Printer Friendly

A phylogenetic analysis of the subfamily Aristolochioideae (Aristolochiaceae).

Resumen

Se presenta un analisis cladistico de la subfamilia Aristolochiaceae (Aristolochiaceae), basado en caracteres morfologicos. El grupo de estudio (grupo propio) incluye 65 taxones, los cuales representan todas las tribus, subtribus, generos y taxones infragenericos descritos formalmente dentro de la subfamilia Aristolochioideae sensu Schmidt. El analisis muestra que. Aristolochia s.l. es parafiletico y que Euglypha y Holostylis no son linajes diferentes de Aristolochia. Dos de los tres subgeneros reconocidos dentro de Aristolochia (Siphisia y Pararistolochia) son monofileticos. El tercer subgenero (Aristolochia) es parafiletico. Muchos taxones a nivel de seccion, subseccion, serie y subserie son polio parafileticos. Los caracteres tradicionalmente usados en la circunscripcion de estos taxones son evaluados y nuevos caracteres son empleados. Finalmente y con base en este analisis, se presenta la clasificacion revisada de la subfamilia, la cual consta de dos tribus, dos subtribus y cinco generos.

Palabras clave: Aristolochia; Aristolochiaceae; Euglypha; Holostylis; Pararistolochia; Siphisia.

Gonzalez, F. & D.W. Stevenson: A phylogenetic analysis of the subfamily Aristolochioideae (Aristolochiaceae). Rev Acad. Colomb. Cienc. 26(98): 25-60, 2002. ISSN 0370-3908.

A cladistic analysis of the subfamily Aristolochioideae (Aristolochiaceae) based on morphological characters is presented. The analysis includes 65 taxa within the ingroup, which represent all the tribes, subtribes, genera, and infrageneric taxa formally described within the subfamily Aristolochioideae sensu Schmidt. The analysis shows lhal Aristolochia s. 1. is paraphyletic and that Euglypha and Holostylis are not different lineages from Aristolochia. Two of the three subgenera recognized within Aristolochia (Siphisia and Pararistolochia) are shown to be monophyletic. The third subgenus (Aristolochia) is paraphyletic. Most taxa at lower rank levels (sections, subsections, series, and subseries) are shown to be either polyphyletic or paraphyletic. The characters traditionally used for the recognition of these taxa are evaluated and new characters are introduced. Finally, a revised system of classification of the Aristolochioideae based on monophyletic groupings and consisting of two tribes, two subtribes, and five genera is proposed here.

Key words: Aristolochia-, Aristolochiaceae; Euglypha; Holostylis; Pararistolochia; Siphisia.

Introduction

The Aristolochiaceae consist of ca. 500 species, most of which inhabit the tropics and subtropics of both hemispheres. The sparse fossil records of the family date back to the early Tertiary and perhaps the late Cretaceous of India (Kulkarni & Patil, 1977), Europe (Kolakovski, 1957, 1964), and North America (MacGinitie, 1953,1969, 1974). Although generic circumscription within the family is currently in dispute, most authors recognize six genera in two subfamilies. Asaroideae, with an actinomorphic perianth, consists of three genera and about 130 herbaceous species: Asarum, with ca. 100 species, distributed in temperate areas of North America, Europe, and Asia; the monotypic Saruma, endemic from central China; and Thottea with ca. 30 species restricted to tropical Asia. Aristolochioideae, with a monosymmetric perianth, consists of three genera: Aristolochia, with ca. 400 species, principally tropical, but with some species found in subtropical and temperate areas of both hemispheres; and the monotypic Euglypha and Holostylis, both endemic to South America.

The most consistent synapomorphies of the Aristolochiaceae are in the seed coat. The cells of the inner layer of the outer integument have crystals, and the outer and inner layers of the inner integument are parallel to the seed axis whereas the middle layer is transversely oriented, thus forming cross fibers (Kratzer, 1918; Periasamy, 1966; Corner, 1976; Huber, 1985, 1993; Mohana Rao, 1989). In addition, the following assemblage of uniquely combined morphological characters suggests that Aristolochia, Asarum, Euglypha, Holostylis, Saruma, and Thottea form a monophyletic group: alternate, distichous leaves with reticulate, palmate venation; adaxial prophylls; oil cells; perianth essentially trimerous; androecium and gynoecium essentially hexamerous; and pollen in monosulcate or inaperturate monads.

The taxonomic position of the Aristolochiaceae is controversial. There are three competing hypotheses about their closest relatives: (1) Members of the order Magnoliales (Cronquist, 1981; Dahlgren, 1983; Leins & Erbar, 1995; Takhtajan, 1996), based mainly on the presence of P-type sieve-element plastids (Behnke, 1988, 1991), ethereal oil cells, aporphine alkaloids, and several carpels that are apocarpous and pluriovulate. Additional embryological (see Cocucci, 1983), karyological (Morawetz, 1985), and ultra-structural (Hennig et al., 1994) evidence has been presented in support of this concept. (2) The Rafflesiales (Brown, 1821; Bartling, 1830; Solereder, 1889b; Delpino, 1893; Baldacci, 1894; Hutchinson, 1969; Endress, 1990, 1994; Kubitzki, 1993), based on the similarities in floral structure, particularly the presence of a simple, fleshy, sapromyophilous perianth, with connate portions and a ring-like structure at the entrance, the extrorse anthers, the fusion of stamens and styles into a gynostemium, the ring-like, uninterrupted stigmas, and the inferior, pluriovulate ovary. (3) The so-called paleoherbs (Donoghue & Doyle, 1989; Loconte & Stevenson, 1991; Tbcker & Douglas, 1996; Nandi et al., 1998) from which two sister groups have been proposed for the Aristolochiaceae, the piperalean Lactoridaceae and the monocots. The relationship between Aristolochiaceae and Lactoridaceae, anticipated by Dahlgren & Bremer (1985), is supported by wood anatomy (Carlquist, 1993), and molecular data (Qiu et al., 1999; Soltis et al., 1997), although these families strongly differ in morphological, embryological, karyological, and palynological characters (Lammers et al., 1986; Loconte & Stevenson, 1991; Tobe et al., 1993; Tucker & Douglas, 1996). On the other hand, the sister-group relationship between Aristolochiaceae and monocots, proposed by Stevenson & Loconte (1995), among others, is supported by the presence of adaxial prophylls, trimerous flowers, monosulcate or inaperturate pollen, and sieve-element plastids of the specific type Pile. The latter relationship is supported by 18S ribosomal DNA sequences (Bharathan & Zimmer, 1995). Since Jussieu's (1789) placement of the Aristolochiaceae as the closest member to the monocots, this relationship has been repeatedly emphasized over time (Blume, 1827; Bartling, 1830; Lindley, 1853; Suessenguth, 1921; Huber, 1977, 1985; Dahlgren & Clifford, 1982; Leins & Erbar, 1985; Behnke, 1988, 1991; Erbar & Leins, 1994).

Systematics of the Aristolochiaceae. Adanson (1763) proposed the placement of Aristolochia close to Asarum, for the first time. Jussieu (1789) established the Aristolochiaceae with the genera Aristolochia, Asarum and Cytinus. Brown (1821) added the genus Thottea and questioned the inclusion of Cytinus in the family. The latter genus was transferred to the Rafflesiaceae by Lindley (1831), who at the same time, assigned Trichopus to the Aristolochiaceae, a genus that was later placed into the Dioscoreaceae by Klotzsch (1859). By the middle of the 19th century, the core of the family (i. e. Aristolochia, Asarum, Thottea, and some of their segregates) was established. Since then, three more monotypic genera, Holostylis, Saruma, and Euglypha have been added to the family.

Eight systems of classification, based primarily on floral and fruit morphology, have been proposed at the infrafamilial level: (1) Klotzsch (1859) divided the family into two groups (Table 1): the Cleistostigmata (Asarum, Thottea and some of their segregates), with free anthers, a solid style, and discoid or radiate stigmas which are closed at the middle; and the Aristolochieae (Aristolochia and some of its segregates), with anthers fused to the hollow styles and stigmas. (2) Duchartre (1864) divided the family into three groups (Fig. 1A; Table 1), the Asareae (Asarum), the Bragantieae (Thottea), and the Aristo lochieae (Aristolochia and Holostylis). This system was followed by Solereder (1889b), and Gregory (1956; Fig. IF). (3) Baldacci (1894) proposed two groups, one consisting of Thottea and the other consisting of Aristolochia, Asarum and Holostylis (Fig. 1C; Table 1). The latter group was proposed because the shape of the perianth of Holostylis seems to be intermediate between that of Asarum and Aristolochia. (4) Van Tieghem (1900) proposed a close relationship between Hocquartia (an Aristolochia segregate) and Holostylis (Fig. ID), implicitly placing into question the monophyly of Aristolochia. (5) Schmidt (1935) formally proposed the subfamilies Asaroideae for the members with actinomorphic flowers (Asarum, Saruma, and Thottea), and Aristolochioideae for the members with a monosymmetric perianth (Aristolochia, Euglypha, and Holostylis). This system (Fig. IE; Table 1) has been adopted by many authors (e.g., Hoehne, 1942; Cheng & Yang, 1988; Hwang, 1988; Ma, 1990). (6) Nakai (1936) placed Aristolochia, Thottea, and their segregates along with Euglypha and Holostylis in the Aristolochiaceae (Table 1), and raised Asarum and Saruma to the family level, the Asaraceae and the Sarumataceae. (7) Huber (1985, 1993) recognized the two subfamilies proposed by Schmidt (1935) but transferred Thottea to the Aristolochioideae (Fig. 1G; Table 1), because it shares with Aristolochia, Euglypha, and Holostylis the presence of hooked hairs, epigynous flowers, a constriction between the perianth and the ovary, a perianth shedding after anthesis, stamens frequently 6, and fruits usually dehiscent. (8) Weintraub (1995) implicitly called into question the monophyly of Aristolochia in proposing

Euglypha and Holostylis as sister groups, forming a crown clade that is merged within Aristolochia plus Pararistolochia (Fig. 1H).

Subfamily Aristolochioideae. This subfamily (equivalent to the tribe Aristolochiineae sensu Huber, 1985, 1993), as proposed by Schmidt (1935), is supported by the following synapomorphies: monosymmetric, tubular perianth differentiated into utricle, tube and limb; and six uniseriate stamens, which are fused with the styles/stigmas forming a gynostemium (Gonzalez, 1997). Within Aristolochioideae, the large and complex genus Aristolochia stands in contrast with the monotypic Euglypha and Holostylis. The latter two genera have been recognized by many authors (Masters, 1875; Solereder, 1889b; Schmidt, 1935; Hoehne, 1942; Wyatt, 1955; Ahumada, 1967; Huber, 1993), but its taxonomic placement is controversial (Fig. 1; Table 1).

The genus Aristolochia. Despite the fact that many authors treat Aristolochia in its broad sense (Duchartre, 1854a, 1864; Hoehne, 1942; Davis & Khan, 1961; Pfeifer, 1966, 1970; Hou, 1984; Nardi, 1984, 1991; Phuphathanaphong, 1987; Ma, 1989), several generic segregates have been proposed (Tables 1-3; see also Figs. 1, 11), on the basis of differences in the morphology of the perianth and the gynostemium. Most of the segregate genera correspond to infrageneric taxa proposed by authors such as Duchartre (1854a, 1864), and Schmidt (1935)(Table 3). Recently, Huber (1985, 1993) re-established some of the segregates made by Rafinesque (1836), Klotzsch (1859), and Hutchinson & Dalziel (1927) by splitting Aristolochia into six genera (Tables 1, 2) based on characters related to the leaf anatomy, gynostemium morphology, inner surface of the flower, fruit and seed morphology, and to some extent, karyology. Huber's scheme recognizes two subtribes (Table 1): the Isotremantinae, with the genera Endodeca and Isotrema and the Aristolochiinae, with the genera Aristolochia s. str., Einomeia, Euglypha, Holostylis, "Howardia", and Pararistolochia. However, the detailed observations on seed anatomy presented by Huber (1985) neither provides clear evidence for the recognition of relationships within the segregates nor unique features for them. This is obvious in his recent treatment of the Aristolochiaceae (Huber, 1993), in which the segregates are retained but are defined mostly on the basis on floral morphology. Moreover, no further hypothesis on the relationships between the six members of the Aristolochiinae is presented there (Fig. 1G).

Schmidt (1935) proposed three subgenera of Aristolochia s. 1., based on the perianth morphology and the number of gynostemium lobes: Subgenus Siphisia, with a 3-lobed perianth and 3-lobed gynostemium, which is essentially Duchartre's (1854a, 1864) Group I; subgenus Pararistolochia, with a 3-lobed perianth, and 6-12-lobed gynostemium, which is based on the genus Pararistolochia proposed by Hutchinson & Dalziel (1927); and subgenus Orthoaristolochia, with a 1-2-lobed perianth and 5-6-lobed gynostemium, which equals Group II of Duchartre (1854a, 1864).

Most of the infrageneric taxa were first described by Duchartre (1854a; Tables 3, 4). Klotzsch (1859) independently proposed a classification, which is essentially the same as that proposed by Duchartre (1854a), but raised several groups as distinct genera (Table 3). Duchartre (1864), rather than use Klotzsch's segregates, kept his previous system intact. Duchartre's system has been the most widely used system since then, having undergone no substantial changes (e.g. in Masters, 1875; Bentham & Hooker, 1880; Schmidt, 1935; Hoehne, 1942; Wyatt, 1955; Ahumada, 1967; Ma, 1989). The characters that define sections, subsections, series and subseries are based on the morphology of the perianth and the gynostemium.

Hoehne (1942) used the presence or absence of the so-called pseudostipules (Fig. 2A, E; see also Duchartre, 1854b; Gonzalez, 1990) as the primary criterion of classification (Table 4), and recommended abandoning Duchartre's scheme because it "nao representa um sistema de afinidades baseado nos orgaos em geral". However, Hoehne's secondary set of characters is also strongly based on the shape and the size of the perianth. Gonzalez (1990, 1991) suggested that the perianth has been over-emphasized in the recognition of infrageneric taxa, resulting in a single character taxonomy. Instead, he has found characters such as the presence of an abscission zone on the petiole (Fig. 3B, D) and the peduncle, the architecture of inflorescences, and the morphology of fruits and seeds (Fig. 4), which have been useful to reevaluate the systematics and to propose an alternative classification for the Neotropical species of Aristolochia.

Unfortunately, recent authors have focused on the rank at which these taxa should be recognized (see e.g. Huber, 1985, 1993; Parsons, 1996), rather than on the relationships and/or the monophyly of the groups. This paper presents a cladistic analysis of the Aristolochioideae, based on morphological characters. The analysis was conducted to evaluate the relationships between Aristolochia, Euglypha, and Holostylis-, to test the monophyly of the infrageneric taxa of Aristolochia, including the segregate genera of the latter (Tables 1-3); and to evaluate the congruence of floral characters that are traditionally used in the classification of the Aristolochioideae with other characters that appear not to have been exploited.

Materials and Methods

The classification followed here for sampling essentially corresponds to that of Schmidt (1935), at both subfamilial (Table 1) and subgeneric (Table 3) ranks, although additional species from Australia and New Guinea have been included in subgenus Pararistolochia, following Parsons (1996, who treated the group as a distinct genus). The ingroup taxa include Euglypha, Holostylis, and a large sampling within Aristolochia (Table 5), the latter treated in its broad sense. Sampling within Aristolochia includes 61 species representing all subgenera, sections and subsections, and most of the series and subseries (Table 5). Most of the segregates (Table 2) described by Dumortier (1822), Rafinesque (1828, 1836), Klotzsch (1859), Hutchinson & Dalziel (1927), and Huber (1985, 1993) were sampled, thus including a broad range of morphological diversity and geographical distribution within Aristolochia. Taxa below subgeneric level essentially follow Duchartre (1854a, 1864; Tables 3, 4), Hoehne (1942; Table 4), Ma (1989), and Gonzalez (1990, 1991). However, some lower rank taxa described by Duchartre (1854a, 1864), Hoehne (1942), and Ma (1989) were not considered because they were delimited primarily by minor differences in floral shape, size or indument which are not discrete and, therefore, are not realistically codable. In addition, the analysis includes two supraspecific taxa, subsection Pentandrae (Duchartre, 1854a, 1864) with 33 of the 37 species examined and section Dipharus (Klotzsch, 1859) with 12 of the 18 species examined (Table 5). Subsection Pentandrae and section Dipharus are justifiable as single terminals because the species of each group are very homogeneous. This is reflected in the low number of polymorphic characters scored for each (three and one, respectively). The monophyly of each of these two taxa is very likely because each has characters that are unique within Aristolochia, as for example, five anthers and five carpels in all species of subsection Pentandrae (Pfeifer, 1970), and flowers with an adaxial and an abaxial lip in all the species of section Dipharus (Duchartre, 1854a, 1864; Hoehne, 1942).

The outgroups for the present analysis are the other three genera of the family Aristolochiaceae, Asarum, Saruma and Thottea. They were chosen on the basis of the cladistic analyses presented by Loconte & Stevenson (1991) and Kelly (1997, 1998). Two species of Asarum and three of Thottea were included in order to cover floral morphological variation within these genera.

The majority of the morphological characters included in this analysis were taken from our own collections, herbarium and fixed specimens, and field observations. Literature has been employed only when material was unavailable for study. The matrix contained 72 characters with a total of 100 apomorphic states. A complete list of characters, character states, and source of data from the literature are given in Appendix 1. The data matrix (Appendix 2) was compiled using Winclada (Nixon, 2001). All multistate characters were treated as nonadditive (unordered). A parsimony analysis was run using NONA (Goloboff, 1993), with the hold 1000, h/10, mult*1000, max* options. The consensus tree was obtained using the inters command. The resulting trees and the character distribution were examined in CLADOS (Nixon, 2001). Bremer support values (Bremer, 1988) were calculated on the consensus tree using the bs command in NONA.

Results

The analysis produced five equally parsimonious trees of 196 steps, CI = 0.49, and RI = 0.85. The results support a sister group relationship between Thottea and the subfamily Aristolochioideae sensu Schmidt (= tribe Aristolochieae sensu Huber; compare Table 1 and Fig. IE with Fig. 5). The analysis also supports the monophyly of the Aristolochioideae and of two major lineages within this subfamily (Fig. 5). Synapomorphies of the Aristolochioideae include: perianth differentiated into utricle, tube, and limb (character 25), adaxially curved (26), stamens sessile (45) and fused to the stigmas into a gynostemium (43). Other characters that support the subfamily are the flowers having a tubular perianth (22), and long anthers (46).

The First Major Clade: Aristolochia subgen. Siphisia (Figs. 5, 6): The first major clade within the Aristolochioideae conforms to the previously proposed subgenus Siphisia. This clade is defined by the fusion of the carpellary apices into three gynostemium lobes (character 56). Other characters that support this clade are the presence of an annulus (34) and grouped stamens (42) with the latter known outside of the subfamily only in some species of Thottea.

Resolution within subgenus Siphisia further supports two clades. The first, containing the sister species Aristolochia reticulata and A. serpentaria is defined by being herbaceous plants (character 0) with reduced subtending leaves (13), clasping bracts (15), and short inflorescence internodes (18). The second clade within Siphisia (Fig. 5) contains two subclades. The first subclade, with A. tomentosa at the base and consisting primarily of temperate species, has U-shaped petiole base (character 10; Fig. 3A). This first subclade, partially resolved, also includes A. cucurbitifolia, A. kaempferi plus two pairs of sister species, A. californica and A. punjabensis which lack an annulus (34) and A. macrophylla and A. manshuriensis which have flattened seeds (66) that are not attached to the funicle (character 69; Fig. 4C). The second subclade, with primarily subtropical and tropical species, is defined by the possession of a monosymmetric perianth limb (35). Within this second subclade, the first two branches are Asian species followed by a crown group of Central American species. The Central American clade is defined by the presence of an abscission zone in the base of the peduncle (character 20), and the seed being free from the funicle (69). Three groups are found here, Aristolochia panamensis plus A. paracleta both with an incomplete syrinx (29) and uniflowered inflorescences (12), A. arborea and A. impudica whose flowers have a lower protrusion at the flower entrance (39), and A. malacophylla and A. tricaudata with tail-like appendages on the flowers (37). The latter four species form a crown clade defined by the possession of large supratectal warts on the pollen wall (50).

The Second Major Clade: Aristolochia subgen. Pararistolochia + A. subgen. Orthoaristolochia + Euglypha + Holostylis (Figs. 5, 7): The second major clade consists of two subclades, one corresponding to subgenus Pararistolochia and the other equivalent to subgenus Orthoaristolochia plus the genera Euglypha and Holostylis. The synapomorphies that link these taxa are the slightly curved tube (character 31) and the conical trichomes inside the flower (33). The only member of the clade in which these trichomes are missing is Holostylis. Aristolochia lindneri, previously reported as lacking trichomes on the inner surface of the flower (Hoehne, 1942), have conical trichomes that are extremely short.

The analysis supports the monophyly of Pararistolochia (Figs. 5, 7, 8). Characters that define this group include a markedly differentiated ridge on the pollen wall (character 49) and indehiscent fruits (62) with a warty surface (59), a strongly lignified pericarp (60), and a fleshy mesocarp (61). Two suclades are found within subgenus Pararistolochia. The first consists of A. deltantha and A. momandul and is defined by the distally inflated perianth tube (character 32, otherwise present only in the Neotropical A. grandiflora) and flattened seeds (66) with a filiform funicle (70). The second subclade includes six species (A. leonensis, A. goldieana, A. triactina, A. decandra, A. macrocarpa, and A. promissa) that share the stem being constricted and becoming 'figure 8'-shaped in transverse section (5) and flowers in partial florescences arranged spirally (19). The first branch within the latter subclade consists of A. leonensis which is the sister group of the crown clade of five species (A. goldieana, A. triactina, A. decandra, A. macrocarpa, and A. promissa) whose flowers have an annulus (34). The latter four species share the possession of 8-10 stamens (40), 8-10 gynostemium lobes (56) and a complete syrinx (29). Three of these (A. decandra, A. macrocarpa, and A. promissa) have a monosymmetric perianth limb (35) and form an unresolved crownclade.

Subgenus Orthoaristolochia is paraphyletic because Euglypha and Holostylis are nested within it (Figs. 5, 7, 10). Characters that define this third and most complex clade are the abaxially concave perianth (character 26), the monosymmetric limb (35), the fusion of the three perianth parts into one lobe (36), and the ventricidal (62), acropetal (63) capsule. The data support two subclades within this major clade. The first corresponds to the section Diplolobus as described by Duchartre (1854a, 1864; Fig. 9). This clade, poorly resolved, contains A. clematitis and other European species plus a number of tropical Asian and Australasian species such as A. acuminata, A. indica, A. philippinensis, and A. thozeiti. The second subclade, exclusively Neotropical, includes the bulk of the species of Aristolochia sect. Gymnolobus (- Howardia) + Eoglypha + Holostylis (Figs. 5, 10).

Within the Neotropical clade mentioned above (Fig. 10), the first crown clade is formed by Aristolochia melastoma at the base, followed by A. acutifolia and the sister species A. maxima and A. trianae. All these species correspond to series Thyrsicae as described by Gonzalez (1990, 1991). The second crown clade is unresolved at its base, with a trichotomy formed by: section Pentandrae-, the unresolved A. burelae + A. grandiflora + A. lindneri supported by the presence of peltate bracts (character 16), an abscission zone in the base of the peduncle (20), and psilate pollen (47); and the remaining crown clade defined by non-bracteate flowers (14) which have an incomplete syrinx (29) and containing Euglypha, Holostylis and all the Neotropical species of Aristolochia. The latter crown clade is also unresolved with a trichotomy formed as follows: a clade with A. xerophytica plus the sister species A. passifloraefolia and A. tigrina, all with fimbriate flowers (38); a clade with species having 'pseudostipules' (8) and the tube oblique with respect to the utricle (30; Fig. 10); and a clade containing several species of Aristolochia plus Euglypha plus Holostylis and defined by concave-convex seeds (66) with a massive funicle (70). Whereas the position of Euglypha is not precisely defined, Holostylis emerges as the sister taxon of Aristolochia subser. Anthocaulicae as described by Gonzalez (1990, 1991). This sister group relationship is based on the presence of flowers in lateral racemes (11) and reduced subtending leaves (13).

Discussion

The analysis shows that Aristolochia s. 1. is paraphyletic because the two other genera, Euglypha and Holostylis, are nested inside one of the crown clades of Aristolochia (Figs. 5, 7, 10). Therefore, the recognition of the tribes Aristolochieae and Euglypheae (sensu Schmidt, 1935), and the genera Euglypha and Holostylis is no longer tenable. Consequently merging of these two genera within Aristolochia has recently been proposed (Gonzalez, 1997, 1999c). Molecular data from trtT-trnF sequences have also shown that Holostylis is nested within Aristolochia (Neinhuis et al., 1999). The two major clades generated in the present analysis are congruent with the two subtribes described by Huber (1985, 1993; Table 1). On the basis of their monophyly these groups merit taxonomic status regardless of the rank at which they are recognized (see below).

According to this analysis, Aristolochia s. str. and the segregate genera Endodeca, Siphisia (=Isotrema), and Pararistolochia are each supported as monophyletic units (Fig. 11). The monophyly of each of the other minor Rafinesque's segregates (Ambuya, Diglosselis, Hexaplectris, Pistolochia, Plagistra, Psophiza, Pteriphis, and Tropexa; Table 2) is not subject to evaluation because their specific composition was not fully described by Rafinesque (1828, 1836). Howardia (= Sect. Gymnolobus Duchartre, 1854a, 1864), the largest segregate genus which was originally proposed by Klotzsch (1859; Tables 2, 3) and maintained by Huber (1984, 1993), is paraphyletic and thus does not merit recognition as a taxon (Fig. 11).

The analysis supports the monophyly of subgenus Siphisia (-Isotrema) but also requires the inclusion of Aristolochia arborea as a member of that subgenus (Figs. 5, 6, 11). A. arborea was misplaced as a member of subgenus Orthoaristolochia by Duchartre (1864) and Schmidt (1935). The present analysis shows that this species is a member of subgenus Siphisia and confirms the observations by Wyatt (1955) and Pfeifer (1966) that the gynostemium of A. arborea has three lobes as do all the other members of this subgenus. Molecular evidence also supports the monophyly of subgenus Siphisia (Murata et al., 1999; Neinhuis et al., 1999).

Duchartre (1854a, 1864) divided his subgenus Siphisia into three different sections, Asterolytes, Siphisia, and Hexodon, that were subsequently maintained by Wyatt (1955). The first section consisting of Aristolochia reticulata and A. serpentaria (Figs. 5, 6), equivalent to the Rafinesque's (1828) segregate Endodeca (Table 3), is shown to be monophyletic. Klotzsch (1859) described Endodeca as having a six-lobed gynostemium. Our observations indicate, however, that the gynostemium in both species is primarily trilobed (Gonzalez & Stevenson, 2000b). With respect to the remaining two sections, two species of section Siphisia (A. macrophylla and A. tomentosa) and one of section Hexodon (A. kaempferi) were included in the present analysis. A. kaempferi is nested inside the clade that contains the other two suggesting that section Siphisia is not monophyletic unless section Hexodon is included. A phylogenetic analysis based on sequences of the matK gene show similar results (Murata et al., 1999). These sections were described by Duchartre (1854a, 1864) and based primarily on minor differences in the shape of the gynostemium at maturity as detected on herbarium specimens. However, the gynostemium in Aristolochia undergoes significant changes during its development (Gonzalez & Stevenson, 2000b) and its reconstruction from herbarium specimens is not accurate.

A phylogenetic analysis based on trnT-trnF sequences is congruent with our results in that it supports a sister group relationship between Aristolochia reticulata and A. serpentaria on the one hand and the remaining species of subgenus Siphisia on the other (Neinhuis et al., 1999). In addition, karyological evidence supports the hypothesis that subgenus Siphisia forms a lineage distinct from at least subgenus Orthoaristolochia (Gregory, 1956; Sharma & Varma, 1959; Nardi, 1984; Morawetz, 1985; Fiorini, 1987; Sugawara & Murata, 1992). Unfortunately, karyotype information is not known for species of subgenus Pararistolochia. All chromosome counts are 2n=28 or 32 in species of subgenus Siphisia and 2n=8, 12, or 14 in species of subgenus Orthoaristolochia (one count of A. longa, however, has been reported as 2n=28 by Gregory, 1956).

The second large clade contains two major lineages Aristolochia subgen. Pararistolochia and its sister group a complex of Aristolochia subgen. Orthoaristolochia plus Euglypha plus Holostylis (Figs. 5, 7). This relationship is in agreement with the recognition of subtribe Aristolochiineae (Huber, 1985, 1993; Table 1) regardless of the rank at which the former clades are recognized. However, molecular evidence based on trnT-trnF sequences suggests that subgenus Pararistolochia is the sister-group to subgenus Siphisia (Neinhuis et al., 1999). Based on the regular floral limb and the high number of stamens, Wyatt (1955) and Ma (1989) proposed that subgenus Pararistolochia is the most primitive subgenus of Aristolochia. This assumption is not confirmed here because subgenus Pararistolochia is not basal within the Aristolochioideae (Fig. 5) based upon the morphological analysis presented here as well as on molecular evidence (Neinhuis et al., 1999). The position of subgenus Pararistolochia is still equivocal given the disparity between the results of morphological and molecular analyses.

Pararistolochia, described as a genus by Hutchinson & Dalziel (1927) and subsequently maintained by Poney (1978), was redelimited by Parsons (1996) as consisting of the 8-10 West and Central African species traditionally recognized (Poney, 1978; Ma, 1992) plus 24 other species from Malesia, New Guinea, and Australia. This close relationship was anticipated by Duchartre (1864) who joined the African Aristolochia macrocarpa and the Australian A. praevenosa while at the same time recognizing that these two species did not belong to any of the other groups that he had established. Hou (1984), Huber (1985, 1993), and Ma (1992) also pointed out the similarity of some species from Malasia, Australia, and New Guinea to the African members of this taxon. The present analysis, as well as others based on molecular evidence (Murata et al., 1999; Neinhuis et al., 1999), indicate that Pararistolochia is a monophyletic lineage regardless of the rank at which it is recognized and that there is a sister group relationship between Australasian and African taxa. However, the available data do not precisely indicate the position of the Malesian A. decandra which forms an unresolved clade with the African A. macrocarpa and A. promissa. Perhaps, this trichotomy could be resolved when fruits and seeds of A. decandra become available for study.

The clade Aristolochia subgen. Orthoaristolochia + Euglypha + Holostylis (Figs. 5, 7) has, in turn, two clades. The first clade corresponds to the monophyletic Aristolochia sect. Diplolobus (Fig. 9) described by Duchartre (1854a, 1864) and is equivalent to Aristolochia s. str. (Klotzsch, 1859; Huber, 1985, 1993; Table 3). The lack of resolution within the clade prevents an evaluation of the monophyly of the two subsections traditionally recognized, Euaristolochia and Podanthemum (Table 3). Within section Diplolobus, Duchartre (1864) described a third subsection, Acerostylis, composed only of the East African Aristolochia rigida. This species was not included in the analysis because it has coding identical to other species of subsection Euaristolochia. Duchartre (1864) described subsection Acerostylis as having a truncate gynostemium which is a misinterpretion as observations of Franchet (1882) as well as our own (based on the specimen Thesiger s.n., BM) have shown. The gynostemium of this species has essentially the same morphology as the other members of subsection Euaristolochia.

The second clade includes Aristolochia sect. Gymnolobus (= Howardia) plus Euglypha plus Holostylis (Figs. 5, 10, 11). The recognition of these latter two genera (see below), as well as the segregate Einomeia (=A. subser. Pentandrae) would make Sect. Gymnolobus paraphyletic (Fig. 11). The first subclade within this complex corresponds to Aristolochia ser. Thyrsicae as proposed by Gonzalez (1990, 1991) and this series is monophyletic (Fig. 10). The placement of A. subser. Pentandrae is unclear (Figs. 5, 10, 11-). The limited resolution within the clade that contains subseries Pentandrae is due to conflicting characters which militates against resolution of a sister group relationship between this subseries and either A. grandiflora plus A. burelae plus A. lindnerii or the clade that contains Euglypha, Holostylis, and the remaining Aristolochia spp. The pentandrous species have in common with the first potential sister group the presence of a single, bracteate flower per node (character 14) and the complete syrinx (29). They have in common with the second potential sister group, the absence of an abscission zone at the base of the peduncle (20) and fossulate pollen (47).

Euglypha is part of an unresolved clade formed by a group of species with concave-convex seeds (character 66) and a massive funicle (70). Euglypha has been maintained as a distinct genus (Schmidt, 1935; Hoehne, 1942; Ahumada, 1967; Huber, 1993) because of the presence of a stipe at the base of the perianth (23), extremely shortened capsules that fail to dehisce (62), and usually only one seed per carpel (65). The latter three characters are autapomorphies of Euglypha. The stipe (23) is also present in a number of species of section Diplolobus (Fig. 9) but their vasculature is different suggesting an independent origin. In Euglypha, the vascular plexus of the base of the perianth is complete (Gonzalez & Stevenson, 2000a) and there are additional second order veins along the stipe (28), whereas in the species of section Diplolobus, the plexus is incomplete and the second order veins are lacking (Gonzalez & Stevenson, 2000a).

The genus Holostylis is the sister group of Aristolochia subser. Anthocaulicae (Gonzalez, 1990, 1991; Fig. 10). The synapomorphies are the presence of lateral racemes (character 11) and dramatically reduced leaves subtending the individual flowers (13). This is consistent with additional anatomical characters that support a close relationship between Aristolochia and Holostylis (Solereder, 1889a; Carlquist, 1993) especially the presence of idioblasts filled with brown, tanniferous material in Holostylis (Solereder, 1889a) and at least in one species of its sister group such as A. leuconeura (Gonzalez, 1990). The subseries Anthocaulicae is a monophyletic group defined by cauliflorous inflorescences with extremely shortened internodes (18; Fig. 10).

The infrageneric taxa proposed within Aristolochia subsect. Hexandrae (Duchartre, 1854a, 1864; Hoehne, 1942; Schmidt, 1935) which are based primarily on habit and shape and size of the flowers are not monophyletic. For example, the group Bilabiatae which contains all the species with a 2-lobed perianth is polyphyletic (Figs. 12, 13). This is consistent with the fact that the 2-lobed perianth in p. ej. A. ringens and A. ridicula develop differently (Gonzalez & Stevenson, 2000a). The analysis also shows that Aristolochia ser. Hexandrae as described by Gonzalez (1990, 1991; Table 5) is paraphyletic. This series was originally characterized by the absence of an abscission zone at the base of the petiole (character 9) and the floral peduncle (20), the absence of bracts (14), the flowers in racemes (11), the fruits with entire septae (64), and the seeds lacking wings or having one wing (68). All these traits are now shown to be symplesiomorphies of series Hexandrae.

Character Evolution--Inflorescence Morphology: The cladistic analysis indicates that monopodial growth (character 1) is a synapomorphy of Thottea and the Aristolochioideae (Fig. 5) although some exceptions may occur in some species of subgenus Pararistolochia from Australia and New Guinea which may have sympodial growth (Gonzalez, 1999b). Within the Aristolochioideae, a transformation from thyrsic to racemose inflorescences has occurred via a reduction in the number of flowers to one per node and the loss of the bract (12 and 14, respectively). Whereas partial florescences with one flower have arisen several times in the Aristolochioideae (at least twice within subgenus Siphisia and twice within subgenus Orthoaristolochia), the loss of the bract (i.e. non-bracteate flowers) has evolved independently only two times, once in the majority of the Neotropical species of Aristolochia plus Euglypha and Holostylis and once in a few species of Aristolochia sect. Diplolobus (14; Fig. 14).

In addition, the analysis shows that helicoid cymes (character 19) are a derived feature and flowers arranged in a spiral in partial florescences occur at least in two different clades, once in the African species of Aristolochia subgen. Pararistolochia and twice within section Diplolobus. The analysis also indicates that buds arranged in two rows occur as a derived character, which is present only in some species of section Diplolobus, e. g. A. acuminata, A. clematitis, A. contorta, A. indica, A. petersiana, A. pistolochia, and A. tubiflora. The low resolution within this clade, however, prevents further interpretation of this character as uniquely derived in these species.

Lateral racemes with shortened internodes (character 11) and reduced subtending leaves (13) are both derived (Fig. 14). Whereas the first supports a sister group relationship between Holostylis and A. subser. Anthocaulicae, the second appears independently in two clades, once within subgenus Siphisia (in the sister species A. reticulata and A. serpentaria) and once as a synapomorphy for A. subser. Anthocaulicae plus Holostylis.

Character Evolution--Floral Morphology: Monosymmetry in flowers of Aristolochia, Euglypha and Holostylis is due to two independent structural transformations, one causing the curvature of the perianth and the other affecting the symmetry of the limb. Thus, flowers of some species of subgenera Siphisia and Pararistolochia maintain the plesiomorphic condition, i.e. a regular perianth limb even though they have a curved perianth (Gonzalez & Stevenson, 2000a). According to the present analysis, the curvature (character 26) evolves prior to the monosymmetric limb (35; Fig. 15). The latter has evolved three times, once in a clade within Aristolochia subgen. Siphisia, once in a clade within subgenus Pararistolochia, and once as a synapomorphy for the subgenus Orthoaristolochia + Euglypha + Holostylis (Fig. 15).

The present analysis suggests that a monosymmetric floral limb and/or early fusion of the perianth primordia might play an important role in the morphological diversification of the flowers of the Aristolochiaceae. The actinomorphic limb might limit further elongation and expansion of the apex where the three meristematic areas are located and from where most of the morphological variation is derived ("tails," "wings," "antennae," etc.). For example, within Aristolochia subgen. Siphisia floral shape in the clade composed of species with an actinomorphic limb is not as morphologically diverse as in its sister clade that includes species with flowers having tails (e.g. A: tricaudata; Fig. 15) or protrusions of the limb (e.g. A. arborea). Similarly, the most remarkable variation in perianth shape and size occurs in Aristolochia subsect. Hexandrae where an early fusion of the perianth primordia occurs resulting in the perianth tip growing as a single unit (Gonzalez & Stevenson, 2000a). This is not the case in the species of Aristolochia sect. Diplolobus particularly those of subsection Podanthemum where the tips of the perianth parts remain distinct until maturity. In the latter, limb shape is uniform. This is consistent with the low diversification of the shape of actinomorphic flowers of Asarum (Cheng & Yang, 1983; Kelly, 1997, 1998) and Thottea (Hou, 1984).

A perianth limb with two lobes, although restricted to some members of Aristolochia sect. Hexandrae (Group Bilabiatae in Figs. 12, 13) is not homologous in all cases because there are at least two different developmental processes. The first of these occurs in the species A. labiata and A. ringens in which one lobe (corresponding to the median perianth lobe) is adaxial and the other lobe (formed by the fusion of the two lateral perianth lobes) is abaxial. In contrast, in A. ridicula the two lateral lobes develop as distinct lateral extensions that are much larger than the median perianth lobe at maturity (Gonzalez & Stevenson, 2000a).

The stipe in the perianth, traditionally used as a diagnostic trait to define the subsection Podanthemum within Aristolochia section Diplolobus (Table 3) and the genus Euglypha, has evolved independently in these two taxa (character 23 in Figs. 9, 10). However, it is not clear if it evolved in parallel several times within section Diplolobus (Fig. 9). Another derived character related to the base of the perianth in Aristolochia is the strongly asymmetrical perianth base (24) which plays a role in positioning the flower during anthesis. This emerges as a synapomorphy of the Neotropical crown clade formed by A. mishuyacensis, A. trilobata and the species of section Dipharus.

The syrinx (character 29) and the annulus (34) seem to have been acquired independently several times. A complete syrinx appears twice, once within subgenus Pararistolochia in the clade composed of A. triactina, A. decandra and A. macrocarpa and once in subgenus Orthoaristolochia subsect. Gymnolobus. Within the latter, an incomplete syrinx is a synapomorphy of a clade composed of Aristolochia subsect. Hexandrae plus Euglypha plus Holostylis. Three reversals (lack of syrinx) occur, once in section Dipharus, once in the clade A. odoratissima, A. didyma and A. ridicula, and once in Holostylis. The annulus appears independently four times, once in subgenus Siphisia (with two losses inside), once in some species of subgenus Pararistolochia (i.e. the clade composed of A. goldieana plus A. triactina plus A. macrocarpa), once in the pentandrous species A. secunda, and once in A. grandiflora. The conical trichomes on the inside of the tube evolved, however, as a unique event in the lineage composed of subgenus Pararistolochia and subgenus Orthoaristolochia.

In the present analysis, traits such as tail-shaped appendages (character 37) or fimbriae (38) on the limb arise independently in different species (Fig. 15). For example, tail-like appendages develop in one species of subgenus Siphisia (A. tricaudata), one of subgenus Pararistolochia (A. promissa), one of subsection Pentandrae (A. nelsonii), two of subsection Hexandrae (A. mishuyacensis and A. trilobata), once in group Dipharus (A. pohliana), and once in A. grandiflora. Fimbriae are restricted only to some species of subsection Gymnolobus-, however, they have evolved independently at least three times, one in A. lindnerii, one in A. didyma plus A. ridicula, and one in the A. passifloraefolia + A. tigrina+A. xerophytica clade.

Changes in stamen and carpel merosity within Aristolochia are all derived traits, with respect to the plesiomorphic hexamerous condition. The presence of more than six stamens in some members of subgenun Pararistolochia is a derived trait. The presence of five stamens, five stigmatic lobes, and five carpels are also derived traits that appear as unique events in the lineage Aristolochia subsect. Pentandrae. These characters are not simply correlated with each other, because the number of carpels in other members of the family does not always correspond to the number of stamens; for example, there are twelve stamens and six carpels in Asarum and Saruma, four carpels and 6-36 stamens in Thottea, or six stamens and three gynostemium lobes in Aristolochia subgen. Siphisia. The correspondence in number between the stamens and the carpels in most species of Aristolochia, including Euglypha and Holostylis, might be related to the fact that both stamen and carpel primordia develop in close contact with each other (Gonzalez & Stevenson, 2000b).

Character Evolution--Seed dispersal: Seeds of many species of Aristolochia are adapted to at least two different dispersal mechanisms, anemochory and zoochory (Fig. 4). Winged, flattened seeds are found in a number of species. Whereas rectangular seeds with two wings (Fig. 41) are a synapomorphy for the clade A. acutifolia, A. maxima and A. trianae, 1--winged, triangular or rhomboidal (Fig. 4H) seeds have evolved three different times, once in a clade within subsection Diplolobus, and two times within subsection Gymnolobus (Fig. 16).

On the other hand, sticky funicular outgrowths (arils) that play a role in zoochory (including myrmecochory) evolved four different times in the Aristolochiaceae, once in Asarum, once in Aristolochia odoratissima, once in A. leuconeura, and once in A. didyma (Fig. 16). This is reflected in at least three distinct structural differences of these arils. In Asarum, sticky arils are formed by 2-4 layers of large, translucent cells formed from the funicle (Fig. 4B). In Aristolochia, it consists of a massive secretion from the funicle plus the chalaza (in A. leuconeura, Fig. 4F), or from epidermal and subepidermal cells of the funicle (in A. didyma and A. odoratissima; Fig. 4G).

A Brief Comment on Biogeography. The analysis suggests that the two major clades (subgenus Siphisia vs. the remaining Aristolochioideae; Fig. 5) more or less coincide with the Laurasian-Gondwanic vicariant event. Subgenus Siphisia is found primarily in North America and W temperate Asia. In addition, late cladogenesis events for the Central American species (i.e. Aristolochia arborea, A. impudica, A. malacophylla, A. panamensis, A. paracleto, and A. tricaudatoe. Fig. 6) coincide with a later formation of most of Central America with respect to North America (see e.g., Briggs, 1987). Within the temperate species, two pairs of sister species are disjunct between temperate Asia and North America, A. californica + A. punjabensis', and A. macrophylla + A. manshuriensis (Fig. 6). The latter are an Eastern North American-Eastern Asian disjunct pair that are remarkably similar in terms of morphological characters. The current analysis, as well as molecular data (Murata et al., 1999), shows them as sister species which argues against the viewpoint of Wen (1999) that such disjuncts may not be sister species. The remaining species of subgenus Siphisia in Asia are mainly temperate and subtropical. The tropical species are fewer and do not extend beyond India to the west or the Wallace line to the east.

The two major clades of subgenus Pararistolochia are also disjunct, one formed by the Australian and the New Guinean species and its sister group formed primarily by West African species (Fig. 8).

The third subgenus, Orthoaristolochia, has a much wider geographical distribution but the two major lineages within the subgenus are primarily Paleotropical (section Diplolobus)-Neotropical (section Gymnolobus + Euglypha + Holostylis) vicariants (Fig. 7).

Two major geographic regions are important in term of sympatric distribution of major clades: Southeast Asia and Central America. Members of all the three subgenera occur together only in Malesia where several species of subgenus Orthoaristolochia, a few species of subgenus Siphisia, and one species of subgenus Pararistolochia (A. decandra) are found sympatrically (Hou, 1984). On the other hand, in Mexico and Central America, several species of the subgenus Siphisia are sympatric with several species of subgenus Orthoaristolochia. It is also in this area where the approximately 35 pentandrous species of Aristolochia have evolved, an important fact in terms of diversity within subgenus Orthoaristolochia.

Several authors (e.g. Raven & Axelrod, 1974; Simpson & Neff, 1985) have assumed a North-South dispersal route of Aristolochia in America. The present analysis argues agains that point of view because the Laurasian elements have not been found south of Panama. In addition, Aristolochia in America is not a monophyletic group, indicating that sympatry of differente clades in Central America is secondary in terms of the presence of the predominantly Laurasian subgenus Siphisia and the predominantly Gondwanian sect. Gymnolobus.

Conclusions

The present analysis supports the concept of the monophyly of Thottea + Aristolochia (Fig. 5) and this warrants to the conclusion that these two genera form a single lineage within the Aristolochiaceae as was implicit in Huber's (1985, 1993) system of classification (Fig. 1G). The analysis also shows that Aristolochia s.l. is paraphyletic and that most of the infrageneric taxa within Aristolochia are either para- or polyphyletic. Most of the traits related to the floral shape of the perianth, upon which these groups have been recognized, are shown to be independently acquired. Based on the resulting monophyletic groups, a revised classification of the subfamily Aristolochioideae consisting of two tribes, two subtribes, and five genera is proposed here. The new combinations and nomenclatural aspects of infrageneric taxa will be published elsewhere. For practical reasons, we are in favor of recognizing Aristolochia in a broader sense than that given by Huber (1985, 1993), because the generic recognition of Euglypha, Holostylis and Einomeia (i.e. the pentandrous species; Fig. 11) would require the establishment of as many as 12 distinct genera, and would collapse the nomenclature of the largest groups of species of Aristolochia. Thus, the formal classification proposed here is:

Aristolochioideae

Tribe Bragantieae Klotzsch

Thottea Rottboll

Tribe Aristolochieae

Subtribe Isotrematinae H. Huber

Endodeca Rafinesque

Isotrema Rafinesque

Subtribe Aristolochiineae

Pararistolochia Hutchinson & Dalziel

Aristolochia L.(including Euglypha Chodat & Hassler and Holostylis Duchartre)

Acknowledgments

The first author is deeply indebted to the Instituto Colombiano para el Desarrollo de la Ciencia y la Tecnologia "Francisco Jose de Caldas", COLCIENCIAS, for all the academic and finantial support received during his Ph. D. studies in the City University of New York (CUNY), as part of the "Programa de Capacitacion de Recursos Humanos para la Ciencia y la Tecnologia" (contract 32-1995). He also thanks the Universidad Nacional de Colombia, for continuously supporting his research on the systematics and morphology of Aristolochiaceae. The present paper is part of his Ph. D. dissertation at CUNY, for which he is indebted to members of its Graduate School and University Center. Finally, the first author is deeply grateful to Dr. Jim Grimes, at the Royal Botanic Gardens, Melbourne, Australia, for his important comments on this research, and especially for all the training on cladistic and laboratory (LM and SEM) techniques received from him.

Literature Cited

Adanson, M. 1763. Familles des plantes. Paris.

Ahumada, L.Z. 1967. Revision de las Aristolochiaceae argentinas. Opera Lilloana 16: 1-148.

Baldacci, A. 1894. Affinita delle Aristolochiacee e dei generi Aristolochiacei. Boll. Soc. Bot. Ital. 1894: 49-54.

Bartling, F. T. 1830. Ordines Naturales Plantarum, eorumque characteres et affinitates adjecta generum enumeratione. Gottingae.

Behnke, H. D. 1988. Sieve-element plastids, phloem protein, and evolution of flowering plants: III. Magnoliidae. Taxon 37: 699-732.

--1991. Distribution and evolution of forms and types of sieve element plastids in the dicotyledons. Aliso 13: 167-182.

Bentham, G. & J. D. Hooker. 1880. Aristolochiaceae. Genera Plantarum 3: 121-125.

Bharathan, G. & E. Zimmer. 1995. Early branching events in monocotyledons partial 18s ribosomal DNA sequence analysis. In P.J. Rudall et at. (eds.) Monocotyledons: systematics and evolution, 1: 81-107. Royal Botanic Gardens, Kew.

Blume, C. L. 1827. Enumeratio Plantarum Javae.

Bremer, K. 1988. The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42: 795-803.

Briggs, J. C. 1987. Biogeography and Plate Tectonics. Elsevier Science Publishers. Amsterdam.

Brown, R. 1821. An account of a new genus of plants named Rafflesia. Trans. Linn. Soc. London 13: 1-34, t. 15-22.

Carlquist, S. 1993. Wood and bark anatomy of Aristolochiaceae; systematic and habitai correlations. IAWA Bull. 14: 341-357.

Cheng, C. Y. & C. S. Yang. 1983. A synopsis of the Chinese species of Asarum (Aristolochiaceae). J. Arnold Arbor. 64: 565-597.

--&--. 1988. Saruma & Asarum. Flora Reipublicae Popularis Sinicae 24: 160-196.

Cocucci, A. E. 1983. New evidence from embryology in Angiosperm Classification. Nordic J. Bot. 3: 67-73.

Corner, E. J. H. 1976. The Seeds of Dicotyledons. Vols. 1-2. Cambridge Univ. Press.

Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York.

Dahlgren, R. T. M. 1983. General aspects of angiosperm evolution and macrosystematics. Nordic J. Bot. 3: 119-149.

--& K. Bremer. 1985. Major clades of the angiosperms. Cladistics 1: 349-368.

--& H. T. Clifford. 1982. The Monocotyledons: a comparative study. Academic Press.

Davis, P. H. & M. S. Khan. 1961. Aristolochia in the Near East. Notes Roy. Bot. Gard. Edinburgh 23: 515-546.

Delpino, F. 1893. Applicazione di nouvi criterii per la classificazione delle piante. Quinta memoria. Mem. Reale Accad. Sei. Ist. Bologna, Ser. V, 240-244.

Dickison, W. C. 1992. Morphology and anatomy of the flower and pollen of Saruma henryi Oliv., a phylogenetic relict of the Aristolochiaceae. Bull. Torrey Bot. Club 119: 392-400.

Donoghue, M. J. & J. A. Doyle. 1989. Phylogenetic analysis of angiosperms and the relationships of Hamamelidae. In P. R. Crane & S. Blackmore (eds.), Evolution, systematics, and fossil history of the Hamamelidae, 1: 17-45, Clarendon Press, Oxford.

Duchartre, P. 1854a. Tentamen methodicae divisionis generis Aristolochia. Ann. Sei. Nat. Bot. ser. 4, 2: 29-76.

--. 1854b. Sur les pretendues stipules des Aristoloches. Bull. Soc. Bot. France 1: 56-60.

--. 1864. Aristolochiaceae. In A. DC. Prodromus 15(1): 421 498.

Dumortier, B. C. 1822. Commentationes Botanicae. Observations botaniques. Tournay.

Endress, P. K. 1990. Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae). Mem. New York Bot. Gard. 55: 5-34.

--. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge.

Erbar, C. & P. Leins. 1994. Flowers in Magnoliidae and the origin of flowers in other subclasses of the Angiosperms. I. The relationships between flowers of Magnoliidae and Alismatidae. PI. Syst. Evol. Suppl. 8: 193-208.

Fiorini, G. 1987. Numero cromosomico di una Aristolochia raccolta in territorio jugoslavo. Inform. Bot. Ital. 19: 265-266.

Franchet, M. A. 1882. Aristolochieae. Sertulum Somalense. Paris.

Goloboff, P. 1993. Nona, version 1.6. Program and documentation. Distributed by the author, Buenos Aires.

Gonzalez, F. 1990. Aristolochiaceae. Flora de Colombia. Monografia No. 12. Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogota

--. 1991. Notes on the Systematics of Aristolochia subsect. Hexandrae. Ann. Missouri Bot. Gard. 78: 497-503.

--. 1997. Hacia una filogenia de Aristolochia y sus congeneres neotropicales. Caldasia 19: 93-108.

--. 1999a: A phylogenetic analysis of the Aristolochioideae (Aristolochiaceae). Ph. D. Dissertation. The City University of New York.

--. 1999b. Inflorescence morphology and the systematics of Aristolochiaceae. Syst. Geogr. PI. 68: 159-172.

--. 1999c. Un nuevo nombre para Holostylis reniformis (Aristolochiaceae). Revista Acad. Colomb. Ci. Exact. 23 (88): 337-339.

--. & D.W. Stevenson. 2000a: Perianth development and systematics of Aristolochia. Flora 195:.370-391.

--&--. 2000b. Gynostemium development in Aristolochia (Aristolochiaceae). Bot. Jahrb. Syst. 122: 249-291.

Gregory, M. P. 1956. A phyletic rearrangement in the Aristolochiaceae. Amer. J. Bot. 43: 110-122.

Hennig, S., W. Barthlott, I. Meusel & I. Theisen. 1994. Mikromorphologie der Epicuticularwachse und die Systematik der Magnoliidae, Ranunculidae und Hamamelididae. Trop. Subtrop. Pflanzenwelt. 90: 1-60.

Hoehne, F. C. 1942. Aristolochiaceas. Flora Brasilica 15(2): 3-141, t. 1-123.

Hou, D. 1981. Florae Malesiana Praecursores LXII. On the genus Thottea (Aristolochiaceae). Blumea 27: 301-332.

--. 1984. Aristolochiaceae. Florae Malesiana Series 10, 1: 53 108.

Huber, H. 1977. The treatment of the monocotyledons in an evolutionary system of classification. PI. Syst. Evol. Suppl. 1: 285-298.

--. 1985. Samenmerkmale und Gliederung der Aristolochiaceen. Bot. Jahrb. Syst. 107: 277-320.

--. 1993. Aristolochiaceae. In: K. Kubitzki (ed.), The families and genera of vascular plants, 2: 129-137.

Hutchinson, J. 1969. Evolution and phylogeny of flowering plants. London, Academic Press.

--. & J. M. Dalziel. 1927. Aristolochiaceae. Fl. West Tropical Africa, Is' edition, pp. 75-78.

Hwang, S.-M. 1988. Thottea and Aristolochia. Flora Reipublicae Popularis Sinicae 24: 196-245.

Jussieu, A. L. de. 1789. Aristolochiae. Gen. PI. 74-75. Paris.

Kelly, L. 1997. A cladistic analysis of Asarum (Aristolochiaceae) and implications for the evolution of herkogamy. Amer. J. Bot. 84: 1752-1765.

--. 1998. Phylogenetic relationships in Asarum (Aristolochiaceae) based on morphology and ITS sequences. Amer. J. Bot. 85: 1454-1467.

Klotzsch, F. 1859. Die Aristolochiaceae des Berliner Herbariums. Monatsber. Konigl. Preuss. Akad. Wiss. Berlin 1859: 571-625.

Kolakovsky, A. A. 1957. Pervoe dopolnenie k kodorskoj flore (MeoreAtara) (in Russian). Trudy Suhumsk. Bot. Sada. 10.

--. 1964. Pliotsenovaja flora Pitsundi. Trudy Suhumsk. Bot. Sada. 14. (in Russian).

Kratzer, J. 1918. Die verwandtschaflichen Beziehungen der Cucurbitaceen auf Grund ihrer Samenentwicklung. Flora 110: 275-343.

Kubitzki, K. 1993. (ed.) The families and genera of vascular plants. Vol. 2. Springer Verlag.

Kulkarni, A. R. & K. S. Patil. 1977. Aristolochioxylon prakashii from the Deccan Intertrappean Beds of Warda District, Maharashtra. Geophytol. 7: 44-49.

Lammers, T. G., T. F. Stuessy & M. O. Silva. 1986. Systematic relationships of the Lactoridaceae: An endemic family of the Juan Fernandez Islands, Chile. PI. Syst. Evol. 152: 3-4.

Leins, P. & C. Erbar. 1985. Ein Beitrag zur Blutenentwicklung der Aristolochiaceen, einer Vermittlergruppe zu den Monokotylen. Bot. Jahrb. Syst. 107: 343-368.

--&--. 1995. Das fruhe Differenzierungsmuster in den Bluten von Saruma henryi Oliv. (Aristolochiaceae). Bot. Jahrb. Syst. 117: 365-376.

--, --. & W. A. van Heel. 1988. Note on the floral development of Thottea (Aristolochiaceae). Blumea 33: 357-370.

Lindley, J. 1831. Introd. Nat. Syst. Bot. New York, G. C. & H. Carville.

--. 1853. The Vegetable Kingdom. Third edition. London, Bradbury & Evans.

Loconte, H. & D. W. Stevenson. 1991. Cladistics of the Magnoliidae. Cladistics 7: 267-296.

Ma, J.S. 1989. A revision of Aristolochia Linn, from E. & S. Asia. Acta Phytotax. Sin. 27: 321-364.

--. 1990. The geographical distribution and the system of Aristolochiaceae. Acta Phytotax. Sin. 28: 345-355.

--. 1992. A taxonomic revision on genus Aristolochia subgenus Pararistolochia. Acta Phytotax. Sin. 30: 508-514.

MacGinitie, H. D. 1953. Fossil plants of the Florrissant Beds, Colorado. Publ. Carnegie Inst. Wash. 599: 1-197.

--. 1969. The Eocene Green River flora of northwestern Colorado and northeastern Utah. Univ. Calif. Publ. Geo. Sei. 83:1-140.

--. 1974. An early middle Eocene flora from the Yellowstone Absaroka Volcanic province, northwestern Wind River Basin, Wyoming. Univ. Calif. Publ. Geo. Sei. 108: 1-103.

Masters, M. T. 1875. Aristolochiaceae. In: C.F.P. von Martius (ed.), Fl. Brasiliensis 4(2): 77-114, t. 17-26.

Mohana Rao, P. R. 1989. Seed and fruit anatomy in Aristolochia and Asarum with a discussion on the affinities of Aristolochiaceae. J. Swamy Bot. Cl. 6: 105-119.

Morawetz, W. 1985. Beitrage zur Karyologie und Systematik der Gattung Thottea (Aristolochiaceae). Bot. Jahrb. Syst. 107: 329-342.

Murata, J., H. Murata & T. Sugawara. 1999. Molecular phylogeny of Aristolochia. Abstracts XVI Intl. Botanical Congress, St. Louis, Missouri, p. 707.

Nakai, T. 1936. Aristolochiaceae. Flora Sylvatica Koreana 21: 1-28, t. 1.

Nandi, O. I., M. W. Chase & P. K. Endress. 1998. A combined cladistic analysis of the angiosperms using rbcL and nonmolecular data sets. Ann. Missouri Bot. Gard. 85: 137-212.

Nardi, E. 1984. The genus Aristolochia L. (Aristolochiaceae) in Italy. Webbia 38: 221-300.

--. 1991. The genus Aristolochia L. (Aristolochiaceae) in Greece. Webbia 45: 31-69.

Neinhuis, C., T. Borsch & K. W. Hilu. 1999. Phylogenetic relationships within Aristolochiaceae based on trnT-trnF sequences. Abstracts XVI International Botanical Congress, St. Louis, Missouri, p. 351.

Nixon, K. 2001. Winclada verision 0.9.99.m24. Program and documentation. Published by the author. Ithaca, New York.

Parsons, M. J. 1996. New species of Aristolochia and Pararistolochia (Aristolochiaceae) from Australia and New Guinea. Bot. J. Linn. Soc. 120: 199-238.

Periasamy, K. 1966. Studies on seeds with ruminate endosperm. VI. Rumination in the Araliaceae, Aristolochiaceae, Caprifoliaceae and Ebenaceae. Proc. Indian Acad. Sei. 64, sect. B. 1966.

Pfeifer, H. W. 1966. Revision of the North and Central American hexandrous species of Aristolochia (Aristolochiaceae). Ann. Missouri Bot. Gard. 53: 115-196.

--. 1970. A taxonomic revision of the pentandrous species of Aristolochia. Univ. Connecticut Publ. Series, 134 pp.

Phuphathanapong, L. 1987. Aristolochiaceae. In: T. Smitinand & K. Larsen (eds.), Flora of Thailand 5(1): 1-31.

Poney, O. 1978. Le genre Pararistolochia, Aristolochiaceae d'Afrique tropicale. Adansonia, ser. 2, 17: 465-494.

Qiu, Y. L., J. Lee, E Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer, Z. Chen, V. Savolainen & M. W. Chase. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404407.

Rafinesque, C.S. 1828. Medicinal Flora 1: 61-65.

--. 1836. Flora Telluriana, Centur. I-XII. pp. 97-99.

Raven, P. H. & D. I. Axelrod. 1974. Angiosperm biogeography and past continental movement. Ann. Missouri Bot. Gard. 61: 539-673.

Schmidt, O. C. 1935. Aristolochiaceae. Die naturlichen Pflanzenfamilien. Ed. 2, 16b: 204-242.

Sharma, A. K. & B. Varma. 1959. The somatic chromosomes of five species of Aristolochia. Phyton (Argentina) 12: 101-108.

Simpson, B. B. & J. L. Neff. 1985. Plants, their pollinating bees, and the great American interchange. Pp. 427-452 In: F.G. Stehli & S.D. Webb (eds.). The Great American Interchange. Plenum Press, New York.

Solereder, H. 1889a. Beitrage zur vergleichenden Anatomie der Aristolochiaceen. Bot. Jahrb. Syst. 10: 410-524.

--. 1889b. Aristolochiaceae. Die naturlichen Pflanzenfamilien, pp. 264-273.

Soltis, D., P. S. Soltis, D. L. Nickrent, L. A. Johnson, W. H. Hahn, S. B. Hoot, J. A. Sweere, R. K. Kuzoff, K. A. Kron, M. W. Chase, S. M. Swensen, E. A. Zimmer, S-M. Chaw, L. J. Gillespie, W. J. Kress & K. J. Sytsma. 1997. Angiosperm phylogeny inferred from 18S ribosomal DNA sequences. Ann. Missouri Bot. Gard. 84: 1-49. 1997.

Stevenson, D. W. & H. Loconte. 1995. Cladistic analysis of monocot families. In P. J. Rudall et al. (eds.) Monocotyledons: systematics and evolution, 2: 543-578. Royal Botanic Gardens, Kew.

Sugawara, T. & J. Murata. 1992. Chromosome numbers of eight species of Aristolochia (Aristolochiaceae) from East Asia. Acta Phytotax. Geobot. 43: 27-30.

Suessenguth, K. 1921. Beitrage zur Frage des systematischen Anschlusses der Monocotylen. Beih. Bot. Centralbl. 38: 1-79.

Takhtajan, A. L. 1996. Diversity and classification of flowering plants. Columbia University Press, 643 pp.

Tobe, H., T. F. Stuessy, P. H. Raven & K. Oginuma. 1993. Embryology and karyomorphology of Lactoridaceae. Amer. J. Bot. 80: 933-946.

Tucker, S. & A. W. Douglas. 1996. Floral structure, development, and relationships of paleoherbs: Saruma, Cabomba, Lactoris, and selected Piperales. Pp. 141-175 In: D.W. Taylor & L. J. Hickey (eds.), Flowering plant origin, evolution and phylogeny. New York, Chapman & Hall.

Van Tieghem, P. 1900. Sur le genre Hocquartia. J. Bot. (Morot) 14: 65-68. 1900.

Weintraub, J. D. 1995. Host plant association patterns and phylogeny in the tribe Troidini (Lepidoptera: Papilionidae). Pp. 307-316 In: J. M. Scriber, Y. Tsubaki & R. C. Lederhouse (eds.) Swallowtail butterflies: their ecology and evolutionary biology. Scientific Publishers, Inc.

Wen, J. 1999. Evolution of Eastern Asian and Eastern North American disjunct distributions in flowering plants. Ann. Rev. Ecol. Syst. 30: 421-455.

Wyatt, R. 1955. Floral morphology and phylogeny of the Aristolochiaceae. Ph.D. thesis, University of North Carolina.

Appendix 1. Characters and character states used in the cladistic analysis

0. Habit. (0) herbaceous, (1) woody at least in the roots and/or rhizomes. 2 steps. CI = .50 RI = .75

1. Growth units. (0) sympodial, (1) monopodial. 2 steps. CI = .50 RI = .66. Whereas growth units of Saruma and Asarum are sympodial, those of Aristolochia, Euglypha, Holostylis, and Thottea are monopodial; some Australian and New Guinean species of subgenus Pararistolochia (e.g. A. deltantha) might have sympodial growth units (Gonzalez, 1999a, b).

2. Elongating shoots. (0) nearly straight (Fig. 2B), (1) strongly sinuous (Fig. 2A). 1 step. CI = 1.00 RI = 1.00

3. Number of axillary buds. (0) one, (1) two or more (see Gonzalez,1999a, b). 2 steps. CI = .50 RI = .66

4. Arrangement of axillary buds. (0) uniseriate, (1) biseriate. 5 steps. CI = .20 RI = .33. When two or more buds occur in the same leaf axil, they are arranged either in one or in two rows (Gonzalez, 1999a, b).

5. Mature stems. (0) circular, (1) medially constricted. 5 steps. CI = .20 RI = .55. Stems in some species of Aristolochia become medially constricted thus producing a "figure 8" form in transverse section.

6. Hooked trichomes. (0) absent, (1) present. 1 steps. CI = 1.00 RI = 1.00

7. Leaf expansion. (0) normal, (1) delayed. 1 step. CI = 1.00 RI = 1.00. In most of the Aristolochiaceae, the leaf primordium begins differentiation into petiole and blade in plastochrone 3-4 and the blade expands relatively

I rapidly (Fig. 2C); in other species the differentiation occurs at a late stage, and blade expansion is delayed (Fig. 2D).

8. Vegetative prophyll. (0) non-pseudostipular (Fig. 2B), (1) pseudostipular (Fig. 2E). 1 step. CI = 1.00 RI = 1.00. In a group of Neotropical species, the prophyll of each renewal shoot develops into a sessile, round, clasping leaf called a pseudostipule (Duchartre, 1854b; Gonzalez, 1990).

9. Petiole abscission zone. (0) absent (Fig. 3C), (1) present (Fig. 3D). 2 steps. CI = .50 RI = .94

10. Petiole base. (0) U-shaped (Fig. 3 A), (1) semicircular (Fig. 3B). 2 steps. CI = .50 RI = .88

11. Position of the partial florescence. (0) along leafy, elongated, main branches, (1) in lateral racemes, (2) along bracteate, terminal portions of the main axis, which usually have shortened internodes (see Gonzalez, 1999b). 2 steps. CI = 1.00 RI = 1.00. It is unclear if partial florescences in Thottea grandiflora are cymose. Thus, we have coded this character as unknown in this species.

12. Partial florescence. (0) uniflowered, (1) bi/multiflowered (see Gonzalez 1999 b). 11 steps. CI = .09 RI = .64. Inflorescence development of Thottea corymbosa and T. grandiflora is unknown, preventing the coding of this and characters 13-19 in these species.

13. Subtending leaves (0) expanded, (1) reduced (Gonzalez, 1999b). 3 steps. CI = .33 RI = .66

14. Flower. (0) bracteate, (1) non-bracteate (see Gonzalez, 1999b). 2 steps. CI = .50 RI = .94

15. Bract expansion. (0) non-clasping, (1) clasping. 5 steps. CI = .20 RI = .71

16. Bract base. (0) non-peltate, (1) peltate. 1 step. CI = 1.00 RI = 1.00

17. Bract shape. (0) similar in shape and size to leaves, (1) reduced. 2 step. CI = .50 RI = .66

18. Inflorescence internodes. (0) elongated, (1) shortened (see Gonzalez, 1999b). 2 steps. CI = .50 RI = .75. Internodes along the main axis of the inflorescences are elongated (> 2 cm); in some species of Aristolochia, the internodes are extremely shortened (< 1 cm).

19. Inflorescence phyllotaxis. (0) distichous, (1) spiral (helicoid; see Gonzalez, 1999b). 3 steps. CI = .33 RI = .80

20. Peduncle abscission zone. (0) absent, (1) present (see Gonzalez, 1999b). 4 steps. CI = .25 RI = .81

21. Perianth series. (0) two, (1) one. 1 step. CI = 1.00 RI = 1.00

22. Perianth shape. (0) rotate, (1) campanulate, (2) tubular. 3 steps. CI = .66 RI = .80

23. Perianth. (0) non-stipitate, (1) stipitate. 4 steps. CI = .25 RI = .50. This character is not applicable to Asarum and Saruma, because the perianth in these genera is continuous with the peduncle. In the other genera, the perianth may have a basal stipe or not (see Gonzalez & Stevenson, 2000a).

24. Perianth base. (0) symmetrical, (1) strongly asymmetrical (see Gonzalez & Stevenson, 2000a). 1 step. CI = 1.00 RI - 1.00

25. Perianth. (0) not differentiated, (1) differentiated into utricle, tube and limb. 1 step. CI = 1.00 RI = 1.00

26. Perianth concavity. (0) absent, (1) adaxial, (2) abaxial. 3 steps. CI = .66 RI = .96. In Aristolochia subgen. Siphisia and subgen. Pararistolochia, and in A. grandiflora the concave side of the flower is formed on the adaxial side of the flower, i.e. away from the median perianth lobe. In the remaining species, the concavity is formed on the abaxial side of the flower (see Gonzalez & Stevenson, 2000a).

27. Perianth abscission zone. (0) absent, (1) present. 1 step. CI = 1.00 RI = 1.00. In all species of Aristolochia and Thottea, a constriction is formed above the ovary that functions as an abscission zone by means of which the perianth and the gynostemium fall off (see Gonzalez & Stevenson, 2000a).

28. Second order perianth veins. (0) present, (1) absent (see Gonzalez & Stevenson, 2000a). 1 step. CI = 1.00 RI = 1.00

29. Syrinx. (0) absent, (1) incomplete, (2) complete. 8 steps. CI = .25 RI = .76. The syrinx is an inner flange formed between the utricle and the tube. This and the characters 30-32 are not applicable to Asarum, Saruma and Thottea, because the flowers in these genera are not differentiated into utricle and tube.

30. Tube position. (0) longitudinal, (1) oblique. 3 steps. CI = .33 RI = .81. At anthesis, the tube extends straight out from the utricle or is oblique to it, thus forming a sharp angle.

31. Tube curvature. (0) strong (U-shaped), (1) slight (see Gonzalez & Stevenson, 2000a). 2 steps. CI = .50 RI = .94. Within Aristolochia subsect. Pentandrae, most of the species have a slightly curved tube; however, A. acontophylla, A. cardiantha, A. foetida, A. micrantha, A. monticola, and A. tresmariae have a U-shaped tube. Therefore this character was coded as polymorphic for this subsection.

32. Tube. (0) distally inflated, (1) not inflated, (2) evenly inflated and almost as wide as the utricle. 3 steps. CI = 66 RI = 94

33. Conical perianth trichomes. (0) absent, (1) present (see Gonzalez & Stevenson, 2000a). 2 steps. CI = .50 RI = .95

34. Annulus. (0) absent, (1) present. 6 steps. CI = .16 RI = .58. The annulus is a circular flange at the flower entrance. One species of subsection Pentandrae (A. secunda) has an annulus, thus we coded this character as polymorphic for this subsection.

35. Limb symmetry. (0) regular, (1) monosymmetric. 3 steps. CI = .33 RI = .89

36. Limb lobes at anthesis. (0) three, (1) one, (2) two, one upper and one lower, (3) two, lateral (see Gonzalez & Stevenson, 2000a). 4 steps. CI = .75 RI = .96

37. Tail-like appendage(s) on perianth. (0) absent, (1) present. 4 steps. CI = .25 RI = .40. In some species oi Aristolochia, the perianth ends in a tail(s). One species of subsection Pentandrae (A. nelsonii) and one of section Dipharus (A. pohliana) have a tail-like appendage, thus, we have coded this character as polymorphic in both taxa.

38. Perianth limb. (0) non fimbriate, (1) fimbriate. 3 steps. CI = .33 RI = .60. Some species of Aristolochia have fimbriae on the limb.

39. Limb protrusion. (0) absent, (1) present (see Gonzalez & Stevenson, 2000a). 1 step. CI = 1.00 RI = 1.00. In a few species of Aristolochia subgen. Siphisia, the limb base has a massive process that projects in front of the flower entrance.

40. Stamen number. (0) 12, (1) 24, (2) 8-10, (3) 6, (4) 5, (5) >25. 6 steps. CI = .83 RI = .85. We have coded 8-10 stamens (and 8-10 gynostemium lobes in character 56) because this range corresponds to the infraspecific variation in most of the species of Aristolochia subgen. Pararistolochia where it occurs (Poney, 1978).

41. Stamen series. (0) two, (1) one. 2 steps. CI = .50 RI = .66

42. Stamens. (0) equidistant, (1) grouped. 2 steps. CI = .50 RI = .94. In some species of Thottea and in Aristolochia subgen. Siphisia, the stamens are grouped. This character is not simply related to the presence of three gynostemium lobes in subgenus Siphisia because in Thottea stamens are grouped even though there is no gynostemium (see Gonzalez & Stevenson, 2000b).

43. Stamens. (0) free, (1) fused forming a gynostemium (see Gonzalez & Stevenson, 2000b). 1 step. CI = 1.00 RI = 1.00

44. Stamen dehiscence. (0) functionally introrse (see Dickison, 1992), (1) extrorse. 1 step. CI = 1.00 RI = 1.00

45. Anthers. (0) with filament, (1) sessile. 1 step. CI = 1.00 RI = 1.00

46. Anther length. (0) less than half the length of the gynostemium, (1) > half the length of the gynostemium. 2 steps. CI = .50 RI = .94

47. Pollen sculpturing. (0) reticulate, (1) microreticulate, (2) fossulate, (3) areolate, (4) psilate (see Gonzalez 1999a). 6 steps. CI = .66 RI = .88

48. Pollen aperture. (0) sulcate, (1) porate, (2) inaperturate. 2 steps. CI = 1.00 RI = 1.00

49. Pollen ridge. (0) absent, (1) poorly differentiated, (2) markedly differentiated (see Gonzalez, 1999a). 3 steps. CI = .66 RI = .87. A long, broad ridge of exine is formed in pollen of all members examined of subgenus Pararistolochia.

50. Supratectal warts. (0) none, (1) small, (2) large (see Gonzalez, 1999a). 4 steps. CI = .50 RI = .66

51. Ovary position. (0) semiinferior, (1) inferior (see Gonzalez & Stevenson, 2000b). 2 steps. CI = .50 RI = 0

52. Ovary shape. (0) globose, (1) elongated and narrow. 1 step. CI = 1.00 RI = 1.00

53. Carpels. (0) partially apocarpous, (1) syncarpous (see Gonzalez & Stevenson, 2000b). 1 step. CI = 1.00 RI = 1.00

54. Mature carpels. (0) 6, (1) 5, (2) 4. 2 steps. CI = 1.00 RI = 1.00. In Thottea only four of the six carpels develop (Gonzalez & Stevenson, 2000b).

55. Stigmas. (0) free, (1) connate (see Gonzalez & Stevenson 2000b). 2 steps. CI = .50 RI = 0. Presence of true stigmas in Thottea is controversial (Leins et al., 1988), so we have coded this and the next character as unknown in this genus.

56. Gynostemium lobes. (0) 6, (1) 5, (2) 3, (3) 8-10, (4) 12. 4 steps. CI = 1.00 RI = 1.00. We have coded this character as partially polymorphic in Aristolochia reticulata and A. serpentaria, based on the number of lobes in mature flowers; however, in both species, only three lobes initiate, and additional lobes in these species occur by secondary division of the three lobes. Holostylis, usually described as having an entire gynostemium, has 6 vestigial lobes (Gonzalez & Stevenson, 2000b) and is here coded as state (0). The number of gynostemium lobes is not simply correlated to the number of stamens; for example, all species of Aristolochia subgen. Siphisia have 6 stamens but only 3 gynostemium lobes; numbers are also different in some species of subgen. Pararistolochia (Poney, 1978), especially in A. goldieana, where there are 12 gynostemium lobes and 24 stamens.

57. Stigmatic papillae. (0) present, (1) absent. 1 step. CI = 1.00 RI = 1.00

58. Position of the stigmatic papillae. (0) terminal, (1) lateral/basal. 3 steps. CI = .33 RI = .92. By the time of anthesis these papillae are either terminal and marginal or lateral/basal with respect to the gynostemium lobes. In Aristolochia, the latter occurs because of a strong outgrowth of the papillate zone, which remains at the base of the gynostemium lobes, giving the impression of a roof-like evagination above the anthers. Aristolochia subsection Diplolobus has traditionally been described as having the latter condition, but this is also present in the species of subgenera Siphisia and Pararistolochia (Gonzalez & Stevenson, 2000b).

59. Fruit surface. (0) smooth, (1) warty. 1 step. CI = 1.00 RI = 1.00

60. Pericarp. (0) membranous to chartaceous, (1) strongly lignified. 1 step. CI = 1.00 RI = 1.00

61. Mesocarp. (0) dry, (1) fleshy. 2 steps. CI = .50 RI = .87

62. Fruit. (0) ventricidal, (1) septifragal, (2) irregularly dehiscent, (3) indehiscent. 5 steps. CI = .40 RI = .89

63. Fruit dehiscence. (0) basipetal, (1) acropetal. 4 steps. CI = .25 RI = .86

64. Fruit septae. (0) entire, (1) lattice-like. 1 step. CI = 1.00 RI = 1.00

65. Seeds per carpel. (0) >5, (1) 1-2. 1 step. CI = 1.00 RI = 1.00

66. Seed contour. (0) concave-convex, (1) flattened, (2) trigonous. 8 steps. CI = .25 RI = .80. In transverse section, the contour of the seed proper appears concave-convex (Fig. 4A, B, D), flattened (Fig. 4C, E-I), or extremely curved and with the margins touching each other (Gonzalez, 1999a; Hou, 1981; Huber, 1985).

67. Shape of the seed proper. (0) ovoid (Fig. 4), (1) ellipsoid. 1 step. CI = 1.00 RI = 1.00

68. Seed wings. (0) absent or vestigial (Figs. 4A-G), (1) two, rectangular (Fig. 41), (2) one, triangular-rhomboidal (Fig. 4H). 4 steps. CI = .50 RI = .81. Vestigial wings sometimes exist, as very short, incomplete, spongy projections peripheral to the seed proper; they do not surround the seed margin completely.

69. Funicle. (0) free from the seed /Fig. 4C, D), (1) fused to the seed (Fig. 4A, B, E-I). 3 steps. CI = .33 RI = .77

70. Funicle. (0) massive (Fig. 4A-D, F), (1) filiform (Fig. 41), (2) papery, incomplete (Fig. 4H), (3) papery, complete (Fig. 4E, G). 10 steps. CI = .30 RI = .69. When the funicle is papery, it can completely cover the adaxial side of the seed (i.e. complete; Fig. 4E) or not (i.e. incomplete; Fig. 4H).

71. Sticky aril. (0) absent, (1) chalazal-funicular, (2) Asarum type, (3) funicular. 4 steps. CI = .75 RI = .50. Whereas in Asarum the aril is formed by 2-4 layers of large cells originating from the funicle (Fig. 4B), in Aristolochia leuconeura and A. odoratissima, the aril consists of excretions from the funicle and the chalaza in the former (Fig. 4F) or from epidermal and subepidermal cells of the whole funicle in the latter (Fig. 4G).

Caption: Apendix 2. Data Matrix, -inapplicable; ?=unknown; A=l,2; B=0,1

Favio A. Gonzalez (1) and Dennis W. Stevenson (2)

(1) Profesor Asociado, Facultad de Ciencias, Universidad Nacional de Colombia, Ap. Ae. 7495, Bogota; fgonzg@ciencias.unal.edu.co.

(2) Director Institute of Systematic Botany and Senior Curator, The New York Botanical Garden, Bronx, New York 10458; dws@nybg.org.

Caption: Figure 1. A-G. Implicit generic relationships in seven different systems of classification of the Aristolochiaceae. H. Published cladogram of the Aristolochiaceae by Weintraub (1995), redrawn.

Caption: Figure 2. Some vegetative characters used in the cladistic analysis. A. Aristolochia ringens (Gonzalez 3584), strongly sinuous elongating shoot (character state 2-1). B. A. leuconeura (Gonzalez 3290), straight elongating shoot (2-0) showing also a non-pseudostipular prophyll (arrowed; 8-0). C. A. ringens (Gonzalez 3584), apical meristem showing plastochrones 2 and 3 (normal leaf expansion; 7-0; bar = 50 mm). D. A. maxima, apical meristem showing plastochrones 2 and 3 (delayed leaf expansion; 7-1; bar = 50 mm). E. A. ringens (Gonzalez 3584), pseudostipule (8-1).

Caption: Figure 3. A, B. Petiole base, frontal view. A. Aristolochia macrophylla (Gonzalez 3578), U-shaped base (character state 10-0; bar = 0.5 mm). B. A. maxima (Gonzalez 3248), semicircular base (10-1 ; bar = 0.5 mm). C, D. Stem-petiole junction, lateral view. C. A. nummularifolia (Gonzalez 1258), petiole without basal abscission zone (9-0; bar = 0.1 mm). D. A. maxima (Gonzalez 3248), petiole with basal abscission zone (arrowed; 9-1; bar = 0.5 mm).

Caption: Figure 4a. Seeds in Aristolochiaceae (from left to right: abaxial side, adaxial side, lateral view, and transverse section through the middle level). A. Saruma henryi (Pruski 3748). B. Asarum virginicum. C. Aristolochia macrophylla (Gonzalez 3578). D. A. paracleto (Gonzalez 3417).

Caption: Figura 4b. E. A. burelae (Marunak et al. 486). F. A. leuconeura (Gonzalez 3290)\ the sticky aril is shown by the dotted area. G. A. odoratissima (Gonzalez 3399); the sticky aril is shown by the dotted area. H. A. contorta (Li 10853). I. A. maxima (Gonzalez 3568). In all, bar = 1 mm; f, funicle; w, wing.

Caption: Figure 5. Consensus tree of the five most parsimonious trees obtained in the present analysis (length = 196, CI = 0.49, RI = 0.85). Character and state numbers for the ingroup are mapped on Figs. 6, 8-10, on which numbers above and below the marks indicate character number and state number, respectively. Larger numbers on the nodes correspond to the Bremer support values. For Figs. 5-10 solid black marks represent apomorphies, and white or grey marks represent homoplasies.

Caption: Figure 6. Clade corresponding to Aristolochia subgen. Siphisia (=Isotrema).

Caption: Figure 7. Clade corresponding to Aristolochia subgen. Pararistolochia + A. subgen. Orthoaristolochia + Euglypha + Holostylis.

Caption: Figure 8. Clade corresponding to Aristolochia subgen. Pararistolochia.

Caption: Figure 9. Clade corresponding to Aristolochia sect. Diplolobus.

Caption: Figure 10. Clade corresponding to Aristolochia sect. Gymnolobus + Euglypha + Holostylis.

Caption: Figure 11. Clades corresponding to the Aristolochia segregates. Segregate Howardia is not monophyletic as Einomeia, Euglypha and Holostylis are nested within it.

Caption: Figure 12. Infrageneric taxa as defined by Duchartre (1854a, 1864) and Schmidt (1935) mapped on the cladogram.

Caption: Figure 13. Infrageneric taxa as defined by Hoehne (1942) mapped on the cladogram.

Caption: Figure 14. Distribution of character states: lateral racemes, reduced pherophylls, and non-bracteate flowers.

Caption: Figure 15. Distribution of character states: monosymmetric, tailed or fimbriate perianth limb.

Caption: Figure 16. Distribution of characters related to seed appendages.
Table 1. Comparison of five different classification
systems of the Aristolochiaceae

Authority      Subfamily (or       Tribe (or         Subtribe
                equivalent)       equivalent)

Klotzsch     Cleistostigmata     Asarineae
(1859)

                                 Bragantieae

                                 Cyclodiscineae

             Aristolochieae

Duchartre    Asareae
(1864)

             Bragantieae

Baldacci
(1894)

             unnamed

Schmidt      Asaroideae          Sarumeae
(1935)
                                 Asareae

                                 Bragantieae

             Aristolochiodeae    Aristolochieae

                                 Euglypheae

Nakai
(1936)

Huber        Asaroideae
(1993)

             Aristolochioideae

                                 Aristolochieae   Isotremantinae

                                                  Aristolochiinae

Authority      Subfamily (or          Genus
                equivalent)

Klotzsch     Cleistostigmata     Asarum
(1859)                           Heterotropa

                                 Bragantia
                                 Thottea

                                 Cyclodiscus

             Aristolochieae      Aristolochia
                                 Endodeca
                                 Einomeia
                                 Howardia
                                 Siphisia

Duchartre    Asareae             Asarum
(1864)                           Saruma

             Bragantieae         Bragantia
                                 Thottea
                                 Aristolochia
                                 Holostylis

Baldacci                         Aristolochia
(1894)                           Asarum
                                 Holostylis
                                 Bragantia

             unnamed             Lobbia
                                 Thottea

Schmidt      Asaroideae          Saruma
(1935)
                                 Asarum

                                 Apama
                                 Thottea

             Aristolochiodeae    Aristolochia
                                 Holostylis

                                 Euglypha

Nakai                            Apama
(1936)                           Aristolochia
                                 Bragantia
                                 Cyclodiscus
                                 Euglypha
                                 Hocquartia
                                 Holostylis
                                 Pararistolochia
                                 Thottea

Huber        Asaroideae          Asarum
(1993)                           Saruma

             Aristolochioideae   Asiphonia
                                 Thottea

                                 Endodeca
                                 Isotrema
                                 Aristolochia

                                 Einomeia
                                 Euglypha
                                 Holostylis
                                 "Howardia "
                                 Pararistolochia

Table 2. Segregate genera from Aristolochia sensu lato

Dumortier        Rafinesque     Klotzsch (1859)     Hutchinson &
(1822)          (1828, 1836)                       Dalziel (1927);
                                                    Poney (1978);
                                                   Parsons, (1996)

Aristolochia    Ambuya         Aristolochia        Aristolochia
Hocquartia      Aristolochia   Einomeia Endodeca
                Dasyphonion                        Pararistolochia
                Dictyanthes    Howardia Siphisia
                Diglosselis
                Einomeia
                Endodeca
                Hexaplectris
                Isiphia
                Isotrema
                Pistolochia
                Plagistra
                Psophiza
                Pteriphis
                Siphisia
                Tropexa

Dumortier        Rafinesque         Huber
(1822)          (1828, 1836)     (1985, 1993)

Aristolochia    Ambuya         Aristolochia
Hocquartia      Aristolochia   Einomeia
                Dasyphonion    Endodeca
                Dictyanthes    Howardia
                Diglosselis    Isotrema
                Einomeia       Pararistolochia
                Endodeca
                Hexaplectris
                Isiphia
                Isotrema
                Pistolochia
                Plagistra
                Psophiza
                Pteriphis
                Siphisia
                Tropexa

Table 3. Systems of classification of Aristolochia by Duchartre
(1854a, 1864), Bentham & Hooker (1880), and Schmidt (1935), and
the corresponding segregates (bold capital letters) by Klotzsch
(1859)

Duchartre (1854a, 1864)             Klotzsch          Bentham &
                                     (1859)         Hooker (1880)

Aristolochia                                      Aristolochia
Group I                                           Sect. Siphisia
 Sect. Asterolytes               ENDODECA
 Sect. Siphisia                  SIPHISIA
 Sect. Hexodon

Group II                                          Sect. Gymnolobus
 Sect. Gymnolobus
  Subsect. Pentandrae            EINOMEIA
  Subsect. Hexandrae             HOWARDIA
   Ser. Unilabiatae
   Ser. Bilabiatae
   Ser. Peltiflorae

 Sect. Diplolobus                ARISTOLOCHIA     Sect. Diplolobus
   Subsect. "Calyx sessile"      Euaristolochia
   Subsect. "Calyx stipitate"    Podanthemum
 Sect. Acerostylis                                Sect. Polyanthera

Duchartre (1854a, 1864)                Schmidt (1935)

Aristolochia                     Aristolochia
Group I                          Subgen. Siphisia
 Sect. Asterolytes                Sect. Asterolytes
 Sect. Siphisia                   Sect. Siphisia
 Sect. Hexodon                    Sect. Hexodon

Group II                         Subgen. Orthoaristolochia
 Sect. Gymnolobus                 Sect. Gymnolobus
  Subsect. Pentandrae              Subsect. Pentandrae
  Subsect. Hexandrae               Subsect. Hexandrae
   Ser. Unilabiatae                 Ser. Unilabiatae
   Ser. Bilabiatae                  Ser. Ecaudata
   Ser. Peltiflorae                 Ser. Alatae
                                    Ser. Bilabiatae
                                    Ser. Peltiflorae

 Sect. Diplolobus                 Sect. Diplolobus
   Subsect. "Calyx sessile"         Subsect. Euaristolochia
   Subsect. "Calyx stipitate"       Subsect. Podanthemum
 Sect. Acerostylis                  Subgen. Pararistolochia

Table 4. Summary of the infrageneric systems of classification
of Aristolochia sensu lato. Taxonomic levels were not
specified by Hoehne (1942)

Authority           Subgenus              Section

Duchartre,      Siphisia            Asterolytes
(1854a,                             Siphisia
1864);                              Hexodon
Schmidt                             Pentodon
(1935); Ma                          Odontosiphisia
(1989, 1992)                        Leptosiphisia
                                    Nepenthesia
                                    Obliquosiphisia
                Orthoaristolochia   Gymnolobus

                                    Diplolobus
                Pararistolochia     Pararistolochioides
                                    Pararistolochia
                                    Aristolochioides
Masters                             Peltiflorae
(1875)
                                    Unilabiatae

                                    Bilabiatae

Hoehne
(1942)

Authority            Subsection           Series         Subseries

Duchartre,
(1854a,
1864);
Schmidt
(1935); Ma
(1989, 1992)

                Hexandrae              Unilabiatae     Adenoracus
                                                       Ancyclanthemum
                                                       Stenanthemum
                                                       Schismotus
                                                       Macrotelus
                                                       Cyphomanthemum
                                                       Pedinochilus
                                                       Cercanthemum
                                                       Brachychilus
                                       Alatae
                                       Bilabiatae
                                       Peltiflorae
                                       unnamed group
                Pentandrae

Masters         'Flores racemose'
(1875)          'Flores solitarii
                vel gemini'
                Caudatae
                Ecaudatae
                'Perianthii labia
                subequilonga'
                Perianthii labium
                superior longisimum'
Hoehne          Pseudostipulosae       Peltiflorae     Macranthae
(1942)                                                 Mediocriflorae
                                                       Parviflorae
                                       Bilabiatae      Parviflorae
                                                       Macranthae
                                                       Caudatae
                                                       Alatae
                                       Caudatae        Trilobatae
                                                       Integrifolia
                Exstipulosae           Volubilis       Subpeltiflorae
                                                       Euunilabiatae
                                                       Hiantiflorae
                                                       Alatilobae
                                                       Ciliatilobae
                                       Fruticulosae

Table 5. Formal classification of the Aristolochiaceae followed
here, based on Duchartre (1854a), Schmidt (1935), Ma (1989) and
Gonzalez (1990, 1991). Species sampled in the cladistic analysis
are listed. Numbers in parenthesis indicate number of species
sampled/approximate number of species.

Subfamily Asaroideae Schmidt
  Tribe Sarumeae Schmidt (1/1)
         Saruma henryi Oliv.
  Tribe Asareae Duchartre (2/100)
         A sarum caudatum Lindl.; A. virginicum L.
  Tribe Bragantieae Schmidt (3/30)
         Thottea corymbosa (Griff.) Ding Hou; T. grandiflora Rottb., T.
         siliquosa (Lamk.)'Ding Hou
Subfamily Aristolochioideae Schmidt
  Tribe Aristolochieae Schmidt
   Holostylis reniformis Duchartre (1/1)
   Aristolochia L.
     Subgenus Siphisia Schmidt
       Section Asterolytes Duchartre (2/2)

         A. reticulata Nutt., A. serpentaria L.
       Section Siphisia (Raf.) Duchartre (13/40)
         A. californica Torr., A. cucurbitifolia Hayata, A. fulvicoma
         Merr. & Chun, A. impudica Ortega, A. macrophylla Lamk.,
         A. malacophylla Standi., A. manshuriensis Komarov, A.
         panamensis Standi., A. paracleta Pfeifer, A. punjabensis
         Craib,
           A. stevensii K. Barringer, A. tomentosa Sims, A. tricaudata
              Lem.
       Section Hexodon Duchartre (1/2)
         A. kaempferi Willd.
       Section Nepenthesia Klotzsch (1/3)
         A. hainanensis Merr.
     Subgenus Orthoaristolochia Schmidt
       Section Gymnolobus
         Subsection Pentandrae Duchartre (33/37)
              A. bracteosa Duchartre, A. brevipes Bentham, A. buntingii
            Pfeifer, A. cardiantha Pfeifer, A. conversiae Pfeifer, A.
            cordata Eastwood, A. coryi Johnst., A. duranguensis Pfeifer,
            A. erecta L., A. flexuosa Duchartre, A.foetida H.B.K., A.
            islandica Pfeifer, A. karwinskii Duchartre, A. micrantha
            Duchartre, A. monticola Brandg., A. mutabilis Pfeifer, A.
            nana
            Watson, A. nelsonii Eastwood, A. oaxacana Eastwood, A.
            palmeri Watson, A. pentandra Jacq., A. porphyrophylla
            Pfeifer, A. pringlei Rose, A. secunda Pfeifer, A. sinaloae
            Brandg., A. socorroensis Pfeifer, A. tequilana Watson, A.
            teretiflora Pfeifer, A. tresmariae Ferris, A. variifolia
            Duchartre, A. versabilifolia Pfeifer, A. watsonii Wooton &
            Standi.,
            A. wrightii Seem.
         Subsection Hexandrae
            Series Thyrsicae F. Gonzalez (4/16)
              A. acutifolia Duchartre, A. maxima Jacq.,.A. melastoma
                Manso, A. trianae Duchartre
         Series Hexandrae
              Subseries Anthocaulicae F. Gonzalez (3/14)
                A. cordiflora Mutis ex H.B.K., A. iquitensis Schmidt,
                leuconeura Linden
            Subseries Hexandrae (28/ca. 100)
          A. arborea Lindl., A. burelae Herz., A. cymbifera Mart.
               & Zucc., A. deltoidea H.B.K., A. didyma S. Moore, A.
               esperanzae O. Kuntze, A. galeata Mart. & Zucc., A.
               gehrtii Hoehne, A. gibertii J.D. Hook., A. grandiflora
               Sw.,
               A. hians Willd., A. inflata H.B.K., A. labiata Willd.,
               A. lindneri Berg., A. lingulata Ule, A. loefgrenii
               Hoehne, A.
               mishuyacensis Schmidt, A. nummularifolia H.B.K., A.
               odoratissima L., A. passifloraefolia A. Rich., A. pilosa
               H.B.K., A. pohliana Duchartre, A. ridicula Brown, A.
               ringens Vahl, A. tigrina A. Rich., A. trilobata L., A.
               warmingii Mast., A. xerophytica Schultes
   Section Diplolobus Duchartre (13/115)
     Subsection Euaristolochia (Klotzsch) Schmidt
        A. clematitis L., A. contorta Bunge, A. pistolochia L., A.
          rotunda L., A. tubiflora Dunn.
     Subsection Podanthemum (Klotzsch) Duchartre
          A. acuminata Lamk., A. bracteolata Lamk., A. debilis Sieb, et
          Zucc., A.foveolata Merrill, A. indica L., A. petersiana
        Kl., A. philippinensis Warb., A. thozetii F. Muller.
     Subgenus Pararistolochia (Hutch. & Dalz.) Schmidt
       Section Pararistolochioides Ma (1/1)
         A. goldieana Hook. f.
     Section Pararistolochia (4/6)
       A. decandra Hou, A. macrocarpa Duchartre, A. promissa Mast., A.
          triactina Hook. f.
     Section Aristolochioides Ma (1/2)
       A. leonensis Mast.
     Unplaced Australasian taxa (2/9-22)
       A. deltantha F. Muell., A. momandul K. Sch.
Tribe Euglypheae Schmidt (1/1)
       Euglypha rojasiana Chod. & Hassl.
COPYRIGHT 2002 Academia Colombiana de Ciencias Exactas, Fisicas y Naturales
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2002 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Botanica
Author:Gonzalez, Favio A.; Stevenson, Dennis W.
Publication:Revista de la Academia Colombiana de Ciencias Exactas, Fisicas y Naturales
Date:Mar 1, 2002
Words:13912
Previous Article:Las especies de la sect. Lappagopsis del genero neotropical Axonopus (Poaceae, Panicoideae, Paniceae).
Next Article:Las gramineas en Colombia.
Topics:

Terms of use | Privacy policy | Copyright © 2018 Farlex, Inc. | Feedback | For webmasters