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1 Department of Botany, MRC-166, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560 USA; and 2 The Ohio State University Herbarium, Museum of Biological Diversity, 1315 Kinnear Road, Columbus, Ohio 43212 USA
Received for publication January 1, 1999. Accepted for publication June 8, 1999.
ABSTRACT
The floral organogenesis and subsequent ontogenies of the Hawaiian endemic species Schiedea pubescens from Maui, Moloka'i, and Lana'i, and the Wai'anae Mountains, O'ahu, populations previously considered to be varietally distinct, were examined using the scanning electron microscope (SEM). The O'ahu population consistently produced only five fertile stamens, those of the inner whorl. The five stamens of the alternisepalous or outer whorl abort prior to microsporogenesis and fail to elongate. Additional vegetative differences between the two taxa, combined with the floral morphology characters, merit the description of the O'ahu population as a new species, S. pentandra, described herein.
Key Words: Caryophyllaceae • endangered species • floral development • Hawaiian Islands • scanning electron microscopy • Schiedea
The genus Schiedea (Alsinoideae: Caryophyllaceae) comprises 29 species endemic to the Hawaiian islands and along with the related genus, Alsinidendron, the lineage constitutes the fifth largest Hawaiian angiosperm radiation (Wagner, Herbst, and Sohmer, 1990
; Wagner, Weller, and Sakai, 1995
; Weller, Wagner, and Sakai, 1995
, Sakai et al., 1997
). The genus is uniformly apetalous (with a few occasional aberrant exceptions), an unusual state for the Alsinoideae (Bittrich, 1993
). After the initial colonization event to the Hawaiian Islands, the genus underwent extensive radiation, exhibiting different growth habits and breeding systems to exploit different habitats (Weller et al., 1990
; Wagner, Weller, and Sakai, 1995
; Weller, Wagner, and Sakai, 1995
; Sakai et al., 1997
). One of the species, Schiedea pubescens Hillebr., found on the islands of O'ahu, Moloka'i, Lana'i, and Maui, is of particular interest due to the variability among populations in the number of fertile stamens produced. In the most recent taxonomic treatment of the genus two varieties were recognized: Schiedea pubescens var. pubescens from Moloka'i, Lana'i, and Maui, and S. pubescens var. purpurascens Sherff (a never validly published name) restricted to the Wai'anae Mountains of O'ahu. Ontogenetic studies of Maui and O'ahu S. pubescens undertaken as a part of a larger study of the entire genus (as well as the closely related genus Alsinidendron) indicate that differences in floral morphology coupled with vegetative morphological differences are consistent and great enough to merit the elevation of the latter taxon to species level, described herein as Schiedea pentandra.
Schiedea pubescens and S. pentandra are members of a clade of ten species with large one-nerved leaves, open inflorescences, strongly reflexed, slightly asymmetrical sepals with attenuate apices, and ciliate margins that occur in mesic to wet forest habitats on six of the eight main Hawaiian Islands. The Maui, Moloka'i, and Lana'i populations of S. pubescens differ from S. pentandra on O'ahu in their larger and broader leaves (3–7.5 cm wide) that are weakly falcate, clambering or sprawling vining habit, subglabrous inflorescence, and ten fertile stamens, rather than five, whereas S. pentandra has narrowly, strongly falcate leaves 0.8–2.5 cm wide, reclining vining habit with stems apparently readily rooting at the nodes, densely pubescent inflorescence, and five fertile stamens. The two whorls of stamens in all populations of S. pubescens are strongly differentiated in length, the anthers of the shorter, outer whorl apparently having lower pollen production, a common occurrence in the Caryophyllaceae (Thomson, 1942
). In S. pentandra, the alternisepalous or outer whorl of stamens is never fertile, and the stamens are present at anthesis only as small misshapen structures that are barely noticeable.
Taxonomic background
Schiedea pentandra, long known as S. pubescens var. purpurascens, is unique in the Hawaiian Alsinoideae in producing only five fertile stamens, by partial suppression of one whorl during development. The name Schiedea pubescens Hillebr. var. purpurascens Sherff (1943, 1945)
was never validly published because when Sherff provided a name for the unnamed S. pubescens var. 
of Hillebrand (Fl. Hawaiian Isl. 32. 1888) he did not provide a Latin diagnosis or description (ICBN Art. 36.1).
MATERIALS AND METHODS
Plants were grown in the Biological Sciences greenhouses at the University of California at Irvine from wild-collected seed or cuttings of S. pubescens and S. pentandra. Vouchers of the wild-collected plants were made for S. pubescens from ‘Iao Valley, West Maui [Perlman & Marr 1977 (BISH, PTBG, US)], and for S. pentandra from near summit of Kanehoa, Wai'anae Mountains, O'ahu (Weller & Sakai 796, holotype, US). Additional voucher specimens from cultivated plants were deposited at Bishop Museum (BISH, Honolulu, Hawaii), and at the United States National Herbarium at the Smithsonian Institution (US, Washington, DC). Inflorescences were killed and fixed in formalin/acetic acid/50% ethyl alcohol (FAA, 5:5:90) in the greenhouse, and were later transferred to 70% ethyl alcohol for storage. The preserved material was dissected, and pertinent material was dehydrated in an ethanol/acetone series and processed in a Samdri PVT (trade name) critical-point dryer. Specimens were mounted, sputter coated with gold-palladium, and studied with a Cambridge Stereoscan 250 Mk2 (at 5 or 10 kV) or a Hitachi 570 (at 10 kV) scanning electron microscope (SEM), and representative micrographs were taken. For the taxonomic description of S. pentandra and the study of its geographical range 41 collections were examined; these will be cited in a forthcoming monograph of the Hawaiian Alsinoideae (Wagner, Weller, and Sakai, unpublished data).
RESULTS
Ontogeny
Schiedea pubescens
The floral primordium is initiated as a low dome with a width of ~75 µm (not shown), and the five sepals are the first organs to be produced (Fig. 1) in a 2/5 phyllotaxy. After the initiation of the sepals, the remaining floral meristem is distinctly pentamerous and will remain so as the next floral organs, the stamen primordia, are initiated (Fig. 2). No petal primordia were observed, nor was there an unoccupied space on the floral primordium where they might have been expected to be inserted. The antisepalous stamen primordia appear to arise next, delimiting the remaining floral primordium. Even at this early stage, the antisepalous stamen primordia can be reliably assigned to the inner whorl, as they are noticeably higher up the receptacle and closer to the raised portion of the floral primordium that will form the gynoecium. The alternisepalous stamen primordia (equivalent to the antipetalous stamens of taxa that do possess petals) become distinct very shortly thereafter and are located on radii farther out than the antisepalous stamen primordia. This difference in location is maintained throughout development and can be noted at anthesis (Fig. 7). The distal portion of the floral primordium continues to enlarge to form the three carpels of the fused gynoecium (Fig. 3). At about the same stage, the antisepalous stamen primordia have already broadened terminally as the thecae of the anther are delimited. The alternisepalous stamen primordia are much delayed in development and are barely capitate in shape. Also at this stage, the first swellings at the base of the filament of the antisepalous stamen primordia herald the initiation of the five nectaries. The apex of each carpel elongates to form a style (Figs. 4, 5), while the base of the gynoecium enlarges to produce the ovary (Fig. 5). The alternisepalous stamen primordia continue to develop (Fig. 4), although they continue to lag behind the antisepalous stamens in relative stage of development and size. The nectary primordia continue to bulge out, forming a slightly smiling-mouth shaped structure. The "lips" of the nectary elongate to form the hollow shaft, while the subtending tissue enlarges and broadens to form the nectariferous tissue "bulb" at the base of each nectary (Figs. 5–7). At anthesis, the sepals are reflexed (Fig. 7); the nectaries and stamens are exserted (Figs. 7, 8). The inner and outer whorl of stamens are easily distinguished; there is still a size differential (most easily noticed in the filament length) and the different levels of insertion are marked, due to the enlarged base of the nectaries that serve to elevate the antisepalous stamens. An unusual feature occurring only in S. pubescens and S. pentandra is that the stamens are erect in anthesis (vs. spreading in other species).
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DISCUSSION
Many aspects of the floral ontogeny of these two taxa are extremely similar, if not identical a phenomenon that is not surprising and has been documented elsewhere between two closely related taxa e.g., two species in the Asteraceae genus Trixis (Harris, 1995
). As far as the floral ontogeny is concerned, the main characteristics separating the Schiedea taxa are the events related to the alternisepalous stamens.
Numerous taxa in the Caryophyllaceae have lost one or more floral organs during their evolution (Thomson, 1942
; Bittrich, 1993
; Hill, 1996
). Indeed, apetalous flowers are considered plesiomorphic in the order Caryophyllales, rendering the petals that do appear as secondarily derived and of a staminodial origin (Cronquist, 1981
). Several investigators have proposed that these secondarily derived petals arise from the conversion or dedoublement of the primordia of the outer whorl of stamens (Eichler, 1875
; Pax, 1893, 1927
) and indeed the placement of the petal primordia on the same radius as the outer stamen whorl (Payer, 1857; E. Harris, personal observation, OSU) lends credence to this theory.
Related to the nature of the petals is the possible occurrence of obdiplostemony in the Caryophyllaceae. Obdiplostemony has been defined by Harris and Harris (1994)
as "having two whorls of stamens, the outer whorl opposite the petals and the inner whorl opposite the sepals." This issue has been raised and investigated by several authors (Eckert, 1966
; Rohweder, 1967, 1970
; Hofmann, 1994
), all of whom concluded that "true obdiplostemony" does not exist in the family and putative examples are "faint" (Eckert, 1966
) or "of no primary importance" (Rohweder, 1970
).
The differences described between these two taxa in their floral development show that they are closely related, but that the O'ahu plants are more specialized as a result of the abortion of one of the whorls of stamens. This difference, found only in this taxon within the genus, is the basis for recognition of it at the specific level, as S. pentandra, separate from the Moloka'i, Lana'i, and Maui populations of S. pubescens. Both of these species are part of a clade of ten species in this endemic Hawaiian radiation referred to as the " Schiedea nuttallii clade" in recent phylogenetic studies (Wagner, Weller, and Sakai, 1995
; Soltis et al., 1997
; Sakai et al., 1997
). Schiedea pentandra appears to be the sister species to S. pubescens. These two species, along with S. helleri Sherff and S. diffusa A. Gray, have the strongest development of the vining habit in the genus; S. pubescens and S. pentandra are the only species that have erect stamens during anthesis. Schiedea pubescens is the only species in the "Schiedea nuttallii" clade that also has dimorphic anthers with the antisepalous ones larger. All species of this clade have dimorphic staminal filaments, but the length difference is most extreme in S. pubescens and taken a further step to abortive stamens in S. pentandra. Dimorphic staminal filaments, however, are not unique to the "Schiedea nuttallii" clade. Several other species with at least one species from each of the other three clades have dimorphic stamens, although the degree of difference in length of the staminal filaments is much less than that in the "nuttallii" clade.
Taxonomy
Schiedea pentandra W. L. Wagner & E. Harris, sp. nov.—TYPE: Hawaiian Islands. O'ahu, Wai'anae Mountains, Huliwai-Kalua'a Ridge, near summit of Kanehoa, 2600 ft [790 m], 21 June 1985, S. G. Weller & A. Sakai 796 (US-3218732, holotype). See Fig. 17.
A S. pubescens foliis anguste lanceolatis praecipue subfalcatis, staminibus antisepalis fertilibus, staminibus ceteris minutis et abortivis differt.
Reclining vines, primary stems 10–60 dm long, apparently readily rooting at the nodes, purple or green with a purple tinge, glabrous below, puberulent in the inflorescence. Leaves opposite, the blades 4.5–11 cm long, (0.8–)1–2.5 cm wide, coriaceous, narrowly lanceolate, usually somewhat falcate, purple tinged, especially along the midrib, with only the midvein evident, the midvein excentric, ± purple, occasionally with a few scatterd hairs on abaxial side, margin slightly thickened and usually slightly scarious, occasionally with a few scattered hooked hairs ca. 0.1 mm long, apex attenuate to long-acuminate, base cuneate, petioles 0.2–0.9 cm long. Flowers perfect, protandrous, in dichasia on the main and upper lateral branches, these forming diffuse, pendant, panicle-like inflorescence 30–50(–150) cm long, moderately to densely puberulent in the inflorescence, the hairs purple or purple tinged, 0.05–0.15 mm long; bracts green, purple tinged, narrowly lanceolate to subulate, those of central axis 2.5–11 mm long, those of branches and flowers 1.5–3 mm long; pedicels 6–18 mm long. Sepals 2.3–3 mm long, lanceolate, purple, or green with a purple midvein, opaque, strongly reflexed in the proximal 1/4, producing a large transverse bulge, distal part strongly navicular and somewhat involute toward the apex, oriented at 10°–30° angle to the pedicel, densely puberulent, margins scarious and densely ciliate, apex long-attenuate. Nectary base 0.5–0.6 mm long, dark yellowish orange or purple tinged, the nectary shaft 2.25–2.5 mm long, at 90° angle to the axis, apex usually not divided, less developed on one side. Stamens 10, the antisepalous whorl fertile and usually erect, the alternate set minute and abortive; filaments of fertile stamens 3–3.2 mm long, usually erect in anthesis and becoming slightly twisted and recurved at the end of anthesis, those of the abortive set ~0.5 mm long, rarely one developing; anthers attached near the middle, 0.5 mm long, the abortive set 0.3 mm long, empty, yellow. Styles 3(4). Capsules 2.5–3 mm long, ovoid. Seeds 0.9–1.1 mm long, orbicular-reniform, compressed, the surface transversely rugose.
Distribution
Scattered in rapidly degrading diverse mesic forest, 600–900 m, Maunakapu to Mount Ka'ala, Wai'anae Mountains, O'ahu. This species is rather rare and could easily become endangered if its habitat should become more degraded. Apparently only a few hundred individuals distributed in ~15 populations are still known to be extant (J. Lau, The Nature Conservancy, personal communication). The current threats to populations include alien wild goats and plants such as Lantana camara L., Schinus terebinthifolius Raddi, Clidemia hirta (L.) D. Don, Myrica faya Aiton, and Grevillea. Probably the greatest single threat is fire, which has occurred relatively frequently in the Wai'anae Mountains.
FOOTNOTES
1 The authors thank the Scholarly Studies Program and the Office of the Director, National Museum of Natural History, for support of this research, and the Smithsonian Institution Botanical Walcott Fund for support for illustration work; Steve Perlman, Ann Sakai, and Steve Weller for field collections for propagation and study material; Mike Sisson and Robynn Shannon for assistance in the lab; Joel Lau for comments on population status information; Alice Tangerini for her excellent illustration from living material of Schiedea pentandra; Steve Weller for useful comments on a presubmittal manuscript; and reviewers Jeffrey Hill and John McNeill for useful comments. 
4 Author for correspondence (wagner.warren{at}nmnh.si.edu)
.
5 E-mail: harris.690{at}osu.edu
LITERATURE CITED
Bittrich, V. 1993 Caryophyllaceae. In K. Kubitzki, J.G. Rohwer, and V. Bittrich [eds.], The families and genera of vascular plants. 207–229. Springer-Verlag, Berlin, Germany.
Cronquist, A. 1981 An integrated system of classification of flowering plants. Columbia University Press, New York, New York, USA.
Eckert, G. 1966 Entwicklungsgeschichtliche und blütenanatomische Untersuchungen zum Problem der Obdiplostemonie. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 85: 523–604.
Eichler, A. W. 1875 Blüthendiagramme, vol. I. Leipzig, Germany.
Harris, E. M. 1995 Inflorescence and floral ontogeny in Asteraceae: a synthesis of historical and current concepts. Botanical Review 61: 93–280.
Harris, J. G., and M. W. Harris. 1994 Plant identification terminology—an illustrated glossary. Spring Lake Publishing, Spring Lake, Utah, USA.
Hill, J. P. 1996 Heterochrony in the anther. In W. G. D'Arcy and R. Keating [eds.], The anther, form, function and phylogeny. 118–135. Cambridge University Press, Cambridge, UK.
Hofmann, U. 1994 Flower morphology and ontogeny. In H.-D. Behnke and T. J. Mabry [eds.], Caryophyllales, evolution and systematics. 123–166. Springer-Verlag, Berlin, Germany.
Payer, J. B. 1857 Traité d'organgenie comparée de la fleur, 336–340. Paris; Reprint, 1966, J. Cramer, New York, New York, USA.
Pax, F. 1893 Caryophyllaceae. In A. Engler [ed.], Die Natürlichen Pflanzenfamilien. Leipzig, Germany.
———. 1927 Zur Phylogenie der Caryophyllaceae. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 61: 223–241.
Rohweder, O. 1967 Centrospermen-Studien 3. Blütenentwicklung und Blütenbau bei Silenoideen (Caryophyllaceae). Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 86: 130–185.
———. 1970 Centrospermen-Studien 4. Morphologie und Anatomie der Blüten, Früchte un Samen bei Alsinoideen und Paronychioideen s. lato. (Caryophyllaceae). Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 90: 201–271.
Sakai, A. K., S. G. Weller, W. L. Wagner, P. S. Soltis, and D. E. Soltis. 1997 Phylogenetic perspectives on the evolution of dioecy: adaptive radiation in the endemic Hawaiian genera Schiedea and Alsinidendron (Caryophyllaceae: Alsinoideae), In T. J. Givnish and K. J. Sytsma [eds.], Molecular evolution and adaptive radiation, 455–473. Cambridge University Press, New York, New York, USA.
Sherff, E. E. 1943 Some additions to our knowledge of the genus Schiedea Cham. & Schlecht. American Journal of Botany 30: 606–608. [CrossRef][ISI]
———. 1945 Revision of the genus Schiedea Cham. & Schlecht. Brittonia 5: 308–335. [CrossRef]
Soltis, D. E., P. S. Soltis, S. G. Weller, A. K. Sakai, and W. L. Wagner. 1996 [1997]. Molecular phylogenetic analysis of the Hawaiian endemics Schiedea and Alsinidendron (Caryophyllaceae). Systematic Botany 21: 365–379. [CrossRef][ISI]
Thomson, B. F. 1942 The floral morphology of the Caryophyllaceae. American Journal of Botany 29: 33–349.
Wagner, W. L., D. R. Herbst, and S. H. Somer. 1990 Manual of the flowering plants of Hawaii. University of Hawaii Press and Bishop Museum Press, Honolulu, Hawaii, USA.
———, S. G. Weller, and A. K. Sakai. 1995 Phylogeny and biogeography in Schiedea and Alsinidendron (Caryophyllaceae). In W. L. Wagner and V. A. Funk [eds.], Hawaiian biogeography: evolution on a hot spot archipelago. Smithsonian Institution Press, Washington, DC., USA.
Weller, S. G., A. K. Sakai, W. L. Wagner, and D. R. Herbst. 1990 Evolution of dioecy in Schiedea (Caryophyllaceae: Alsininoideae) in the Hawaiian Islands: biogeographical and ecological factors. Systematic Botany 15: 266–276. [CrossRef][ISI]
———, W. L. Wagner, and A. S. Sakai. 1995 A phylogenetic analysis of Schiedea and Alsinidendron (Caryophyllaceae: Alsinoideae): implications for the evolution of breeding systems. Systematic Botany 20: 315–337. [CrossRef][ISI]
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