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03-C. Tutsumi-4.02 Bull. Natl. Mus. Nat. Sci., Ser. B, 36(1), pp. 21–25, February 22, 2010 Rhizome Morphology and Patterns of Leaf Production of Secondary Hemiepiphytic Oleandra pistillaris (Oleandraceae) Chie Tsutsumi* and Masahiro Kato Department of Botany, National Museum of Nature and Science, Amakubo 4–1–1, Tsukuba, 305–0005 Japan *E-mail: [email protected] (Received 12 December 2009; accepted 18 December 2009) Abstract Secondary hemiepiphytic Oleandra pistillaris and Nephrolepis are characterized by rhizome dimorphism; the rhizomes are erect and creeping (stolon). The erect rhizome produces leaves in apparent whorls at subequal internodes, but the creeping rhizome of O. pistillaris is dor- siventral with variously long internodes, and the creeping stolon of N. cordifolia grows without any leaves. It is in contrast to the general monomorphic rhizome with regular phyllotaxy in other life forms of related ferns. Key words : internodes, leaf production, Nephrolepis, Oleandra pistillaris, rhizome, secondary hemiepiphyte. ing Davalliaceae and Polypodiaceae (Tsutsumi Introduction and Kato, 2006). This group was then sister to a Hemiepiphytes grow both epiphytic and terres- clade of Arthropteris clade consisting of climb- trial during their life history, and this life form is ing Arthropteris beckleri (Hook.) Mett., litho- among remarkable plant lives, e.g., terrestrial, phytic Tectaria phaeocaulis (Rosenst.) C. Chr. epiphytic, lithophytic, and aquatic. Hemiepi- and Quercifilix zeylanica (Houtt.) Copel. The phytes are classified into two, based on ontoge- clade of these ferns formed a monophyletic clade netic sequences of their life forms; one is prima- together with secondary hemiepiphytic Nephro- ry hemiepiphytes, which grow as epiphytes at the lepis acuminata (Houtt.) Kuhn, N. cordifolia (L.) early stage of the life history and later become C. Presl and climbing Lomariopsis spectabilis terrestrial by rooting into the soil (e.g., Ficus). (Kunze) Mett. Then, this clade was sister to some The other is secondary hemiepiphytes, which are Dryopteridaceae. These phylogenetic relation- terrestrial at the early stage of the life history and ships infer that secondary hemiepiphyte of Ole- later become epiphytic by maturity (Putz and andra and Nephrolepis was of independent ori- Holbrook, 1986). In ferns, some species of Ole- gin. Based on a character evolution of life forms andra (Oleandraceae), Nephrolepis (Lomariopsi- using the phylogenetic tree, a hypothesis was daceae), Colysis, Pyrrosia, Microsorum (Polypo- proposed that obligate epiphytic Davalliaceae diaceae; Tsutsumi and Kato, 2006), and Tri- and Polypodiaceae evolved from climbers or sec- chomanes (Hymenophyllaceae, treated as hemi- ondary hemiepiphytes. It inferred that secondary epiphytic climber in Dubuisson et al., 2003) are hemiepiphyte is an intermediate life form be- secondary hemiepiphytes. tween terrestrial plant and obligate epiphyte in A molecular phylogenetic tree deduced from the group examined (Tsutsumi and Kato, 2006). rbcL and accD sequences showed that Oleandra In general, vascular plants have leaves on the (O. pistillaris (Sw.) C. Chr. and O. wallichii stems in a consistent pattern over space and time, (Hook.) C. Presl) was sister to a clade compris- forming the regular architecture of the plant to 22 Chie Tsutsumi and Masahiro Kato achieve high productivity (Steeves and Sussex, rhizome branches (Fig. 1A–C). The long, creep- 1989). In contrast, secondary hemiepiphytic Ole- ing rhizome was dorsiventral, branched on the andra pistillaris shows anomalous rhizome mor- lateral sides, and produced roots on the ventral phology; the lengths of internodes are various side and a few leaves on the dorsal side. The and they sometimes reach as much as 2 m, result- lengths of the internodes were various ranging ing in an irregular phyllotaxy. To reveal the un- from ca. 1 cm to 150(Ϫ240) cm. The erect rhi- usual architecture of the secondary hemiepiphyt- zome elongated to some extent without leaves ic Oleandra pistillaris and another secondary after branching and produced units of pseudo- hemiepiphytic Nephrolepis cordifolia, we exam- verticillate leaves at nearly constant intervals. ined their shoot apices using scanning electron The erect rhizome was rarely branched and had microscopy. few roots. In a greenhouse, when the rhizome apex was damaged, another rhizome apex in the same individual happened to change into the Materials and Methods other rhizome type. Samples of Oleandra pistillaris were collected The number of leaf primordia per rhizome from Gunung (ϭMt.) Salak, Java, Indonesia apex in the creeping rhizomes examined was var- (vouchers; IN28, IN39, IN96, IN102) and Gu- ious; apparently no primordium (Nϭ5), one (Nϭ nung Arab, Sabah, Malaysia (ML116). Rhizomes 2), and three primordia (Nϭ1) (Fig. 1F–I). In the were cut at 5 mm apart from the apex, and scales erect rhizomes, no leaf primordium was some- were carefully removed. For scanning electron times observed immediately after branching from microscopy (SEM), the molds of fresh materials the creeping rhizome (Nϭ3). In more or less were created by a dental impression material elongated rhizomes, several leaf primordia were (Provil Novo, Heraeus Kulzer, Hanau, Germany). produced on the apex without recognizable phyl- Based on the molds, positive replicas were creat- lotaxy (Nϭ8) (Fig. 1D–E). ed using epoxy resin (Williams et al., 1987). In In the secondary hemiepiphytic Nephrolepis, case of fixed materials by FAA (formalin : acetic two distinct shoots were also reported; long, acid : 50% ethyl alcohol, 5 : 5 : 90, v/v/v), sam- creeping stolons with roots and buds, and short ples were dehydrated in an ethyl alcohol and erect shoots with fascicled leaves, roots and isoamyl acetate, and then dried in a critical point stolons (Holttum, 1955). In N. cordifolia, the dryer (HCP-2, Hitachi, Tokyo, Japan). The repli- short shoot generated fascicled leaves and cas or the dried materials were coated with plat- stolons. In contrast, the stolon had no leaf, and inum-palladium using a sputter coater (Ion Sput- regularly generated resting buds alternately on ter E-1030, Hitachi, Tokyo). Observations were the lateral sides, which may grow into a short made using a JSM-820S SEM (Jeol, Tokyo) at 5– shoot or a stolon. By gross morphological obser- 15 kV. For the observation of Nephrolepis cordi- vations, however, it could not be determined folia, a plant cultivated in the Botanical Garden, which shoot type is produced from a resting bud. Graduate School of Science, the University of The growth of the dormant buds irregularly Tokyo, was used. Vouchers are deposited in the occurred, and thus, the length of the bud-derived Herbarium of National Museum of Nature and stolon between short shoots varied from 2.5 cm Science (TNS). to 173 cm. Results Discussion The rhizome of the secondary hemiepiphytic In the secondary hemiepiphytic Oleandra pis- Oleandra pistillaris was dimorphic, comprising a tillaris, the erect rhizomes always generated long, creeping rhizome and erect, relatively short pseudo-whorled leaves in the later stage after Rhizome Morphology of Oleandra 23 Fig. 1. Rhizomes of Oleandra pistillaris. A, Diagram showing rhizome dimorphism. Erect rhizome (red) with apparently whorled leaves and creeping rhizome (blue) with (a) few leaves. B, C, Plants in the field. Red arrows indicate erect rhizomes and blue arrow indicates creeping rhizome. D–I, SEM images of rhizome apices. White circles enclose leaf primordia. SAMs indicate shoot apical meristems. D, Erect rhizome with apparently whorled leaf primordia. E, Erect rhizome without leaf primordium immediately after branching. F, G, Creeping rhizomes without leaf primordium. H, Creeping rhizome with one leaf primordium. I, Creeping rhizome with three leaf primordia. Scalesϭ100 mm. 24 Chie Tsutsumi and Masahiro Kato branching from the creeping rhizome, while the Nephrolepis with rhizomes (stolons) climbing creeping rhizomes produced a few leaves, if any, trees, the long creeping rhizome (stolon) and the at indeterminate sites. It is in contrast to the rhi- erect rhizome producing leaves seem correspond zomes of Davalliaceae and related ferns with a to the long leafless shoots and the leafy short regular phyllotaxy (Croxdale, 1976; Hirsch and shoots of those lianas, respectively. Further stud- Kaplan, 1974; Wardlow, 1943). Another sec- ies are necessary to clarify the functions and eco- ondary hemiepiphytic Nephrolepis had also di- logical adaptations of the dimorphic rhizomes of morphic rhizomes with leafy, short, erect shoots the secondary hemiepiphytes. on the long stolon. The long stolon lost leaves in N. cordifolia. McAlpin and White (1974) report- Acknowledgments ed that the stolon of N. multiflora does not pro- duce leaf primordia until a new plant is organized We thank D. Darnaedi, G. G. Hambali, R. after a prolonged period of growth. The rhizome Imaichi, H. Okada and T. Ng. Praptosuwiryo for habit is distinct from the monopodial rhizome of helping us collect materials in Indonesia. This climbers and obligate epiphytes, rhizome elonga- study was supported by a Grant-in-Aid for Scien- tion and leaf formation are sylleptic. Considering tific Research from the Japan Society for the Pro- that the two secondary hemiepiphytes evolved motion of Science. independently (Tsutsumi and Kato, 2006), the dimorphic rhizomes were in association with sec- References ondary hemiepiphyte and not with phylogeny. The assumption of the association will be made Caesar, J. C. and MacDonald, A. D. 1984. Shoot develop-
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