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Morphological Studies Toward an Improved MORPHOLOGICAL STUDIES Tatyana V. Shulkina,2 John F. Gaskin,2,3 4 TOWARD AN IMPROVED and W. M. M. Eddie CLASSIFICATION OF CAMPANULACEAE S. STR.1 ABSTRACT Growth and seedling morphology of 144 species representing 30 genera of Campanulaceae s. str. were studied. Two types of seedlings were found: Group A, with an elongated epicotyl and elongated internodes, and Group B, with a shortened (not visible) epicotyl and usually shortened internodes. These two types appear to be correlated with other vegetative characters. Thus, plants from Group A have an opposite leaf arrangement (at least early in ontogenesis), rhythmic seasonal growth with a long dormant period, and sympodial branching. Plants from Group B have a spiral leaf arrangement, continuous growth (at least in the non-¯owering period), and sympodial and monopodial branching. Taxa in Group A are distributed mostly in Asia, whereas representatives in Group B occur almost worldwide. The two groups do not coincide with current taxonomic classi®cations but correspond remarkably well with the distribution of other characters such as pollen-grain morphology and correlate with groups based on molecular analysis; therefore, these two groups may re¯ect two lineages. Growth and seedling morphology are of taxonomic signi®cance in Campan- ulaceae and can be used for treatments in conjunction with other characters. Taxonomic changes, which are supported by molecular data, are proposed. Key words: Campanulaceae, growth and seedling morphology and development, taxonomy. Campanulaceae herein are treated in a narrow modate Merciera (De Candolle, 1839). SchoÈnland circumscription (without Lobeliaceae) as a mono- (1889) also divided the tribe Campanuloideae phyletic group with a distinct geographical distri- (Campanulaceae s. str. here) into three groups, bution and with well-de®ned morphological char- based on mode of dehiscence and ovary position, acters. Campanulaceae s. str., despite their size and but these three groups differed in composition from importance in temperate ¯oras, remain unrevised. those of De Candolle. These two classi®cations be- This family, with about 50 genera and 800 species came the basis for all future treatments (Table 1). distributed worldwide, is the largest and most prim- Although the current systems differ greatly from the itive and basal one within the order Campanulales old ones in number of genera, as many taxa have (Lammers, 1992; Takhtajan, 1997). Although rep- been added during the last century, it is easy to resentatives of the family occur on all continents understand what classi®cation each particular au- except Antarctica, the vast majority of genera and thor is following. SchoÈnland's treatment has been species are found in temperate regions of the Old used often and remains a currently useful refer- World. Raven and Axelrod (1974) considered the ence. family to have a Laurasian±African origin. The cen- Fedorov (1957), on the contrary, followed in gen- ters of distribution and diversity include the Med- eral De Candolle's position and published a de- iterranean, East Asia, and South Africa (Shulkina, tailed classi®cation for Campanulaceae growing in 1978; Kolakovsky, 1995; Hong, 1995; Eddie, the former Soviet Union (FSU). Fedorov proposed 1997). 8 tribes (6 new) based on capsule dehiscence, co- De Candolle's (1830) comprehensive monograph rolla shape, and presence and shape of appendages on the Campanulaceae provided a solid basis for between the calyx lobes. Kolakovsky (1995) pro- all subsequent works. He divided the family into posed a new system with 4 subfamilies and 22 two tribes and later added a third tribe to accom- tribes based on internal fruit structure. He 1 We are indebted to Ihsan Al-Shehbaz, Peter Stevens, and Peter Hoch for reading the text and providing useful remarks. Many thanks to Victoria Hollowell for careful editing. T. Shulkina thanks the people who helped her obtain Campanulaceae seeds from different parts of the world: J. P. M. Brenan, A. Cronquist, A. Dolukhanov, R. Gagnidze, R. Kamelin, A. Kolakovsky, N. Morin, H. B. Rycroft, and P. Wendelbo. 2 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299, U.S.A. [email protected]. 3 Present address: USDA, ARS-NPARL, P.O. Box 463, Sidney, Montana 59270, U.S.A. 4 Section of Integrative Biology, University of Texas at Austin, Texas 78712, U.S.A. Present address: Of®ce of Lifelong Learning, University of Edinburgh, 11 Buccleuch Place, Edinburgh, Scotland, U.K. [email protected]. ANN.MISSOURI BOT.GARD. 90: 576±591. 2003. Volume 90, Number 4 Shulkina et al. 577 2003 Morphological Studies of Campanulaceae Table 1. Treatment of genera in Campanulaceae. ered to not warrant subfamilial status. Eddie's Pla- tycodoneae subdivided into the following subtribes: De Candolle (1830, 1839) SchoÈnland (1897) Ostrowskiinae, Cyananthinae, Echinocodinae, Fam. Campanulaceae Subfam. Campanuloideae Codonopsinae, Platycodinae, Campanumoeinae, Tribe Campanuleae Subtribe Campanulinae and Canarininae. His Campanuleae comprised the Adenophora Adenophora following: Wahlenberginae, Jasioneinae, Musschi- Campanula Campanula inae, Azorininae, and Campanulinae. Musschia Heterocodon There is considerable disagreement among all Michauxia Michauxia prior classi®cations of Campanulaceae. Further- Petromarula Ostrowskia more, there is no common opinion about generic Phyteuma Peracarpa limits or higher relationships among the major sub- Symphyandra Phyteuma divisions of the family. Taxonomic problems in this Trachelium Legousia family can be explained by the fact that nearly all Symphyandra of these earlier classi®cations had a geographical Trachelium rather than biological basis. Thus, ¯oristic treat- Tribe Wahlenbergieae Subtribe Wahlenberginae ments differ considerably in the generic delimita- Campanumoea Campanumoea tion of the Campanulaceae for the former U.S.S.R. Canarina Cephalostigma (Fedorov, 1957), Europe (Fedorov & Kovanda, Cephalostigma Codonopsis Codonopsis Cyananthus 1976; Tutin, 1976), Turkey (Damboldt, 1976), and Edraianthus Edraianthus China (Hong, 1983). Jasione Heterochaenia Genera crossing diverse geographical regions Lightfootia Jasione need multidisciplinary study, including research on Microcodon Leptocodon the development of vegetative organs, morphology Platycodon Merciera and anatomy of fruits and seeds, pollen grain struc- Prismatocarpus Prismatocarpus ture, as well as molecular and serological data. As Roella Rhigiophyllum stated by Takhtajan (1997: 6), ``We cannot establish Wahlenbergia Roella phyletic relationships and construct phyletic line- Siphocodon ages using only ¯oral characters. It is all the more Treichelia Wahlenbergia impossible to reconstruct phyletic lineages on the Tribe Merciereae Subtribe Platycodinae basis of the characters of the vegetative organs Merciera Microcodon only.'' The greater the number of characters from Musschia different correlation groups taken into consider- Platycodon ation, the closer we can approximate the evolution- ary phylogeny of the family. Vegetative characters in higher plants are ac- described 9 new genera within Campanula, which corded only a limited place in classi®cation, de- have not yet been included in the Vascular Plants spite the angiosperms being ®rst divided into two of Russia and Adjacent Countries (Czerepanov, great subclasses according to the number of coty- 1995) due to their contradictory descriptions. Takh- ledons as early as the 13th century by Albertus tajan (1997) divided the family into 4 subfamilies Magnus. Publications in which the importance of and 16 tribes, taking into consideration not only vegetative characters is supported are not numer- the fruit structure but also pollen-grain structure, ous (e.g., Stebbins, 1974; Tomlinson, 1984). How- ovary position, as well as the presence or absence ever, life forms and growth patterns, ultimately in- of appendages between the calyx lobes. Subfamily ¯uencing the structure of the mature plant, are Cyananthoideae includes the genera Cyananthus, often ignored or little emphasized because of the Codonopsis, Campanumoea, Leptocodon, and Pla- common opinion that all these characters are adap- tycodon; subfamilies Ostrowskioideae and Canari- tive. However, life forms include many distinctive noideae are monotypic. The last subfamily, Cam- vegetative characters that can be taxonomically panuloideae, consists of 12 tribes and includes all valuable if they are stable. remaining genera. Genera described by Kolakovsky The goals of this study are (1) to study vegetative were not included in the system. Hong (1995) ten- organs and development of life forms in represen- tatively divided the genera into 6 unnamed groups tative species across Campanulaceae; (2) to select based primarily on various morphological charac- characters that are common to species groups that ters. Eddie (1997) divided the family into two major may have taxonomic value; (3) to compare the tribes, with the differences between them consid- groups suggested by these characters with formal 578 Annals of the Missouri Botanical Garden classi®cations for congruence with other morpho- tanical Institute in early spring (March) during logical and molecular data. 1973±1990. Observations were made every other We examined seedling morphology, growth pat- day during germination and early stages of seedling terns, leaf arrangement, seasonal development and growth and once a week for maturing plants. Sam- behavior, and branching patterns before and after ple size per collection (species investigated)
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