Bot. Bull. Acad. Sin. (1997) 38: 277-284

Morris and Lammers — Pollen of Codonopsis

Circumscription of Codonopsis and the allied genera Campanumoea and Leptocodon (Campanulaceae:

Campanuloideae). I. Palynological data

Kari E. Morris^1,2 and Thomas G. Lammers^2,3

¹Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60608, USA

²Department of Botany, Center for Evolutionary and Environmental Biology, Field Museum of Natural History, Chicago, IL 60605-2496, USA

(Received January 28, 1997; Accepted May 16, 1997)

Abstract. Pollen from 23 accessions of Codonopsis and the allied genera Campanumoea and Leptocodon was examined via light microscopy, scanning electron microscopy, and transmission electron microscopy. All grains examined were of four types. Type I grains (found in all accessions of Campanumoea sect. Campanumoea, Codonopsis subg. Codonopsis, and Leptocodon) were oblate sphaeroidal, circular in polar outline, 4_10-colpate, with long colpi, short spinules, and thin nexine. Type II grains (found in all accessions of Campanumoea sect. Cyclocodon) were oblate sphaeroidal, semi-angular in polar outline, 3-colporate, with long colpi, long spinules, and thick nexine. Type III grains (found in all accessions of Codonopsis subg. Pseudocodonopsis) resembled Type I grains, but had the long spinules characteristic of Type II; further, the colpi were much shorter than in Type I and II. Type IV grains (found in all accessions of Codonopsis subg. Obconicicapsula) likewise resembled Type I grains, but had colpi of a length intermediate between Type I and Type III. The uniformity of pollen morphology in Campanumoea sect. Campanumoea, Codonopsis subgen. Codonopsis, and Leptocodon might be interpreted as supporting their merger as a single genus, while the distinctness of Type I and Type II pollen might be interpreted as supporting the recognition of Cyclocodon as a genus distinct from Codonopsis. However, the palynological data are less clear as to the disposition of Codonopsis subg. Pseudocodonopsis and subg. Obconicicapsula, and a realignment of generic boundaries must await completion of studies involving additional data sets.

Keywords: Campanulaceae; Campanuloideae; Campanumoea; Codonopsis; Cyclocodon; Electron microscopy; Leptocodon; Pollen; Palynology; Ultrastructure.

Introduction

Codonopsis* (Campanulaceae: Campanuloideae) comprises 55 species endemic to eastern Asia, from Kamchatka and Japan south to Afghanistan, Pakistan, the Himalayas, southern China, and Taiwan (Fedorov, 1957; Rechinger and Schiman-Czeika, 1965; Hong, 1983; Shimizu, 1993). The plants are perennial with tuberous roots; scandent, twining, or less commonly erect or ascending herbaceous stems; solitary or paired axillary or terminal flowers; 3_5-locular ovary with a 3_5-lobed stigma; and capsular fruits loculicidally dehiscent at apex; most have a pungent skunk-like or `foxy' odor of uncertain chemistry. Chromosome number has been determined for eight species; all show n = 8 (Rosén, 1931; Gadella, 1966; Lee, 1967; Zhukova, 1967; Krasnoborov et al., 1980; Nishikawa, 1985; Sui et al., 1985; Jee et al., 1989; Yoo and Lee, 1989; Ge and Wang, 1990). The most recent classification of the genus (Hong, 1983) recognized three subgenera: Codonopsis, Obconicicapsula, and Pseudocodonopsis.

Some authors (Moeliono and Tuyn, 1960; Van Thuan, 1969; Lammers, 1992) have expanded the circumscription of Codonopsis to include Campanumoea. This genus of five species is likewise endemic to eastern Asia, though its distribution extends farther south than Codonopsis, to tropical India, Indochina, the Philippines, Malaysia, Indonesia, and New Guinea (Moeliono and Tuyn, 1960). Campanumoea indeed resembles Codonopsis, but differs in its baccate fruit; furthermore, it lacks the distinctive foxy odor found in most Codonopsis, and the ovary is often 6-locular with a 6-lobed stigma. The species have been divided (Clarke, 1881; Tsoong, 1935; Hong, 1983; Shimizu, 1993) between two sections: Campanumoea and Cyclocodon. According to Hong (1995), the chromosome number of the former is n = 8, while that of the latter is n = 9.

Recently, Grey-Wilson (1990) has proposed that Codonopsis be enlarged further through the incorporation of Leptocodon, a genus of two species endemic to the Himalayas, from India to Burma. Leptocodon resembles Codonopsis overall, but differs in the possession of a unique set of five glands atop the ovary, alternate with the stamens. The chromosome number of Leptocodon is unknown.

³Corresponding author. E-mail: lammers@fmppr.fmnh.org

*Authorities for all scientific names will be found in Table 1.

Botanical Bulletin of Academia Sinica, Vol. 38, 1997

Simple incorporation of Campanumoea into Codonopsis is complicated by the results of a palynological analysis of the former genus. Murthy (1983) discovered that pollen of sect. Campanumoea was identical to that reported for Codonopsis: suboblate, 5_7-colpate, with spinules ca. 1 µm long. In contrast, the species of sect. Cyclocodon had pollen grains that were oblate sphaeroidal and 3-colporate, with spinules ca. 3 µm long. On this basis, Murthy proposed that Campanumoea be divided, with the species of sect. Campanumoea transferred into Codonopsis but sect. Cyclocodon treated as a distinct genus.** Murthy did not examine pollen of Codonopsis himself, but only referred to published descriptions, which represented a mere eight species, all of which belonged to subg. Codonopsis. Though subsequent studies have described the pollen of one or more species of that subgenus, as well as subg. Psuedocodonopsis (Dunbar, 1984; Lee et al., 1988; Yoo and Lee, 1989; Nowicke, 1992; Shrestha and Tarasevich, 1992), the sampling still is not comprehensive, and there has been no synthesis of palynological data in the group as a whole.

The purpose of the present study, therefore, is to re-examine Murthy's (1983) findings in Campanumoea, and to expand upon it by surveying pollen in a larger and more comprehensive representation of Codonopsis species. In particular, we wish to determine if the type of pollen seen in Campanumoea sect. Cyclocodon is truly unique to that group or whether it can also be found among the species of Codonopsis. Additionally, we want to examine Leptocodon to determine if palynological data are consistent with its inclusion in Codonopsis.

Materials and Methods

Herbarium specimens (Table 1) provided the pollen samples examined in this study. A total of 23 samples was examined. This included 14 samples of Codonopsis, representing 13 species and all three subgenera recognized by Hong (1983); eight samples drawn from all five species of Campanumoea; plus a single sample of Leptocodon.

Whole anthers were removed and acetolyzed following procedures outlined by Erdtman (1966). For light microscopy (LM), all 23 samples had pollen grains mounted in glycerin jelly and the cover slip sealed with paraffin. For scanning electron microscopy (SEM), grains from all 23 samples were sputter-coated with gold, then examined and photographed with an Amray 1810 or a Hitachi 570. For transmission electron microscopy (TEM), pollen from 20 samples was fixed in agar with osmium tetroxide, stained with uranyl acetate, and embedded in L. R. white. After sectioning, the pollen was stained in lead citrate and examined via a JEOL 100 or JEOL 1200. Characters recorded for each sample were grain shape, grain outline,

polar diameter, equatorial diameter, aperture number, aperture type, colpus length, spinule length, and nexine thickness.

Results

The results of our study are presented in Table 1, together with all previously published palynological data on these genera. Despite Murthy's (1983) statement that the pollen of Campanumoea and Codonopsis fell into two shape classes, suboblate and oblate sphaeroidal, all pollen examined in our study could be assigned to a single category, oblate sphaeroidal (Punt et al., 1994). However, we did observe two classes as regards outline in polar view: circular and semi-angular. Grains with a circular outline had polar diameters (means in parentheses) of 26-(39)-56 mm and equatorial diameters of 29-(40)-66 mm. Grains with a semi-angular outline averaged a little smaller, with polar diameters of 25-(32)-39 mm and equatorial diameters of 26-(33)-40 mm. As regards aperture number and type, grains were either 3-colporate or 4_10-colpate. Colpus lengths fell into three classes: short (covering less than 1/4 the distance from pole to pole), medium (covering between 1/4 and 1/2 the distance from pole to pole), and long (covering more than 2/3 of the distance from pole to pole). Spinules fell into two length classes: short (ca. 1 mm long) and long (2_3 mm long). Nexine thickness likewise fell into two classes: thin (0.1_0.5 mm thick) and thick (0.6_1 mm thick).

On the basis of the distribution of these character states, four types of oblate sphaeroidal pollen grains could be distinguished. Judging from all available palynological literature, these four types are unique to Codonopsis and its allies. Type I was circular in polar outline, 4_10-colpate, with long colpi, short spinules, and thin nexine; it was found in all samples of Codonopsis subg. Codonopsis (Figures 1_3), Leptocodon (Figures 10_12), and Campanumoea sect. Campanumoea (Figures 13_15). Type II was semi-angular in polar outline, 3-colporate, with long colpi, long spinules, and thick nexine; it occurred in all samples of Campanumoea sect. Cyclocodon (Figures 16_18). These are the two types reported by Murthy (1983); the other two types were not. Type III was circular in polar outline, 4_6-colpate, with short colpi, long spinules, and thin nexine; it was observed in all samples of Codonopsis subg. Psuedocodonopsis (Figures 7_9). Type IV was circular in polar outline, 5_7-colpate, with medium colpi, small spinules, and thin nexine; it was present in all samples of Codonopsis subg. Obconicicapsula (Figures 4_6). Thus, Types III and IV are essentially similar to Type I grains with two exceptions: Type III has the long spinules characteristic of Type II grains and uniquely short colpi, while Type IV possesses colpi of length intermediate between Type I and Type III.

**Though Murthy retained the name Campanumoea for this genus, the rules of nomenclature (Greuter et al., 1994) dictate that the correct name for a genus thus constituted would be Cyclocodon Griff.; Campanumoea would become a synonym of Codonopsis.

Morris and Lammers — Pollen of Codonopsis

Table 1. Characteristics of pollen grains of Campanumoea, Codonopsis, and Leptocodon.

Taxon Voucher or reference Origin Shape Outline¹ Size (µm)² Aperture condition Colpus length³ Spinule length⁴ Nexine⁵

Campanumoea Blume sect. Campanumoea

C. inflata C. B. Clarke Clark 26420 (BM) INDIA Oblate spheroidal Circular 34-(36)-40 × 40 6-8 colpate Long Short Thin Gamble 9740 (K) INDIA Oblate spheroidal Circular 33-(37)-39 × 29-(36)-39 6-7 colpate Long Short Thin

Murthy (1983) INDIA Suboblate — 32-(35)-40 × 40-(45)-50 6-7-colpate Long Short Thin

C. javanica Blume Dunbar (1975)⁶ CHINA Suboblate — 30 × 35 5-6-colpate⁷ Long Short —

Hooker & Thompson INDIA Oblate spheroidal Circular 39-(44)-46 × 39-(44)-49 5-6-colpate Long Short Thin

2024 (K)

Murthy (1983) INDIA Suboblate — 31-(35)-36 × 36-(41)-43 5-6-colpate — Short Thin

Campanumoea sect. Cyclocodon (Griff.) C. B. Clarke

C. celebica Blume Forrest 24903 (K) INDIA Oblate spheroidal Semi-angular 33-(36)-39 × 29-(33)-39 3-colporate Long Long Thick

Murthy (1983) INDIA Oblate spheroidal Semi-angular 28-(30)-32 × 32-(35)-37 3-colporate Long Long Thick

van Beusekom 6786 (K) THAILAND Oblate spheroidal Semi-angular 29-(31)-33 × 29-(31)-33 3-colporate Long Long Thick

C. lancifolia (Roxb.) Merr. Dunbar (1975) SUMATRA Suboblate — 25 × 31 3-colporate — Long —

Huang (1972) TAIWAN Oblate to suboblate — 25-31 × 32-40 3-colporate — Long Thick

Steward et al. 291 (BM) CHINA Oblate spheroidal Semi-angular 29-(33)-33 × 26-(31)-33 3-colporate Long Long Thick

C. parviflora (A. DC.) Benth. Bor 6299 (K) INDIA Oblate spheroidal Semi-angular 26-(31)-33 × 29-(33)-36 3-colporate Long Long Thick

Erdtman (1952) INDIA Suboblate — 24 × 30 3-colporate — — — Murthy (1983) INDIA Oblate spheroidal Semi-angular 27-(30)-31 × 35-(36)-40 3-colporate Long Long Thick

Schlagintweit 208 (BM) INDIA Oblate spheroidal Semi-angular 30-(31)-34 × 30-(31)-32 3-colporate Long Long Thick

Codonopsis Wall. subg. Codonopsis

C. affinis Hook. f. & Thompson Crawford et al. 64 NEPAL Oblate spheroidal Circular 33-(34)-36 × 33-(34)-39 5-6 colpate Long Short Thin

C. bulleyana Diels Chapman (1967) CHINA Suboblate — 38 × 45 7-colpate — Short — Nowicke (1992) CHINA Oblate spheroidal — 41-(44)-48 × 41-(46)-49 6-8-colpate Long Short —

C. cardiophylla Kom. Erdtman (1952) — Oblate spheroidal — 49 × 52 7-9-colpate Long Short —

C. clematidea (Schrenk) C. B. Dunbar (1975) CHINA Oblate spheroidal — 40 × 44 8-colpate Long Short — Clarke Dunbar (1984) CHINA Oblate spheroidal — 40 × 44 8-colpate — Short Thin

Erdtman (1952) TURKESTAN Oblate spheroidal — 45 × 50 8-colpate — Short —

Stainton 2907 (E) INDIA Oblate spheroidal Circular 46-(51)-52 × 42-(47)-49 6-8-colpate Long Short Thin

C. kawakamii Hayata Huang (1972) TAIWAN Oblate to prolate- — 28-46 × 35-47 6-7-colpate Long Short Thin

spheroidal

C. lanceolata (Sieb. & Zucc.) Chapman (1967) — — — — 9-colpate — Short — Trautv. Lee et al. (1988) KOREA Oblate spheroidal — 26-(27)-28 × 33-(36)-39 9-10-colpate Long Short Thin

Yao 9168 (CAS) CHINA Oblate spheroidal Circular 29-(33)-36 × 33-(35)-39 9-colpate Long Short Thin

Yoo & Lee (1989) KOREA Oblate spheroidal Circular 28-(32)-35 × 38-(40)-42 9-10-colpate Long Short —

C. micrantha Chipp Maire 454 (E) CHINA Oblate spheroidal Circular 42-(43)-46 × 39-(43)46 7-8-colpate Long Short Thin

C. minima Nakai Yoo & Lee (1989) KOREA Oblate spheroidal Circular 27-(33)-40 × 30-(36)-47 8-10-colpate Long Short Thin

C. ovata Benth. Shrestha & Tarasevich INDIA — — 50-56 × 54-66 7-8-colpate — — —

(1992)

C. pilosula (Franch.) Nannf. Dunbar (1975)⁸ CHINA Oblate spheroidal — 38-48 × 40-46 7-colpate Long Short —

Lee et al. (1988) KOREA Oblate spheroidal — 35-(39)-42 × 45-(47)-51 6-7 colpate Long Short —

Ho 1057 (CAS) CHINA Oblate spheroidal Circular 39-(42)-49 × 39-(40)-46 5-6-colpate Long Short —

Yoo & Lee (1989) KOREA Oblate spheroidal Circular 32-(38)-40 × 40-(44)-46 6-7 colpate Long Short Thin

Botanical Bulletin of Academia Sinica, Vol. 38, 1997

Table 1. (Continued)

Taxon Voucher or reference Origin Shape Outline¹ Size (µm)² Aperture condition Colpus length³ Spinule length⁴ Nexine⁵

C. rotundifolia Benth. Ludlow s.n. (E) TIBET Oblate spheroidal Circular 36-(40)-43 × 36-(39)-43 7-colpate Long Short Thin

C. tangshen Oliv. Wilson 1023 (K) CHINA Oblate to prolate Circular 33-(36)-39 × 33-(34)-36 6-colpate Long Short Thin

spheroidal

C. thalictrifolia Wall. Long 454 (E) INDIA Oblate spheroidal Circular 42-(47)-52 × 42-(44)-46 7-colpate Long Short Thin

C. tubulosa Kom. McClaren s.n. (K) CHINA Oblate spheroidal Circular 33-(36)-39 × 36-(37)-39 6-7-colpate Long Short Thin

C. ussuriensis (Rupr. & Maxim.) Kobayashi 1210 (CAS) JAPAN Oblate spheroidal Circular 33-(34)-36 × 33-(35)-39 8-colpate Long Short Thin

Hemsl. Lee et al. (1988) KOREA Oblate spheroidal — 38-(40)-42 × 47-(49)-50 8-10-colpate Long Short —

Lee et al. (1988) KOREA Oblate spheroidal — 31-(32)-32 × 36-(37)-38 8-10-colpate Long Short —

Yoo & Lee (1989) KOREA Oblate spheroidal Circular 28-(36)-37 × 38-(31)-46 8-10-colpate Long Short —

C. viridiflora Maxim. Dunbar (1975) — Oblate spheroidal — 36 × 40 8-colpate Long Short —

C. volubilis Nannf. Erdtman (1952)⁸ CHINA Suboblate to oblate — 38 × 43 6-7-colporoidate — Short —

spheroidal

Codonopsis subg. Obconicicapsula Hong

C. dicentrifolia (C.B. Clarke) Crawford et al. 62 (K) NEPAL Oblate spheroidal Circular 50-(54)-56 × 48-(49)-50 5-7-colpate Medium Short —

W.W. Smith Smith s.n. (E) INDIA Oblate spheroidal Circular 49-(50)-56 × 49-(50)-52 5-7-colpate Medium Short Thin

Codonopsis subg. Pseudocodonopsis Kom.

C. convolvulacea Kurz Nowicke (1992) CHINA Oblate spheroidal Circular 38-(42)-48 × 43-(46)-51 6-colpate Short Long Thin

C. forrestii Diels Rock 6036 (NY) CHINA Oblate spheroidal Circular 40-(42)-44 × 44-(45)-46 6-colpate Short L ong —

C. pinifolia (Hand.-Mazz.) Tén 139 (E) CHINA Oblate spheroidal Circular 34-(37)-42 × 38-(39)-40 6-colpate Short Long —

Grey-Wilson

C. vinciflora Kom. Erdtman (1952) CHINA Suboblate — 37 × 43 4-6-colpate Short Long —

Leptocodon Lem.

L. gracilis (Hook. f.) Lem. Erdtman (1952) INDIA Suboblate — 41-56 × 54-66 8-colpate — — —

Forrest 22158 (C) CHINA Oblate spheroidal Circular 29-(34)-36 × 33-(35)-36 9-colpate Long Short Thin Hong and Ma (1991) CHINA Oblate spheroidal — — 8-colpate Long Short —

Shrestha & Tarasevich INDIA — — 31 × 38 9-colpate — — —

(1992)

L. hirsutus Hong Hong and Ma (1991) TIBET Oblate spheroidal — — 7-colpate Long Short —

¹In polar view.

²Minimum-(mean)-maximum polar diameter × minimum-(mean)-maximum equatorial diameter.

³Short = covering less than 1/4 the distance from pole to pole; medium = covering between 1/4 and 1/2 the distance from pole to pole; long = covering more than 2/3 the distance from pole to pole.

⁴Short = ca. 1 µm long; long = 2-3 µm long.

⁵Thin = 0.12-0.59 µm thick; thick = > 0.60 µm thick.

⁶Identified as C. maximowiczii Honda; cf. Hong (1983).

⁷Originally as "colporate" but corrected by Dunbar (1984).

⁸Identified as C. handeliana Nannf.; cf. Hong (1983).

Morris and Lammers — Pollen of Codonopsis

supports Grey-Wilson's (1990) proposal to merge Leptocodon with Codonopsis.

However, other results of our study suggest caution in accepting the revision of generic boundaries proposed by Murthy (1983) and Grey-Wilson (1990). Specifically, we discovered more variation among the species of Codonopsis than was indicated by Murthy (1983). All species known to him palynologically were members of subg. Codonopsis and had pollen corresponding to our Type I. While the additional samples of this subgenus examined by us likewise showed Type I pollen, the samples of subg. Pseudocodonopsis and subg. Obconicicapsula examined in our study differed. Though both resembled Type I grains in their shape, size, aperture type, aperture number, and nexine, they differed from both Type I and Type II in having shorter colpi: covering less than 1/4 the distance from pole to pole in subg. Pseudocodonopsis (Type III) and of intermediate length in subg. Obconicicapsula (Type IV). The former also differed from

Discussion

Our results confirmed the primary finding of Murthy (1983): pollen of Campanumoea sect. Campanumoea is essentially indistinguishable from that of the species of Codonopsis examined previously, while pollen of sect. Cyclocodon is quite distinct. In fact, we detected an additional feature distinguishing the two types of pollen recognized by Murthy (1983): thickness of the nexine. Though Murthy distinguished them on the basis of shape, aperture condition, and spinule length, we found that the nexine of Type II pollen was demonstrably thicker than that of Type I (compare Figures 3 and 15 to Figure 18). This result adds additional support to Murthy's suggestion that sect. Cyclocodon be recognized as a distinct genus while sect. Campanumoea is subsumed into Codonopsis. Furthermore, we determined that pollen of Leptocodon was likewise indistinguishable from the species of Codonopsis examined previously. This similarly

Figures. 1_9. Electron micrographs of Codonopsis pollen. 1, C. lanceolata, polar view, via SEM (1215×). 2, C. lanceolata, equatorial view, via SEM (1333×). 3, C. tangshen, cross section through wall, via TEM (3960×). 4, C. dicentrifolia, polar view, via SEM (983×). 5, C. dicentrifolia, equatorial view, via SEM (1060×). 6, C. dicentrifolia, cross section through wall, via TEM (4800×); note thin nexine relative to sexine. 7, C. convolulacea, polar view, via SEM (1200×); note the long spinules and short colpi. 8, C. convolulacea, equatorial view, via SEM (790×). 9, C. convolulacea, cross section through wall, via TEM (7920×).

Botanical Bulletin of Academia Sinica, Vol. 38, 1997

Figures. 10_18. Electron micrographs of Leptocodon and Campanumoea pollen. 10, L. gracilis, polar view, via SEM (1175×). 11, L. gracilis, equatorial view, via SEM (1110×). 12, L. gracilis, cross section through wall, via TEM (3170×). 13. C. inflata, polar view, via SEM (1210×). 14, C. javanica, equatorial view, via SEM (1200×). 15, C. javanica, cross section through wall, via TEM (7920×). 16, C. celebica, polar view, via SEM (1160×). 17, C. lancifolia, equatorial view, via SEM (1465×). 18, C. lancifolia, cross section through wall, via TEM (4750×).

Acknowledgments. This paper represents a portion of a thesis submitted by KEM in partial fulfillment of the requirements of the degree Master of Science at the University of Illinois at Chicago. She wishes to express her sincerest appreciation to Joan Nowicke (Smithsonian Institution) for training in palynological methods, and for much practical advice and guidance. We thank Betty Strack (Field Museum) for her help with SEM preparations and photography. We also express our sincere appreciation to the curators and administrators of the following herbaria for the loan of specimens: B, BM, CAS, E, F, HAST, K, KUN, MAK, MU, NY, PNH, and SNU.

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Botanical Bulletin of Academia Sinica, Vol. 38, 1997

®Ü±ð¬ì Codonopsis ¤Î¨ä¾Fªñ Campanumoea, Leptocodon ¤GÄݪº¬É¤À I. ªá¯»¸ê®Æ

Kari E. Morris^{1, 2} and Thomas G. Lammers²

¹Department of Biological Sciences, University of Illinois at Chicago

Chicago, IL 60608, USA

²Department of Botany, Center for Evolutionary and Environmental Biology

Field Museum of Natural History, Chicago, IL 60605-2496, USA

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