EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus.

Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.

All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group, [] contains explanatory material, () features common in clade, exact status unclear.


Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.

[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.


Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].


Vascular tissue + [tracheids, walls with bars of secondary thickening].


Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].


Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.


Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].


Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].


Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.


Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open, pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; 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, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; 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, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [], dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [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 short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; 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, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.

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

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

[CHLORANTHALES [[MAGNOLIALES + LAURALES] [CANELLALES + PIPERALES]]]: sesquiterpenes +; (microsporogenesis also simultaneous); seed endotestal.

[[MAGNOLIALES + LAURALES] [CANELLALES + PIPERALES]] / MAGNOLIIDS / MAGNOLIANAE Takhtajan: (neolignans +); vessels solitary and in radial multiples, (with simple perforation plates in primary xylem); (sieve tube plastids with polygonal protein crystals); lamina margins entire; A many, spiral [possible position here], extrorse; ovules with hypostase, nucellar cap +, raphal bundle branches at the chalaza; antipodal cells soon die.

[CANELLALES + PIPERALES]: flavonols, aporphine alkaloids +; nodes 3:3; G whorled.

PIPERALES Dumortier  Main Tree.

Plant ± herbaceous [not trees], growth sympodial; sesquiterpenes [e.g. γ-elemene] +; primary stem with distinct bundles; wood storied, with broad rays, interfascicular cambium lacking fusiform initials, vessel elements in radial files, with simple perforation plates; starch grains compound; nodes often swollen; ?stomata; leaves two-ranked, lamina heart-shaped, secondary veins palmate; A in 3's; G occlusion?; seed ± tegmic, endotegmen tanniniferous; PHY E gene absent. - 4 families, 17 genera, 4090 species.

Age. Magallón and Castillo (2009: note topology) offer estimates of 175 and 119 m.y. for relaxed and constrained penalized likelihood datings of crown group Piperales, Wikström et al. (2001) an age of (139-)133, 122(-116) m.y., Bell et al. (2010) ages of (138-)119, 104(-87) m.y.a., and Magallón et al. (2013, 2015) ages of around 110 m.y.a. and 105.4 m.y.a. respectively; ages of (124-)101(-76.5) m.y. were suggested by Naumann et al. (2013), and (158.1-)151.6, 105.6(-88.1) m.y. by Massoni et al. (2015a).

For an Early Cretaceous fossil showing some similarities with this group, see Friis et al. (1995).

Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).

Evolution: Divergence & Distribution. Friis et al. (2005b) suggested that Appomattoxia, from the Early Cretaceous, might belong somewhere around Piperales (c.f. Friis et al. 1995, 2011), but relationships with Chloranthaceae or Amborella have also been suggested (Doyle & Endress 2010).

For the evolution of woodiness in the order, see Trueba et al. (2015). Although I have tentatively called Piperales as a whole herbaceous, this depends on the definition of "woody" (see also Wagner et al. 2014; Trueba et al. 2015). For some thoughts on floral evolution in Piperales, see Remizowa et al. (2005b). Piperales are characterised by having notably small seeds, other magnoliids and ANITA grade angiosperms having substantially larger seeds (Moles et al. 2005a; Sims 2012).

Ecology & Physiology. G. Liu et al. (2014) noted that the litter of Piperales tended to break down fast compared with that of other magnoliids, and they noted that many members of this order were smallish plants and hence are unlikely to have had a substantial effect on nutrient cycling.

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

Genes & Genomes. For the PHY gene, see Matthews et al. (1995).

Chemistry, Morphology, etc. Carlquist et al. (1995) suggest a number of wood anatomical characters that may be common to this clade, for instance, wood in some Aristolochiaceae and Piperaceae is storied (Carlquist 1992a, 1993); Trueba et al. (2015: esp. Table 1) compared wood anatomy across the order. Isnard et al. (2012) disucuss growth form and anatomy in Piperales in some detail; Aristolochia and Piper are particularly variable in growth habit. Most taxa in the clade are sympodial in that the stem is put together by succesive axillary innovations. Inflorescences are in general terminal, rarely axillary, although Isnard et al. (2012: Fig. 17B) suggest that growth in Piperaceae is monopodial; the climbing stage of Asian Piper is monopodial, but the inflorescences are terminal in sympodial plagiotropic branching systems.

The much reduced flowers of the [Piperaceae + Saururaceae] clades can be described as monosymmetric (Tucker 1984), and it is conceivable that this is an apomorphy for the whole order. Variation in embryo sac morphology in the whole clade is very considerable, but there are now attempts to put this in a phylogenetic context (e.g. Madrid & Friedman 2008a, 2008b, 2009).

For some information on lianes, etc., see Rowe and Speck (2005), on crystals, etc., Horner et al. (2013, esp. 2015 - considerable variation), and for floral development, see Tucker and Douglas (1996).

Phylogeny. The pairing [Piperaceae + Saururaceae] has usually been strongly supported as sister to Aristolochiaceae (e.g. Neinhuis et al. 2001, Nickrent et al. 2001), and discussion over other relationships in the order hinge on the circumscription of Aristolochiaceae. 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: Lactoridaceae sister to Aristolochioideae, support weak). 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). Kelly and González (2003) claimed that a morphological phylogenetic analysis strongly refuted the idea that Aristolochiaceae s. str. were not monophyletic; molecular data and the coding of morphological data were to "blame" (ibid.: p. 240) for the possibility that Lactoris might end up in the family. See also the various analyses in Naumann et al. (2013: supplementary material).

Relationships of the parasitic Hydnoraceae were initially uncertain, although they clearly went in this general area (e.g. Barkman et al. 2007: see also Nickrent & Duff 1996; Blarer et al. 2000; Nickrent et al. 2001, 2002). Nickrent and Blarer (2005) found moderate support for the clade [Hydnoraceae + Aristolochioideae], while the inclusion of a number of single-copy nuclear genes found that thius relationships However, Massoni et al. (2014) recovered the relationships [Asaroideae [Hydnora {Lactoris + Aristolochioideae]]], although support was mostly rather weak. Eventual inclusion of Hydnoraceae in Aristolochiaceae is likely.

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.

Piperales tree

Includes Aristolochiaceae, 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

ARISTOLOCHIACEAE Jussieu   Back to Piperales


Flavonols +; ring of fibres (+ sclereids) in cortex; stomata anomocytic; prophyll single, adaxial; lamina vernation conduplicate; inflorescence cymose; flowers quite large, polysymmetric; P with odd member adaxial, uniseriate, 3, valvate, connate; A 6, in tepal-opposed pairs, anthers extrorse, filaments ± 0, connective extended apically; carpels basically free; ovules many/carpel, outer integument ca 2 cells across, inner integument 2-3 cells across, micropyle endostomal, nucellar cap +, parietal tissue?; 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, embryo undifferentiated.

7-9[list]/490. World-wide, not Arctic (map: from Poncy 1978; Fl. N. Am. III 1997; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; de Groot et al. 2006 - S. America?, Australia's Virtual Herbarium xii.2012) - four groups below.

Age. Wikström et al. (2001) suggested an age for crown Aristolochiaceae of (128-)122, 108(-102) m.y., Bell et al. (2010) ages of (126-)104, 91(-72) m.y., Naumann et al. (2013) an age of about 103.4 m.y., and Massoni et al. (2015a) ages of (147.3-)140, 81.7(-52.4) m.y. old; an age of ca 102.6 m.y. for a clade [Lactoridaceae + Aristolochiaceae] was suggested by Tank et al. (2015: Table S2).

Assign to 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; nectaries or secretory hairs on tube; (filaments slender), tapetal cells multinucleate, pollen ektexine semitectate-reticulate, granular(-columellate), style hollow, stigma dry or wet;

1. Asaroideae O. C. Schmidt

Plants rhizomatous; (wood rayless - Saruma); sieve tube plastids lacking starch, with cuneate protein crystalloids and a large polygonal protein crystal; (pericyclic fibres 0); crystals and crystal sand +; flowers solitary, terminal; (inner whorl of P +, at most minute - Asarum), (P = K + C - Saruma); (compitum + - Asasrum); G inferior, (free from one another - Saruma), (superior), 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.]

Age. Wikström et al. (2001) suggested an age of (52-)44, 36(-28) m.y. for crown-group Asaroideae and Naumann et al. (2013) and age of about 14.8 or 13.7 m. years.

Synonymy: Asaraceae Ventenat

[Lactoris [Hydnoroideae + Aristolochioideae]]: growth monopodial; plant ± woody; inflorescence axillary; bracts distinct.

Age. Wikström et al. (2001) suggested an age of (112-)107, 85(-80) m.y. for the [Lactoris + Aristolochia] clade, Bell et al. (2010) an age of (114-)91, 78(-54) m.y., and Naumann et al. (2013) an age of about 99.4 or 98 m.y..

Lactoripollenites is widespread in Late Cretaceous deposits from S.W. Africa (Turonian-Campanian) to Oligocene deposits in Australia, etc., i.e. from around 92 m.y.a. and later (Zavada & Benson 1987; Macphail et al. 1999; Gamerro & Barreda 2008; Srivastava & Braman 2010).

2. Lactoris Philippi


Plant a shrublet; ?chemistry; ?cork; wood rayless [internodal regions]; sclereids associated with pericyclic fibres; nodes 1:2; crystal sand +; petiole?; plant glabrous; cuticle waxes as parallel platelets; lamina elliptic, secondary veins subpinnate, stipule +, sheathing, intrapetiolar, adnate to the petiole; plants polygamo-dioecious; inflorescence axillary; thyrsoid, bracteoles 0; flowers small; P separate, members with but a single trace; A in two whorls, 6, (inner or both whorls staminodial); pollen in tetrads, saccate, ektexine granular, (subcolumellate); G 3, basically free, alternating with P; ovules 4-8/carpel, pendulous, epitropous, parietal tissue ?0, endothelium +, funicle long; seed coat cells collapsed, two cuticular layers persisting, endothelium also ± persistent; endosperm nuclear, with chalazal haustorium; n = 20.

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

Synonymy: Lactoridaceae Engler, nom. cons.

[Hydnoroideae + Aristolochioideae]: G inferior; compitum + [Hyd.?].

Age. The age of this node is variously estimated to be (105-)91.4(-78) m.y. (Naumann et al. 2013), their preferred estimate, (124.4-)101.4(-76.5) m.y. ([Piperaceae + Saururaceae] sister - Table 2), or (122-)111(-99) m.y. old.

3. Hydnoroideae Walpers


Root parasites, echlorophyllous, ± herbaceous, rhizomatous; starch grains?; vascular tissue 4-6-angled, (bundles scattered); cork well developed, mid cortical; sieve tube plastids without starch or protein inclusions, perivascular fibres 0; mucilage cells +; stomata?, cuticle wax crystalloids 0; leaves 0; flowers arising endogenously from roots, 3-4(-5)-merous, large, polysymmetric; P very thick and fleshy, stamens = P, adnate to and opposite P, connate, (also adaxially connate, forming solid body - Prosopanche), anthers polythecate (5< thecae), (staminodes ± deeply lobed, alternating with P, retrorse and ligule-like, below A); pollen (extruded in threads), variously sulcate or trichotomocolpate, ektexine homogeneous; G alternating with P, placentation lamellate, parietal or apical, style 0, stigma broad, cushion-shaped; ovules 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.

2/7. Arabian Peninsula, Africa, Madagascar; Costa Rica and S. South America (map: from the Parasitic Plants Website 2004; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; Machado & de Queiroz 2012). [Photo - Prosopanche Staminate Flower © L. Musselman, Flower © R. Polhill & Paolo, Fruit © G. Williams.]

Age. Crown-group Hydnoroideae are estimated to be (74-)55(-36) m.y.o. (Naumann et al. 2013: (86.9-)58.2(-29.5) m.y. - Table 2) or around 54 m.y. old.

Synonymy: Hydnoraceae C. Agardh

4. Aristolochioideae Link

Plants lianes or vines (shrubs; herbs); benzylisoquinoline alkaloids +; (sieve tube plastids also with polygonal protein crystalloids and peripheral protein fibres); (secondary thickening odd); ring of pericyclic fibres; groups of silicified cells +, often druses (nothing - Thottea); hairs hooked; axillary buds several, superposed, prophyll well developed, stipule-like; (lamina lobed), base of petiole U- or V-shaped; inflorescence usu. axillary; (flower with median tepal abaxial), floral primordia monosymmetric, (flowers monosymmetric - Aristolochia); (nectaries on adaxial surface of C [hairs; glandular]); A 3-12(-40<, centripetal - Thottea), (in a single whorl); (microsporogenesis successive - Aristolochia); pollen inaperturate; G [(2-)4-6], (alternate with A - Aristolochia s.l.), apically constricted, stigma dry or wet, (commissural - Aristolochia); parietal tissue ca 4 cells across, (funicle massive - A. bracteata); fruit septicidal and also opening adaxially, (schizocarp, berry), K not persistent; seed winged, (arillate); n = (4-)6-7(8+).

2-5/405: "Howardia" (150), Aristolochia (120), Isotrema (50). Tropics (temperate), relatively less diverse in Africa (inc. Madagascar), few in N. Australia. [Photos - Flowers, Fruits.]

Age. The age of crown-group Aristolochioideae is estimated at around 39.5 or 35.1 m.y. (Naumann et al. 2013).

Evolution: Divergence & Distribution. The recently-described fossil Hexagyne philippiana whose 3-merous flowers have 6 carpels and 3 (?or 6) perianth parts ends up in Aristolochiaceae in morphological analyses, although positions in basal eudicots and even in monocots are only one step longer (Coiffard et al. 2014: note topology). The discovery of this plant, found in deposits in eastern Brazil 115-112 m.y.o., perhaps supports a Gondwanan origin of Aristolochiaceae (Coiffard et al. 2014).

Within Aristolochia subgenus Isotrema there are two North American-East Asian disjuctions; these and other events are dated by González et al. (2014) to around 30 m.y.a., the initial divergence of the two herbaceous species from the rest of the subgenus, which is woody, is earlier.

Physiology & Ecology. Wagner et al. (2012) discuss the evolution of (weakly) shrubby members of Aristolochia which nevertheless retain many elements of the distinctive stem anatomy, including the broad rays, of their primitively climbing relatives. The climbing habit is likely to be an apomorphy for the genus, and woodiness perhaps derived (Wagner et al. 2014, q.v. for much other information). All told, there are perhaps 395 species of twining climbing/lianoid Aristolochioideae (see also Gentry 1991). Busch et al. (2010) describe how the percicyclic cylinder is repaired when it breaks; adjacent cells may divide and their walls become lignified.

Pollination Biology & Seed Dispersal. There are reports of thermogenesis in the flowers of some Aristolochiaceae, including Hydnoroideae (Cocucci & Cocucci 1996; Seymour 2001; Bolin et al. 2009; Seymour et al. 2009). Various forms of fly pollination are common in the family (Oelschlägel et al. 2014; Gottsberger 2016 and references). Many taxa trap the flies, specialized multicellular hairs allowing insects entrance into the floral chamber where they remain until the hairs wither and the corolla also often changes colour (Sakai 2002; Oelschlägel et al. 2009; Rintz 2009). Nectar in Aristolochia may be produced on the inside of the perianth tube to feed the temporarily-trapped pollinators (Erbar 2014 and references), and it has even been suggested that flies may sup from the copious stigmatic exudate (Baker et al. 1973). Some pollinators also oviposit on the flowers, and the relationship between plant and pollinator may be specific (Sakai 2002); phorid flies may oviposit on rotting flowers (see Jürgens et al. 2013 for the various odour syndromes involved). The inside of the perianth tube of Aristolochia arborea looks as if it has a small mushroom growing in its mouth, and this and a number of species of Asarum with similar structures are pollinated by fungus gnats (Vogel 1978a; Sinn et al. 2015 and references). In a wrinkle on fly pollination, chemicals in the rather weak (to us) scent of the European Aristolochia rotunda specifically attract dipteran chloropid flies - these are the same chemicals as are produced by recently-dead mirid bugs. The flies are kleptoparasitic, stealing food from other insects, and also eating the secretions produced by mirid bugs when they are eaten by other arthropods (Oelschlägel et al. 2014).

Pollination of the foetid flowers of Hydnora is by flies and beetles and oviposition may also occur (Bolin et al. 2006b, 2009; Gottsberger 2016); 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 "schaumige" (frothy); dispersal is by mammals. Seeds with arils are probably dispersed by ants.

Plant-Animal Interactions. Aristolochia is eaten by caterpillars of the magnificent birdwing butterflies (Ornithoptera) of the Papilionidae-Papilioninae-Troidini. The association between caterpillars of these butterflies and Aristolochiaceae - they are apparently not found on Saruma, although larvae of the related Luehdorfia and other genera of the Parnassiinae are found here - has been studied in some detail (e.g. Weintraub 1995). Papilionidae are the only butterflies whose larvae eat Aristolochiaceae (Condamine et al. 2011), but there seems to be no particular association between the phylogeny or chemistry of Aristolochiaceae and the phylogeny of the butterflies (Silva-Brandão & Solferini 2007; Simonsen et al. 2011). Based on relationships in a morphological phylogeny [Cressida [Pharmacophagus + Ornithoptera] [Battus etc.]]] and correlation with geography Parsons (1996) invoked continental drift to explain the distributions of birdwings and their relatives, but the butterfly relationships he found are very different from those suggested elsewhere - even if there is still hardly any general agreement about relationships. Furthermore, estimates of when Papilionidae diversified vary by a factor of over two (Simonsen et al. 2011 for literature), Condamine et al. (2011) even suggesting that it began in the early Caenozoic (62.5-)52(-46) m.y. ago. Aristolochiaceae may be the original larval food for the larvae of all Papilionidae (minus Baronia: Condamine et al. 2011; see also Ehrlich & Raven 1964), while Simonsen et al. (2011) invoked two major shifts onto the family, and some swallowtails also eat Aristolochia (Berenbaum & Feeney 2008). Swallowtails have also shifted their host to Apiaceae, Rutaceae, etc. (Fordyce 2010; Simonsen et al. 2011; Condamine et al. 2011).

Genes & Genomes. At some 24 kb, the plastid genome in Hydnora visseri is the smallest known; plastid genes, now non-functional, are scattered in the mitochondrial genome (Naumann et al. 2014).

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 do not abscise. The shrubby habit is derived within Aristolochia, and the cork is (eventually) deep seated (Wagner et al. 2014), although in the illustrations in Carlquist (1993, q.v. for anatomical features common in the family) it appears to be outer cortical. 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.

The anatomy of Hydnoroideae needs attention, and one problem is understanding the morphological nature of the organs being examined. In Prosopanche burmeisteri and Hydnora africana the vascular bundles of the angled "rhizoid" are in a strongly medullated star-like arrangement with a varying number of rays (Schimper 1880). The vascular bundles on the rays of the star face away from each other, and in P. burmeisteri the ring is interrupted so there seem to be two systems of vascular bundles. The outer of the rhizoid cells have suberin, and cork develops somewhat later. "Appendages" of P. burmeisteri, which develop along the angles of the rhizoids, had a small amount of vascular tissue in the centre. Wagner et al. (2014) confirmed the cauline nature of the rhizoids. However, Schimper (1880) drew the rhizoids of H. abyssinica as being round in t.s. and with numerous scattered vascular bundles, an anatomy which would seem to have nothing to do with that of either Prosopanche and Hydnora africana.

There has been much discussion about the nature of the perianth in the family. The uniseriate perianth may be derived from the outer whorl of a biseriate perianth (González & Stevenson 2000). In any inner whorl, whether in Asarum, Saruma or Thottea, "petal" bases are narrow, while the bases of members of the outer whorl are very broad and encircle the floral axis. It has been suggested that "petals" are derived from stamens (see also Leins & Erbar 1995; Kelly 2001; Ronse De Craene et al. 2003); they were drawn as staminodes and described as petal appendages by Ronse de Craene (2010). Their position in some species of Asarum, in the angles of the outer whorl, makes any staminodial origin unlikely and would also suggest that the perianth tube is hypanthial. In Asarum, there are stamens more or less adnate to the style. However, in Thottea structures in the positions of petals may be stamens (Leins et al. 1988). Jaramillo and Kramer (2004) describe the basic perianth condition for the family as being unipartite (= uniseriate), with its ancestors having "multiple" whorls. For the development og monosymmetry in Aristolochia, in which CYC genes are not much in evidence, see Horn et al. (2014).

The median outer perianth member is adaxial (González & Stevenson 2000a) 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) have 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.

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 - or even more - styles; these surround an open gynoecium (Leins et al. 1988; c.f. Endress 2014). Leins and Erbar (1995) described the flowers of Saruma, which are rather different from those of the rest of the family (see also Sinn et al. 2015). There sepals and petals are quite distinct and the nine carpels are adnate to the hypanthium, but are largely free from one another. All in all, rather confusing. An illustration in Engler (1888) shows a bistomal micropyle.

See also Engler (1887), Carlquist (1964), Ding Hou (1984: Malesian taxa), Kubitzki (1993) and Huber (1993) for general information, Hegnauer (1964, 1966, 1989), Chen and Zhu (1987) and Crawford et al. (1986) for chemistry, Metcalfe (1987) and Carlquist (1990b: Lactoris; 1993: other genera) for anatomy, Behnke (2001, esp. 2003) for sieve tube plastids, González (1999) for inflorescence morphology, Tucker and Douglas (1996) and Leins et al. (1988) for floral development, Mulder (2003) for pollen, González et al. (2001) for microsporogenesis, Johri and Bhatnagar (1955) for embryology, González and Rudall (2001) for ovule and seed development, Huber (1985) for seed characters, and Sugawara (1982 and references) for the cytology of Asarum s.l.. See also Bouman (1971: ovule), Tobe et al. (1993: embryology and karyomorphology), and González and Rudall (2001: morphology of Lactoris) for more details.

In Hydnoroideae, carpel orientation is suggested by stigma position (see Baillon 1888). Other information is taken from Schimper (1880: vegetative anatomy), 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; other information may be found at the Parasitic Plants website (Nickrent 1998 onwards) and Heide-Jørgensen (2008).

Phylogeny. For the circumscription of Aristolochiaceae and relationships within in, see above.

Morphology and molecules (ITS) suggest similar relationships in Asarum (Kelly 1998, c.f. 1997), and a recent study suggests that A. epigynium, from Taiwan, may be sister to the rest of the genus (Sinn et al. 2015). Although the monophyly of Aristolochia s.l. is not in question, it encompasses quite a lot of variation. There are four main clades that are all well supported, one of which includes just two species (González & Stevenson 2002; Neinhuis et al. 2005; Wanke et al. 2006b; Ohi-Toma et al. 2006). González et al. (2014) looked at relationships within subgenus Isotrema; the herbaceous North American A. reticulata and A. serpentaria are sister to the rest of the group. Within Thottea, T. piperiformis is sister to the rest of the genus (Oelschlägel et al. 2011).

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), but Aristolochia s.l. is immediately recognizable (Buchwalder 2014)!

Previous relationships. Lactoris had until recently been placed in its own family, Lactoridaceae, and included in Magnoliales (Cronquist 1981), or by itself in Lactoridanae - but on the page after Aristolochiaceae (Takhtajan 1997. Hydnorales were placed in Rafflesiales by Cronquist (1981) and Rafflesianae by Takhtajan (1997); Cocucci and Cocucci (1996) saw connections between Hydnoraceae and Annonaceae.

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 indeterminate, spicate, flowers dense, sessile, small [<8 mm across], monosymmetric; 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.

Age. Wikström et al. (2011) suggested an age of (106-)100, 90(-84) m.y. for this node, Magallón et al. (2013, 2015) ages of around 64.1 m.y.a. and 65.5. m.y.a. (wide confidence intervales) respectively, and Bell et al. (2010) an age of (96-)78, 67(-45) m.y.; 76.5 and 62.2 m.y. are the ages in Naumann et al. (2013), ca 74.8 m.y. in Tank et al. (2015).

Evolution: Divergence & Distribution. There was a major decrease in the rate of diversification at this node (Massoni et al. 2015a).

Madrid and Friedman (2010) thought that there might be a connection between the evolution of perisperm and the great variability in embryo sac morphology in this clade, however, other clades with perisperm such as core Caryophyllales and Zingiberales are much less adventurous in terms of such variation.

Pollination Biology & Seed Dispersal. Generalist pollination predominates here (Gotttsberger 2016).

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. Madrid and Friedman (2009) suggest that the basic embryo sac development 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) and Tucker (1984: floral development).

PIPERACEAE Giseke   Back to Piperales


Growth monopodial; plant habit various, also lianes; piperamides + [R-(C=O)-NH2, one or two H atoms variously replaced], flavonols, tannins 0; (cork in outer cortex); cambium storied; (vessel elements with scalariform perforation plates); stem endodermis +; mucilage canals +; petiole bundles arcuate; prophyll single, basal, adaxial to lateral, often ± reduced, with a fairly prominent axillary bud; lamina (secondary 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, endothecium from outer secondary parietal cell layer, inner secondary parietal cell layer dividing; pollen ektexine tectate, punctae surrounded by papillae [Zippelia], endexine 0; G [2-5]; ovule single, basal, outer integument 3-5 cells across, inner integument 3-5 cells across, micropyle endostomal, 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; plane of first cleavage of zygote vertical [whole family?]; n = 11, 13, 19.

5[list]/3615. Pantropical (map: from Jaramillo & Manos 2001; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Wilson 2007; M. A. Jaramillo, pers. comm.) - three groups below.

Age. Ca 54.4 m.y. is the age for crown-group Piperaceae in Naumann et al. (2013) and (96.8-)77.7, 58(-37.8) m.y. in Massoni et al. (2015a).

1. Verhuellioideae Samain & Wanke

Secondary thickening 0; vascular tissue reduced, central; druses +; inflorescence axillary; A 2; pollen inaperturate, surface with clavate microechinate processes; ovule unitegmic.

1/3. Cuba and Hispaniola.

[Zippelioideae + Piperoideae]: vascular bundles in 2 rings (scattered).

Age. The age for this node is given as around 45.9 m.y. in Naumann et al. (2013).

2. Zippelioideae Samain & Wanke

Raphides +; A 4, 6; (endosperm nuclear - Zippelia).

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

Age. This node has been dated to around 28.5 m.y.a. (Naumann et al. 2013).

3. Piperoideae Arnott

(Small trees), (cormose geophytes, epiphytes - some Peperomia); druses or crystal sand, (also raphides), mucilage cells in stem [?extent]; (lamina peltate, elliptic, etc. - Peperomia); A 2-6; (G 1 - Piper), (micropyle bistomal - Piper-Heckeria), (ovule unitegmic, integument ca 2 cells across - Piper), (inner integument to 7 cells across Macropiper); (endosperm nuclear - some Piper).

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

Age. Wikström et al. (2011) suggested an age of (51-)47, 41(-37) m.y. for this node; the age is about 91.2 m.y. in Smith et al. (2008), 90.8 m.y. in Chomicki and Renner (2015), and only 34.3 m.y. in Naumann et al. (2013). Symmank et al. (2011) dated stem Peperomia to ca 57 m.y. while Martínez et al. (2014) dated crown Piper to (114-)111(-110) m.y.a. - Piperaceae are another clade with conflicting estimates of ages (see also below).

Indeed, fossil evidence led Martínez et al. (2012, esp. 2014) to think that Piper originated in the early Cretaceous, a crown-group age of (117-)111(-109) m.y.a. being driven by the attribution of a Late Cretaceous Colombian fossil to the stem group of the extant Schilleria clade of neotropical Piper.

Synonymy: Peperomiaceae A. C. Smith

Evolution: Divergence & Distribution. The discovery that Verhuellia is sister to the rest of the family (Wanke et al. 2007b) changes hypotheses about the apomorphies of the family. However, of the three genera in the two clades that are successively sister to Piper and Peperomia, we know little about two.

There was a major uptick in diversification rates at the Piperoideae node (Massoni et al. 2015a; see also Tank et al. 2015). J. F. Smith et al. (2008) estimated that although crown group diversification in Piper and Peperomia began ca 71.75 and 88.9 m.y.a. respectively, much species diversification was mid-Caenozoic and later (in Peperomia ca 57 m.y.a.). Martínez et al. (2012, esp. 2014: note topology, comparison with Lactoris, etc., not relevant) estimated that the stem age of New World Piper was (106-)93, 69(-67) m.y.a., and with the older estimate diversification in South America was well under way by the end of the Eocene, although much diversification was much younger - thus they suggest that that the Macrostachys and Radula clades, which between then include around half the 1,300 neotropical species of the genus, began diversifying around ca 45 m.y.a., the average age of the species examined being 7 and 11 m.y.a. respectively. Although Symmank et al. (2011) dated stem Peperomia to ca 57 m.y.a., estimates of diversification were again much later. Diversification in the largely South American Peperomia subgenus Tildenia - distinctive, the plants are cormose and have peltate leaves - started ca 15 m.y.a., and it twice dispersed to Central America (Symmank et al. 2011; see also Naumann et al. 2011).

Smith et al. (2008) suggested ages for various clades within both Piper and Peperomia, and noted the extent of geographical signal of the clades; extensive migration occurred in both genera. For ranges of neotropical species of Piper and their distribution patterns, see Quijano-Abril et al. (2006: track-compatability analyses) and Paul and Tonsor (2008). Jaramillo and Manos (2001) discuss the phylogeny and morphology of Piper.

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. There is considerable variation in the nature (druses, raphides) and pattern of oxalate deposition in the leaf (Horner et al. 2009, 2012, 2015 - spectacular under polarizing light), but there is not that much correlation with phylogeny; Kuo-Huang et al. (2007) suggest how the druses might be involved in photosynthesis. Piper is also one of the major components of the understory in neotropical lowland rainforests, with fifty or more species occuring in quite limited areas. As noted below, it is a member of associations involving numerous species of diverse groups of insects and other organisms (references in Dyer & Palmer 2004), in particular, it is a major source of food for Carollia bats.

Gentry (1991) estimated that there were some 125 species of scandent Piperaceae in the New World, while practically all Old World Piper are climbers of one sort or another (for additional references, see Schnitzer et al. 2015). All told, there are around 675 climbing species of Piper ranging from vines to quite large lianes (Gentry 1991; Rani Asmarayani pers. comm. xii.2015).

In the single-layered palisade tissue in Peperomia a druse in the centre of each cell may help deflect light to the surrounding chloroplasts; the thylakoids in the chloroplasts are at right angles to the druse (Horner 2012).

Pollination Biology & Seed Dispersal. For a summary of pollination, see Gottsberger (2016).

The four to five (to nine?) species of Carollia bats (Phyllostomidae) are abundant, wide-ranging New World bats that preferentially eat and disperse the relatively high-quality (nutritionally) fruits of Piper (and some Peperomia), 45-47% of the diet of C. perspicillata consisting of Piper, with maybe 34 spikes being eaten a night (Fleming 1988, 2004); they are fast feeders, ingesting the whole fruit, the seeds being dispersed in the faeces. Piper lives in the understory and in early successional habitats, and the altitudinal ranges of the bats and plant are similar (Fleming 1986). The bats can be attracted by essential oil extracts (Mikich et al. 2003; Muscarella & Fleming 2008; Lobova et al. 2009). There are a lot of species of Piper - maybe up to ca 1,500, with up to 64 at a single l.t.r.f. location (Salazar & Marquis 2012) - in the New World, and only a few species of Carollia. Although Piper specialists eat Piper when it is available, local stocks of fruits may soon be exhausted and the bats turn to a variety of other genera for food (Fleming 1986; Muscarella & Fleming 2008). Carollia is on occasion insectivorous (Datzmann et al. 2010), and it may also disperse larger-seeded plants (Melo et al. 2009), while the phyllostomid Sturnira, usually a Solanum specialist, sometimes also eats Piper (Fleming 1986).

All the evidence suggests that Piper diversification began a long time before that of the bats, ca 72 m.y.a. (see above) vs (26-)20(-18) m.y., the latter being the stem-group age for the bats (Fleming 2004; Datzmann et al. 2010), so how the current apparently close relationship between the two developed is unclear. Old World species of Piper are bird-dispersed (Fleming 2004). See also Clade Asymmetries.

Plant-Animal Interactions. Neotropical Piper in particular has numerous associations with insects, and Piper insects are in turn associated with other insects, all in all being an important contributor to insect diversity, and both the number of species of Piper and the diversity of their secondary metabolites are contributing factors (Richards et al. 2015). Maybe as many as 500-1,000 species of the geometrid moth Eois (species numbers here are very uncertain) feed on Piper in the neotropics, and the crown age of the neotropical members of the moth (they form a clade) is dated to around (36-)32(-16) m.y.a. (Strutzenberger & Fiedler 2011). This age is in line with that of extensive diversification of Piper itself, estimated at occuring after 21.5 m.y.a. (Smith et al. 2008, but see above), and also with the uplift of the Andes. These moths only rarely occur on other Piperaceae, on Chloranthaceae, etc., and there is only a single record from a plant not containing ethereal oils (!Gesneriaceae, see Strutzenberger et al. 2010). Most diverse at mid elevations, Eois may comprise 10% of the geometrids there. Diversification in the moth was estimated to have occurred within the last 23 m.y.a., with radiation of small clades of Eois on single species of Piper (lineage duplication) happening within the Pleistocene, i.e. in the last 2.6 m.y., however, there is no signal of strong co-evolution of the two (Strutzenberger & Fiedler 2011).

Relationships are complex. Herbivores that may eat plants other than Piper also attacked a number of species of Piper, while specialist herbivores occurred where Piper species were diverse chemically; predators avoided these animals (they contained nasty chemicals from Piper that they had sequestered), but parasitoids attacked them (there were no predators around) (Richards et al. 2015). A potentially very large number of braconid wasps (Parapanteles) are parasitoids on Eois caterpillars (there are other parasitoids), although less is known about its radiation, but this, too seems be Pleistocene in age (J. S. Wilson et al. 2011a). Ants are associated with some species of Piper at lower elevations and protect them (e.g. Letourneau 2004; Chomicki & Renner 2015, q.v. for dates - quite recent); obligate myrmecophytism has evolved more than once in the genus (Tepe et al. 2004, 2007: anatomy of Piper). Bats eat Eois (also primarily at lower elevations) and also the fruits of Piper (see above), beetles eat the ants, while mirid bugs, herbivory by leaf cutter ants and other generalist herbivores, etc., are all part of the complex set of associations centred on Piper (Gastreich & Gentry 2004; Rico-Gray & Oliveira 2007; Fincher et al. 2008; Richards et al. 2010; J. S. Wilson et al. 2011a).

Many of the plant-animal interactions both of Piper and Peperomia have been linked to the possession by 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 (Dyer et al. 2004). Piperamides deter generalist herbivores in particular, and individual species of Piper may have distinctive piperamides to which particular species of Eois, for example, may be adapted (Dyer et al. 2004; Richards et al. 2010).

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

Chemistry, Morphology, etc. Aerial roots of Piper have superficial cork cambium and a vascular cylinder with a very broad pith (Raman et al. 2012). Vascular bundles in the stem may develop acropteally, basipetally from the leaves, There is some confusion surrounding the terms used to describe the leaf. The petiole is more or less broadly sheathing and with lateral flanges 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).

The inflorescence of Zippelia is described as being racemose, but with the flowers being arranged sympodially (Lei et al. 2002). For 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 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. There is also 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 Bornstein (1991) and Tebbs (1993: general), Hegnauer (1969, 1990: chemistry), Piperno (2006: phytoliths), Weberling (1970: stipules), Burger (1972: Central American Piper), Blanc and Andraos (1983, 1984: growth patterns), Johnson (1914), Murty (1959), Kanta (1963), and Johri et al. (1992), all embryology, 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).

Phylogeny. Relationships may be [Verhuellia [[Zippelia + Manekia] [Piper + Peperomia]]] (Jaramillo & Callejas 2004; Wanke et al. 2006a, 2007a, b; Naumann et al. 2013: these relationships not always obtained; Z.-D. Chen et al. 2016); this entails redrawing the old subfamilial boundaries. Massoni et al. (2015a) found a clade [Zippelia + Manekia]

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), Samain et al. (2009: but c.f. outgroup, characters used) and Naumann et al. (2011). Many of the characters previously considered to be systematically important in Peperomia have evolved in parallel (Samain et al. 2009).

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). Frenzke et al. (2015) assign 80% of the species of the genus to 14 well-supported monophyletic subgenera that they characterize in detail.

Thanks. I am grateful to Diego Salazar for information on what eats new World Piper and to S. Wanke for estimates of species numbers.

SAURURACEAE Richard   Back to Piperales


Plant rhizomatous or stoloniferous, herbaceous; leucanthocyanins +, alkaloids 0; (vascular bundles in two rings - Saururus); cambium mostly in fascicular areas, wood ?not storied, rayless [?always], vessel elements often with scalariform perforation plates; (stem endodermis +); druses or crystal sand +; petiole bundles arcuate or annular; cuticle waxes as parallel platelets; (lamina vernation involute - Anemopsis, Saururus), stipules +, intrapetiolar; inflorescence terminal/leaf opposed, bracts at base large, petal-like (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, free except at base, or [3-4], placentation parietal, (inferior, ± embedded in inflorescence axis), stigma dry; ovules (1-2 - Saururus)4-13/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, Saururus Inflorescence © E. Pontieri.]

Age. Possible crown-group ages for the family are (84-)78, 75(-69) m.y. (Wikström et al. 2001), (77-)54, 47(-26) m.y. (Bell et al. 2010), or (80.8-)63.9, 51.8(-46.7) m.y.a. (Massoni et al. 2015a).

Evolution: Divergence & Distribution. Smith and Stockey (2007b) described a fossil assigned to Saururaceae, Saururus tuckerae, from the Middle Eocene ca 44.3 m.y.a., and although its stamen number differs from those normally associated with the family, there is clearly much variability here (see also Massoni et al. 2015b). For other records of fossils, see Friis et al. (2011).

Pollination Biology. Saururus cernuus has a stigmatic self-incompatibility mechanism (Pontieri & Sage 1999). Armbruster et al. (2002) described Houttuynia as being partly syncarpous and with a compitum.

Chemistry, Morphology, etc. Anemopsis, alone in the family, has a relatively well developed vascular cambium and also vessel elements with simple perforations (Carlquist et al. 1995). The stomata of Houttuynia are surrounded by cells that are arranged spirally (Peterson et al. 2010). According to Murty (1960) the single intrapetiolar stipule represents two, connate stipules (see also Lactoris above).

The small individual floral bracts of Anemopsis are petal-like. Ovules of Houttuynia lack parietal tissue. 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; Massoni et al. 2014), although they are not found in morphological studies.