EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans], lignin +; chloroplasts per cell, lacking pyrenoids; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + 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 dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.

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, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.


Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].


Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].


Sporophyte branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; (endomycorrhizal associations + [with Glomeromycota]); tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.


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


Plant 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 [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; 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; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; apical cell 0, male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], 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.


Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, 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, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; 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 cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic; protogynous; parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, 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], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), 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; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, 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, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; 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, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small [], dry [no sarcotesta], exotestal; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, 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; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size <1.4 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; 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]].

[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]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; 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 [possible position]; pollen tube growth intra-gynoecial; 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] +; starch grains compound; primary stem with distinct bundles; vessel elements in radial files, with simple perforation plates; wood with broad rays, interfascicular cambium lacking fusiform initials; nodes often swollen; stomata not paracytic; leaves two-ranked, lamina heart-shaped, secondary veins palmate; inflorescences/flowers terminal; 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 between ca 111.7 and 101.3 m.y. were suggested by Naumann et al. (2013).

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

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many 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 is the not-so-trivial issue of how 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).

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. Liu et al. (2014) noted that the litter of Piperales tended to break down fast compared with that of other Magnoliids, and this was perhaps connected with the small size of many members of this order..

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, thus wood in some Aristolochiaceae and Piperaceae is storied (Carlquist 1992a). I have tentatively called Piperales as a whole herbaceous; this depends in part on the definition of "woody" (see also Wagner et al. 2014). 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 are indeed 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), and for floral development, see Tucker and Douglas (1996).

Phylogeny. Relationships around Aristolochiaceae were for some time rather unclear, although the pairing [Piperaceae + Saururaceae] was 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: 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).

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 +; wood storied; (perivascular fibres +); 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, ovary inferior; 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., and Naumann et al. (2013) an age of about 103.4 m.y. ago.

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; sieve tube plastids lacking starch, with cuneate protein crystalloids and a large polygonal protein crystal; (pericyclic fibres 0); (inner whorl of P +, at most minute - Asarum), (P = K + C; G free from one another - 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.]

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; 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


Plant a shrublet; ?chemistry; ?cork; rays 0 [internodal regions]; sclereids associated with pericyclic fibres; nodes 1:2; petiole?; plant glabrous; cuticle waxes as parallel platelets; lamina elliptic, secondary veins subpinnate, stipule +, sheathing, intrapetiolar, adnate to the petiole; plants polygamo-dioecious; inflorescence 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]: ?

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, 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 woody, 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 crystals and/or druses (not - Thottea); hairs hooked; axillary buds several, superposed, prophyll well developed, stipule-like; (lamina lobed), base of petiole U- or V-shaped; (flower with median tepal abaxial), floral primordia monosymmetric, (flowers monosymmetric - Aristolochia); 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 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 fossil, 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). 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 several 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 and references). Many taxa trap 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). 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. The inside of the perianth tube of Aristolochia arborea looks as if it has a small mushroom growing in its mouth, and this and other members of the family are pollinated by fungus gnats (Vogel 1978a). 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 from 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 (Bolin et al. 2006b, 2009); each flower has up to 35,000 ovules. In Hydnora triceps both flower and fruit are underground. Selfing may be common in some species of Asarum (Kelly 1997).

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 butterfly relationships he found are very different from those suggested elsewhere, although there is still hardly any general agreement about relationships. Furthermore, estimates of the timing of diversification in Papilionidae varies by a factor of over two (Simonsen et al. 2011 for literature), Condamine et al. (2011) even suggesting that it began in the earkly 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), while Simonsen et al. (2011) invoked two major shifts onto the family, and some swallowtails also eat Aristolochia (Berenbaum & Feeney 2008). There have also been host shifts 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 are not abscised. The shrubby habit is derived within Aristolochia, and the cork is (eventually) deep seated (Wagner et al. 2014). 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 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.

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 seem very different from those of the rest of the family. 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), Kubitzki (1993) and Huber (1993) for general information, Chen and Zhu (1987) and Crawford et al. (1986) for chemistry, Metcalfe (1987), and Carlquist (1990b) for anatomy, Behnke (2001, esp. 2003) for sieve tube plastids, Johri and Bhatnagar (1955) for embryology, Tucker and Douglas (1996) for floral development, Hegnauer (1964, 1966, 1989), Sugawara (1982 and references) for the cytology of Asarum s.l., Huber (1985) for seed characters, González (1999) for inflorescence morphology, González et al. (2001) for microsporogenesis, 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 Bouman (1971: ovule), Ding Hou (1984: Malesian members of the family), Tobe et al. (1993: embryology and karyomorphology), and González and Rudall (2001: morphology of Lactoris) for more details.

For 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. See Kelly (1998) for relationships in Asarum; morphology and molecules (ITS) suggest similar relationships (c.f. Kelly 1997). Kelly and González (2003) suggested 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) for the relationships above.

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 spicate, dense; flowers 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).

Evolution. Divergence & Distribution. 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.

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); calcium oxalate fibres +, 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).

1. Verhuellioideae Samain & Wanke

Secondary thickening 0; vascular tissue reduced, central; 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

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, crystal sand common, 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), only 34.3 m.y. in Naumann et al. (2013), while Symmank et al. (2011) dated stem Peperomia to ca 57 m.y. - another clade with conflicting estimates (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 its apomorphies. Furthermore, of the three genera in the two clades that are successively sister to Piper and Peperomia, we know little about two.

J. F. Smith et al. (2008) suggested that crown group diversification in Piper and Peperomia may have begun ca 71.75 and 88.9 m.y.a. respectively, but both thought that much species diversification was mid-Caenozoic and later (in Peperomia in Smith et al. 2008 - ca 57 m.y.a.). However, 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 Symmank et al. (2011) dated stem Peperomia to ca 57 m.y.a., estimates of diversification were again much later.

Smith et al. (2008) suggested ages for various clades within both Piper and Peperomia, and noted the extent of geographical signal for clades; extensive migration occurred in both. 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). Symmank et al. (2011; see also Naumann et al. 2011) think that the largely South American Peperomia subgenus Tildenia diversified starting ca 15 m.y.a., and has since twice dispersed to Central America. The subgenus is quite distinct, the plants being cormose and with peltate leaves.

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 the epiphytes. Piper is one of the major components of the understory in neotropical lowland rainforests, with fifty or more species occuring in quite limited areas. 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 (Fleming 2004; see also below).

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).

Plant-Animal Interactions. 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. The crown origin of neotropical members of the moth (they form a clade) is dated to somewhere between (36-)32(-16) m.y.a. (Strutzenberger & Fiedler 2011), in line with the age of extensive diversification of Piper itself, estimated at occuring after 21.5 m.y.a. (Smith et al. 2008), and also with the uplift of the Andes. These moths only rarely occur on other Piperaceae, Chloranthaceae, etc., and 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 some species of Piper and protect them (e.g. Letourneau 2004; Chomicki & Renner 2015), bats that eat the moths (both primarily at lower elevations), beetles that eat the ants, mirid bugs, a potentially very large number of braconid wasps (Parapanteles) that are parasitoids on Eois caterpillars (there are other parasitoids), 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; Fincher et al. 2008; Richards et al. 2010; J. S. Wilson et al. 2011a). Obligate myrmecophytism has evolved more than once in the genus (Tepe et al. 2004, 2007: anatomy of Piper).

There is no signal of strong co-evolution of Piper with Eois. Diversification in the latter 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.. Less is known about the radiation of the braconid hyperparasite Parapanteles, but it, too seems to have happened during the Pleistocene (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 may be adapted (Dyer et al. 2004; Richards et al. 2010).

Pollination Biology & Seed Dispersal. The four to five (to nine?) species of Carollia bats (Phyllostomidae) are abundant, wide-ranging New World bats that eat and disperse the relatively high-quality (nutritionally) fruits of Piper (and some Peperomia) almost exclusively; they are fast feeders, ingesting the fruit, seeds being dispersed in the faeces (Fleming 1986; Muscarella & Fleming 2008). 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 spp, 64 at a single l.t.r.f. location (Salazar & Marquis 2012) - in the New World, and only a few species of Carollia. 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 stem-group age for the bats (Fleming 2004; Datzmann et al. 2010), so details of the evolution of the current apparently close relationship between the two is unclear. Carollia is on occasion insectivorous (Datzmann et al. 2010), and it may also disperse larger-seeded plants (Melo et al. 2009), while Stunira, usually a Solanum specialist, sometimes also eats Piper (Fleming 1986). Old World species of Piper are bird-dispersed (Fleming 2004). See also Clade Asymmetries.

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). 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). There is considerable variation in the nature (druses, raphides) and pattern of oxalate deposition in the leaf (Horner et al. 2009, 2012 - spectacular under polarizing light), but there is not that much correlation with phylogeny.

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 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).

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); this entails redrawing the old subfamilial boundaries.

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).

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); vessel elements often with scalariform perforation plates; petiole bundles arcuate or annular; crystals 0; cuticle waxes as parallel platelets; (lamina vernation involute - Anemopsis, Saururus), stipules +, intrapetiolar; bract at base of inflorescence 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, 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, Saururus Inflorescence © E. Pontieri.]

Age. A possible crown-group age for the family is (84-)78, 75(-69) m.y. (Wikström et al. 2001) or (77-)54, 47(-26) m.y. (Bell et al. 2010).

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

Pollination 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 vessel elements with simple 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; Massoni et al. 2014), although they are not found in morphological studies.