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Anatomy and Morphology |
Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Departamento de Biologia, Universidade de São Paulo, Avenida Bandeirantes 3900, Ribeirão Preto 14040-901, São Paulo, Brazil
Received for publication March 11, 2004. Accepted for publication January 25, 2005.
ABSTRACT
Siphocampylus is a neotropical genus that comprises 221 species distributed from Costa Rica to Argentina and in the Greater Antilles. Twenty-eight species have been reported from Brazil, mainly occupying mountainous terrain. The floral venation patterns and the origin of the hypanthium in eight Brazilian species, including three varieties, are described. Eleven ovarian vascular bundles depart from the siphonostele or receptacular stele: five of these bundles result from sepalar and staminal adnation and are alternate to five petalar bundles; the remaining bundle is central carpellary. The staminal bundles diverge from the sepalar bundles at the sinus, while the carpellary bundles form a cross, resulting in four ventral bundles; two of these feed the ovules; the other two feed the style. Apparently, the dorsal carpellary bundles diverge at the same site and then ramify profusely. The venation pattern observed is unprecedented in Siphocampylus and is quite different from other reports on genera of Campanulaceae. Further, these findings suggest that the origin of the hypanthium is appendicular, increasing knowledge of venation in this group, thus providing data for phylogenetic considerations.
Key Words: appendicular hypanthium • Campanulaceae • flower venation patterns • inferior ovary • Siphocampylus
Siphocampylus Pohl is a neotropical genus containing 221 recognized species, distributed from Costa Rica to Argentina and in the Greater Antilles, occupying mainly mountainous terrain (1000 to 3000 m) (Lammers, 1998
). The genus exhibits various modified features, such as connate petals with resupinate flowers, a one- or two-lipped corolla, connate anthers, and a half inferior ovary (Wimmer, 1953
). These characteristics identify the genus as an important group for investigations of a morpho-anatomical nature, the results of which may help us to understand such highly modified characters and their implications in phylogenetic and evolutionary approaches. Further, very little is known about the morphology of the genus, which has led to incorrect diagnoses and has hindered comprehension of species that present complex floral structures and different degrees of fusion and adnation of their whorls and vascular bundles.
Floral vascularization has always constituted a relevant topic of investigation in taxonomic and phylogenetic research. It is an important tool for understanding any changes in external morphological patterns and the sequence of these changes, particularly because it is generally assumed that the characters associated with floral vascularization are evolutionarily more conserved than others (Puri, 1951
). Floral venation is also useful in studies of homologies and in determining the origin of floral structures (Gustafsson, 1995
).
The origin of the inferior ovary is one of the more controversial topics among various issues concerning plant morphology issues (Douglas, 1944
; Puri, 1951
). Two different, conflicting theories have been established: according to the receptacular theory, the ovary reached its current inferior position owing to the sinking of the carpels into the tip of the floral receptacle; the appendicular theory, however, postulates that the inferior ovary is the result of the concrescence of the bases of the outer floral whorls in an extreme degree of adnation to the carpel wall. Kaplan (1967)
analyzed the origin of the appendicular hypanthium in Downingia bacigalupii Weiler (Campanulaceae) and commented on the usefulness of anatomical studies in analyzing this structure, demonstrating that differences in floral vascularization reflect differences in ontogenetic development among flowers with receptacular and appendicular hypanthia. This issue, together with various data concerning the receptacular nature of the inferior ovary in species of Rosaceae (Jackson, 1934
; Posluszny et al., 1993
), Salantaceae (Smith and Smith, 1942
), and Calycanthaceae (Smith, 1926
) provide evidence of the independent occurrence of two types of hypanthium, in specific plant groups, that may characterize the convergence of these events.
The purpose of this analysis of the floral venation patterns of eight species and three varieties of Brazilian Siphocampylus is to (1) increase our knowledge of venation morpho-anatomy, (2) disclose the nature of the hypanthium, (3) determine the relationships between the outer and inner floral whorls and (4) provide data for phylogenetic considerations.
MATERIALS AND METHODS
Taxa examined
Siphocampylus convolvulaceus (Cham.) G. Don, S. duploserratus Pohl var. duploserratus, S. lauroanus Handro & M. Kuhlm., S. longipedunculatus Pohl, S. macropodus (Thunb.) G. Don, S. nitidus Pohl, S. sulfureus E. Wimm. var. sulfureus and var. glaber (Zahlbr.) E. Wimm. and S. westinianus (Thunb.) Pohl. All specimens were collected from natural populations in various locations throughout Brazil, including areas of differing vegetal complexity such as the Atlantic Forest, Boulder Fields, and Cerrado savannah (Appendix, see Supplemental Data with online version of this article). The samples were collected following the usual recommendations for field taxonomy, and the respective vouchers have been included in the Herbarium of the Department of Biology of the University of São Paulo (SPFR). Flowers were fixed in formalin-acetic-alcohol (FAA50) (Sass, 1958
).
Bleaching procedure
Two, complete, mature flowers from each sampled specimen (Appendix) were sectioned longitudinally, dehydrated in an ethanol series (50% for 3 d, 70% for 1 d, and 80% for 10 d), and were bleached for between 1 to 5 h. After thorough bleaching, they were washed five times in distilled water, placed in 70% ethanol and stained with 1% safranin in 50% ethanol for from 10 min to 12 h (depending on the nature of the material), then dehydrated in a 50 to 80% ethanol series and stored in 80% glycerin. This procedure is based on Fuchs (1963 apud Kraus and Arduin, 1997
) with some modifications. The floral venation patterns were examined using a Zeiss (Germany) STEMI 2000-C stereomicroscope coupled to a camera lucida for drawings.
Histology
For vascular anatomical studies, two mature flowers from each specimen analyzed were used (Appendix). Only the hypanthia were prepared for cross sections. Dehydration was performed in an ethanol/xylene series, and the structures were embedded in paraffin according to Johansen (1940)
. The material was transversely serially sectioned at 11 µm thickness, and the sections were stained with 1% toluidine blue. Slides were prepared using Canada balsam and examined using a Zeiss AXIOLAB drb KT microscope, with a camera lucida for drawings. Photomicrographs were obtained with a Zeiss AXIOSCOP 2 MOT microscope equipped with a Zeiss 80DX camera.
RESULTS AND DISCUSSION
A brief comment on floral morphology
Several floral features are useful for distinguishing among the species of Siphocampylus investigated: shape and color of the corolla, shape of the hypanthium, and shape and position of the ovary, especially when associated with foliar data. Three species have verticillate leaves: S. duploserratus var. duploserratus, S. sulfureus var. sulfureus and var. glaber, and S. westinianus. Siphocampylus sulfureus has the least attractive corolla, which is sulphur colored with one of the lobes separate from the base; the varieties can be recognized by the scabrous floral indumentum, trichomes (papilla), and obconical hypanthium in S. sulfureus var. sulfureus (Figs. 2 and 3). Siphocampylus westinianus (Figs. 1 and 4) differs from S. duploserratus (Fig. 5) by its deep red, tubelike corolla, and yellow basal lobes, which become green toward their apices. The other species have alternate leaves (Fig. 6): S. convolvulaceus (Fig. 7) is a vine, S. longipedunculatus is distinguished by its lanceolate leaves, and S. lauroanus (Fig. 8) is very different owing to its linear and narrow leaves, ventricose corolla and geographical distribution that seems to be endemic to the Atlantic rain forest ("Serra do Mar"). Siphocampylus nitidus (Fig. 9) and S. macropodus (Fig. 10) can be distinguished by their bright foliage and corolla features.
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) set apart radially can be seen; 10 of the bundles are positioned around the central bundle (Figs. 16, 17, 25, and 26). Five of the peripheral bundles result from sepalar and staminal adnation, and are alternate to the five petalar bundles (Figs. 17 and 26). The petalar bundles lie in an inner position, which allows two rings to be distinguished in the upper third of the hypanthium. The sepalar bundle separates from the staminal bundle in the upper level of hypanthium near the bases of the calyx lobes (Figs. 18, 19, 27, and 28). The staminal bundle is recognizable, at least up to the anther tube base, and although its point of divergence from the corolla could not be ascertained, this may occur at the subjacent level of the two adnate whorls (isthmus). The sepalar bundle trifurcates (Fig. 12); the central ramification follows a straight course and branches profusely; the two lateral ramifications diverge at a 15–25° angle and branch almost perpendicularly to their axes. The adjacent, lateral, sepalar ramifications anastomose. A similar anastomosis can be seen between the lateral and central ramifications of the same lobe; the sepals exhibit a profuse vascular reticulum with anterior endings from their margin (Fig. 12). The perianth ring, reported by several researchers for members of the Campanulaceae, seems to derive from the anastomosis of the lateral sepalar ramifications of adjacent lobes. Morphologically, these anastomoses, seen as a protuberance from the lobe calyx base, together appear to have an annular-pentagonal shape. Each of the five petalar bundles (Figs. 12, 13, 16–21, 25–29) remains recognizable throughout the hypanthium, and branch profusely after the separation of the corolla from the inner whorls at the upper level of the hypanthium. Secondary veins of adjacent petals anastomose in a way that suggests the marginal petalar bundles may have been suppressed. The vascular ramifications terminate before the petalar margin and have the same vascular pattern as the calyx lobes. A cross divergence can be observed where the ventral carpellary bundles depart from the central ovarian bundle, and results in two, distinctive ventral bundles for each carpel (Figs. 16–18 and 25): two of these bundles, one from each carpel, branch and feed the axial placentas (Figs. 18 and 27). The carpellary bundles do not take a descending course to feed the ovules, which is typical of the vascular receptacular system as reported by Puri (1951)
. Unfortunately, the dorsal carpellary bundles were not well visualized, but they seem to diverge from the central ovarian bundle at the same ventral carpellary position, and then branch profusely (Figs. 27–29). These ramifications seem to correspond to a dense vascularization that crosses the ovarian walls, the ovarian nectary, and the hypanthium, as observed in transverse sections.
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, 1968
) for Downingia bacigalupii. However, the species of Siphocampylus that were analyzed have a very different vascular hypanthium pattern: the stele of Siphocampylus is divided in to 11 ovarian bundles as opposed to the penta-dissected Downingia bacigalupii stele; the petalar bundle of Siphocampylus diverges directly from the receptacular stele and not from the perianth ring as observed by Kaplan (1967
, 1968
). Apparently, the perianth ring in Siphocampylus corresponds to the anastomoses of the lateral sepalar bundles, and not to the horizontal ramifications of the ovarian bundle, as reported for Downinigia bacigalupii. This may be due to the far larger flowers found in Siphocampylus vs. the tiny flowers in Downingia, and supports Kaplan's theory (Kaplan, 1968
) that the reduced corollas in Downingia are derived by a simple process of neoteny. However, we believe it is premature to establish such a relationship before studies of floral ontogeny in Siphocampylus have been performed.
There are few data available on the perianth or floral development in the Lobelioideae. We note Payer's (1857 apud Kaplan, 1968
) early organogenetic analysis, a brief description of petalar venation by Chrtek (1962 apud Kaplan, 1968
), and Kaplan's (1967
, 1968
) studies on floral organogenesis, and structure and development of the perianth in Downingia bacigalupii. Kaplan (1968)
observed only a single vascular trace to each of the five corolla lobes in an adaxial-alternate position; after divergence of the perianth ring, the vascular trace is divided into three, resulting in a median vein that follows a straight course towards the apex, and two lateral veins that branch profusely and anastomose with the median vein giving rise to a complex reticulate arrangement. In the tubular corolla portion, the median veins do not branch and the lateral veins exhibit third order ramifications. However, Siphocampylus species do not show marked lateral veins, and a dense reticulum is formed from the corolla tube base similar to Gustafsson's (1995)
description of various other Lobelioideae species. Although the main floral venation patterns seen in S. duploserratus var. infundibularis, S. fluminensis, S. lycioides, and S. verticillatus were only analyzed macroscopically, they are similar to those observed in other species.
This discussion portrays the importance of this kind of investigation, while emphasizing the need for including more groups of Campanulaceae to verify the diagnostic potential of the appendicular condition and whether or not this character should be considered a synapomorphy for Siphocampylus.
This study also suggests that additional investigations on other related groups of sympetalous plants may disclose the existence of different degrees of the appendicular condition of the inferior ovary. New data would be useful to clarify organophyletic and phylogenetic questions concerning the Asterales-Campanulales complex.
FOOTNOTES
1 The authors thank Dr. Wagner Ferreira dos Santos, Antônio J. Colusso (Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto USP), Dr. Terezila Machado Coimbra (Departamento de Fisiologia, Faculdade de Medicina de Ribeirão Preto USP), and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo [State Research Development Foundation]). 
2 Rua Antônia Carrara Orlandini, 1182, CEP 14092 070, Ribeirão Preto, São Paulo, Brazil
3 Rua Breno Vieira de Souza, 457, CEP 14090 620, Ribeirão Preto, São Paulo, Brazil
4 Avenida Bandeirantes, 3900, FFCLRP/USP/BIOLOGIA, CEP 14040 901, Ribeirão Preto, São Paulo, Brazil
5 Corresponding author (e-mail: sapgodoy{at}ffclrp.usp.br
)
LITERATURE CITED
Douglas G. E. 1944 The inferior ovary. Botanical Review 10: 125-186
Gustafsson M. H. G. 1995 Petal venation in Asterales and related orders. Botanical Journal of the Linnean Society 118: 1-18[CrossRef]
Jackson G. 1934 The morphology of flowers of Rosa and certain closely related genera. American Journal of Botany 48: 967-974
Johansen D. A. 1940 Plant microtechnique. McGraw-Hill Book Company, New York, New York, USA
Kaplan D. R. 1967 Floral morphology, organogenesis and interpretation of the inferior ovary in Downingia bacigalupii. American Journal of Botany 54: 1274-1290[CrossRef][ISI]
Kaplan D. R. 1968 Structure and development of the perianth in Downingia bacigalupii. American Journal of Botany 55: 406-420[CrossRef][ISI]
Kraus J. E. M. Arduin 1997 Manual básico de métodos em morfologia vegetal. Editora Universidade Rural, Seropédica, Rio de Janeiro, Brasil
Lammers T. G. 1998 Review of the neotropical endemics Burmeistera, Centropogon, and Siphocampylus (Campanulaceae: Lobelioideae), with description of 18 new species and a new section. Brittonia 50: 233-262[CrossRef][ISI]
Posluszny U. J. M. Gerrath P. G. Kevan R. Kemp 1993 Floral development of Rosa setigera. Canadian Journal of Botany 71: 74-86[ISI]
Puri V. 1951 The role of floral anatomy in the solution of morphological problems. The Botanical Review 18: 471-553
Sass J. E. 1958 Botanical microtechnique, 3rd ed. Iowa State College Press, Ames, Iowa, USA
Smith F. H. E. C. Smith 1942 Anatomy of the inferior ovary of Darbya. American Journal of Botany 29: 464-471[CrossRef][ISI]
Smith G. H. 1926 Vascular anatomy of Ranalian flowers. I. Ranunculaceae. Botanical Gazette 87: 507-530
Wimmer E. F. 1953 Campanulaceae-Lobelioideae, II. Teil. In R. Mansfeld [ed.], Das Pflanzenreich Teil 4, 276 b, i–viii, 261–814. Akademie-Verlag, Berlin, Germany
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