Southern . The California taxon has within one genus, Polygonum. Thus far, the pollen been treated as L. chilensis ssp. californica Gross, morphology would support Reveal’s concept (Reveal or as a species of Chorizanthe, C. coriacea Good- and Howell, 1976) of the subfamily Eriogonoideae. man, who had to select another specific epithet Twelve of the 13 genera that he assigned to this since “californica” was already applied. The pollen subfamily, have been examined by light microscopy of Lastarriaea chilensis (Figure 137), L. coriacea, and/or SEM, and all are 3-colporate with either and Chorizanthe species (Figures 84, 85) are all very punctate or punctate-striate ektexines, the most similar, 3-colporate with a punctate ektexine. This common pollen type in the Polygonaceae. However, is the most common morphology in the family, an unusual characteristic illustrated by TEM, a however, and the similarity does not necessarily granular inner surface of the tectum, is known thus indicate that Lastarriaea is congeneric with Chori- far to be restricted to the Eriogonoideae: Chori- zanthe or is closely related. For the same reason, zanthe (Figures 145, 146); Eriogonum (Figures 148, the close similarity of the pollen in the two species 149); Nemacaulis (Figure 157); Oxytheca (Figure of Lastarriaea does not, a priori, indicate a single 158). Another genus in this subfamily, Harfordia species. Careful observation of the floral morphol- (Figure 152), is slightly granular. Examination of ogy when sampling for pollen, however, revealed additional genera by TEM might well reinforce the that the flowers of the plants from Chile and from value of this characteristic and also the validity of California are nearly identical in structure. Good- the subfamily. man (1934), in a revision of the North American species of Chorizanthe that included the California taxon, described the genus as having nine , PRIMULACEAE rarely six or three. The California and Chilean species of Lastarriaea have only three stamens. FIGURES174-200 Within limits of the taxa investigated (Table 4), Twenty-nine species (Table 5) representing 22 a number of pollen types were found in only one genera were examined by light microscopy and species, and such cases are discussed separately here. SEhI, and 9 of these were sectioned and examined Polygonella fimbriata (Figure 130). Grains 3- by TEM. colporate, the endoaperture zonorate; the tectum The structure of the aperture in the Primulaceae variable: finely punctate in the region of the col- is more complex than in the Plumbaginaceae and pus, conspicuously reticulate at the mesocolpial in the Centrospermae. If the number is three or ridges and more so at the poles. The TEM also four, the apertures are generally compound, and indicates that P. fimbriata is distinctive for the the endoaperture is easily seen in light microscopy. family. This conclusion is based on the presence of A number of taxa with 3-colporate grains had a a well-developed foot-layer and a thickened en- bridge over the endoaperture formed by the exten- dexine (Figure 161), two characteristices that were sion of the two lateral margins of the colpus (Fig- rarely combined. See also the earlier discussion of ures 175, 180-184). One species, Lysimachiopsis Polygonum convolvulus and allied species. hillebrandia, had 4-colporate grains in which each Polygonella polygama (Figure 131). Grains 3- side of an endoaperture frequently terminated in a colporate, the endoaperture zonorate, the nexine V-shaped process. Sometimes the V from one endo- 12 SMITHSONIAN CONTRIBUTIONS TO BOTANY aperture and that of the adjacent one formed the (1974, pl. 14: figs. 1, 2) that the identification of outline of a diamond. Grains with 5-8 apertures, Redfield s.n. was rechecked and verified, but still a e.g., some Primula species, are generally zonocol- second sample, Haakana s.n. from Finland, was pate (Figure 186). In some taxa, eg., Cortusa examined, and these grains were more similar to matthioli L. (Figure 188), the colpi fuse at the poles those illustrated by Punt, et al. (1974). The differ- to form a triangular apocolpial field. ences in Glaux pollen may be due to heterostyly, Different surface patterns were due largely to not reported in the literature to our knowledge, variation in the perforation of the tectum. In some or the pollen grains of this species may be simply grains the surface was finely punctate ( rather variable. There are also some differences hybrida, Figure 175; Douglasia montana, Figure between our illustration of Hottonia palustris (Fig- 182), in others prominently punctate (Coris mon- ure 185) and that of Punt, et al. (1974, pl. 4: figs. speliensis, Figure 174; Cyclamen neopolitanum, 11, 12; pl. 5: figs. 1-6), but the distinctly prolate Figure 181), irregularly perforate (Naumbergia shape shown in Figure 185 may be an artifact of thrysifio~~,Figure 176), or microreticulate (Hot- preparation, i.e., collapse. JVe acknowledge the tonia palustris, Figure 185; Primula veris, Figures existence of heterostyly in the Primulaceae and 186, 187; Omphalogramma vinciflorum, Figure dimorphic pollen (as in the Plumbaginaceae) but 191). Still others (Lysimachia terrestris, Figure 177; did not want the present study to be diluted by a Stimpsonia chamaedryoides, Figures 178, 179) might detailed examination of this phenomenon. JVhether be described as finely reticulate. Additionally, in it is the long- or short-styled form that is illustrated some grains the tectal perforations were most pro- for Hottonia, Primula, and other Primulaceae, both nounced in the mesocolpial regions (Coris, Figure authors feel strongly that the alternate form will 174; Nazimbergia, Figure 176; Lysimachia terrestris, not be shown to have the ektexine characteristic of Figure 177; Anagallis, Figure 183). so many of the centrospermous taxa (Figures 1-12). Transmission electron microscopy indicates a For detailed descriptions and measurements, the variability of exine structure within the family. reader is advised to consult the article by Punt, Most taxa examined have a well-developed foot- et al. (1974). layer and tectum, e.g., Anagallis (Figure 192), Glaztx (Figure 194), Naiimbergia (Figure 196), Discussion and Conclusions Onzphalog?-amma (Figure 197), k short columellae, e.g., Glntix (Figure 194), Naumbergia (Figure 196), Of the three families examined in this study, the and an endexine that is massive in the region of the Pollgonaceae is the most frequently considered as colpus and thinner but still prominent in the meso- being related to the Centrospermae. Of the families colpial regions, e.g., Anagallis (Figure 192), Glaux that comprise this order, the Caryophyllaceae ap- (Figure 194), Nazimbergia (Figure 196), Onzphalo- pears to be the most likely family from which the gramma (Figure 197), Stimpsonia (Figure 199). In Po1)gonaceae could be derived or related to, since Lysimachia hy brida (Figure 195) the irregular tec- both have the anthocjanin pigments. The data tuin, incomplete columellae, and possibly the exten- from plastic1 structure, however, does not support sive endexine, are due to oblique section. Two a relationship between the Polygonaceae and Caryo- species of Primzila, P. officinalir (Figure 198) and phjllaceae; the Caryoph)llaceae not only have P. ueris (Figure 200), are exceptional, the foot-layer the protein or P-type plastid characteristic of the seemingly absent. Centrospermae, but the plastids have a central crys- Heterostyly and dimorphic pollen grains are talloid with a distinctive polygonal shape Behnke, known to occur in the Primulaceae. Punt, et el. 1976:42); the Polygonaceae have the more common (1974) acknowledge this condition in some species starch or S-t)pe plastid, but admittedlj this char- of Primiila and in Hottonia palust?-is, as well as acteriration is based on a small number of species. dimorpliic pollen grains in Trientalis europaea, The data presented in this palynological study due apparently to polyploidy. In Glaux maritima indicate that the Polygonaceae and Car)ophyllaceae the collection of Redfield s.n. from Maine was dis- are not related. Although the Polygonaceae is a tinct enough from that illustrated by Punt, et al. large and paljnologically diverse family, examina- NUMBER 37 18 tion of 85 species representing 36 genera (Figures velopment of two layers-the endexine and foot- 82-173), revealed no pollen types similar to those layer. The endexine can be absent (apparently) as in the Caryophyllaceae. (For additional information in Podopterus (Figure 160), thin but recognizable on Caryophyllaceae, see Nowicke, 1975; Skvarla and as in Chorizanthe paniculata (Figure 146), well de- Nowicke, 1976). The pollen data do not support veloped as in Atraphaxis (Figure 143) and Nema- a relationship between the subtribe Illecebrinae caulis (Figure 157), and greatly enhanced as in (Caryophyllaceae) or the larger Illecebraceae and Eriogonum spp. (Figures 148, 149). The foot-layer any of the Polygonaceae examined in this study. has a similar range of variation: from apparently The grains of Illecebrum verticillatum are almost absent in (Figure 145) and identical to those of Herniaria glabra (Figure 15): Nemacaulis (Figure 157) to prominently thickened in both species the pollen has a distinctive tetra- in Coccoloba cordata (Figure 147) and Podopterus hedal shape with a large aperture on each of the (Figure 160), with many intermediate stages repre- three (four?) faces. Cardionema ramosissima (Figure sented in other taxa. 16) has pantoporate grains, roughly cube-shaped Another unusual characteristic is the granular and with a spinulose and tubuIiferous/punctate inner surface of the tectum found in a number of ektexine. The unusual grains of Illecebrum verti- closely related genera: Chorizanthe spp. (Figures cillatum and Herniaria glabra have not been found 145, 146), Eriogonzirn (Figure 149), Nemacaulis in any other taxa examined to date, including (Figure 157), and Oxytheca (Figure 158). those remaining in the order Centrospermae, as well While the tectum tends to be thin in the above as the Plumbaginaceae, Polygonaceae, and Primu- taxa, in others, Fagopyrum (Figure 150) and Tri- laceae. These results would support Hutchinson’s plaris (Figure 173), it is much thicker. (1959) inclusion of Herniaria in the Illecebraceae, The structure of the exine in the Bistorta com- but not necessarily the family status since the re- plex of Polygonurn (Figures 164, 168), densely maining species examined, including another species packed columellae, is unique in all the taxa exam- of Herniaria, H. hirsuta, all have a common panto- ined with TEM in this study or previously (Skvarla porate grain. and Nowicke, 1976) and thus diminishes the pos- An argument could be raised that the pollen of sibility that the Centrospermae and the Poly- the Bistorta complex in Polygonum (Figures 124- gonaceae could be linked by this group. In fact, it 129) and that of Muehlenbeckia cunninghamii (Fig- seems quite notable that in spite of the diverse ures 100, 101) provide some evidence for a rela- exine structures in this family, there is very little tionship to the Centrospermae. However, we think similarity to the Centrospermae. it much more likely that the occurrence of this The spinulose and punctate ektexine surface ektexine surface in a limited number of species is found in the Polygonaceae or in the Centrospermae, a reflection of the enormous palynological diversity for that matter, is simple enough to have arisen in the Polygonaceae: ektexines that are 3- psilate, independently in any of these taxa. However, the punctate, punctate-striate, conspicuously spinulose, significance attached to this ektexine in the Cen- perforate with small spines, microreticulate, finely trospermae is that in every betalain family, as well reticulate to coarsely reticulate; apertures that are as in the Caryophyllaceae and Molluginaceae, the porate, pantocolpate or colporate with variable overwhelming majority of the species examined had endoapertures; and grains that are probably unique pollen grains with a spinulose and tubuliferous,’ (limited to the Polygonaceae), such as those of Poly- punctate ektexine, which, moreover, were some- gonella fimbriata (Figure 130) and related species, times identical between families. Insofar as pollen Polygonum convolvulus (Figures 140, 141) and re- structure is concerned, a more defensible relation- lated species, or Coccoloba cordata (Figures 110, ship could be proposed between the Polygonaceae 111). and any dicot family with a preponderance of It is also clear that a diversity of structural forms punctate ektexines. Pollen grains with a promi- exist in the Polygonaceae. These observations par- nently reticulate ektexine are widely (and ran- allel the sculpturing pleomorphism illustrated by domly?) distributed among dictoyledon families, SEM. The TEM reveals wide variation in the de- but this may be due to parallel evolution and does 14 SMITHSONIAN CONTRIBUTIONS TO BOTANY not necessarily mean that these families are related Plumbago forms (Figures 29-40). Admittedly the to each other or to the Polygonaceae. two forms of the Plumbago type are based on re- This study reinforces current opinion (Cronquist, sults from only two species, but the Plumbago 1968; Philipson, 1975:74; Takhtajan, 1969:220) ektexine type has not been found in any other that the Primulaceae are not related to nor derived taxon in this study or in earlier related ones from the Centrospermae. According to Cronquist (Nowicke, 1975; Skvarla and Nowicke, 1976). The (1968:177, 223) the only special feature in common coarsely reticulate form of the Armeria type has a between the Caryophyllales (Centrospermae) and superficial resemblance to some reticulate grains the Primulales is the free-central . The in the Pol>gonaceae, but the formation of the muri results of pollen analysis indicate that the ancestors in the Pollgonaceae is distinctive, alternate dupli- and/or relatives of the Primulaceae are not in the baculate (Figures 112-1 17, 122, 123), versus sim- centrospermous families. Although the pollen of the plibaculate in the Armeria forms (Figures 41-58). Primulaceae exhibits some variation (Figures 174- In reticulate grains found in the Centrospermae 200), none of the taxa examined had grains with a and in the Polygonaceae (Figures 113-1 IS), the counterpart in the Centrospermae. lumina usually have at least some free columellae Unlike the Primulaceae, the Plumbaginaceae are (or bacula), whereas in both Armeria forms (Figures still regarded as being related to the Centrospermae 42, 44, 46, 48, 51, 55, 56), the lumina are consistently (Takhtajan, 1969:2 15), although Cronquist (1968: free of any columellar material (the data of Praglow- 185) refers to the family as “somewhat more iso- ski and Erdtman, 1969, notwithstanding). lated but: may also be derived from the Caryo- In the Plumbaginaceae the pollen data, plastid phyllales” and Philipson (1975:74) considers the structure, and pigmentation (unless the tie is to Plumbaginaceae-Centrospermae relationship as more the Caryophyllaceae and ’or llolluginaceae) suggest debatable (than that of the Polygonaceae-Centro- that this family is not related to the Centrospermae spermae). The pollen of the Plumbaginaceae and that its phylogenetic position needs to be (Figures 29-81) consists of the two major types, reevaluated. designated previously as Armeria and Plumbago, Like the Plumbaginaceae, the Primulaceae has the each of which can be dimorphic in heterostyled anthoqanin pigments, and has the starch type species. This results in four distinctive types, all plastid structure (Behnke, pers. comm.). However, 3- (or 4-)colpate (Ceratostignza willmottianum and most authors (Cronquist, 1968; Philipson, 1975; monopetalunz notwithstanding): Takhtajan, 1969) do not regard the Primulaceae as finely and coarsely reticulate Armeria forms (Figures related to the Centrospermae and the pollen data 41-58), and pointed-verrucae and rounded-verrucae presented here reinforces that view. Literature Cited

Baker, H. G. Pollen Morphology in Armeria maritima and 1948. Dimorphism and Monomorphism in the Plumba- Armeria sibirica. Grana Palynologica, 6:338-354. ginaceae, I: A Survey of the Family. Annals of Goldblatt, P., J. W. Nowicke, T. J. Mabry, and H. D. Behnke Botany, 12:207-219. 1976. Gyrostemonaceae: Status and Affinity. Botanica 1953. Dimorphism and Monomorphism in the Plumba- Notiser, 129:201-206. ginaceae, 11: Pollen and Stigmata in the Genus Goodman, G. Limonium. Annals of Botany, 17:433-445. 1934. A Revision of the North American Species of the 1966. The Evolution, Functioning and Breakdown of Genus Chorizanthe. Annals Missouri Botanical Gar- Heteromorphic Incompatability Systems, I: The den, 21:l-102. Plumbaginacea. Evolution, 20:349-368. Hedberg, 0. Pollen Morphology in the Genus Polygonurn L. Behnke, H. D. 1947. S. lat. and Its Taxonomical Significance. Svensk 1971. Sieve-tube Plastids of Magnoliidae and Ranun- culidae in Relation to Systematics. Taxon, 20:723- Bo tan isk Tidskrift , 40: 3 7 1-404. Horton, H. 730. J. 1963. A Taxonomic Revision of Polygonella (Polygona- 1975. Hectorella caespitosa: Ultrastructural Evidence ceae). Brittonia, 15:177-203. against Its Inclusion into Caryophyllaceae. Plant Hutchinson, J. Systematics and Evolution, 124:31-34. 1959. Dicotyledons. Volume 1 of Families of Flowering 1976. Delimitation and Classification of the Order Caryo- Plants. xi + 510 pages. London: Oxford University phyllales (Centrospermae) According to Ultrastruc- Press. tural Data from Sieve-Element Plastids: A Survey Kohler, E. Based on 146 Species. Plant Systematics and Evolu- 1976. Pollen Dimorphism and Heterostyly in the Genus tion, 126:31-54. Waltheria (). Pages 147-161 in I. K. Behnke, H. D., and B. L. Turner Ferguson and J. Muller, editors, The Evolutionary 1971. On Specific Sieve-tube Plastids in Caryophyllales: Significance of the Erine. London: Academic Press. Further Investigations with Special Reference to the Mabry, T. J., A. Taylor, and B. L. Turner Bataceae. Taxon, 20:731-737. 1963. The Betacyanins and Their Distribution. Phyto- Cronquist, A. c h em is try, 2: 6 1-64. 1968. The Evolution and Classification of Floulering Nowicke, J. W. Plants. x + 396 pages. Boston: Houghton Mifflin Co. 1975. Pollen Morphology in the Order Centrospermae. Dammer, U. Grana. 15:51-77. 1893. Polygonaceae. Pages 1-36 of volume la in Engler Pax, F., and K. Hoffman and Prantl, Die Naturlichen Pflanzenfamilien Ill. 1934. Caryophyllaceae. Pages 275-364 of volume 16c in Leipzig: Englemann. Engler and Prantl, Die Naturlichen Pflanzen- Dulberger, R. familien 11. Leipzig: W. Engelmann. 1975. Intermorph Structural Differences between Stig- Philipp, 31. matic Papillae and Pollen Grains in Relationship 1974. hforphological and Genetical Studies in the Armeria to Incompatibility in Plumbaginaceae. Proceedings maritima Aggregate. Botanisk Tidsskrift, 69:40-51. of the Royal Society (London), series B, 188:257-274. Philipson, W. R. Eckhardt, T. 1975. Evolutionary Lines within the Dicotyledons. New 1964. Engler's Syllabus der Pflanzenfamilien. 12th edition, Zealand Journal of Botany, 13:73-91. volume 2. Berlin: Gebruder Borntraeger. [Centro- Philipson, W. R., and J. P. Skipworth spermae, pages 79-101 J. 1961. Hectorellaceae: A New Family of Dicotyledons. Erdtman, G. Transactions of the Royal Society of New Zealand, 1966. Pollen Morphology and Plant : Angio- 1:31. sperms. xii + 553 pages. Stockholm: Almquist & Praglowski, J., and G. Erdtman Wiksell. 1969. On the Morphology of the Pollen Grains in Armeria 1970. Uber Pollendimorphie in Plumbaginaceae-Plumba- sibirica in Specimens from between Longitude 30° W gineae. Svensk Botanisk Tidskrift, 64: 184-188. and 60' E. Gram Palynologica, 9:72-91. Erdtman, G., and A. Dunbar Punt, W., J. De Leeuw van Weenen, and W. A. P. van Oostrum 1966. Notes on Electron Micrographs Illustrating the 1974. Primulaceae. In Janssen, Punt, and Reitsma, editors,

15 16 SMITHSONIAN CONTRIBUTIONS TO BOTANY

The Northwest European Pollen Flora, 3. Review Skvarla, J. J., and D. A. Larson of Paleobotany and Palynologp, 17(3/4):31-70. 1969. An Electron Microscopic Study of Pollen hlorphol- Reveal, J. L., and J. T. Howell ogy in the Cornpositae with Special Reference to 1976. (Polygonaceae), a New Genus from Cali- the Ambrosiinae. Grana Palynologica, 6:210-269. fornia. Brittonia, 28:245-251. Skvarla, J. J., and J. XV. Nowicke Roberty, G., and S. Vautier 1976. The Structure of the Exine in the Order Centro- 1964. Les Genres de Polygonacees. Boissiera, 10:7-128. spermae. Plant Systematics and Evolution, 126355-78. Roland, F. Takhtajan, A. 1968. Etude de L'ultrastucure des Aperures, 11: a 1969. Flowering Plants, Origin and Dispersal. x + 310 Sillons. Pollen et Spores, 103479-519. pages. Washington, D. C.: Srnithsonian Institution Skvarla, J. J. Press. 1973. Pollen. Pages 456459 in P. Gray, editor, Encyclo- Thorne, R. F. pedia of Microscopy and Microtechnique. New 1968. Synopsis of Putatively Phylogenetic Classification of York: Van h'ostrand Reinhold. the Flowering Plants. Aliso, 6:57-66.

TABLE1.-Results of pollen analysis of taxa examined for ektexine characteristics

Spinolose + Tubulif erous/ Taxa Species Genera Punctat e Otner Plumbaginaceae ...... 20 9 0 21 Polygonaceae ...... 85 36 4? El Frimlaceae ...... 29 22 0 29 Betalain fanilies plus C aryophy llaceae and Molluginaceae ...... 217 184 33

TABLE2.-Centrosperrnae specimens examined, arranged alphabetically by family (pollen types I, 11, and I11 are 3-colpate, pantoporate, and pantocolpate respectively, all with a spinulose and tubuliferous or punctate ektexine; Spec. = specialized, any type not included in 1-111)

Taxa Collector Location Pollen Figure description numbers

~ ~~ AIZOCEAE I Geocarpon minim Mackenzie ...... Palmer 5517 Missouri I1 9 Mesembryanthemm variabile Haworth ...... Wal ther s . n. California I 1, 8, 19 Tetragonia arbuscuZa Fenzl ...... Bayliss 2171 S. Africa I AMARANTHACEAE I Achgranthes aspera L...... Philipson 10510 New Zealand I1 altissima (Jacquin) H.B.K...... Curtiss 269 Cuba I1 Dicraurus aZternifoZius (Watson) Uline & Bray. Carter et al. 2061 Mexico I1 PsiZotrichm ampZm Suessenguth ...... Burger 3248 Ethiopia I1 13, 20 PtiZotus corymbosm Gaudichaud-Beaupre...... Pritzel 58 I1 P. obouatm Gaudichaud-Beaupre ...... Lazarides 4333 Australia I1 17 NUMBER 37

TABLE2-Continued

Taxa Collector Location Pollen Figure description numbers

BASELLACEAE

Anredera scandens Moquin ...... Nelson 1666 Mexico I1 3, 21

CACTACEAE

Borzicactus tenuiserpem (Rauh & Backeberg) Kimnach...... Hutchison L Wright Peru 1 11 4448 Hamatocactus setispinus Britton & Rose...... Pratt 9483 111 12 Gpuntia lindheheri Engelmann ...... Griffiths 9031 Texas Spec. 17, 22

CARYOPHYLLACEAE

Achyronychia cooperi A. Gray ...... Parker et al. 7768 I1 Cardionema ramosissha A. Nelson L Macbride,.. Fosberg 22540 Ecuador I1 16 Gymocarpos fruticosm Persoon...... Chevall ier 28 Algeria I1 4, 23 Hemiaria glabra L...... Staszkiewicz in Poland Spec. 15, 24 Plantae Poloniae, 527 H. hirsuta L...... Mandaville 139 Saudi Arabia I1 Illecebm verticellatm L...... MO 176804 France Spec. campestris Aiton...... Wood 591 S. Africa I1 SiZene meria L...... Klein 2621 Brazil I1 Siphonychia americana (Nuttall) Torrey L A. Gray ...... Thorne 15254 Florida I1 14 Tunica stricta (Bunge) Fischer L Meyer...... Goloskokov s.n. USSR I1

CHENOPODIACEAE

Chenopodim ambrosioides L...... Guinea 112 Spain I1 5, 25

HECTORELLACEAE

LyalZia kergueZensis Hooker...... Transit of Venus Expd. New Zealand I1

MOLLUGINACEAE

Limem viscosm Fenzl...... Seydel 751 SW Africa I 2, 7, 26 Mollugo oppositifolius L...... Gandhi 2092 India I

NYCTAGINACEAE

Abronia angustifolia Greene...... Peebles L Harrison Arizona Spec. 18, 27 3949 Bougainvillea peruviana H.B.K...... Hutchison 1415 Peru Spec. MirabiZis alipes Watson...... Atwood 4550 I1 Selinocarpus diffusus A. Gray ...... Wooton s.n. New Mexico I1

PHYTOLACCACEAE

Agdestis clematidea Mocino & Sesse...... Pringle 3276 Mexico I Microtea mypurensis (H.B.K.) G. Don ...... Bang 1589 Bolivia I1 Stegnosperma cubense A. Richardson ...... Goldsmith 99 Mexico 1

PORTULACACEAE

Lenzia chumaepithys Philippi...... Johnston 6091 Argentina I Lewisia colmbiaw (Howell) Robinson...... Jones 214 Idaho I Montia meridensis Friedrich...... Hammen 1194 Colombia Spec. Naiocrene parvifollia (Moquin) Rydberg ...... Applegate 2556 Oregon I11 6, 10, 28 18 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE3.-Plumbaginaceae specimens examined (all 3-colpate except as noted; A = Armeria type, AC = coarsely reticulate Armeria form, AF = finely reticulate Armeria form, P = Plum- bag0 type, PP = pointed verrucae Plumbago form, PR = rounded verrucae Plumbago form)

Species Collector Location Pollen Figure description numbers

Acantho limon glurnacem Boissier ...... Unknown collector Cultivated Hort. AC Brussels A. olivieri Jaubert & Spach.. Koelz 15794 Iran AC 65,66 A. phrygiwn Boissier ...... Bo rnmu Iler 5511 Turkey AF Armeria maritima (Miller) Willdenow ...... Mathiesen & Pedersen s.n. Denmark AC 45, 46, 67 Svenson s.n. 'Scandinavia' AF 43, 44, 68 Thedenius s.n. Sweden AC A. maritima var. sibirica (Turczaninow) Lawrence.. ... Bartlett 147 Greenland A Calder 2014 Canada A Cody 1794 Greenland A Ekblaw 610 Greenland A Lindager s.n. Greenland A Stein 175 Greenland A A. scabra Pallas...... H. Smith s.n. Sweden AC Ceratostigma griffithti C. B. Clarke ...... Rock 6577 China PP 31, 32, 70 Rock 11578 China PR 29, 30, 69 C. minus Stapf ...... Schneider 2584 China P C. willmottianurn Stapf ...... Kingdon-Ward 12530 MO India PP 61, 62 Wilson 1373 China PPl 59, 60, 71 Dyerophytm africanm (Lamarck) 0. Kuntze ...... Goldblatt 2250 MO S. Africa PR Werdermann & Oberdieck 594 S. Africa P 63, 64, 72 Seyel 4025 MO Namibia P collinm (Grisebach) Boissier ...... Rechinger f. 10375 Greece AC 53, 54, 73 Limoniastrwn guyonianm Durieu de Maisonneuve...... Chevallier 82 Algeria AF 74 L. monopetalurn Boissier...... Puech s.n. France AC2 Limoniwn viciosoi Pau ...... Vicioso s.n. Spain AC 41, 42, 75 L. vulgare Miller ...... Holm-Nielsen s.n. MO Denmark AF 52 Hubbard 13206 MO Britain AC Moss MO Britain AC Lawalree 3820 MO Belgium AC 51 Lamarck ...... Bayliss 1187 GH S. Africa PR 39, 40 Bayliss 3106 MO S. Africa P ?. europaea L...... Raine s.n. GH 'Almunarro' PP 37, 38 Sporiks s.n. GH Persia PR 35, 36 P. rosea L...... Urban 5490 GH Puerto Rico PP 33, 34 ?. scandens L...... Woytkowski 5592 Peru P 76 Statice sinuata L...... Maire & Wilczek 1048 Morocco AF 57, 58, 77, 78 Vaccari 495 Greece AC 55, 56, 79, 80 S. tenella Turczaninow...... Chaney 517 Mongolia AC 47, 48, 81 Chaney 517a Mongolia AF 49, 50

Pan tocolpa te 4-5 zonocolpate NUMBER 37 19

TABLE4.-Polygonaceae specimens examined (3C = 3-colporate, PC = pantocolpate, PP = pantoporate)

Species Collector Location Pollen Figure description numbers Afrobmnnichia erecta Hutchison & Dalziel...... Baldwin 11489 Liberia 3C, punctate guatemalense Meisner ...... Laughlin 2635 Mexico 3C, punctate-striate 142 AtraphLwris buxifolia Jaubert & Spach ...... Woronow s. n. USSR 3C, striate-punctate 98, 99, 143 Brtolnichia cirrhosa Banks.. Biltmore Herb. 1678 B Alabama 3C, punctate-striate Calligonum cornosum L'Heritier ...... Mandaville 69 Saudi Arabia 3C, punctate-striate 94, 95, 144 Centrostegia thurberi A. Gray ...... Hoover 4373 California 3C, clustered punctate Chorizanthe breweri S. Watson ...... Hoover 11393 California 3C, finely punctate 145 C. fimb24ata Nuttall...... Wiggins 9908 Mexico 3C, clustered punctate 84 C. rnembranacea Bentham..... Bruce 155 California 3C, clustered punctate C. paniculata Bentham ...... Bro. Claude Joseph 2997 Chile 3C, punctate 85, 146 Chorizanthe sp...... Simon 289 Chile 3C, punctate Coccoloba barbeyana Lindau. Schunke 76 Peru 3C, deeply punctate- striate C. cordata Chamisso...... Hatschbach et al. 13352 Brazil 3C, columnar-pyramidal 110, 111, 147 C. diversifolia Jacquin.. .. Bro. Clemente s.n. Cuba 3C, punctate-striate C. obovata H.B.K...... Duke 4988 Panama 3C, prominently punctate C. parimensis Bentham...... Ducke 1289 Brazil 3C, microreticulate C. swartzii Meisner...... Webster et al. 10296 Bahamas 3C, punctate-striate C. venosa L...... Harris & Britton 10756 Jamaica 3C, punctate Dedeckera eurekensis Reveal & Howell ...... Reveal et al. 3909 California 3C, punctate hex austraZis Steinheil... Scheepers 928 MO S. Africa 3C, perforate and spinulose Seydel 2975 SW Africa 3C, perforate and 136 spinulose E. spinosa (L.) Campdera.. . Koelz 14304 Iran 3C(?), perforate and spinulose Eriogowm come 1lii Reveal. Reveal & Davidse 883 Texas 3C, finely punctate E. inflaturn Torrey & Fremont ...... Gentry 14437 Mexico 3C, clustered punctate E. marifoliurn Torrey & A. Gray ...... Holmgren & Reveal 2706 Oregon 3C, finely punctate- 90, 91, 148 striate E. parishii S. Watson...... Wiggins & Demaree 4913 Mexico 3C, clustered punctate 149 E. racernosum Nuttall ...... Eggleston 5847 Colorado 3C, clustered punctate E. thomasii Torrey...... Jones s.n. California 3C, punctate-striate Fagopyrwn esculentum Moench ...... Braun s.n. Ohio 3C, deeply punctate 87, 150 Gilrnania luteolum (Coville) Coville...... Gilman 1520 California 3C, punctate Gymnopodium antigonoides (Robins on? ) Blake...... Gaumer & Sons 23207 Mexico 3C, punctate-striate Goldman 743 Mexico 3C, punctate-striate 92, 93, 151 Harfordia macroptera (Bentham) Greene & Parry. Wiggins 7601 Mexico 3C, punctate-striate 96, 97, 152 Hollisteria lanata S. Watson ...... Hoover 3496 California 3C, punctate Koenigia islandica L...... Koelz 6424 India PP, spinulose Lastarriaen chilensis Remy. Worth & Morrison 16270 UC Chile 3C, punctate Worth & Morrison 16338 UC Chile 3C, punctate 137 L. coriacea (Goodman) Hoover ...... Leiberg 3260 California 3C, punctate Howell 32083 California 3C, punctate kcrowa californica Bentham...... Grinnell s.n. California 3C, finely punctate- 88, 89 striate MuehZenbeckia chitensis Meisner ...... E. & M. Holway 199 Chile 3C, punctate-striate 102, 103, 153 M. cunninghamii Mueller.... Aston 904 Australia 3C, sparsely spinulose 100, 101, 155 and punctate Constable 18440 Australia 3C, sparsely spinulose and punctate Lazarides 5745 Australia 3C, sparsely spinulose and punctate 20 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE+Continued

Species Collector Location Pollen Figure description numbers

.M. polgbotryar Meisner.. ... Pritzel 399 Au s t r a1ia 3C, punctate-striate 156 M. tmifolia (HBK) Meisner. Balls 5804 Ecuador 3C, punctate-striate 104, 105, 154 Neomi 1 lspaughia paniculata (Donnell-Smith) Blake. ... Edwards P 675 Honduras 3C, punctate-striate Nemacaulis denudata Nuttall...... Cleveland s.n. California 3C, finely punctate 82, 157 Oqgonun atriplicifolium Martelli ...... Piemeisel & Kephart 56 Kenya 3C, punctate and microreticulate 3. dregeanm Meisner...... Bayliss 4515 S. Africa 3C, microreticulate 3. zeyheri Sonder ...... Galpin 13075 S. Africa 3C, microreticulate Oxyyria digynia (L.) Hill.. . Neilson 902 Canada 3 colpate-very thin walled Oxytheca dendroidea Nuttall ...... Eastwood L Howell 7353 3C, finely punctate- striate Wagenknecht 18118 Chile 3C, finely punctate- striate 0. luteola Parry...... Pringle s.n. California 3C, finely punctate- striate Walther 14379 California 3C, finely punctate- striate 0. parishii Parry...... S. L W. Parish 993 California 3C, punctate 0. trilobata A. Gray ...... Abrams 3807 California 3C, finely punctate- 83, 158 striate Persicaria coccinea Greene. Eastwood 1427 California PC, finely reticulate 112 Podopterus mexicanus Kunth. Langlassi 922 Mexico 3C, microreticulate 132, 160 Polygonel la fimbriata (Elliot) Horton ...... Ward L Smith 2236 Florida 3C, finely punctate and 130, 161 reticulate P. polygma (Ventenat) Engelmann L A. Gray...... Bright 6309 S. Carolina 3C, microreticulate 131 Polygonun acwninatwn Kunth. Irwin & Souza 9565 Brazil PP, reticulate 113 P. affine D. Don ...... Staunton et al. 1328 Nepal 3C, finely punctate and 124 spinulose P. amphibiiu? L...... Braun 29 Indiana PC, finely reticulate 120, 121, 162, 163 P. bistorta L...... Cantlon L Gillis 57-439 Alaska 3C, finely punctate and spinulose Cantlon & Malcolm 580085 Alaska 3C, finely punctate and 128, 129, 164 spinulose Calder & Billard 3833 Canada 3C, finely punctate and spinulose P. capitatum D. Don ...... Tsiang 4503 China 3C, reticulate 122, 123 P. ailinode Michaux ...... Hardin 722 N. Carolina 3C, finely punctate- striate P. convolvulus L...... Horr L McGregor E495 Kansas 3C, psilate and spinulose 140, 141, 165 P. cristatm Engelmann L Gray ...... Graham 25 Texas 3'2, psilate and spinulose P. cuspidatun Siebold L Zuccarini ...... Makino 13368 Japan 3C, deeply punctate P. cyanandrim Diels ...... Rock 5935 China PP, spinulose 134, 135 P. dielsii Leville (?)..... Henry 9379 China 3C, coarsely reticulate 116, 117, 166 P. dumetonvn L...... Makino 13491 Japan 3C, psilate and spinulose P. forrestii Diels ...... Rock 9697 China PC, spinulose 133, 167 P. rnuZtiflorwn Thunberg.. , . Makino 15020 Japan 3C, deeply punctate P. orientale L...... Johnson s.n. New York PP, reticulate 114, 115, 159 P. vaccinifolium Wallich.. . Koelz 976 India 3C, punctate 126, 127, 168 P. virginianun L...... Standley 8342 Missouri PC, finely reticulate 118, 119, 169 P. viviparm L...... Alm s.n. Sweden 3-4C, very finely 125 sp inulo se Pteropym aucheri Jaubert 6 Spach...... Rechinger 27660 Pakistan 3C, punctate-striate drymariaides Fischer & Meyer ...... Gillespie 5495 Arizona 3C, punctate-striate A?hem delavayi Franchet.... Rock 16256 China 312, punctate Fwnex acetosa L...... Greuter L Hainard 567 Switzerland 3(-4)C, perforate and 138, 139, 170 spinulose R. acetosella L...... Rouleau 67 Canada 3(-4)C, perforate and sp inu lose NUMBER 37 21

TABLE+Continued

Species Collector Location Pollen Figure description numbers

R. aquaticus L...... Heikkinen s.n. Finland 3(-4)C, perforate and spinulose R. crispus L...... Standley 18083 Montana 3C, perforate and spinulo se R. scutatus L...... Pfister 1158/2 France 3C, perforate and spinulose Ruprechtia lmiflora Meisner ...... Hatschbach 13161 Brazil 3C, deeply punctate- 106, 171 striate R. pallida Standley ...... Neman 17 Mexico 3C, perforate-rugulose 107, 172 R. ramiflora (Jacquin) Meyer ...... Haught 3914 Colombia 3C, deeply punctate- 108, 109 striate Symeria paniculata Bentham ...... Ducke 650 MO Brazil 3c, 2 psilate L. .... Pittier 12204 Venezuela 3C, punctate- 86, 173 striate 22 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE5.-Primulaceae specimens examined (3C = 3-colporate, 4C = 4-colporate)

Species Collector Location Pollen Figure description numbers

Anagallis iinifolia L...... Reverchon 388 Spain 3C, prominently punctate 183, 192 Androsace septentrionalis L. Tarleton 8 Alaska 3C, punctate Apochoris pentapetala Duby.. Zimmermann 257 China 3C, microreticulate Ardisandra wittsteinii R. Wagner ...... Greenway & Kanuri 15044 Kenya 3C, punctate MO Centunciilus pentandrus R. Brown ...... Standley 12941 Florida 3C, microreticulate Coris monspeliensis L...... Tidestrom 13554 France 3C, sculptured & psilate 174, 193 Cortusa natthioli L...... Koelz 4994 India 3-syncolporate, granular 188 Cyclamen neapolitanm Tenore ...... Stefani s.n. Corsica 3C, punctate 184 3ionysia nira Wendelbo ...... Mandaville 3600 Oman 6-8 zonocolpate, deeply punctate Dodecatheon alpinm (A. Gray) Greene...... Maguire & Holmgren 26449 Oregon 3C, punctate-granular 180, 181 Douglasia montuna A. Gray.. . Thompson 13766 Idaho 3C, punctate 182 Glaw maritima L...... Haakana s.n. Finland 3C, punctate-striate Redfield s.n. Maine 3C, irregularly punctate- 190, 194 striate Hottonia palustris L...... Cernohorsky & Kraj ina Czech0 Slovakia 3C, microreticulate 185 286 Lysimachia ciliata L...... Cronquist & Jones 5956 Idaho 3C, psilate-finely punctate L. hybrida Michaux ...... Leonard & Killip 871 Maryland 3C, finely punctate 175, 195 L. terrestris (L.) Britton, Stern & Poggenberg ...... Mac Kenzie 2720 Yew Jersey 3C, microreticulate 177 Lysimachiopsis hillebrandii Heller ...... Degener 21278 NO Hawaii 4C, punctate-psilate .Vambergia thyrsiflora (L.) Reichenbach ...... Andersen s.n. Norway 3C, irregularly 176, 196 microreticulate Omph~logr~~n~avincaeflora Franchet...... Rock 3573 China 3C, microreticulate 191, 197 Prirnula farinosa L...... St. John 90675 Quebec 4-syncolporate, microreticulate P. incisa Franchet...... Rock 17474 China 3C, microreticulate P. officinalis (L.) Jacquin. Ludera s.n. Poland 6-8 zonocolpate, 198 microreticulate ?. veris L...... Charpin et al. s.n. France 6-10 zonocolpate, 186, 187 microreticulate Skvortsoo s.n. USSR 6-8 zonocolpate, 200 microreticulate P. vulgaris Hudson...... Pfister s.n. Switzerland 6-8 zonocolpate, microreticulate (many abnormal grains) Samolus ebracteatus Kunth... Francis 8a Florida 3C, punctate SoZdaneZZa alpina L...... Treffer, 1362 in Flora Austria 3-colpate (syncolpate?), 189 Exsiccata Austro- scabrate-spinulose Hungar ica S. austriaca Vierhapper ..... Keller s.n. Austria 3-colpate (syncolpate?), scabrate-spinulose Stimpsonia chmaedryoides C. Wright ...... Ying Hu 10001 Hang Kong 312, finely reticulate 178, 179, 199 Trientalis americana (Persoon) Pursh ...... Palmer 1370 Canada 3C, punctate FIGURES1-6.4entrospermae pollen, SEM: 1, Aizoaceae, Mesembryanthemum variabile Haworth, equatorial view, x 4100; 2, Molluginaceac, Limeum viscosum Fenzl, equatorial view, x 3900 3, Basellaceae, Anredera scandens Moquin, x 3550; 4, Caryophyllaceae, Gymnocarpos fruticosum Pcrsoon, X 3350; 5, Chenopodiaceae, ambrosioides L., x 3600; 6, Portulacaceae, Naiocrene pawifoh (Moquin) Rydberg, x 1900. (Photo reduced to 81v2 percent.) n z0 4z c:W 2 0 FIGURES 7-12.-centrospermae pollen, SEM: 7, Molluginaceae, Limeum uiscosum, ektexine sur- mz face, X 7500; 8, Aizoceae, Mesembryanthenium variabile, ektexine surface, x 7500; 9, Aizoaceae, 4 Geocarpon minimum Mackenzie, ektexine surface, x 7500; 10, I’ortulacaceae, Naionene parui- 0 folia, X 7500; 11, Carlaceae, Borricuctur tem~iserpens(Rauh & Backeberg) Kimnach, ektexine surface, X 7500; 12, Cactaceae, Ilarnatocuclu5 seti\pinus Britton & Rose, ektexine surface, x 7500. (Photo reduced to 7GS percent.) FICURFS13-18.-Centrospermae pollen, SEM: 13, Amaranthaceae, Psilotrichurn arnpZum Sussen- guth. X 4000; 14, Caryophyllaceae. Siphonychia arnericana (Nuttall) Torrey & A. Gray, x 4600; 15, Caryophyllaceae, Herniaria @bra L., x 6000; 16, Caryophyllaceae, Cardionema ramosissirna A. Nelson & Macbride, x 5500; 17, Cactaceae, Opuntia Zindheimeri Engelmann, x 840; 18, Nyctaginaceae, Abronia angustifolia Greene, equatorial view, x 2870. (Photo reduced to 81 percent.) 26 SMMITHSONIAN CONTRIBUTIONS TO BOTANY FICURE~19-23.4entrospermae pollen, TEM: 19, Aizocaceae, Mesembryanthemum variabile, the foot layer is extremely thickened and is underlain by a thin but consistent endexine; the break in the endexine at extreme right may be a ruptured area; 20, Amaranthaceae, Psilotri- churn amplum, an endexine is entirely absent; the thin-layered aperture contains a large pointed fragment of ektexine; 21, Basellaceae, Anredera scandens, a wedge of endexine is prominent beneath the colpus, but in the mesocolpial regions it is less distinct and has an electron density similar to that of the foot layer; however, the endexine is fibrillar and the inset (arrows) shows the fibrils to at least superficially resemble unit membranes; 22, Cactaceae, Opuntia lindheimeri, section is through one of the large apertures (Figure 17) with numerous flecks of ektexine; 23, Caryophyllaceae, Gyrnnocarpos fruticosurn, it is difficult to distinguish a foot layer or endexine; the inset suggests that there are two layers with an irregular separation. (Scales equal 1 em.) 28 SMITHSONIAN CONTRIBUTIONS TO BOTANY uW

FIGURES24-28.4entrospermae pollen, TEM: 24, Caryophyllaceae, Herniuriu glubra, an irregular but notablc endexine is characteristic of this taxon; the absence of spines or pcrforations in a section is consistent with the surface depicted by SEM (Figure 15); 25, Chenopodiaceae, Chenopodium nmbrorioides, the equatorial section and that contained in the inset (polar section) indicate a thin foot-layer, a highly irregular and granular endexine, and “internal foramina-like” openings in the thickened tectum; 26, Molluginaceae, Lirneuni uiscosum, micrograph includes sections through mesocolpial (upper) and apcrtnral (lower) regions; aperture has numerous flecks of ektexine; 27, Nyctaginaceae, Abronia ungustifoliu, the irr~gularstructures are due to an oblique section through a coarsely reticulate ektcxine; an endexine is not evident in this taxon; 28, Portulacaceae, Naiocrene parvifolia, the endexine is evident in the apcrturc region while in the mesocolpial regions it is either reduced or absent. (Scales equal 1 am.) FIGURFS2%34.--Plumbaginaceae pollen, SEM. Cerutostigma gri@thii C. B. Clarke: 29, equatorial X 11578, 4 view, 1250; 30, ektexinc surface, x 7500 (29, 30, Rock rounded verrucac Plumbago 0 Iorm); 31, equatorial view, x 1450; 32, ektexine surface, x 7500 (31, 32, Rock 6577, pointed verrucac Plumbago form). Plumbago rosen L.: 33, equatorial view, x 1500; 34, ektexine surface. X 7500 (33, 34, pointed verrucae Plumbago form). Photo reduced to 74 percent.) FIGURFS35-40.-Plumbaginaccae pollen, SEM. PZurnbago europaea L.: 35, polar view, X 1700; 36, ektexirie surface, x 7500 (35, 36, Sporiks s.n. GH, rounded verrucac Plurnbago form); 37, polar view, X 1700; 38, ektexine surface, x 7500 (37, 38, Rnine 5.n. GH, pointed verrucac Plumbago form). Plumbago auriculala Lamarck: 39, polar view, x 1250; 40, ektexine surface, x 7500 (39, 40, Bayliss 1187 GH, rounded verrucae Plumbago form). (Photo reduced to 7694 percent.) FlGURFS 414G.-Plnmhaginaceae pollen, SEM. Liinoniunl uiciosoi Pau: 41, equatoiial view, X 1250; 4 42, ektexine surface, x 3000 {coarsely reticulate Armeria form). Arrneria rnaritirna {Miller) 0 Willdenow: 43, equatorial view, x 1150; 44, ektexine surface, x 5000 (43, 44, Suenson s.n., finely reticulate Armeria form); 45, polar view, x 1250; 46, cktexine surface, x 3000 (45, 46, Mathiesen Q Pedersen s.n., coarsely reticulate Armeria form). (Photo reduced to 77 percent.) FIGURE47-52.-Plumbaginaceae pollen, SEM. Statice tenella Turczaninow: 47, polar view, X 1500; 48, ektexine surface, x 5000 (47, 48, Chaney 517, coarsely reticulate Armeria form); 49, polar view, x 1500; 50, ektexine surface, x 7500 (49, 50, Chaney 517a, finely reticulate Armeria form). Lirnonium vulgare Miller: 51, ektexine surface, x 5000 (Lawalree 3820 MO, coarsely reticulate Armeria form); 52, ektexine surface, x 7500 (Holm-Nielsen s.n. MO, finely reticulate Armeria form). (Photo reduced to 79 percent.) n z0

FIGURES53-58.-Plumbaginaceae pollen, SEM. Goniolitnon collinuin (Grisebach) Boissier: 53, polar view, X 1600; 54, ektexine surface, x 5000 (coarsely reticulate Armeria form). Statice 4 0 sinuatu L.: 55, polar view, x 1500; 56, ektexine surface, x 4000 (55, 5G, Vuccari 495, coarsely reticulate Armeria form); 57, polar view, x 1550; 58, ektexine surface, x 7500 (57, 58, Maire 6. WilczeR 1048, finely reticulate Armeria form). (Photo reduced to 76 percent.) 2 c!

WU

FIGURES 5!?-64.-Plumbaginaceae pollen, SEM. Ceratostigma willmottianurn Stapf 59, X 1150; 60, ektexine surface, x 5000 (59, 60, Wilson 1373, pantocolpate Plumbago form); 61, polar view, X 1300; 62, ektexine surface, x 5000 (61, 62, Kingdon-Ward I2530 MO, 3-colpate Plumbago €ortn). Dyerofihyturn africanurn (Lamarck) 0, Kuntze: 63, polar view, x 2000; 64, ektexine sur- face, x 5000 (Werderrnann 6 Oberdieck 594, pointed? verrucae Plumbago form). (Photo reduced to 79% percent.) 36 SMITHSONIAN CONTRIBUTIONS TO BOTANY FICURE~65-68.-Plumbaginaceae pollen, TEM. olivieri Jaubert & Spach: 65, oblique section in aperture region; note thin but distinct endexine and random internal foramina (small holes) in the ektexine; 66, oblique section emphasizing thin endexine (arrow) and numerous internal foramina (coarsely reticulate Armeria form). Arrneria maritirna: 67, a line network of sporopollinen surrounds the muri and the inset, a tangential section, clarified this interpretation and correlates with images obtained from SEM (Figures 44 and 46); arrows point to internal foramina partially filled with electron dense material (Mathiesen dr Pedersen s.n., coarsely reticulate Armeria form); 68, in this section of an aperture the endexine is evident although highly fragmented; note that the outer surface of the muri appears somewhat ridged due to an off-center cut through the smaller spines (Svenson s.n., finely reticulate Armeria form). (Scales equal 1 am.) 38 SMITHSONIAN CONTRIBUTIONS TO BOTANY FIGURES6%74.-Plumbaginaceae pollen, TEM. Cerutostigrnu grifithii: 69, the section is some- what oblique and therefore the two levels of columellae appear incomplete; note that the terminal portions of the incompletely depicted outer collumellae consist of fine bristle-like structures; the endexine is absent in the mesocolpial areas (Rock 11578, rounded verrucae Plumbago form); 70, morphology similar to Figure 69 except that the terminal portion of outer columellae appears more massive (Rock 6577, pointed verrucae Plumbago form). C. wihot- tianurn: 71, note thin, plate-like endexine (arrow) in aperture region (Wilson 1373, pantocolpate Plumbago form). Dyerophyturn ofricanum: 72, radial section illustrates characteristics of inner columellae, smaller in diameter but almost equal in length to the outer columellae (Werder- mann & Oberdierk 591, pointecl? verriicae Plumbago form). Goniolirnon collinurn: 73, in contrast to Figures 69-72, all one form or the other of the Plumhago type, this section illustrates the single layer of columellae characteristic of the Armeria type; the foot layer has perforations but at the present time they are not considered to be internal foramina; arrow points to endexine in the region of the aperture; the granular material surrounding the outer part of the exine appears to be acetolysis resistant and is thought to be a component of the anther rather than the pollen wall (coarsely reticulate Armeria form). Lirnoniactrurn guyonionurn Durieu de Maisonueuve: 74, arrows point to endexirie in regions of apertures (finely reticulate Armeria form). (Scales equal 1 @m.) 40 SMITHSONIAN CONTRIBUTIONS TO BOTANY FIGUWS75-81.-Plumbaginaceae pollen, TEM. Limonium viciosoi: 75, arrows indicate internal foramina in ektexine; the lower part of the foot layer is somewhat lamellar and may be a thin endexine (coarsely reticulate Armeria form). Plumbago scandens L.: 76, oblique section (rounded? verrucae Plumbago form). Statice sinuata: 77, very oblique section; 78, section -I- tangential (77, 78, Maire d. Wilcxek 1048, finely reticulate Armeria form); 79, section +- tangential; 80, note fragmented but visible endexine (79, 80, Varcari 495, coarsely rcticu!ate Armeria form). Statice tenella: 81, oblique section, fragmented area on right indicates aperture region (Chaney 517, coarsely reticulate Armeria form). (Scales equal 1 Gm.)

6 FIGURES82-87.-Polygonaceae pollen, SEM: 82, Nemacaulis denudata Nuttall, mesocolpial view, X 3100; 83, Oxytheca trilobata A. Gray, mesocolpial view, x 1850; 84, Chorizanthe fimbriata Nuttall, mesocolpial view, X 1950; 85, C. paniculata Bentham, equatorial view, X 2750; 86, Triplaris americana L., equatorial view, X 2650; 87, Fagopyrum esculentum Moeuch, equatorial view, X 1600 (Photo reduced to 77v2 percent.) d E P uW

F~CURES88-93.-Polygonaceae pollen, SEM: 88, Mucronea californica Bentham, equatorial view, X 2525; 89, ektexine surface, x 7500; 90, Eriogonum marifolium Torrey k A. Gray, equatorial view, X 3250; 91, ektexine surface, x 7500; 92, Gymnopodiunz antigonoides (Robinson?) Blake, equatorial view, x 2425 (Goldman 743); 93, ektexine surface, x 7500 (Goldman 743). (Photo reduced to 76 percent.) FIGURES9499.-Polygonaceae pollen, SEM: 94, Calligonum comosum L’Heritier, equatorial view, 4 0 X 2500; 95, ektexine surface, X 7500; 96, Hurfordia mucropleru (Bentham) Greenc & Parry, equatorial view, x 3050; 97, cktexine surface, x 7500; 98, Atraphaxis buxifolia Jaubert & Spach, equatorial view, x 2800; 99, ektcxine surface, x 7500. (Photo reduced to 84 percent.) FICURFS100-105.-Polygonaceae pollen, SEM: 100, Muehlenbeckiu cunningkamii Mueller, equa- torial view, x 2730 (Aston 984); 101, ektexine surface, x 7500 (Aston 984); 102. M. chilensis Meisner, equatorial view, x 3570; 103, ektexine surface, x 7500; 104, M. tamnifolia (H.B.K.) Meisner, equatorial view. x 3600; 105, ektexine surface, x 7500. (Photo reduced to 83% percent.) +l FIGURESlOC%111.-Polygonaceae pollen, SEM: 106, Ruprechtia laxiflora Meisner, equatorial view, 0 X 3400; 107, R. pullida Standlcy, equatorial view, x 2500; 108, R. romiflora Uacquin) Meyer, equatorial view, X 2700; 109, ektexine surface, x 5000; 110, Coccoloba cordata Chamisso, equa- torial view, X 2520; 111, ektexine surface, x 7500. (Photo reduced to 79 percent,) FIGURES112-117.-Polygonaceae pollen, SEM: 112, Persicaria coccinea Greene, X 1575; 113, Polygonurn acuminaturn Kunth, x 1575; 114, P. orientale L., x 1600; 115, ektexine surface, X 7500; 116, P. dielsii Leville(?), oblique view, colpus horizontal in lower half, X 2200; 117. ektexine surface, colpus in center, x 5000. (Photo reduced to 76 percent.) FIGURES118-123.-Polygonaceae pollen, SEM: 118, Polygonurn virginianurn I>., x 2000; 119, arnphibiurn L., 1400; 121, ektexine surface, x 5000; 120, P. X ektexiue surface, colpus lower 4 right, X 9000; 122, P. capilutum D. Don, polar view, x 2500; 125, ektcxiue surface, x 7500. 0 (Pholu reduced to 77v2pcrceiit.) FIGURES 124-129.-Polygonaceae pollen, SEM. Polygonurn a@ne D. Don: 124, equatorial view, X 2200. p. viviparurn L.: 125, slightly oblique equatorial view, x 1700. P. vaccinifoliurn Wallich: 126, equatorial view, X 1900; 127, ektexine surface x 5000. P. bistorta L.: 128, mesocolpial view, X 2300; 129, ektexine surface, x 5000 (128, 129, Cantlon 6. Malcolm 580085). (Photo reduced to 83 percent.) FIGURES 130-135.-Polygonaceae pollen, SEM: 130, Polygonella fimbriata (Elliot) Horton, meso- +I colpial view, X 3400; 131, P. polyguma (Ventenat) Engelmann & A. Gray, equatorial view, 0 X 5750; 132, Podopterus mexicanus Kunth, equatorial view, X 2970; 133, Polygonum forrestii Diels, X 2900; 134, P. cyanandrium Dick, x 3600; 135, ektexine surface, x 8500. (Photo re- duced to 74 percent.) FIGURES136--14l.-Polygonaceae pollen, SEM: 136, Emex australis Steinheil, equatorial view, X 2990 (SeydeZ2975); 137, Lastarriaea chilensis Remy, mesocolpial view, x 3400 (Worth Q Morrison 16338 UC); 138, Rumex acetosa L., equatorial view, x 4400; 139, ektexine surface, x 10,000; 140, Polygonurn conuol~lusL., mesocolpial view, x 3050; 141, ektexine surface, x 7500. (Photo reduced to 78y2 percent.) 52 SMITHSONIAN CONTRIBUTIONS TO BOTANY FIGWRFS142-149.-Polygonaceae pollen, TEM: 142, Antigonon guaternalense Meisner, the endexine is narrow and plate-like; 143, Atraphaxis buxifolia, section somewhat oblique but endexine is thick and partially lamellar; 144, Calligonurn cornosurn, the tectum and columellae are well developed but the foot layer is greatly reduced; 145, Choriranthe breweri S. Watson, the tectum is thin and the lower part highly globular; the foot layer is rednced (or absent?) and the endcxine narrow but uniform; 146, C. paniculata, this section is very similar to that of Figure 145, but there is a very thin foot layer and endexine; 147, Coccoloba cordata, section somewhat oblique; foot layer is extremely thick while the columellae and tectum are of smaller dimensions: extending from the tectum are large, irre\gularly shaped components; a vestigial endexine is suggested but additional work is necessary for confirmation: 148, Eriogonurn rnari- foliurn, foot layer is very reduced as in Figures 144 and 145, but the endexine appears massive due largely to section through aperture: 149, E. parishii, S. Watson, very similar to Figure 145. (Scales equal 1 pm.) 54 SMITHSONIAN CONTRIBUTIONS TO BOTANY FIGURES 150-156.-Polygonaceae pollen, TEM: 150, Fagopyrurn esculenturn, the section is similar to Antigonon guatemalense (Figure 142) in the thickened tectum with funnel-like depressions (Figure 87), reduced foot layer, and thin but recognizable endexine; 151, Gym- nopodium nntigonoides, the endexine is not clearly evident in this somewhat oblique view, but, the inset of a section including the colpus reveals uniform endexine (Goldman 743); 152, Harfordia macroptera, section through the colpus with prominent endexine; the lower surface of the tectum is irregular (Figures 145, 146, 149, 157, 158); 153, Muehlenbeckia chilensis, except for the aperture regions the endexine is highly reduced; 154, M. tarnnifolia, the endexine appears to be more uniform than in Figure 153; 155, M. cunninghamii, the tectum is thick with few perforations and the highly lamellar endcxine and foot layer are approximately equal in thickness (Aston 984); 156, M. polybotryar Meisner, section somewhat oblique; the foot layer reduced and endexine prominent. (Scales equal 1 am.) 56 SMITHSONIAN CONTRIBUTIONS TO BOTANY FIGURES157-165.-Polygonaceae pollen, TEM: 157, Nemacaulis denudata, the section illustrates several characteristics of the punctate type, i.e., tectum with granular lower snrface, very reduced foot layer, and an endexine which at least in the region of the colpus is very prominent; 158, Oxytheca trilobata, same as 157, the double arrows indicate the extremely thin foot layer, single arrows indicate acctolysis resistant material, which can be readily mistaken for exine layering; 159, Polygonurn orientale, long columellae fused at the apex to form the muri alternate with smaller free columellac in the lumina (Figures 114, 115); a thin endexine can be recognized in the aperture region to the left; 160, Podopterus mexicanus, an endexine cannot he recognized but the lower part of the foot layer appcars to consist of a thin, less electron-dense zone; 161, Polygonella firnhriata, the section reveals a well-developed foot layer and thickened endexine, an unusual combination in the family; 162, Polygonurn arnphibium, section at right angle through muri; 163, P. arnphibium, section parallel through murus; 164, P. bistorta, section, which includes entire pollen grain, is oblique; the densely packed columellae are rare and limited to Bistorta complex (Cantlon Q Malcolm 580085); 165, P. conuolvulus, section through polar region where tectum is psilate; this taxon and Polygonella fimbriata (Figure 161) are the only two in which both the foot layer and endexine are well developed; this supports their parallel exomorphology observed in SEM (Figures 130, 140, 141) and discussed in text. (Scales equal 1 am.) 58 SMITHSONIAN CONTRIBUTIONS TO BOTANY FIGURES166-173-Polygonaceae pollen, TEM: 166, Polygonum dielsii, section 5 oblique, solid tectum indicates section is through muri; 167, P. jorrestii, the most distinctive member of the genus in TEILI; the endexine is thin, the ektexine contains abundant holes or internal foramina, and the tectum is composed of very large, solid spines on an irregular or granular base; 168, P. vaccinijolium, very similar to Figure 164. densely packed columellae and also a member of the Bistorta complex; 169, P. virginianum, the discontinuous tectum reflects reticulate sculpture; 170, Rumex acetosa, the foot layer is either greatly reduced or absent; endexine thickness and rupture indicate colpus; 171, Ruprechtia laxiflora, foot layer is consistent and well developed; arrows point to what appears to be a lamellar endexine in colpial region; 172, R. pdida, similar to Figure 171 but endexine somewhat better developed; the accumulation of apparent foot layer material in colpus region is unusual; 173, Triplaris americana, similar to Figure 151, thickened tectum, thin foot layer and endexine. (Scales equal 1 @m.) Q, 0

z8

FIGURES174-179.-Primulaceae pollen, SEM: 174, Coris monspeliensis L., equatorial view, X 2500; 175, Lysimachia hybrida Michaux, equatorial view, x 5000; 176, Naumbergia thyrsiflora (I..) Reichenbach, mesocolpial view, x 4620; 177, I.ysimachia terrcstris (L.) Britton, Stern, & Poggenberg, mcsocolpial view, x 4400; 178, Stimpsonia chamaedryoides C. Wright, equatorial view, X 3200; 179, ektexine surface, x 7500. (Photo reduced to 72 percent.) FIGURES180-185.-Primulaceae pollen, SEM: 180, Dodecatheon alpinum (A. Gray) Greene, equa- torial view, x 4000; 181, ektexine surface, x 7500; 182, Douglasia montana A. Gray, meso- colpial view, x 4250; 183, AnagaZZis Zinifolia L., equatorial view, x 3900; 1% Cyclamen neapolitanum Tenore, mesocolpial view, x 6500; 185, Hottonia palwtris L., equatorial view, x 5250. (Photo reduced to 78 percent.) n z0

i $0 FIGURES18&191.-Primulaceae pollen, SEM: 186, Prirnula veris L., oblique view, x 3200; 187, ektexinc surface, x 7500 (186, 187, Charpin et al. s.n.); 188, Cortusa matthioli L., polar view with triangular apocolpial field, x 5000; 189, Soldanella alpina L., equatorial view, X 6060; 190, Glaux maritima L., equatorial view, x 4300 (Redfield s.n.); 191, Omphalograrnma vincaeliora Frauchet, equatorial vicw, x 3550. (Photo redut crl to 76 perccrit.) W-4

FIGURES192-195.-Primulaceae pollen, TEM: 192, Anagallis linifolia, a uni- form endexine is notable as is the prominent foot layer; 193, Cork rnonsfieliensis, the section includes the entire grain and reflects the varia- tion of the sculpture as seen in SEM (Figure 174); the endexine is greatly thickened in the region of the apertures; 194, GZaux rnaritirna, the foot layer and endexine are both prominent and approximately equal in thick- ness (Redfield s.n.); 195, Lysimachia hybrida, the oblique section enhances the thickness of the foot layer and endexine. (Scales equal 1 Gm.) FIGURES196-200.-Prirnulaceae pollen, TEM: 196, Nuumbergiu thrysifloru, thickened tectum is supported by reduced columellae on a well-defined foot layer and prominent endexine; 197, Omphalogrammu uincuelloru, simi- lar to Figure 196 except for more massive columellae; 198. Primula oficinulis (L.) Jacquin, in contrast to all other taxa of Primulaceae ex- amined in TEM, those in the genus Prirnulu are without a foot layer; however in light microscopy and SEM, the samples appeared at least par- tially sterile; 199, Stimpsoniu chamaedryoides, oblique section of entire grain illustratirig consistcnt foot layer, and an endexine that is massive in aperture regions and thin but recognizable in the mesocolpial areas; 200, Primulu ueris L., see Figure legend 198 (Skuortsoo s.n.). (Scales equal 1 Gm.)

4 0