The Questionable Affinities of Lactoris: Evidence from Branching Pattern, Inflorescence Morphology, and Stipule Development

by Favio González, Paula Rudall
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Title:
The Questionable Affinities of Lactoris: Evidence from Branching Pattern, Inflorescence Morphology, and Stipule Development
Author:
Favio González, Paula Rudall
Year: 
2001
Publication: 
American Journal of Botany
Volume: 
88
Issue: 
12
Start Page: 
2143
End Page: 
2150
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Language: 
English
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Abstract:

American Journal of Botany 88(12): 2143-2150. 2001.

THE QUESTIONABLE AFFINITIES OF LACTORIS: EVIDENCE FROM BRANCHING PATTERN, INFLORESCENCE MORPHOLOGY, AND STIPULE DEVELOPMENT^
FAVIO GONZALEZ~,~ AND PAULA RUDALL~

>Institute de Ciencias Naturales, Universidad Nacional, Ap. Ae. 7495, BogotB, Colombia; and 3Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK

The phylogenetically ambivalent monotypic genus Lactoris presents sympodial (determinate) branching, as a terminal flower is present on each main branch. The synflorescence is thyrsoid. Partial inflorescences are rhipidia with up to three flowers. The ochrealike stipule is formed by the fusion of two lateral stipules, which forms an adaxial ligule-like structure and a two-flanked leaf sheath that encircles the parental axis. The leaf sheath elongates with the growth of the preceding internode. Although sympodial growth and a sheathing leaf base are present in all Piperales (Aristolochiaceae, Lactoridaceae, Piperaceae, and Saumraceae), the presence of stipules is confined to Lactoris, Saumraceae, and some Piperaceae. These characters are consistent with the placement of Lactoris within Piperales, although its phylogenetic position within the order remains equivocal, except for the possible sister group relationship suggested by the presence of cymose inflorescences in both Lactoris and Aristolochiaceae.

Key words: Aristolochiaceae; Chloranthaceae; cymes; Lactoris; leaf ontogeny; magnoliids; monocotyledons; Piperaceae; Piper-

ales; sympodial growth.

Lactoris fernandeziana Phil., the sole species of the family Lactoridaceae Engler, is known only from a few remaining endemic populations on Masatien-a Island in the Juan Fernan- dez archipelago, Chile. Luctoris has been the subject of several recent studies because of its uncertain systematic placement among basal angiosperms (for review, see Stuessy et al., 1998). It belongs in the magnoliid clade, which includes Pi- perales, Magnoliales, Laurales, Winterales, and possibly Chlor- anthaceae and monocotyledons, although the relationships of these taxa are still unresolved (APG, 1998; Qiu et al., 2000; Soltis et al., 2000). Morphological treatments have variously linked Lactoris with Magnoliales (Cronquist, 1981; Lammers, Stuessy, and Silva, 1986), Laurales (Takhtajan, 1980; also An- nonales suborder Laurineae; Thorne, 1974), or Piperales (Sau- ruraceae and Piperaceae; e.g., Bentham and Hooker, 1880; Hallier, 1903; McLaughlin, 1933; Meeuse, 1972; Burger, 1977; Carlquist, 1990). Recent molecular data place it firmly in Piperales, together with Aristolochiaceae, Piperaceae, and Saururaceae (e.g., Qiu et al., 1999, 2000), although relation- ships with other magnoliids (including monocotyledons and Chloranthaceae) remain equivocal. More controversially, how- ever, molecular data have indicated a close relationship be- tween Aristolochiaceae and Lactoridaceae, placing Lactoris as sister to (e.g., Neinhuis, Borsch, and Hilu, 1999) or even nest- ed within (e.g., Qiu et al., 1999, 2000) Aristolochiaceae.

Many investigations have sought additional data to explore these putative relationships. These include studies on vegeta- tive anatomy (McLaughlin, 1933; Lemesle, 1953; Carlquist, 1990), ultrastructure (Behnke, 1988; Hennig et al., 1994), flo- ral development and morphology (Tucker and Douglas, 1996), reproductive biology (Skottsberg, 1928; Bernardello et al.,

' received March 2001; 26 June 2001'

The authors thank Hiroshi Tobe for providing fixed material of Lactoris. FG gratefully acknowledges the Latin American Fellowship Reseuch Programme and the ~ ~~ ~ i ~~ ~ for~~ ~ l i

university,colombia,~ supporting his ~ostdoctoral visit to the Jodrell Laboratory. Roval Botanic Gardens. Kew,

.

where this research was conducted. < Author for reprint requests: (e-mail: fgonzg@ciencias.unal.edu.co).

1999), pollen morphology including fossil pollen (Erdtman, 1952; Carlquist, 1964; Zavada and Taylor, 1986; Zavada and Benson, 1987; Sampson, 1995; Macphail, Partridge, and Tru- swell, 1999; GonzBlez, Rudall, and Furness, in press), embry- ology and karyomorphology (Bouman, 1971; Tobe et al., 1993), gynoecium and fruit development (Meeuse, 1971; Me- likian and Brobov, 1999), allozyme and DNA variation (Brau- ner, Crawford, and Stuessy, 1992; Crawford et al., 1994), and phytochemistry (Crawford, Stuessy, and Silva, 1986). How- ever, two morphological traits of Lactoris that have been over- looked for detailed investigation are the branching pattern (in- cluding the position of the flower/inflorescence) and stipule development, the latter briefly commented on by Weberling (1970). These characters have been variously scored for Lac- toridaceae in several cladistic analyses (e.g., Dahlgren and Bremer, 1985; Donoghue and Doyle, 1989; Loconte and Ste- venson, 1991; Stevenson and Loconte, 1995; Tucker and Douglas, 1996). This paper describes inflorescence structure and stipule development in Lactoridaceae and compares them with those of other Piperales (Piperaceae, Saururaceae, and Aristolochiaceae), in the context of systematic relationships within the order.

MATERIALS AND METHODS

Vegetative and flowering branches were obtained from living specimens of the following taxa cultivated at the Royal Botanic Gardens, Kew: Aristolo- chiaceae: Aristolochia elegans Mast. (Kew accession number 000-73.20205), Asarum europeum L. (1969-18007), Saruma henryi Oliv. (1994-1441); Sau- ruraceae: Houttuynia cordata Thunb. (1954-31701), Saururus cernuus L. (1952- 18204); and Lactoridaceae: Lactoris fernandeziana Phil. (199 1-10). Additional fixed material of Lactoris fernandeziana (Stuessy et al. 11178) and Chloranthus erectus (Rudall 91, Irian Jaya) was also examined.

Material was fixed in formalin acetic alcohol (FAA) and stored in 70% ethanol, For scanning electron microscope examination, apical meri-

stems and axillary buds were carefully dissected in 90% ethanol, then dehy- drated in an absolute ethanol : acetone series (90% ethanol. 30 min; absolute

,

ethanol, 30 min; absolute ethanol : acetone in proportions 50 : 50, 10 min; and finally two steps of acetone, 10 min each). Dehydrated material was then critical-point-dried using a Balzer CPD 020 (Balzer Union, Furstentum, Liech-

2148 AMERICANJOURNALOF BOTANY [Vol. 88

by a cross meristem ("Transversalwulst") as in many mag- noliids and monocots (reviewed by Rudall and Buzgo, in press), but rather a structure formed by the fusion of two lat- eral stipules. This conclusion is further supported by the bifid or bilobed apex of the so-called ligule at maturity. This inter- pretation is in agreement with Carlquist (1964), who described the "wings" as "extensions of [the] stipules." It contradicts Lemesle's (1955) statement that stipules of Lactoris "are com- pletely independent from the leaf base but fused to it."

Stipules are lateral appendages of the leaf base. They are present in at least some Saururaceae (Saururus in Figs. 1516; Houttuynia in Fig. 18), some Piperaceae, and some other magnoliids, including Magnoliaceae. In Chloranthus, the leaf base resembles that of Saururaceae, but the leaves are opposite rather than alternate, and the sheath is formed by two fused opposing leaf bases (Figs. 19 and 20). The stipules in Chloranthus are modified, but there is a ligular projection between them. There is striking similarity in stipule morphology and development between Lactoris and members of the families Piperaceae and Saururaceae (see also Gliick, 1919; Roth, 1949; Weberling, 1970), demonstrated by Roth's (1949) illus- tration of Houttuynia. This observation contradicts Carlquist's (1964) view that the stipules of Luctoris are probably not in- dicative of relationship with other stipulate plants. Stipules in Piperaceae and Saururaceae form a ligule-like structure on the adaxial side of the leaf base (i.e., the vaginal lobe, the ochrea- like stipule, or the intrapetiolar stipule of some authors) and a sheath that fuses on the opposite side of the leaf (Fig. 17; see also Ponzo, 1934; Bharathan, 1996). At least in Saururaceae, the ligule-like structure is bifid at the apex (Fig. 18), which indicates that it is formed from the fusion of two lateral stipule primordia, as in Lactoris. On the other hand, in all members of Aristolochiaceae the leaf base is sheathing but stipules are entirely lacking (Figs. 21-23), presumably representing a re- versal for the family. Stipules are relatively rare in monocots, but although it is commonly believed that dicot stipules and monocot ligules have different development origins, there is some evidence from ontogeny (e.g., Roth, 1949) and devel- opmental genetics (Mooney and Freeling, 1997) that this is not the case. The morphology of the leaf tip in Lactoris (Figs. 8, 10) is worth noting in this context, as it closely resembles the precursor tip ("Vorlauferspitze") of many monocotyle- dons, and may be homologous with the upper leaf zone ("Ob- erblatt") (reviewed by Rudall and Buzgo, in press).

ZnJlorescences-Partial inflorescences in Lactoris are not racemose but cymose; when two or more flowers are pro- duced, they are not axillary but organized in monochasia, as Skottsberg (1928) and Bernardello et al. (1999) also observed. Cymose partial inflorescences (rhipidia) are therefore possibly synapomorphic for Lactoris and the Aristolochiaceae. Inflo- rescences of Lactoris have previously been described in vari- ous ways. Engler (1887) and Skottsberg (1928) noted the for- mation of 1-4 flowered axillary monochasia. Bentham and Hooker (1880), Mufioz-Pizarro (1966), and Lammers, Stuessy, and Silva (1986) described the presence of solitary flowers, but they also observed that two or three flowers can occur together. Kubitzki (1993) stated that "what is called inflores- cence is a raceme-like structure that represents a brachyblast producing 1 to 4 leaves each with one axillary flower." Ste- venson and Loconte (1995) and Tucker and Douglas (1996) both coded solitary flowers for Lactoris. Despite this, both their analyses have the cyme as an alternative character state.

Tucker and Douglas (1996) mentioned that the position of the inflorescence is axillary and that each flower is in the axil of a bract, but that basal bracts of the inflorescence are absent. Stuessy et al. (1998) accordingly interpreted inflorescences in Lactoris as raceme-like structures, with single flowers sub- tended by leaves. However, our observations show that the inflorescences occupy the terminal portions as well as the axils of the branches, that the flowers are opposite to bracts, and that there is a basal bract (a prophyll) on each partial inflo- rescence. Saururaceae and most Piperaceae also have terminal inflorescences and sympodial growth.

Doyle and Endress (2000) stated that prophylls in Lactoris are paired and lateral and that rhipidia in Annonaceae and Aristolochiaceae are "assumed to be derived from solitary." Our data indicate the opposite, i.e., that there is a single, ad- axial prophyll in Lactoris and that rhipidia (or cymes of any kind) are plesiomorphic in Aristolochiaceae and Lactorida- ceae, or at least in Aristolochiaceae.

Relationships within magnoliids-A placement for Lactoris within the order Piperales seems highly likely; both mo- lecular evidence (e.g., Qiu et al., 1999, 2000) and several mor- phological characters, including presence of stipules and sym- podia1 growth, are consistent with this position. In a series of insightful papers on comparative wood anatomy in magnoliids, Carlquist (1990, 1992, 1993) and Carlquist, Dauer, and Nish- irnra (1995) demonstrated a potential suite of synapomorphies for Piperales (Lactoris, Piperaceae, Saururaceae, and Aristo- lochiaceae), including simple perforations, fiber-tracheids, scanty vasicentric axial parenchyma, and predominantly up- right ray cells. Many of these characters are also shared with Chloranthaceae. Wood anatomy of Lactoridaceae is "virtually identical to that of Piperaceae" (Carlquist, 1990: 1499). With- in Saururaceae, vascular cambial activity is at best vestigial in Saururus and Houttuynia (as in monocotyledons), but in Anemopsis wood anatomy is highly comparable with that of other Piperales. Igersheim and Endress (1998) noted that "special similarities with monocots are more prominent in the Aristo- lochiales [i.e., Aristolochiaceae and Lactoris] than in other pa- leoherbs," citing trimerous flowers as an example. This state- ment is also true for other Piperales (Saururaceae and Piper- aceae), and relationships between the four families of Piperales and other magnoliids, especially monocots and Chlorantha- ceae, require further exploration.

Relationships within Piperales-Although combined anal- yses of molecular data (e.g., Graham and Olmstead, 2000; Qiu et al., 2000) have indicated the monophyly of the order Pi- perales, the phylogenetic position of Lactoris within Piperales remains equivocal from both the standpoint of molecular and morphological data.

Duvall (2000) assessed phylogenetic placements of Lactoris using analyses of molecular data from different gene loci. He found that placements varied with different loci, from sister to Piperales, sister to Aristolochiaceae, to being nested within Aristolochiaceae (sister to Aristolochia). Graham and Olm- stead (2000) presented an analysis of basal angiosperms using 17 chloroplast genes but with limited taxon sampling: Piper- ales were represented by only Asarum (Aristolochiaceae),Lactoris, and Saururus. They found that a combined analysis of sequence, indel, and intron data from all 17 chloroplast genes resolved Lactoris and Saururus as sister taxa with 89% boot- strap support. In contrast, their combined analysis using only

December 20011 GONZALEZAND RUDALL-VEGETATIVEMORPHOLOGY OF LACTORIS 2149

data from atpB, ndhF and rbcL genes, resolved Asarum and Lactoris as a sister pair with 74% bootstrap support. Lactoris occupies a long branch with respect to both number of sub- stitutions and number of indel events, indicating that its po- sition is still uncertain, in common with the somewhat incon- sistent placements of several other basal angiosperms, includ- ing Chloranthus, Ceratophyllum, and even Acorus. On the oth- er hand, the combined five-gene analyses of Qiu et al. (1999, 2000), which included three other genera of Aristolochiaceae (Aristolochia, Saruma, and Thottea), placed Lactoris as sister to Aristolochia plus Thottea, and these three genera as sister to Asarum plus Saruma. All these genera were in turn sister to Piperaceae plus Saururaceae.

Endress (1994) listed several morphological characters in favor of a close relationship between Lactoridaceae and Ar- istolochiaceae: presence of tepals, anthers strongly extrorse with a broad connective and almost sessile, stamens basally fused with the gynoecium, placenta linear, ovules anatropous, inflorescences with few, noncondensed flowers, one adaxial prophyll per flower, and pollen monosulcate. However, most of these characters are symplesiomorphies of the whole order Piperales, and therefore not indicative of relationships within the order. For example, adaxial prophylls and monosulcate pol- len are commonly present in other Piperales, including Piper- aceae and Saururaceae, and indeed in many other magnoliids. Linear placentae and anatropous ovules are also common in other magnoliids. Furthermore, although in Aristolochia stamens are basally fused with the gynoecium in Saruma, Asa- rum, and Thottea, which represent the probable basalmost clades of Aristolochiaceae (Gonzilez, 1999a), stamens are en- tirely free from the gynoecium. In contrast, in some Saurura- ceae stamens are fused with the gynoecium.

Perhaps the best morphological evidence for a sister group relationship between Lactoridaceae and Aristolochiaceae is the cymose inflorescence; otherwise, there are few consistent mor- phological synapomorphies between these taxa. A trimerous perianth links Lactoridaceae and Aristolochiaceae but is also found in monocotyledons. On the other hand, there are also strong links between Lactoridaceae and Saururaceae; for ex- ample, both Houttuynia and Lactoris have tenuinucellate ovules (Igersheim and Endress, 1998; E Gonzilez and F? J. Rudall, unpublished data), a condition that is rare in other magnoliids. Development and morphology of stipules link Lactoris with Piperaceae and Saururaceae, although presence of stipules may be symplesiomorphic, with absence of stipules in Aristolochiaceae as a derived condition. No single character

u

can independently test relationships. A revised morphological cladistic analysis, possibly combined with molecular data, may help to resolve this conundrum. This requires more compara- tive data on other taxa and will be the subject of future in- vestigation.

LITERATURE CITED

APG [ANGIOSPERM GROUP]. 1998. An ordinal classification for

PHYLOGENY the families of flowering plants. Annals ofthe Missouri Botanical Garden

85: 531-553. BEHNKE, H. D. 1988. Sieve-element plastids, phloem protein, and evolution of flowering plants. 111. Magnoliidae. Taxon 37: 699-732. BENTHAM, G., AND J. D. HOOKER. 1880. Genera Plantarum. Reeve and Co., London, UK.

BERNARDELLO,G., G. J. ANDERSON, P. LOPEZ, M. A. CLELAND, T. E STUESSY,AND D. J. CRAWFORD. 1999. Reproductive biology of Lactoris fer- nandeziana (Lactoridaceae). American Journal of Botany 86: 829-840.

BHARATHAN,

G. 1996. Does the monocot mode of leaf development char- acterize all monocots? Aliso 14: 271-279. BOUMAN,E 1971. Integumentary studies in the Polycarpicae 1. Lactorida-

ceae. Acta Botanica Neerlandica 20: 565-569. BRAUNER,S., D. J. CRAWFORD,

AND T. E STUESSY. 1992. Ribosomal DNA and RAPD variation in the rxe plant family Lactoridaceae. American Journal of Botany 79: 1436-1439.

BURGER,W. C. 1977. The Piperales and the monocots. Alternative hypotheses for the origin of monocotyledoneous flowers. Botanical Revie~j 43: 346-

393. CARLQUIST,S. 1964. Morphology and relationships of Lactoridaceae. Aliso

5: 421-435. CARLQUIST,S. 1990. Wood anatomy and relationships of Lactoridaceae. American Journal of Botany 77: 1498-1505.

CARLQUIST,S. 1992. Wood anatomy and stem of Chloranthus; summary of wood anatomy of Chloranthaceae, with comments on relationships, ves- sellessness, and the origin of monocotyledons. IAWA Bulletin 13: 3-16.

CARLQUIST,

S. 1993. Wood and bark anatomy of Aristolochiaceae; systematic and habital correlations. IAWA Journal 14: 341-357.

CARLQUIST,S., K. DAUER,AND S. Y. NISHIMRA. 1995. Wood and stem anat- omy of Saururaceae with reference to ecology, phylogeny, and origin of the monocotyledons. IAWA Journal 16: 133-150.

CRAWFORD,D. J., T. E STUESSY,M. B. COSNER,D. HAINES, D. WIENS, AND

P. PENALILLO.1994. Lactoris fernandeziana (Lactoridaceae) on the Juan Fernandez Islands: allozyme uniformity and field observations. Conservation Biology 8: 277-280.

CRAWFORD, AND M. SILVA. 1986. Leaf flavonoid chem-

D. J., T. E STUESSY, istry and the relationships of the Lactoridaceae. Plant Systematics and Evolution 153: 133-139.

CRONQUIST,A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York, New York, USA. DAHLGREN,R., AND K. BREMER. 1985. Major clades of the angiosperms. Cladistics 1: 349-368.

DONOGHUE,M. J., AND J. A. DOYLE. 1989. Phylogenetic analysis of angio- sperms and the relationships of Hamamelidae. In P. R. Crane and S. Blackmore [eds.], Evolution, systematics, and fossil history of the Ha- mamelidae, vol. l, 17-45. Clarendon Press, Oxford, UK.

DOYLE,J. A., AND P. K. ENDRESS. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Ztzternational Journal of plant Sciences 161(6 Supplement): S121-S153.

DUVALL,M. R. 2000. Seeking the dicot sister group of the monocots. In K.

L. Wilson and D. A. Morrison [eds.], Monocots: systematics and evo- lution, 25-32. CSIRO, Melbourne, Australia. ENDRESS,l? K. 1994. Floral structure and evolution of primitive angiosperms: recent advances. Plant Systematics and Evolution 192: 79-97. ENGLER,A. 1887. ~ber die Familie der Lactoridaceae. Botanische Jahrbiich- er fur Systematik 8: 53-56.

ERDTMAN,G. 1952. Ein Beitrag zur Kenntnis der Pollen-morphologie von Lactoris fernandeziana und Drymis winteri. Grana Palynologica 5: 33-

39. GLUCK,H. 1919. Blatt- und bliittenmorphologische Studien. G. Fischer, Jena, Germany.

GONZALEZ,E 1999a. A phylogenetic analysis of the Aristolochioideae (Ar- istolochiaceae). Ph.D. dissertation, City University of New York, New York, New York, USA.

GONZALEZ,E 1999b. Inflorescence morphology and the systematics of Ar- istolochiaceae. Systematics and Geography of Plants 68: 159-172.

GONZALEZ,E, P. J. RUDALL, AND C. A. FURNESS. In press. Microsporogen- esis and systematics of Aristolochiaceae. Botanical Jonrnal of the Lin- nean Society.

GRAHAM,S. W., AXD R. G. OLMSTEAD. 2000. Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. American Journal of Botany 87: 1712-1730.

HALLIER, H. 1903. Beitrage zur Morphologie der Sporophylle und des Tro- phophylls in Beziehung zur Phylogenie der Kormophyten. Jahrbuch der Hamburgischen Wissenschaftliclzen Anstalten 19: 1-1 10.

HENNIG,S., W. BARTHLOTT, I. MEUSEL, AND I. THEISEN. 1994. Mikromor- phologie der Epicuticularwachse und die Systematik der Magnoliidae, Ranunculidae und Hamamelididae. Tropische und subtropische Pjan- zenwelt 90: 1-60.

IGERSHEIM,A,, AND P. K. ENDRESS. 1998. Gynoecium diversity and system- atics of the palaeoherbs. Botanical Journal of the Linnean Society 127: 289-370.

2150 AMERICANJOURNALOF BOTANY [Vol. 88

KUBITZKI,K. 1993. Lactoridaceae. In K. Kubitzki, J. C. Rower, and V. Bit- trich [eds.], The families and genera of flowering plants, vol. 2, 359-

361. Springer Verlag, Berlin, Germany.

LAMMERS,T., T. E STUESSY,AND M. SILVA. 1986. Systematic relationships of the Lactoridaceae, an endemic family of the Juan Fernandez Islands, Chile. Plant Systematics and Evolution 152: 243-266.

LEMESLE,R. 1953. Nature des tltments sclertnchymateux de la tige du Lactoris fernandeziana Philippi. Revue Ginirale de Botanique 60: 15-22.

LEMESLE, R. 1955. Contribution a l'ttude de quelques families de dicotyle- dones consid6rtes comme primitives. Phytomorphology 5: 11-45. LOCONTE, H., AND D. W. STEVENSON. 1991. Cladistics of the Magnoliidae.

Cladistics 7: 267-296. MACPHAIL, M. K., A. D. PARTRIDGE, 1999. Fossil

AND E. M. TRUSWELL. pollen records of the problematical primitive angiosperm family Lacto- ridaceae in Australia. Plant Systematics and Evolution 214: 199-210.

MCLAUGHLIN,R. l? 1933. Systematic anatomy of the woods of the Magno- liales. Tropical Woods 34: 3-39.

MEEUSE, A. D. J. 1971. Interpretative gynoecial morphology of the Lacto- ridaceae and the Winteraceae: a re-assessment. Acta Botanica Neerlan- dica 20: 221-238.

MEEUSE, A. D. J. 1972. Taxonomic affinities between Piperales and Poly- carpicae and their implications in interpretative floral morphology. Advances in Plant Morphology 1972: 3-27.

MELIKIAN,A. l?, AND A. V. E CH. BROBOV. 1999. Carp010gy of Lactorida- ceae. Abstracts XVI. Abstract number 4871. International Botanical Con- gress, St. Louis, Missouri, USA.

MOONEY,M., AND M. FREELING. 1997. Using regulatory genes to investigate the evolution of leaf form. Maydica 42: 173-184. MUROZ-PIZARRO,

C. 1966.
Sinopsis de la Flora Chilena. Ediciones de la Universidad de Chile, Santiago, Chile.

NEINHUIS.C., T. BORSCH, AND K. W. HILU. 1999. Phylogenetic relationships within Aristolochiaceae based on TRNT-TRNF sequences. Abstracts

XVI. Abstract number 351. International Botanical Congress, St. Louis,

Missouri, USA. Po~zo, A. 1934. Stipule e guaina. Nuovo Giornale Botanico Italiano, n.s.

41: 1-21. QIU, Y-L., J. LEE, E BERNASCONI-QUADRONI,

D. E. SOLTIS, l? S. SOLTIS, M. ZANIS, E. A. ZIMMER, Z. CHEN, V. SAVOLAINEN,

AND M. W. CHASE. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404-407.

QIU, Y-L., J. LEE, E BERNASCONI-QUADRONI,

D. E. SOLTIS, l? S. SOLTIS, M. ZANIS,E. A. ZIMMER, Z. CHEN, V. SAVOLAINEN,

AND M. W. CHASE. 2000. Phylogeny of basal angiosperms: analyses of five genes from three genomes. International Journal of Plant Sciences 16l(Supplement): S3- S27.

ROTH, I. 1949. Zur Entwicklungsgeschichte des Blattes, mit besonderer Be- riicksichtigung von Stipular- und Ligularbildungen. Planta 37: 299-336.

RUDALL,l? J., AND M. BUZGO. In press. The evolutionary history of the monocot leaf. In Q. Cronk, R. M. Bateman, and J. Hawkins [eds.], De- velopmental genetics and plant evolution. Taylor and Francis, London, IJK.

SAMPSON,E B. 1995. Pollen morphology of Lactoridaceae-a re-examination. Grana 34: 100-107.

SKOTTSBERG,C. 1928. Pollinationsbiologie und Samenverbreitung auf den Juan Fernandez-Inseln. In C. Skottsberg [ed.], The natural history of the Juan Fernandez and Easter Island, vol. 2, 503-547. Almwuist and Wis- kell, Uppsala, Sweden.

SOLTIS, D. E., ET AL. 2000. Angiosperm phylogeny inferred from 18s rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133: 381-461.

STEVENSON, 1995. Cladistic analysis of the mono-

D. W., AND H. LOCONTE. cot families. In P J. Rudall, l? J. Cribb, D. E Cutler, and C. J. Humphries [eds.], Monocotyledons: systematics and evolution, vol. 2, 543-578. Royal Botanic Gardens, Kew, UK.

STUESSY,T. E, D. J. CRAWFORD, G. J. ANDERSON,AND R. J. JENNER. 1998. Systematics, biogeography and conservation of Lactoridaceae. Perspectives in Plant Evolution and Systemarics 1-2: 267-290.

TAKHTAJAN,

A. L. 1969. Flowering plants: origin and dispersal. Smithsonian Institution Press, Washington D.C., USA. TAKHTAIAN,A. L. 1980. Outline of the classification of flowering plants

(Magnoliophyta). Botanical Review 46: 225-359. THORNE, R. E 1974. A phylogenetic classification of the Annoniflorae. Aliso

8: 147-209.

TOBE, H., T. E STUESSY,l? H. RAVEN,AND K. OGINUMA. 1993. Embryology and karyomorphology of Lactoridaceae. American Journal of Botany 80: 933-946. TUCKER, S., AND A. W. DOUGLAS. 1996. Floral structure, development, and relationships of paleoherbs: Sarurna,Cabonzba,Lactoris,and selected Pi- perales. In D. W. Taylor and L. J. Hickey [eds.], Flowering plant origin. evolution and phylogeny, 141-175. Chapman and Hall, New York, New York, USA. WEBERLING,E 1970. Weitere Untersuchungen zur Morphologie des Unter- blattes bei den Dikotylen. V. Piperales. Beitrage zur Biologie der Pflan- zen 46: 403-434. WEBERLING,E 1989. Morphology of flowers and inflorescences. (Translated by R. J. Pankhurst). Cambridge University Press, New York, New York, USA.

ZAVADA,M. S.. AND J. M. BENSON. 1987. First fossil evidence for the prim- itive angiosperm family Lactoridaceae. American Journal of Botany 74: 1590-1594.

ZAVADA,M. S., AND T. N. TAYLOR. 1986. Pollen morphology of Lactori- daceae. Plant Systematics and Evolution 154: 31-39.

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