LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

PIPERALES Dumortier  Main Tree, Synapomorphies.

Plant herbaceous, growth sympodial; sesquiterpenes [e.g. gamma-elemene] +; starch grains compound; primary stem with distinct bundles; vessel elements in radial files, with simple perforation plates; wood with broad rays; nodes often swollen; stomata not paracytic; leaves two-ranked, lamina with 2ndary veins palmate; A in 3's; G occlusion?; seed ± tegmic, endotegmen tanniniferous; PHYE gene absent. - 4 families, 17 genera, 4090 species.

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 201 and 128 and 175 and 119 million years for relaxed and constrained penalized likelihood datings for stem and crown group Piperales respectively - but note topology. For an Early Cretaceous fossil showing some similarities with this group, see Friis et al. (1995).

Floral Biology. There are a number of reports of delayed fertilisation in Piperales, including in some Piperaceae (Sogo & Tobe 2006d for references).

Chemistry, Morphology, etc. Carlquist et al. (1995) suggest a number of wood anatomical characters that may be common to this clade, thus wood both in some Aristolochiaceae and Piperaceae is storied (Carlquist 1992a). There is extensive variation in the differentiation of the embryo in Piperaceae, and the polarity of evolution of this feature is unclear, as is that of micropylar morphology, etc. Variation in embryo sac morphology in the whole clade is also very considerable, but there are now attempts to put this in a phylogenetic context (e.g. Madrid & Friedman 2008a, 2008b, 2009).

For floral development, see Tucker and Douglas (1996).

Phylogeny. Relationships around Aristolochiaceae are unclear, although the pairing [Piperaceae + Saururaceae] is often strongly supported (e.g. Neinhuis et al. 2001, Nickrent et al. 2001). Neinhuis et al. (2000) suggested that Lactoridaceae were not to be included in Aristolochiaceae, although subsequent analyses have tended in the opposite direction (e.g. Neinhuis et al. 2005: weak support for inclusion of Lactoridaceae in Aristolochiaceae as sister to Aristolochioideae). Similar relationships were found by Davis et al. (2004: support rather weak - ±70%, Hydnoraceae not included). In the two-gene analysis of Wanke et al. (2007: Hydnoraceae again not included) support for Lactoridaceae as sister to Aristolochioideae was quite strong (82% bootstrap: see also Borsch et al. 2005; Qiu et al. 2005; Soltis et al. 2007a), however, the position of Asaroideae was uncertain; it might be sister to [Lactoridaceae + Aristolochioideae] (most common) or to [Piperaceae + Saururaceae]; Hilu et al. (2003: matK analysis alone) also thought that Aristolochiaceae were paraphyletic and included the rest of the order (Hydnoraceae were not sampled). Relationships of the parasitic Hydnoraceae are uncertain, although they go in this general area (e.g. Barkman et al. 2007). An association along these lines is suggested by Nickrent and Duff (1996), Blarer et al. (2000) and Nickrent et al. (2001, 2002), while Nickrent and Blarer (2005) found moderate support for the clade [Hydnoraceae + Aristolochioideae].

Previous Relationships. Takhtajan (1997) placed Aristolochiales in Magnolianae, his Lactoridanae were monotypic, although placed immediately after Laurales and before Aristolochiales. In some floral details, Saururaceae are very like Acoraceae (Buzgo & Endress 2000), e.g. they both have monosymmetric flowers, but these probably represent convergences. Similarly, the three-merous perianth and adaxial prophylls that seem to suggest a relationship between Piperales and monocots (and Nymphaeales), the now unlikely paleoherb hypothesis (for which see e.g. Donoghue & Doyle 1987), also represent parallelisms.

Includes Aristolochiaceae, Hydnoraceae, Piperaceae, Saururaceae.

Synonymy: Aristolochiales Berchtold & Presl, Asarales Horaninow, Hydnorales Reveal, Lactoridales Reveal, Saururales Martius - Piperineae Shipunov - Aristolochianae Doweld, Lactoridanae Reveal & Doweld, Piperanae Reveal - Piperidae Reveal - Aristolochiopsida Bartling, Asaropsida Horaninov, Piperopsida Bartling

[Hydnoraceae + Aristolochiaceae]: P uniseriate, 3, connate, outer whorl valvate; anthers extrorse, filaments ± 0; ovary inferior; embryo undifferentiated.

Although these taxa may form a clade, relationships between them are unclear (Nickrent et al. 2002). The connate, valvate perianth, extrorse anthers, successive microsporogenesis, and inferior ovary of Hydnoraceae all suggest a close relationship with Aristolochiaceae, although some of the characters are plesiomorphies and ovary position is clearly very labile around here.

HYDNORACEAE C. Agardh   Back to Piperales

Root parasites, echlorophyllous; starch grains?; sieve tube plastids without starch or protein inclusions, mucilage cells +; stomata?, cuticle wax crystalloids 0; leaves 0; flowers arising endogenously from roots, 3-4(-5)-merous, large; P very thick and fleshy, stamens = adnate to and opposite P, laterally connate, (also adaxially, forming solid body - Prosopanche), polythecate; pollen (extruded in threads), variously sulcate or trichotomocolpate, ektexine homogeneous, (staminodes alternating with P, below A); G alternating with P, placentation of parietal or apical lamellae, style 0, stigma broad, cushion-shaped; ovules many/carpel, straight, unitegmic, integument 2-4 cells across, parietal cells 0, nucellar epidermis persistent, nucellar cap?; embryo sac bi- or tetrasporic; fruit baccate, ± circumscissile or not; exotestal cells with U-thickened inner walls (not), anticlinal walls ± sinuous; endosperm cells with thick walls, arabinose and starch +, perisperm +, ca 1 cell layer across; n = ?; germination via germ tube.

2[list]/7. Arabian Peninsula, Africa, Madagascar; Costa Rica and S. South America (map: from the Parasitic Plants Website 2004). [Photo - Prosopanche Staminate Flower © L. Musselman, Flower © R. Polhill & Paolo, Fruit © G. Williams.]

• Hydnoraceae are leafless and echlorophyllous root parasites that can be recognised by their large flowers with a single, thick, basally connate, valvate perianth whorl that is brownish and cracked outside and coloured inside, stamens opposite the perianth lobes, and inferior ovary; the fruit contains many small seeds, some 90,000 or so.

Evolution. Floral Biology & Seed Dispersal. Pollination of the foetid flowers of Hydnora is by flies and beetles, as in Aristolochiaceae (Bolin et al. 2006b, 2009), and thermogenesis occurs in the flowers of Prosopanche and some Hydnora (Cocucci & Cocucci 1996; Bolin et al. 2009; Seymour et al. 2009). Each flower has up to 35,000 ovules. In Hydnora triceps both flower and fruit are underground. Solms-Laubach (1874) described the thickened testa wall of Prosopanche as "scahaumige" (frothy); dispersal is by mammals.

Chemistry, Morphology, etc. Carpel orientation is suggested by stigma position (Baillon 1888); other information is taken from Solms-Laubach (1874) and Cocucci (1976: embryology) and Cocucci and Cocucci (1996: Prosopanche), and Meijer (1993: general), for germination, see Bolin et al. (2006a). See Hegnauer (1966, 1989) for what little is known about chemistry.

Previous Relationships. Hydnorales were placed in Rafflesiales by Cronquist (1981) and Rafflesianae by Takhtajan (1997); Cocucci and Cocucci (1996) saw connections between Hydnoraceae and Annonaceae.

ARISTOLOCHIACEAE Jussieu   Back to Piperales

Flavonols +; wood storied; stomata anomocytic; prophyll adaxial; lamina heart-shaped, vernation conduplicate; inflorescence cymose: P 3, odd member adaxial; A in 3's, connective extended apically; carpels basically free; micropyle endostomal, outer integument ca 2 cells across, parietal tissue?; inner integument 2-3 cells across, nucellar cap +; fruit a follicle; exotestal cells enlarged and thickened or not, endotesta palisade, usu. crystalliferous, exotegmen and layer underneath crossing fibres, (exotegmen radially elongated), endotegmen with reticulate thickenings; endosperm oily.

5-8[list]/480. World-wide, not Arctic (map: from Poncy 1978; Fl. N. Am. III 1997; de Groot et al. 2006 - S. America?, Australia approximate) - three groups below.

These characters yet to be assigned to their appropriate hierarchical level: hairs uniseriate; petiole with a ring of (three) bundles or incurved U-shaped; cuticle waxes as annular rodlets, palmitone the main wax; P connate, nectaries or secretory hairs on tube; A 5-12, ± connate, usu. initiated in petal?-opposed pairs, (filaments slender), connective prolonged or not, tapetal cells multinucleate, pollen ektexine semitectate-reticulate, granular(-columellate), style hollow, stigma dry or wet;

1. Asaroideae O. C. Schmidt

Sieve tube plastids with cuneate protein crystalloids and a large polygonal crystal; inflorescences/flowers terminal; P connate, inner whorl at most minute [Asarum] (large - Saruma); stigma with multicellular papillae; K persistent, (fruit an irregularly dehiscent capsule - Asarum); elaiosome extending along the raphe; n = 6, 12, 13, 18, 20, 26.

2/75: Asarum (70). N. Temperate, esp. East Asia. [Photos: Saruma Flower, Asarum Flower.]

Synonymy: Asaraceae Ventenat

Lactoris + Aristolochioideae: growth monopodial; bracts distinct.

2. Lactoris

?Chemistry; ?cork; rays 0 [internodal regions]; sieve tube plastids with starch grains; nodes 1:2; petiole?; plant glabrous; cuticle waxes as parallel platelets; leaves elliptic, 2ndary veins subpinnate, stipule sheathing, intrapetiolar, adnate to the petiole; plants polygamo-dioecious; inflorescence thyrsoid, bracteoles 0; flowers small; A 6, (inner or both whorls staminodial); pollen in tetrads, saccate, ektexine granular, (subcolumellate); G 3, alternating with P; ovules 4-8/carpel, pendulous, epitropous, ?tenuinucellate, endothelium +, funicle long; seed coat cells collapsed, two cuticular layers persisting, endothelium also ± persistent; endosperm with chalazal haustorium; n = 20.

1[list]/1: Lactoris fernandeziana. Chile, the Juan Fernandez Islands (for fossil distribution, see Gamerro & Barreda 2008: brown squares). [Photo: Specimen.]

Synonymy: Lactoridaceae Engler, nom, cons.

3. Aristolochioideae

Plant usu. viny (woody); benzylisoquinoline alkaloids +; sieve tube plastids with polygonal protein crystalloids plus starch grains or protein fibres (starch grains alone); (secondary thickening odd); sclereids +; groups of silicified cells +; serially arranged axillary buds; hairs hooked; (lamina lobed), base of petiole U- or V-shaped; inflorescences axillary; (flower resupinate), floral primordia monosymmetric, (flowers monosymmetric - Aristolochia); P connate; A 3-12(-40< - Thottea), (in a single whorl); (microsporogenesis successive - Aristolochia); pollen inaperturate; G [4-6], apically constricted, stigma dry or wet, (commissural - Aristolochia); parietal tissue ca 4 cells across, (funicle massive - A. bracteata); fruit septicidal and opening adaxially-laterally, a schizocarp, or dry-baccate, K not persistent; seed winged, (arillate); n = (4-)6-7(8+).

2-5/405. Tropics (temperate), relatively less diverse in Africa (inc. Madagascar), few in N. Australia. [Photos - Flowers, Fruits.]

• Aristolochiaceae are more or less herbaceous plants (they are quite often vines) that may be recognised by their adaxial prophylls, exstipulate leaves with palmate venation and entire margins, and 3-merous flowers with extrorse stamens. The ovary is usually inferior and the perianth uniseriate and connate. Only Aristolochia has monosymmetric flowers, only Saruma a perianth differentiated into sepals and petals and a largely superior gynoecium of free carpels.

• Lactoris can be recognised by its small, two-ranked leaves with intrapetiolar stipules; the prophylls are adaxial. The flowers are small and have three imbricate perianth members and three free carpels.

Evolution. Divergence & Distribution. Pollen like that of Lactoris has been found in Late Cretaceous deposits from S.W. Africa (Turonian-Campanian - 93-76 million years ago) to Oligocene deposits in Australia, etc. (Zavada & Benson 1987; Macphail et al. 1999; Gamerro & Barreda 2008; Srivastava & Braman 2010).

Plant-Animal Interactions. Aristolochia is eaten by caterpillars of the magnificent birdwing butterflies of the Papilionidae-Papilioninae-Troidini. The association between caterpillars of these butterflies and Aristolochiaceae - they are apparently absent from Saruma, although larvae of the related Luehdorfia (Zerynthiini) have been reported from this plant - has been studied in some detail (e.g. Weintraub 1995); some swallow tails (Papilionini) also eat Aristolochiaceae (Berenbaum & Feeny 2008). However, there seems to be no particular association between the phylogeny or chemistry of the plant and the phylogeny of the butterflies (Silva-Brandão & Solferini 2007; Simonsen et al. 2011: note the variation in divergence times suggested). Larvae of other Papilioninae (and of a few of its sister taxon, Parnasiinae) feed on Aristolochiaceae, although there are host shifts to Apiaceae, Rutaceae, etc. (Fordyce 2010).

Floral Biology & Seed Dispersal. Fly pollination is common throughout the family. The inside of the perianth tube of Aristolochia arborea looks as if it has a small mushroom growing in its mouth, and many taxa trap flies, specialized multicellular hairs allowing insects entrance into the floral chamber where they remain until the hairs wither (Sakai 2002; Oelschlägel et al. 2009). Some pollinators oviposit on the flowers, and in some cases the relationship between plant anbd pollinator is specific (Sakai 2002). The flowers of some Aristolochiaceae are reported to show thermogenesis (Seymour 2001), and selfing may be common in some species of Asarum (Kelly 1997).

Chemistry, Morphology, etc. Aristolochic acid is closely related biosynthetically to benzylisoquinoline alkaloids (Gershenzon & Mabry 1981). Aristolochia has cuticular wax rodlets, but other genera lack crystalloids. Ding Hou (1984) notes that the leaves wither on the plant and are not abscised. The shrubby habit is derived within Aristolochia. The central leaf trace of the woody Aristolochia arborea appears to have three parts, but this may well be a single trace broken up by the broad rays. Aristolochia clematitis appears to have lateral prophylls; González and Rudall (2001) suggested that the stipule of Lactoris is initially paired. Lobed leaves are known from Aristolochia.

There has been much discussion about the nature of the perianth in the family, and there is considerable variation in basic floral organization here. González and Stevenson (2000) suggest that the uniseriate perianth is derived from the outer whorl of a biseriate perianth; interestingly, in any inner whorl, whether in Asarum or Thottea, "petal" bases are narrow, although the bases of members of the outer whorl are very broad and encircle the axis. There are also suggestions that "petals" may be derived from stamens (see also Leins & Erbar 1995; Kelly 2001; Ronse De Craene et al. 2003), although their position in some species of Asarum, in the angles of the outer whorl, perhaps makes this unlikely and would also suggest that the perianth or sepal tube is in fact a complex structure. Obvious stamens are more or less adnate to the style. However, in Thottea these petal-like structures may indeed represent stamens (Leins et al. 1988), and that may be the best interpretation for the reduced petals that alternate with the perianth in Asarum caudatum (cf Leins & Erbar 1985). Jaramillo and Kramer (2004) describe the basic perianth condition for the family as being unipartite (= uniseriate), with its ancestors having "multiple" whorls. The median outer tepal is adaxial (González & Stevenson 2000a), i.e. not in the monocot position, in some taxa, although it is abaxial in Aristolochia s. str., but with the exception of A. grandiflora, and also in Pararistolochia (Neinhuis et al. 2005: ?other taxa). Spichiger et al. (2004) show a floral diagram for Aristolochia where the six stamens and carpels are not opposite to the perianth members - nor would be opposite sepals or petals, if such were present. The perianth members in Lactoris have but a single trace.

González and Stevenson (2000b) note that the stigmas of Aristolochia are commissural (see also Leins & Erbar 1985), and that when there is only a single whorl of stamens in the flower, it is the inner whorl. Endress (1994c) suggested that the androecium in Lactoris was adnate to the gynoecium, as in other Aristolochiaceae, but at most it is adnate to the stipe of the gynoecium; ovary position is variable around here. Thottea has four placentae and presumably four carpels, but there are about twice as many styles (Leins et al. 1988). An illustration in Engler (1888) showed a bistomal micropyle. Finally, see Leins and Erbar (1995) for the flowers of Saruma, which seem very different from those of the rest of the family: Here the sepals and petals are quite distinct, the pollen is sulcate, and the nine carpels are adnate to hypanthium, but are otherwise free. All in all, rather confusing.

See Johri and Bhatnagar (1955) for embryology, Hegnauer (1964, 1989) and Chen and Zhu (1987) for chemistry, Sugawara (1982 and references) for cytological variation within Asarum s.l., Huber (1985) for seed characters, Huber (1993) for general information, González (1999) for inflorescence morphology, González et al. (2001) for microsporogenesis, Behnke (2003) for sieve tube plastids, Kelley and González (2003) for a morphological phylogenetic analysis, Leins et al. (1988) for floral development, González and Rudall (2001) for ovule and seed development, and Mulder (2003) for pollen, which, however, is poorly known. See also Engler (1887: general, anatomy), Carlquist (1964: general, 1990: wood anatomy), Hegnauer (1966, 1989: chemistry), Bouman (1971: ovule), Sugawara (1982 and references: cytology), Crawford et al. (1986: chemistry), Metcalfe (1987: vegetative anatomy), Kubitzki (1993: general), Tobe et al. (1993: embryology and karyomorphology), and González and Rudall (2001) for more details.

Phylogeny. See Kelly (1998) for relationships in Asarum; morphology and molecules (ITS) suggest similar relationships (cf. Kelly 1997). Although the monophyly of Aristolochia is not in question, it is quite variable. In phylogenetic analyses there are four main clades that are all well supported, of which one of which includes just (González & Stevenson 2002; Neinhuis et al. 2005; Wanke et al. 2006b; Ohi-Toma et al. 2006).

• Saruma (Asaroideae) is distinctive: nodes with two traces from central gap; hypanthium +; calyx and corolla distinct, C clawed; pollen sulcate (indistinctly 3-porate); G 9, adnate to hypanthium, otherwise free from each other, (micropyle bistomal).

Classification. See Huber (1985) for an infrafamilial classification. Asarum can be circumscribed broadly, as here, or divided into a number of genera. Huber (1993) suggested that Aristolochia could be divided into eight genera, some of which would be well characterised morphologically. Some splitting, perhaps into four genera, all with synapomorphies, seems to be favoured (González & Stevenson 2002; Neinhuis et al. 2005; Wanke et al. 2006b); Ohi-Toma et al. (2006) proposed that Aristolochia should be divided into two genera.

Previous relationships. Lactoris has until very recently been placed in its own family, Lactoridaceae, and it has not been considered as particularly close to Aristolochiaceae, being placed in Magnoliales by Cronquist (1981).

Thanks. I thank Mauricio Diazgranados for comments.

[Piperaceae + Saururaceae]: root epidermis from inner layer of cap; stomata tetracytic; cuticle wax crystalloids usu. 0; lamina vernation supervolute, leaf base ± sheathing stem, (stipules intrapetiolar, ± on petiole); inflorescence spicate, terminal (axillary); flowers small, monosymmetric by reduction; P 0; filaments rather slender; microsporogenesis simultaneous; pollen grains <20 µm; G with odd member adaxial [when 3], stigma dry, papillate; ovules straight; seed coat exo- and endotegmic; perisperm +, starchy, endosperm ?type, scanty, embryo short, broad.

Evolution. Divergence & Distribution. Madrid and Friedman (2010) suggest that there is a connection between the evolution of perisperm in this clade and the great diversification in embryo sac morphology, however, other clades with perisperm such as core Caryophyllales and Zingiberales are much less adventurous in terms of embryo sac variation.

Chemistry, Morphology, etc. Some taxa in both families have punctate ectexine, the punctae being surrounded by papillae (Smith & Stockey 2007a). See Jaramillo et al. (2004) for the complexities of floral evolution in this group; it is possible that a four-carpellate gynoecium is the basic condition. There is also much variation in the embryo sac development in this clade, and Madrid and Friedman (2009) suggest that the basic condition is bisporic, although it might be more accurate to say that it is unclear.

Some information is taken from Murty (1960: morphology), Blanc and Andraos (1983: growth), and Tucker et al. (1993: morphology and development).

PIPERACEAE Giseke   Back to Piperales

Plants also lianes, (trees), (epiphytic - esp. Peperomia); flavonols, tannins 0; (cork in outer cortex); vascular bundles scattered or in 2 rings; rays 8-45-seriate [other Piperales?]; cambium storied; (vessel elements with scalariform perforation plates); mucilage canals +; petiole bundles arcuate; prophyll single, basal, adaxial to lateral, often ± reduced, with a fairly prominent axillary bud; lamina (2ndary venation pinnate), (margins lobed), (margins ± sheathing, ligule +); (inflorescence racemose), bracts peltate or clavate; A (1-)2(-10, or 3 + 3, latrorse to extrorse, thecae not dehiscing their entire length; pollen ektexine tectate, punctae surrounded by papillae [Zippelia], endexine 0; G [2-5]; ovule 1/carpel, basal, outer integument 3-5 cells across, inner integument 3-5(-7 - Macropiper) cells across, micropyle endostomal (bistomal - Piper-Heckeria), parietal tissue 2-5 cells across; embryo sac tetrasporic, sixteen-celled, eleven cells at the chalazal end; fruit fleshy, berry [or drupe?]; seed with exo- and endotegmic layers well developed, former in particular thick-walled, endotegmen/perisperm interface convoluted; endosperm (nuclear - some Piper, Zippelia), first cleavage of zygote vertical [whole family?]; n = 11, 13, 19.

5[list]/3615. Pantropical (map: from Jaramillo & Manos 2001; Wilson 2007; M. A. Jaramillo, pers. comm.) - three groups below.

1. Verhuellioideae Samain & Wanke

A 2; pollen inaperturate; G 3-4; ovule unitegmic.

1/3. Cuba and Hispaniola.

2. Zippelioideae Samain & Wanke

A 4, 6; G 3-5.

2/6. China to Malesia, Central and South America.

3. Piperoideae Arnott

A 2-6; G 1-4; (integument 1, ca 2 cells across - Piper).

2/3600: Piper (2000), Peperomia (1600). Pantropical. Photo: Peperomia - Flower, Piper - Flower, Fruit.]

Synonymy: Peperomiaceae A. C. Smith

• Piperaceae may be recognised vegetatively by their herbaceous habit and/or their separate vascular bundles in the stem, their swollen nodes, and their soft and/or fleshy leaves that are often cordate at the base. The minute flowers lack a perianth and are often borne in dense spikes; individual flowers are subtended by peltate to clavate bracts. Some species of Piper look remarkably like Araceae!

Evolution. Divergence & Distribution. It has been suggested that Piper and Peperomia diverged in the late Cretaceous, but species diversification in those genera wass mid-Tertiary and later (Smith et al. 2008); Symmank et al. (2011) date stem Peperomia to ca 57 million yaesr ago, aain with much later diversification. Friis et al. (2005b) suggest that Appomattoxia, from the Early Cretaceous, may be in this area (cf. Friis et al. 1995), but it may also be somewhere around Chloranthaceae or Amborella (Doyle & Endress 2010)...

For ranges of neotropical species of Piper, see Paul and Tonsor (2008). Symmank et al. (2011) think that the largely South American Peperomia subgenus Tildenia diversified starting ca 15 million years ago, and has since twice dispersed to Central America.

Ecology & Physiology. Peperomia is a notable component of the epiphytic flora, particularly in the neotropics; the epiphytic habit is derived, as is the geophytic habit - several times (Symmank et al. 2008). Crassulacean acid metabolism is common in these epiphytes. Indeed, many of the characters previously considered to be systematically important in the genus have evolved in parallel (Samain et al. 2009).

Plant-Animal Interactions. Maybe as many 500-1,000 species of the geometrid moth Eois feed on Piper in the neotopics; species numbers are notoriously uncertain. The time of crown origin of neotropical members of the moth (they form a clade) is pegged at somewhere between (36-)31.96(-16) million years ago (Strutzenberger & Fiedler 2011), in line with the age of the diversification of Piper, estimated at after 21.5 million years ago (Smith et al. 2008) and also with the uplift of the Andes. These moths rarely occur on other Piperaceae, Chloranthaceae, etc.; there is only a single record from a plant not containing ethereal oils (!Gesneriaceae, see Strutzenberger et at. 2010). Most diverse at mid elevations, Eois may comprise 10% of the geometrids there. Ants that are associated with Piper and protect it, bats that eat the moths (both these are primarily at lower elevations), parasitoids on the caterpillars, leaf toughness, herbivory by leaf cutter ants and other generalist herbivores, etc., are all part of this complex association (Fincher et al. 2008; Richards et al. 2010).

Many of the plant-animal interactions both of Piper and Peperomia are linked to the possession of the plant of piperamides, a class of nitrogenous compounds with the general formula R-(C=O)-NH2, where one or two of the H atoms are variously replaced. They deter generalist herbivores in particular, and particular species of Piper may have distinctive piperamides to which particular species of Eois may be adapted (e.g. Richards et al. 2010).

Floral Biology & Seed Dispersal. Four to five (to nine?) species of Carollia bats (Phyllostomidae) are abundant fruit-eating New World bats that eat and disperse Piper (and some Peperomia) living in the understorey, being attracted by essential oil extracts (Mikich et al. 2003; Lobova et al. 2009 for records); Old World Piper are bird-dispersed (Fleming 2004). If Carollia is indeed a major seed disperser, there are a lot of species of Piper in the New World, and only a few species of Carollia...

Economic Importance. For the black pepper, Piper nigrum, see Ravindran (2000).

Chemistry, Morphology, etc. There is some confusion surrounding the terms used to describe the leaf. The petiole is more or less broadly sheathing and with a flange for all or some of its length. Prophylls, at least on fertile plagiotropic branches I have seen, are comparable with this basal part of the petiole; there are no structures that can usefully be called stipules. The prophylls of Piper are drawn as being lateral (Blanc & Andraos 1983). The leaves of Piperaceae may be rich in silica (Westbrook et al. 2009). Peperomia shows considerable variation in the nature (druses, raphides) and pattern of oxalate deposition in the leaf (Horner et al. 2009 - spectacular under polarizing light), but with little obvious correlation with phylogeny.

The inflorescence of Zippelia is described as being racemose, but with the flowers being arranged sympodially (Lei et al. 2002). Tor the development of the peltate bracts, see Endress (1975). Syncarpy is weak; Piper has separate carpel primordia. Each carpel has a single ventral bundle. The embryo at least sometimes lacks a suspensor, but I am not sure of the distribution of this feature, while in Zippelia the zygote remains as such up to the maturity of the seed and in Peperomia it may not be much bigger (Madrid & Friedman 2010). In Zippelia and some Piper the endotegmen alone is persistent.

There is considerable variation - some infraspecific - in the particlar kind of tetrasporic embryo sac development in the family (Arias & Williams 2008: Verhuellia not yet studied). The embryo sac of Peperomia is very variable, ranging from three-celled (but with 14 polar nuclei) to a common condition of ten cells with seven polar nuclei (e.g. Fagerlind 1939a, b and references; Madrid & Friedman 2010), that of Zippelia is 16-celled, while that of Piper is 8-celled, the antipodals being polyploid. Madrid and Friedman (2008a, 2009) suggest that the basic embryo sac for the family - at least all the family minus the currently unstudied Verhuellia - may be the Drusa type, which is tetrasporic and with sixteen cells, 11 of which congregate at the chalazal end (three of the megaspores migrate there first). The endosperm ranges from 15n (in Peperomia) to triploid. Kanta (1963) noted that there was extensive division of the antipodal cells during early seed development. The nucellar cells of Peperomia, at least, are in radiating files (Fagerlind 1939a).

Some information is taken from Hegnauer (1969, 1990: chemistry), Weberling (1970: stipules), Burger (1972: Central American Piper), Blanc and Andraos (1983, 1984: growth patterns), Bornstein (1991: general), Johnson (1914), Murty (1959), Kanta (1963), and Johri et al. (1992), all embryology, Tebbs (1993: general), Jaramillo and Manos (2001: phylogeny and morphology of Piper) and Lei et al. (2002: embryology of Zippelia), for floral development, see Lei and Liang (1998: Piper; 1999: Peperomia), Tucker et al. (1993: Zippelia), and Samain et al. (2010a: Verhuellia), and for phytoliths, see Piperno (2006). I thanke S. Wanke for estimates of species numbers.

Phylogeny. Relationships may be [Verhuellia [[Zippelia + Manekia] [Piper + Peperomia]]] (Jaramillo & Callejas 2004; Wanke et al. 2006a, 2007a, b); this entails redrawing the old subfamilial boundaries. The recent discovery that Verhuellia is sister to the rest of the family (Wanke et al. 2007b) changes hypotheses as to the plesiomorphous characters of the family; of the three genera in the two small clades that are successively sister to Piper and Peperomia, we know little about two. Jaramillo and Callejas (2004) and Smith et al. (2005, 2008) found that Piper s. str. was divided into New and Old World clades, the latter, Piper s. str., being divided into a mainland Asian clade, containing both the two endemic African species and a species from Australia, and also a Pacific islands Macropiper clade including the economically very important Piper methysticum (Jaramillo & Callejas 2004 found that one African species they examined grouped with their Pacific clade - see also Jaramillo et al. 2008; Smith et al. 2008). This Pacific clade, the Macropiper clade, is either sister to the rest of the genus or sister to the Asian clade (Jaramillo et al. 2008). Paul and Tonsor (2008) discuss aspects of the diversification of Piper in the New World. Interestingly, in a trnK/matK analysis, Wanke et al. (2007a) found much less resolution within Piper than Peperomia. For the phylogeny of Peperomia, see Wanke et al. (2006a, 2007a) and Samain et al. (2009).

• Peperomia is a morphologically and anatomically very distinctive genus. It has spiral or opposite leaves, usually with narrow insertions on the stem and lacking stipules, the flowers have two bisporangiate/monothecal extrorse stamens, inaperturate pollen, a single carpel with a penicillate stigma, and an unitegmic ovule, the integument being ca 2 cells across.

Classification. For the classification of Piperaceae followed here, see Samain et al. (2008, 2010a); unfortunately, the subfamilies are not easily characterisable. Although Peperomia is so distinctive, its recognition as a separate family would make Piperaceae paraphyletic. Peperomia has the dubious distinction of having the most herbarium names of any genus, about 1,530. These are names known primarily from herbarium sheets and were coined mostly by William Trelease - and are mostly synonyms (Mathieu 2007).

Thanks. I am grateful to Diego Salazar for information on what eats new World Piper.

SAURURACEAE Richard   Back to Piperales

Plant rhizomatous or stoloniferous; leucanthocyanins +, alkaloids 0; (vascular bundles in two rings - Saururus); vessel elements often with scalariform perforation plates; petiole bundles arcuate or annular; cuticle waxes as parallel platelets; (lamina vernation involute - Anemopsis, Saururus); bract at base of inflorescence large, petaloid (not); common bract/flower primordium +/0; A often 3, or 6 or 8 in two whorls, but variable, ± connate in pairs and/or adnate to the ovary or not, introrse; pollen (trichotomosulcate), often boat-shaped, <20 µm long, ektexine tectate-columellate, punctate, punctae surrounded by papillae [not Gymnotheca]; G 4, or [3-4], (inferior, ± embedded in inflorescence axis), placentation often parietal, stigma dry; ovules (1-)2-9(-12)/carpel, micropyle zig-zag (exostomal), outer integument 2-3 cells across, inner integument 3-4 cells across, parietal tissue 1-2 cells across (0 - Houttuynia); fruit dry, achene or follicle; exotestal and tegmic cell walls thickened, former lignified or not; endosperm (helobial), chalazal haustorium +; n = 9, 11, 12.

5[list]/6. North Temperate. (map: from Wu 1983; Ying et al. 1993; Fl. N. Am. III 1997 - in Sumatra?, introduced into Java?; fossil distribution from Smith 2007, green crosses).[Photos - Collection] [Photo - Saururus Habit © E. Pontieri] [Photo - Saururus Inflorescence © E. Pontieri]

• Saururaceae may be recognised by their often aromatic and rather fleshy leaves with broad bases, adaxial stipules, and palmate venation and by their spicate inflorescences that usually have a large, basal inflorescence bract. The flowers are small, without a perianth, but there are clearly three to four carpels.

Evolution. Divergence & Distribution. Smith and Stockey (2007b) describe a fossil Saururaceae, Saururus tuckerae, from the Middle Eocene; although it differs in stamen number from numbers normally associated with the family, there is clearly much variability here.

Floral Biology. Saururus cernuus has a stigmatic self-incompatibility mechanism (Pontieri & Sage 1999).

Chemistry, Morphology, etc. Anemopsis, alone in the family, has a relatively well developed vascular cambium and also simple vascular perforations... (Carlquist et al. 1995). According to Murty (1960) the single intrapetiolar stipule represents two, connate stipules (see also Lactoris above). Houttuynia is tenuinucellate. Each carpel has two ventral bundles, whether or not they are fused.

Some information is taken from Raju (1961: embryology), Wood (1971: general), Hegnauer (1963, 1990: chemistry), Wu and Kubitzki (1993: general), Carlquist et al. (1995: wood anatomy), Tucker (1981 and references) and Liang et al. (1996), both floral development, Liang and Tucker (1990: floral anatomy), and Smith and Stockey (2007a: pollen ultrastructure).

Phylogeny. Houttuynia and Anemopsis are sister taxa and sister to the rest of the family in a matR analysis (Meng et al. 2002, 2003). A clade made up of this pair of genera is also found in a three-gene analysis, but the support is poor; [Saururus + Gymnotheca] is a better-supported clade (Jaramillo et al. 2002). These two pairs of genera are also recovered in other molecular analyses (e.g. Neinhuis et al. 2005), although they are not found in morphological studies.