EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], 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 its length [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band of microtubules [where cell plate will join parental cell wall], phragmoplast + [cell wall deposition spreading from around the spindle fibres], 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.

STOMATOPHYTES

Abscisic acid, L- and D-methionine distinguished metabolically; 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 [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.

POLYSPORANGIOPHYTA†

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

TRACHEOPHYTA†

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

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

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].

[MONILOPHYTA + LIGNOPHYTA]

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]; LITTLE ZIPPER proteins.

LIGNOPHYTA†

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].

SEED PLANTS†

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].

EXTANT SEED PLANTS / SPERMATOPHYTA

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]; 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; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; 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.

ANGIOSPERMAE / MAGNOLIOPHYTA

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.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: ?

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled, calyx and corolla distinct, stamens = 2x K, (often numerous, but then usually fasciculate and/or centrifugal), pollen tricolporate, G [5], G [3] also common, if G [2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; whole genome triplication; RNase-based gametophytic incompatibility system present.

[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].

[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??

[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].

ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.

ROSID I / FABIDAE / [ZYGOPHYLLALES [the COM clade + the nitrogen-fixing clade]]: endosperm scanty.

[the COM clade + the nitrogen-fixing clade]: ?

[CELASTRALES [OXALIDALES + MALPIGHIALES]] / the COM clade: seed exotegmic, cells fibrous.

[OXALIDALES + MALPIGHIALES]: ?

MALPIGHIALES Martius  Main Tree.

Vessel element type?; (sieve tubes with non-dispersive protein bodies); (stomata paracytic); (extra-floral nectaries +); lamina margin toothed [teeth with a single vein running into a congested ± deciduous apex]; stigma dry. - 36 families, 716 genera, 16,065 species.

Age. Crown Malpighiales may have begun to radiate some time in the Cretaceous-late Aptian, some (119.4-)113.8(-110.7) or (105.9-)101.6(-101.1) m.y.a. (Davis et al. 2005a; see also Xi et al. 2012b: table S7). Most other estimates are rather younger. The age of crown group Malpighiales was estimated as (93-)92, 90(-89) m.y., with Bayesian relaxed clock estimates slightly older, to 106 m.y. (H. Wang et al. 2009). Wikström et al. (2001) suggested an age for the crown group of (84-)81, 77(-74) m.y., Magallón and Castillo (2009) estimated a crown-group age of ca 89.3 m.y., and Bell et al. (2010) an age of (97-)92, 89(-88) m. years.

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. The order contains ca 7.8% eudicot diversity (Magallón et al. 1999).

When the phylogeny of the group was considered to be rather like a starburst (see also below), the separation into the 15 or more clades that were then recognised, including individual families like Pandaceae, Caryocaraceae, Euphorbiaceae, Ochnaceae s.l., and Humiriaceae, was thought to have happened very rapidly in the late Aptian (Cretaceous), about 114-101 m.y.a. (Davis et al. 2005a). Even with younger estimates for the age of the order, stem groups of most families were thought to have evolved by the end of the Cretaceous (Wikström et al. 2001).

Diversification rates in the order are thought to have been moderately high (Magallón & Castillo 2009). Xi et al. (2012b: see different methods of analysis) examined diversification rates throughout the clade, and found about eight clades in which the rates of diversification decelerated and about five in which they accelerated; these are mentioned individually below.

Endress et al. (2013; see also Xi et al. 2012b in part) summarized floral variation in the order and found features potentially characterising most of the suprafamilial clades. Three-carpellate gynoecia occur in many families, articulated pedicels are also frequent, while paracytic stomata may characterise a sizeable clade here. Tokuoka and Tobe (2006) integrate testa anatomy and embryology with phylogeny. See also Kubitzki (2013a) for comments. Furness (2011) looked at pollen development, focusing on the parietal-placentation clade; the massive amount of detail that she found is difficult to optimize on a tree, partly at least because of the sampling.

Ecology & Physiology. Malpighiales are particularly important in tropical rainforests where they are a major component of the diversity, especially of the woody understory; they account for up to some 28% of the species and 38% of the total stems there (Davis et al. 2005a); members of Ericales, especially families like Sapotaceae and Lecythidaceae, are another major component of this vegetation. There are 10 families of Malpighiales with one or more species of the 227 species that make up half of all the trees with a d.b.h. 10 cm or more in Amazonian forests (for a total of 43 species, i.e. about 20% - ter Steege et al. 2013).

Cretaceous diversification times for many of the clades in Malpighiales suggest that tropical rainforest was developing then (see also Kubitzki 2013a; Rafflesiaceae, Thismiaceae). However, other evidence suggests that such forest may not have developed until early in the Caenozoic (Burnham & Johnson 2004, see Caenozoic Diversification), somewhat at odds with the dates just mentioned.

Plant-Animal Interactions. Caterpillars of outgroups to Nymphalidae-Nymphalinae and -Melitaeini, etc., are quite common on Mapighiales, especialy on families like Violaceae and relatives, Euphorbiaceae, etc. (Nylin & Wahlberg 2008; Nylin et al. 2013). The butterfly Cymothoë, with about 75 species, has hosts widely scattered in this order (Ackery 1988), although also found on Bignoniaceae (one species) and Rhamnaceae (sometimes another species). Phyllonorycter leaf-mining moths (Lepidoptera-Gracillariidae-Phyllocnistinae), with some 260 species and relatively common in more temperate regions, seem to have diversified on this clade (and especially Fagales) some time in the region of 50.8-27.3 m.y.a., well after the Malpighiales diversified, and after the genus itself evolved, some 76.3-50.3 m.y.a. (Lopez-Vaamonde et al. 2006).

About a quarter of all records of extra-floral nectaries come from Malpighiales (Weber & Keeler 2013).

Genes & Genomes. The intron in the atpF gene has been lost several times in Malpighiales, alone among angiosperms, however, this varies within Euphorbiaceae, Phyllanthaceae, and Picrodendraceae (Daniell et al. 2008).

Chemistry, Morphology, etc. Endress and Matthews (2006b) discuss petal appendages, etc., in the order. Tobe and Raven (2011: see also supplement) provide an invaluable summary of embryological data for the whole order although, as they note, many families are poorly known; they plot the distribution of some characters of embryology and seed on a phylogenetic tree, much of which is unresolved. Endress et al. (2013) summarized the extensive and detailed morphological work that he and his collaborators have carried out on members of the order over the last twenty years and that of other workers; they emphasized that in 13 families (almost 1/3 of the families they recognized) ovules, etc., were largely unknown. For more on pollen morphology and development, still quite poorly known, see Furness (2012, 2013b). Oginuma and Tobe (2010) provide the first chromosome counts for four families in the order.

Phylogeny. Although Malpighiales are now strongly supported as being monophyletic (e.g. Davis et al. 2005a; Wurdack & Davis 2009; Xi et al. 2012b), relationships within them were initially poorly understood (e.g. Soltis et al. 2007a). Studies suggested relationships within particular clades of Malpighiales, e.g. Litt and Chase (1999), Schwarzbach and Ricklefs (2000), Chase et al. (2002), and Davis and Chase (2004), and these were in general agreement with relationships apparent in broader studies. The distinctive Lophopyxidaceae were placed close to Pandaceae (represented by Microdesmis) by Savolainen et al. (2000a; see also Chase et al. 2002); that relationship has held. Davis et al. (2005a) clarified some relationships in Malpighiales in a four-gene (all three compartments) analysis, in particular suggesting an association between the families with parietal placentation (and also Goupiaceae) and that Centroplacus (ex Euphorbiaceae s.l./Pandaceae) should be recognised as a separate family, perhaps sister to Ctenolophonaceae (see also Korotkova et al. 2009 and Soltis et al. 2011 for relationships in Malpighiales). However, Ctenolophonaceae were linked with Erythroxylaceae and Rhizophoraceae, Bhesa with Centroplacaceae, etc. (Wurdack & Davis 2009). A [Balanopaceae [[Trigoniaceae + Dichapetalaceae] [Chrysobalanaceae + Euphroniaceae]]] clade had strong support, e.g. Davis et al. (2005a), Tokuoka and Tobe (2006) and Korotkova et al. (2009). Linaceae had been weakly associated with Picrodendraceae in Chase et al. (2002a), but with Irvingiaceae in Tokuoka and Tobe (2006). It had been suggested that Malpighiaceae were rather weakly associated with Peridiscaceae and were perhaps near Clusiaceae et al. (Chase et al. 2002); for the current position of Peridiscaceae, here in Saxifragales, see e.g. Davis and Chase (2004).

Determining the phylogenetic relationships of Rafflesiaceae has been difficult. Apart from the distinctive and often hard-to-interpret morphologies of Cytinaceae, Apodanthaceae and Mitrastemonaceae, families often associated with Rafflesiaceae, molecular analyses have been problematic in part because of the very long branches in some genes and the general problem of obtaining suitable sequences from holoparasites (e.g. see results from analysing sequences of the mitochondrial atp1 gene - Nickrent et al. 2004a). Indeed, when representatives of all four families were in the same analysis, an apparently monophyletic Rafflesiales could be recovered (Nickrent et al. 2004a). Nickrent (2002) had suggested that Rafflesiaceae themselves might be close to Malvales, however, other analyses, including those in which not all the erstwhile Rafflesiales were included together, suggested a break-up of the group (see also Barkman et al. 2004; Davis & Wurdack 2004; Nickrent et al. 2004a; Davis et al. 2007; Filipowicz & Renner 2010).

Some families have been particularly peripatetic. Irvingia was sister to Erythroxylum in a tree presented by Fernando et al. (1995), and the stipules of Irvingiaceae, Erthroxylaceae and Ixonanthaceae are indeed similar (Weberling et al. 1980). However, Irvingiaceae were weakly associated with Putranjivaceae in Chase et al (2002a) and with Linaceae (close) in Davis et al. (2005a). See Clade 2 below for current ideas of the relationships of Irvingia.

Even in 2011 there were still nine clades composed of two or more families in Malpighiales along with seven separate families that together formed a very substantial polytomy (Davis et al. 2005a; Wurdack & Davis 2009; Xi et al. 2010; Soltis et al. 2011). However, relationships in Xi et al. (2012b) are much more resolved. The major analysis in this study used 78 protein-coding plastome genes and four ribosomal genes; families not included were Lophopyxidaceae, Malesherbiaceae and Rafflesiaceae (the last-named for obvious reasons). Other analyses had included many more taxa but less complete sampling of genes (see Xi et al. 2012b for details).

Malpighiales can now be divided into three main clades, the Salicaceae-Euphorbiaceae, Rhizophoraceae-Clusiaceae, and Malpighiaceae-Chrysobalanaceae clades (clades 1, 2 and 3 below), all with substantial molecular support (>80% ML bootstrap, 1.0 p.p.) and even with a modicum of morphological support. Although at the next level of the tree the clades 2 and 3 have polytomies and clade 1 an only weakly-supported dichotomy, overall the improvement of resolution in the tree is substantial (Xi et al. 2012b), and the relationships suggested there are followed here.

Clade 1. [[Humiriaceae [Achariaceae [[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]]] [[Peraceae [Rafflesiaceae + Euphorbiaceae]] [[Phyllanthaceae + Picrodendraceae] [Linaceae + Ixonanthaceae]]]].

Although support for the [Humiriaceae [Achariaceae [[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]] clade is not strong (Xi et al. 2012b), the part of this clade excluding Humiriaceae (= the parietal clade) has very strong support. Goupiaceae are certainly to be included here, although their association with Violaceae is only weakly supported, as is the position of the combined clade; major relationships in the rest of this clade have strong support (Xi et al. 2012b).

Molecular evidence that a group of families with parietal placentation and (often) three carpels was monophyletic had initially not been compelling (e.g. see Savolainen et al. 2000a; Chase et al. 2002), although part of the rpS 16 gene is absent from Passifloraceae-Passifloroideae and -Turneroideae, Violaceae, and Salicaceae s. str. (and also Linaceae and Malpighiaceae, so really a feature of Malpighiales?: see Downie & Palmer 1992). Salicaceae were weakly associated with Passifloraceae, and in turn with Humiriaceae and Pandaceae, and Violaceae were weakly associated with Achariaceae (and Goupiaceae, Lacistemataceae and Ctenolophonaceae) in Chase et al (2002). Tokuoka and Tobe (2006) found a weakly-supported relationship between the Passifloraceae group and Violaceae (see also Soltis et al. 2007a), and strongly supported relationships between Lacistemataceae and Salicaceae. However, Davis et al. (2005a) found a poorly/moderately supported association of these taxa with parietal placentation (59% bootstrap, 1.00 posterior probability), and also Goupiaceae, with axile placentation, and a similar grouping is also evident in e.g. Wikström et al. (2001), Wurdack and Davis (2009), Korotkova et al. (2009: 83% jacknife, 1.00 pp, Goupiaceae not included) and Soltis et al. (2011: details of relationships unclear). Ixonanthes was rather surprisingly embedded in Achariaceae in the Bayesian analysis of Soltis et al. (2007a), but that was due to misidentification of the material, which was a species of Hydnocarpus (K. Wurdack, pers. comm.).

Indeed, classical morphological studies had suggesed a group that included Salicaceae, Achariaceae and Violaceae, Flacourtiaceae, and Passifloraceae and its segregates, Malesherbiaceae and Turneraceae, in part because of their common possession of parietal placentation, some sort of corona or scales in the flower, nectaries outside the stamens, etc. (e.g. Cronquist 1981). However, a number of other families now known to be quite unrelated, some now in Cucurbitales, were also included. Interestingly, species of the old Flacourtiaceae had one of two kinds of seed coat: the exotegmen was either more or less fibrous - taxa with this kind of exotegmen are now mostly in Salicaceae - or massive and non-fibrous - taxa with this exotegmen are now in Achariaceae (Corner 1976). It was also commonly recognized that Salicaceae were simply an extreme morphology reflecting the wind pollination common in that family, and that they could be linked with some of the old Flacourtiaceae. Distinctive cyclopentenoid cyanogenic glucosides and/or cyclopentenyl fatty acids, including gynocardin, also occur sporadically here (Webber & Miller 2008). The inclusion of Goupiaceae in this clade is the only real surprise since it is morphologically rather distinct.

The other weakly supported clade in Clade 1 is [[Peraceae [Rafflesiaceae + Euphorbiaceae]] [[Phyllanthaceae + Picrodendraceae] [Linaceae + Ixonanthaceae]]]], the euphorbioids. This is an unexpected clade in that the fruits of a rather broadly delimited Euphorbiaceae (inc. both Phyllanthaceae and Putranjivaceae) are very distinctive, with the walls falling away leaving the persistent columella, and that was one of the main characters that I used to use to recognize herbarium material of the extended family. It is hardly surprising that Merino Sutter and Endress (1995) argued for a broad circumscription of the family. However, the clade [[Phyllanthaceae + Picrodendraceae] [Linaceae + Ixonanthaceae]] is strongly supported, as is the [Peraceae [Rafflesiaceae + Euphorbiaceae]] clade (Xi et al. 2012b). The inclusion of Rafflesiaceae in Malpighiales follows the recent findings of Barkman et al. (2004, 2007), Davis and Wurdack (2004), and in particular Davis et al. (2006), who place it with strong support as sister to Euphorbiaceae s. str.

Clade 2. [[Ctenolophonaceae [Erythroxylaceae + Rhizophoraceae]], [Irvingiaceae + Pandaceae], [Ochnaceae [[Clusiaceae + Bonnetiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]]]].

Weak support for an association of [Caryocaraceae [Linaceae + Irvingiaceae]] with [Rhizophoraceae + Erythroxylaceae] (Soltis et al. 2007a), has not been strengthened, although they have a number of features in common, such as a basally connate androecium, epitropous ovules with an endothelium, etc. (Matthews & Endress 2007). Although Ctenolophonaceae, etc., might also be associated, their floral similarities did not seem to be so great. However, Wurdack and Davis (2009) found support for the clade [Ctenolophonaceae [Erythroxylaceae + Rhizophoraceae]], but further relationships were unclear. Erthroxylaceae are commonly well supported as sister to Erythroxylaceae (e.g. Setoguchi et al. 1999; Schwarzbach & Ricklefs 2000; Chase et al. 2002; Korotkova et al. 2009). In the study by Xi et al. (2012b), the clade [Ctenolophonaceae [Erythroxylaceae + Rhizophoraceae]] (= rhizophoroids) had strong support, [Pandaceae + Irvingiaceae] (= pandoids) had rather weak support (64% ML bootstrap, 0.97 PP). Centroplacus was sister to Pandaceae, but with little support (Wurdack et al. 2004); for Centroplacus, see Clade 3 below.

The clade [Ochnaceae [[Clusiaceae + Bonnetiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]]]] has only weak support (70% ML bootstrap, 0.81 p.p.: Xi et al. 2012b), but its composition is consistent with morphology; Ochnaceae and Clusiaceae et al. also have a generally similar flavonoid spectrum (Hegnauer 1990). For relationships in the core Bonnetiaceae-Podostemaceae clade (= clusioids: Xi et al. 2012b), see Wurdack and Davis (2009; esp. Ruhfel et al. 2011, 2013).

Clade 3. [[Lophopyxidaceae + Putranjivaceae], Caryocaraceae, [Centroplacaceae [Elatinaceae + Malpighiaceae]], [Balanopaceae [[Trigoniaceae + Dichapetalaceae] [Chrysobalanaceae + Euphroniaceae]]]].

Although this clade has strong support in Xi et al. (2012b), relationships within it are still poorly understood. The [Balanopaceae [[Trigoniaceae + Dichapetalaceae] [Chrysobalanaceae + Euphroniaceae]]] and [Putranjivaceae + Lophopyxidaceae] clades (= chrysobalanoids and putranjivoids respectively) are well supported, but the [Centroplacaceae [Elatinaceae + Malpighiaceae]] clade (malpighioids) has poor support. The particular position of the distinctive Caryocaraceae is unclear, althougth there is little question that it belongs here (Xi et al. 2012b). There was some support for Picrodendraceae as sister to the chrysobalanoids in Soltis et al. (2007a: as Pseudanthaceae, Phyllanthaceae not included), but this relationship has not been confirmed.

Classification. See Kubitzki (2013a) for a summary. A.P.G. (1998) thought that it would be useful to adopt a narrow circumscription for families that used to be included in Flacourtiaceae and Euphorbiaceae s.l. (both in Clade 1 above). Even if future work were to suggest reaggregation of genera that had been placed in those two families, the composition of the clades that were even then apparent were quite different from those in previous classifications. Indeed, the realignments caused by the break-up of the old Flacourtiaceae and integration with Salicaceae and Achariaceae correlate well with a number of morphological and anatomical characters (Wurdack & Davis 2009). Furthermore, these earlier decisions are compatible with the tree in Xi et al. (2012b). To restore Euphorbiaceae to close to its old broad circumscription would require the inclusion of Linaceae, Ixonanthaceae and Rafflesiaceae, making a very heterogeneous and perplexing group. Similarly, the relationships in the clusioid group necessitated the break-up of the old Clusiaceae/Guttiferae (see also A.P.G. 2003, 2009, 2016).

Previous Relationships. The history of the circumscription and putative relationships of the small family Ixonanthaceae, here sister to Linaceae (Clade 1, with strong support), is an example of problems taxonomists have faced in circumscribing major groups in this whole area, and in justifying relationships - yes, there are distinctive characters, but which reliably indicate relationships? Ixonanthaceae have been associated with a variety of families, although Van Hooren and Nooteboom (1988) noted that they had often been linked to Linaceae. Thus Robson and Airy Shaw (1962) thought that the "spiral convolution of the filaments and style" of Cyrillopsis (Ixonanthaceae) was a point of similarity between this genus and Irvingiaceae (Clade 2). Some species of Ochthocosmus (Ixonanthaceae) also have flowers very similar to those of Cyrillopsis, with the thin calyx reflexed after anthesis (Ixonanthes), while other species of Ochthocosmus have persistent, erect, almost scarious-looking sepals, as is common in Linaceae. Allantospermum has flowers very similar to those of Cyrillopsis, and its relationships have presented particular problems, the genus seeming to be intermediate between the Ixonanthes and Irvingia groups. Forman (1965) placed it with the former group, both groups, he thought, being subfamilies in Ixonanthaceae, while Nooteboom (1967) placed it in the latter group, the two being subfamilies of Simaroubaceae. Pollen suggested to Oltmann (1971) that Allantospermum was in Ixonanthaceae, Irvingiaceae were not related. Takhtajan (1997) included Allantospermum in Irvingiaceae, close to Simaroubaceae, while Ixonanthaceae were in Rutales. Irvingia was included in Simaroubaceae-Sapindales by Cronquist while Ixonanthaceae were in Linales (1981). Bove (1997: morphological phylogenetic analysis), on the other hand, suggested that Ixonanthaceae and Humiriaceae (also Clade 1, but not immediately related) were sister taxa, both having ellagic acid, a "free" annular nectary encircling the ovary, and an entire stigma. In the context of Linales (also including Linaceae, Hugoniaceae, Erythroxylaceae [also Clade 2, not immediately related to Irvingiaceae]: see Cronquist 1981), Ixonanthaceae were rather different in their free stamens, semi-inferior ovaries and pollen grains with supratectal spines (Bove 1997). Byng et al. (2016) link Cyrillopsis with Irvingiaceae, a position with which morphology and chemistry are in general agreement.



Includes Achariaceae, Balanopaceae, Bonnetiaceae, Calophyllaceae, Caryocaraceae, Centroplacaceae, Chrysobalanaceae, Clusiaceae, Ctenolophonaceae, Dichapetalaceae, Elatinaceae, Erythroxylaceae, Euphorbiaceae, Euphroniaceae, Goupiaceae, Humiriaceae, Hypericaceae, Irvingiaceae, Ixonanthaceae, Lacistemataceae, Linaceae, Lophopyxidaceae, Malpighiaceae, Malesherbiaceae (= Passifloraceae-Malesherboideae), Medusagynaceae (= Ochnaceae-Medusagynoideae), Ochnaceae, Pandaceae, Passifloraceae, Peraceae, Phyllanthaceae, Picrodendraceae, Podostemaceae, Putranjivaceae, Quiinaceae (= Ochnaceae-Quiinoideae), Rafflesiaceae, Rhizophoraceae, Salicaceae, Trigoniaceae, Turneraceae (= Passifloraceae-Turneroideae), Violaceae.

Synonymy: Linineae Shipunov, Rhabdodendrineae Shipunov, Rhizophorineae Shipunov - Balanopales Engler, Chailletiales Link, Chrysobalanales Link, Elatinales Martius, Erythroxylales Link, Euphorbiales Berchtold & J. Presl, Flacourtiales Martius, Garciniales Martius, Homaliales Martius, Hypericales Berchtold & J. Presl, Irvingiales Doweld, Lacistematales Martius, Linales Berchtold & J. Presl, Malesherbiales Martius, Marathrales Dumortier, Medusagynales Reveal & Doweld, Ochnales Berchtold & J. Presl, Pandales Engler & Gilg, Passiflorales Berchtold & J. Presl, Phyllanthales Doweld, Podostemales Lindley, Rafflesiales Martius, Rhizophorales Berchtold & J. Presl, Salicales Lindley, Samydales Berchtold & J. Presl, Sauvagesiales Martius, Scyphostegiales Croizat, Stilaginales Martius, Turnerales Link, Violales Berchtold & J. Presl - Euphorbianae Reveal, Ochnanae Doweld, Podostemanae Reveal, Rafflesianae Reveal, Rhizophoranae Reveal & Doweld, Violanae Reveal - Malpighiopsida Bartling, Passifloropsida Brongniart, Podostemopsida G. Cusset & C. Cusset, Salicopsida Bartling, Violopsida Brongniart

[[Ctenolophonaceae [Erythroxylaceae + Rhizophoraceae]], [Irvingiaceae + Pandaceae], [Ochnaceae [[Bonnetiaceae + Clusiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]]]] / Clade 2 of Xi et al. (2012b): cristarque cells +.

Age. The crown age of this clade is (110.9-)106.6, 105.2(-99.9) m.y. (Xi et al. 2012b: Table S7) or around 101.1/100.5 m.y. (Tank et al. 2015: table S1, S2).

[Ctenolophonaceae [Erythroxylaceae + Rhizophoraceae]] / rhizophoroids: leaves opposite, stipules enclosing the terminal bud, interpetiolar; pedicels articulated; nectary outside of A; A 2 x C [usu. 10, of two lengths, antepetalous stamens longer than antesepalous], anthers ± basifixed, connate basally, (minute corona +); G postgenitally united, placentation apical, stigmas capitate/lobed, papillate; ovules 2/carpel, collateral, epitropous, outer integument thinner than the inner, nucellus laterally thin, disintegrates, endothelium +, placental obturator +; K persistent in fruit; seeds arillate, exotestal; endosperm +.

Age. The crown age of this clade is around (68.6-)66.7(-65.4) m.y.a. (Xi et al. 2012b: Table S7).

Chemistry, Morphology, etc. Matthews and Endress (2011) provided many details of the floral morphology of these three families. Tobe and Raven (2011) suggested that all have a multiplicative inner integument, rather, at least sometimes it is very thick by the time of fertilization.

Phylogeny. For relationships in this clade, all well supported, see Xi et al. (2012b).

CTENOLOPHONACEAE Exell & Mendonça   Back to Malpighiales

Ctenolophonaceae

Trees; ellagic acid?; vessel elements with scalariform perforation plates; calcium oxalate as single crystals; cuticle waxes 0; stomata anomo- or anisocytic; petiole bundle arcuate; hairs tufted/stellate; buds perulate; lamina margins entire; inflorescence terminal, ?thyrsoid; K quincuncial, basally connate, (with 1 trace), C protective in bud, contorted, caducous; annular nectary with 10 lobes alternating with A; A basally connate, adnate to base of nectary; pollen 3-9 equatorially colporate [stephanocolporate]; G [2], septae thin, style +, branches short; ovules apical [?level], with zig-zag micropyle, integuments lobed, outer integument ca 5 cells across, inner integument ca 11 cells across; fruit a [?kind] capsule, K swollen; seed single, persisting on columella, columella very thin; aril ± hairy [when dry!], exotestal cells large, subpalisade, the outer wall alone thickened, exotegmic cells laterally flattened, tracheidal; endosperm copious, cotyledons very large, folded; n = ?.

1 [list]/3. W. Africa, Malesia (map: from van Hooren & Nooteboom 1988b; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; fossils [green] from Krutzsch 1989).

Age. The distinctive pollen of Ctenolophon is known fossil from South America and India, the earliest records being from Africa in the Upper Cretaceous ca m.y.a. (Muller 1981; Krutzsch 1989).

Evolution. Divergence & Distribution. The diversification rate in this clade may have decreased (Xi et al. 2012b).

Chemistry, Morphology, etc. Like Humiriaceae, there are "marginal" stomata on the nectary and the anthers have a broad connective (Link 1992b); the wood anatomy is also similar. Takhtajan (1999) perhaps implies that there may be an endothelium, but embryology, etc., are largely unknown.

Some general information is taken from van Hooren and Nooteboom (1984, 1988b) and Kubitzki (2013b); for seed anatomy, see Huber (1991).

Previous Relationships. "Ctenolophon was almost universally recognized as belonging to the Linaceous alliance" (van Hooren & Noteboom 1988: p. 629).

[Erythroxylaceae + Rhizophoraceae]: tropane [hygroline] and pyrrolidine alkaloids, non-hydrolysable tannins +; sieve tube plastids with protein crystalloids; mucilage cells common; stomata paracytic; lamina vernation involute, colleters +; inflorescence cymose; K valvate, postgenitally united, C ± clawed, conduplicate, petals enclosing a stamen/stamens; median G adaxial, style somewhat impressed; (micropyle endostomal); fruit a septicidal capsule; exotestal cells enlarged, thick-walled, ± tanniniferous; endosperm starchy, embryo chlorophyllous.

Age. Estimates for the age of this node are (58-)54, 49(-45) m.y. (Wikström et al. 2001), (63.1-)54.6(-38.4) m.y. (Xi et al. 2012b: Table S7), (79-)63, 60(-44) m.y. old (Bell et al. 2010), or around 74.7 m.y. (Tank et al. 2015: table S2) - Davis et al. (2005a) would put it at (119-)114(-110/(106-)102 m.y., but in the context of a different topology.

Chemistry, Morphology, etc. For floral development, see Matthews and Endress (2007).

Phylogeny. Although an unexpected family pair when contrasting Erythroxylum with mangrove Rhizophoraceae, the latter are very derived, so when comparing Aneulophus (Erythroxylaceae) with non-mangrove Rhizophoraceae, the differences are less stark, and as noted above the two families are united by several synapomorphies.

ERYTHROXYLACEAE Kunth, nom. cons.   Back to Malpighiales

Erythroxylaceae

Smallish trees and shrubs (deciduous); mycorrhizae 0; ellagic acid 0; vessel elements with simple perforation plates; wood commonly with SiO2 grains; nodes with lateral bundles originating well before the central, forming cortical bundles; sclereids +; petiole bundle arcuate to annular with medullary and adaxial bundles; stomata also parallelocytic; branching from previous flush; buds perulate; leaves two-ranked (spiral; opposite), lamina margins entire, stipules intrapetiolar and hooded or interpetiolar; inflorescence often fasciculate; (pedicel not articulated - Aneulophus?), heterostyly common; (hypanthium + - Nectaropetalum); K connate basally, C protective in bud, with fringed bilobed ligule (0); nectary glands just below ligule; A obdiplostemonous, latrorse, (connective not thickened); pollen grains tricellular; G [(2-)3(-4)], adaxial only fertile [Erythroxylum], (short), (stylar canal +), style branches ± well developed, stigma ± capitate; ovule also 1/carpel, outer integument 2-5 cells across, inner integument (ca 3?-)5-9 cells across, parietal tissue 2-4 cells across, nucellus below embryo sac extensive, hypostase 0, 2 vascular bundles in raphe; fruit a drupe, 1-seeded, or septicidal capsule [Aneulophus], A also persistent; (aril 0); testa weakly multiplicative, tegmen strongly multiplicative or not, exotegmen with reticulate thickenings [?all], innermost cuticle well developed; (endosperm 0); n = 12.

4 [list]/240: Erythroxylum (230). Pantropical, esp. American (map: from van Steenis and van Balgooy 1966; Heywood 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower, Fruit.]

Age. The crown age of Erythroxylaceae is (42.5-)19.3(-12.3) m.y. (Xi et al. 2012b: Table S7, An. + Ery.).

Evolution. Divergence & Distribution. The rate of diversification may have increased in Erythroxylaceae (Xi et al. 2012b).

Plant-Animal Interactions. Cocaine is sequestered by the larvae of Eloria noyesi, a lymanitrid moth, that feeds on Erythroxylum.

Chemistry, Morphology, etc. The nodes were described as being unilacunar by Sinnott (1914), however, there are lateral traces although their gaps may be inconspicuous and the traces themselves may depart from the vascular cylinder well before the central trace (Rury 1982). Erythroxylum sometimes has milky exudate. Are the lamina teeth theoid? The leaves of Erythroxylum coca were described as being revolute by Cullen (1978); they are involute (e.g. Peyritsch 1878; Weberling et al. 1980; Rury 1982; Keller 1996).

Matthews and Endress (2011) described the complexity of the postgenital fusion of the petals.

For general information, see van Tieghem (1903d: inc. some anatomy) and Bittrich (2013), for chemistry, see Hegnauer (1966, 1989) and Aniszewski (2007), for foliar anatomy, see van Welzen and Baas (1984), and for ovule and seed, see Rao (1968) and Boesewinkel and Geenen (1980).

Previous Relationships. In the past, Erythroxylaceae have been associated with Linaceae and Humiriaceae, and thence linked with Geraniales (Narayana & Rao 1978b), or the three families together are placed in Linales (Cronquist 1981); some have even toyed with the idea of including Erythroxylaceae and Linaceae in the one family (Boesewinkel & Geenen 1980 and references).

Synonymy: Nectaropetalaceae Exell & Mendonça

RHIZOPHORACEAE Persoon, nom. cons.   Back to Malpighiales

Rhizophoraceae

Trees; ellagic acid +; root hairs 0; vessel elements with simple and/or scalariform perforation plates; true tracheids +; pits vestured; cristarque cells 0; subepidermal laticifers in flower; branching from current flush; inflorescence axis often evident; K (3-)4-5(-16), C small, often hairy, variously lobed, fringed, or with filiform appendages, or aristate; anthers ± dorsifixed, (fasciculate), (free); nectary inside A, on ovary or hypanthium; G opposite sepals when 5, when 2, collateral, septae often thin/disintegrating, style +, stigma also ± punctate, ?type; (micropyle also zig-zag), outer integument 3-6 cells across, inner integument 4-8(-20?) cells across, (endothelium 0), parietal tissue 1-3 cells across; megaspore mother cells several; (endotesta crystalliferous); endosperm with micropylar and chalazal haustoria + [?distribution], embryo (short), green; chromosomes ca 1 µm long; germination epigeal, cotyledonary node unilacunar.

16 [list]/149. Four groups below. Pantropical (map: from Ding Hou 1958; van Steenis 1963; Fl. Austral. 8. 1984; Tomlinson 1986; Juncosa & Tomlinson 1988a; Levin 1992; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower, Flower, Fruit.]

Age. The crown age of this clade is (54.5-)41.7(-30.4) m.y. (Xi et al. 2012b: Table S7, c.f. topology).

[Macariseae + Paradrypetes]: ?

1. Macarisieae Baillon

Nodes 1:1 + split laterals [?all]; calcium oxalate crystals solitary; (leaves bijgate [Cassipourea), ("alternate"), stipules valvate; (hypanthium +); K open; anthers latrorse; G [2-6], stigma not lobed; (seeds winged at micropylar end), (arillate); n = 18, 21, 32; (seedlings with root hairs - Cassipourea).

7/94: Cassipourea (62), Dactylopetalum (15). Tropical America and Africa, also peninsula India and Sri Lanka.

Synonymy: Cassipoureaceae J. Agardh, Legnotidaceae, nom. illeg., Macarisiaceae J. Agardh

2. Paradrypetes Kuhlmann

Raphides +; plant glabrous; lamina with long, zig-zag intersecondary veins; plant dioecious; inflorescence epiphyllous, on petiole; flowers small; P +, uniseriate, 3-4, imbricate; staminate flowers: anthers extrose, filaments ± 0; pollen 4-colporate, surface spiny; nectary 0; pistillode 0; carpellate flowers: staminodes 0[?]; G [3], style 0, stigmas broad; ovule with placental obturator; fruit a drupe, 1-seeded; ; seed coat vascularized; endosperm starchy, abundant, cotyledons plicate, broad; n = ?

1/2. Upper Amazon and Atlantic Forest, Brasil (map above: green).

[Gynotrocheae + Rhizophoreae]: stilt roots present; leaves bijugate (not - Pellacalyx); hypanthium +; ovary ± inferior; obturator 0; fruit indehiscent; aril 0, testa vascularized.

Age. This node has been dated to (15-)13, 9(-7) m.y. (Wikström et al. 2001) and (15-)9, 8(-2) m.y. (Bell et al. 2010), which are very unlikely estimates (see below).

3. Gynotrocheae Engler

(Stilt roots 0 - Pellacalyx); (lamina margins entire), (stipules not sheathing terminal bud); (plant dioecious - Gynothroches); (petals entire); (A 5, opposite K - Carallia); G [3-28], septae ± developed or not, (style branched - Gynotroches); ovules (to 8/carpel), outer integument 2-3 cells across, inner integument 2-6 cells across, parietal tissue 0, endothelium +; (megaspore mother cell 1); fruit a berry; exotesta mucilaginous, tanniniferous, other testal cells crystalliferous, tegmen 0, or fibrous to palisade, meso- and endotegmen persist; cotyledons short, or large, involute [Carallia, Pellacalyx]; n = 14.

4/30: Crossostylis (10). Indo-Malesia, Madagascar.

4. Rhizophoreae Bartling

Nodes 5:5, 7:7, + split-laterals; cortical, etc., fibres; stomata cyclocytic; abaxial hypodermis +; sclerenchymatous sheath of midrib at most weakly developed; lamina vernation supervolute, margins entire; flowers 4-16-merous; (C postgenitally united above base); (anthers locellate - Rhizophora); G [2-3]; outer integument ca 25 cells across, inner integument 5-6 cells across, parietal tissue ca 2 cells across, endothelium ?+; fruit indehiscent, 1-seeded; seeds large, coat undifferentiated, tegmen not persisting; (endosperm overflows from seed); (cotyledons connate Rhizophora; convolute - Rhizophora, Bruguiera); n = 18; seeds viviparous, radicle 0 [Rhizophora]; cotyledonary node tri- or multilacunar.

4/17: Rhizophora (?9). Pantropical, centred on the eastern Indian Ocean, introduced into the central Pacific and Hawaii (map above: blue; Spalding et al. 2010).

Age. Ricklefs et al. (2006) dated crown Rhizophoreae to ca 50 m.y. ago.

Synonymy: Mangiaceae Rafinesque

Evolution. Divergence & Distribution. Crossostylis, with dehiscent fruits and arillate seeds, is embedded in Gynotrocheae, which otherwise have fleshy, indehiscent fruits and seeds without arils. Dehiscent fruits may have evolved in parallel in Crossostylis - Schwarzbach (2013: p. 291) describes dehiscence there as "tardy with distal slits or an operculum", and this seems rather different from the septicidal fruits of Macarisieae, but both may have arillate seeds.

Mangrove taxa are derived within Rhizophoraceae (e.g. Schwarzbach & Ricklefs 2000) and are most diverse in the Southeast Asia-Malesian area. Their seeds have little endosperm and are viviparous (aquatic/marine/mangrove plants commonly have large embryos, and in some the seed starts to germinate before it falls off the plant), and in all genera except Bruguiera the endosperm overflows from the seed, pushing open the micropyle as it does so. After the seed falls from the tree it may float in the water, and after grounding the hypocotyl straightens, lateral roots develop, and the seeding becomes established (Juncosa & Tomlinson 1988b). Depending on the genus, there are either stilt roots, plank roots, or pneumatophores (Gill & Tomlinson 1975). Axillary buds soon die so the plants cannot regenerate when cut or if the twigs are killed by frost, etc. (see Tomlinson 1986 for much useful information). Rhizophoraceae are an example of the relatively uncommon situation in flowering plants where salt tolerance was acquired quite deep in the phylogeny, being retained since (Moray et al. 2015: ?6 inferred origins?).

Ecology & Physiology. The term "mangrove" refers both to members of Rhizophoraceae-Rhizophoreae in particular and also to mangrove vegetation in general, of which Rhizophoreae are a prominent component, but which also includes a few palms and members of several other families. Here I am talking about mangrove vegetation - for general accounts, see Tomlinson (1986), Spalding et al. (2010), Faridan-Hanum et al. (2014: Asian mangroves) and Hogarth (2015). For the evolution of the mangrove ecosystem, which also involves diversification of clades of molluscs, etc. (Reid et al. 2008), see Ellison et al. (1999), especially Plaziat et al. (2001 and references) and Ricklefs et al. (2006).

A mere 34 species in nine genera and five families dominate mangrove vegetation, of these, half are Rhizophoraceae-Rhizophoreae, otherwise the taxa are largely unrelated. There are another 20 species in 11 genera and ten families (only one also including dominant species) that are quite common (Tomlinson 1986, estimates in Spalding et al. 2010 are 38 core species, 73 species of true mangroves). Other mangrove families include Primulaceae-Myrsinoideae (Aegiceras), Lythraceae (Sonneratia, ca 7 spp.), Acanthaceae (Acanthus ilicifolius and Avicennia, unrelated), Tetrameristaceae (Pelliceria) and Combretaceae (Lumnitzera, Laguncularia, 3/8 species of Laguncularieae). Of the dominant species, the palm Nypa fruticans in particular forms monospecific stands growing along rivers to the upper limits of tidal influence.

There are two groups of mangrove species. The eastern group, from east Africa to the western Pacific, is much more speciose and includes ca 40 species, ca 14 of which are Rhizophoraceae, while the western group, from west Africa to the Americas, is made up of only eight species, three of which are Rhizophoraceae. Depending on how species limits are drawn, no major mangrove species is common to the two areas (Tomlinson 1986). This division of mangroves into the Indo-West Pacific and the Caribbean-West Atlantic areas seems to have occurred by ca 20 m.y.a. (Plaziat et al. 2001). No dominant mangrove has a non-mangrove sister taxon restricted to the New World, and diversity in the mangrove ecosystem seems to have increased regularly over time, with little extinction (Ricklefs et al. 2006).

However, fossil and current distributions of some mangrove plants seem to have little to do with each other, and the history of individual mangrove species is complicated. By the Eocene, ca 50 m.y.a., many mangrove genera are known from the fossil record, and several, perhaps including the Central American Pelliciera, are known from both the Old and New Worlds (Plaziat et al. 2001; but c.f. Martínez-Millán 2010 for Pelliciera). Nypa (Arecaceae, q.v. for fossils), today found only in the Indo-Malesian area, is first known from the Upper Cretaceous ca 70 m.y.a. and by the early Palaeocene ca 55 m.y.a. it was growing in both the Old and New Worlds (e.g. Leidelmeyer 1966 for Guyana; Plaziat et al. 2001). Sonneratia may be Oligocene in age (Muller 1984). Fossil hypocotyls identified as Ceriops and preserved with good anatomical detail are known from the Lower Eocene London Clay (Wilkinson 1981), although Collinson and van Bergen (2004) noted that the fossils did not the show distinctive curvature of seedlings of extant Rhizophoreae. At the other geographic extreme, Rhizophoreae are known from the Early Eocene 55-48.5 m.y.a. in western Tasmania, Australia (Pole 2007), and this would seem to be the earliest record of the clade - and pretty much in conflict with the family age in Xie et al. (2012b). Rhizophora is known from the Caribbean in the late Eocene ca 50 m.y.a., but the common ancestor of the existing Caribbean populations may have arrived in the New World only ca 11 m.y.a. (Graham 2006). There may be considerable genetic differentiation within Atlantic populations of mangrove species (Takayama et al. 2008a, b).

Mangrove plants all have physiological and anatomical adaptations to the saline, tidal aquatic hanitat (see Reef & Lovelock 2015 and other papers in Ann. Bot. 115(3). 2015). They also tend to have large seeds/embryos, often considerably larger than their non-mangrove relatives (e.g. Moles et al. 2005a), probably connected with the need for fast establishment in the mangrove habitat where small seedlings could easily be washed away by the tides.

The mangrove ecosystem is very productive and has high carbon flux rates, and it also stores much carbon, especially below ground - at about 1,000 Mg C ha-1, storage is about three times as much as in temperate, boreal or tropical upland forests. Mangroves occupy 13.7-15.2 million hectares, and they may store 4-20 PgC globally (Bouillon et al. 2008; Donato et al. 2011 and references). Other estimates are that they bury 17.0-23.6 TgCy-1, their gross primary productivity is 2087 gCm2y-1, global primary productivity is 417 TgCy-1, but with a rather lower net ecosystem production (221 gCm2y-1> and globally 44 TgCy-1) because of a relatively high respiration rate, at least as compared with sea grasses (Duarte et al. 2005: area estimated at 20 million hectares). See also Clade Asymmetries for more data; the age of carbon in the oldest deposists in a core from Kalimantan, Borneo, may be some 24,000 years (Page et al. 2004). For salt and water balance, see Reef and Lovelock (2015) and other papers in Ann. Bot. 115(3). 2015.

Pollination Biology. Pollen in Rhizophoreae is deposited on to the hairy petals, so there may be secondary pollen presentation, but pollination is basically explosive, the stamens being held in groups by the petals until the flower is tripped by the pollinator. The petals often have an arista or other appendages and are shaped like a tiny bivalve mollusc (Endress & Matthews 2006b). The pollen grains are very small, and in Rhizophora in particular pollination may be by wind (Juncosa & Tomlinson 1988b).

Chemistry, Morphology, etc. Growth in a number of Rhizophoraceae may be continuous, although growth patterns in Macarisieae are unknown. Cork initation in the root is superficial in at least some taxa, perhaps just those with stilt roots (see von Guttenberg 1968 for Carallia), and their aerial roots are polyarch (Gill & Tomlinson 1975). Robert et al. (2009) discuss the hydraulic architecture of the wood of Rhizophora. The leaf teeth are theoid. The colleters of Rhizophoreae, at up to 1.5 mm long, are notably larger than those of other members of the family (Sheue et al. 2013: Paradrypetes not studied).

There is considerable variation in floral merosity in the family, both carpel and stamen number varying considerably (Matthews & Endress 2011). The stamens in polystemonous flowers arise from ring primordia (Ronse de Craene & Smets 1992b). Rhizophora has transversely arranged carpels (Eichler 1876). Variation in testal morphology in Gynotrocheae in particular is considerable, Gynotroches and Pellacalyx, with strongly exotegmic seeds, differing so much from Carallia, which lacks an exotegmen, that Corner (1976) preferred to segregate the former as Legnotidaceae - a comprehensive survey of seed anatomy in the family is desirable.

The morphology of the embryo of the mangrove species is interesting. In Rhizophora, at least, the radicle is deep-seated in origin, and in that genus and Ceriops it seems to be non-functional, the root system of the seedling being developed from axillary roots; Bruguiera does have a functional radicle (Kipp-Goller 1939; Juncosa 1982). The cotyledons of Rhizophora are connate when initiated (Juncosa 1982).

See also Juncosa and Tomlinson (1988) and Schwarzbach (2013), both general, Howard (1970: nodal anatomy), Baranova and Jeffrey (2006: leaf anatomy), Endress and Matthews (2006b: petal morphology), Carey (1934) and Mauritzon (1939a), both embryology, Tobe and Raven (1987e, 1988b: seed coat anatomy); for information on Paradrypetes, see also Levin (1986, 1992) and Radcliffe Smith (2001 - as Euphorbiaceae).

Phylogeny. Schwarzbach and Ricklefs (2000: Paradrypetes not included) found strong phylogenetic structure in the family, with three major clades. At least some Macarisieae have stamens of two lengths and well-developed anther connectives (D. Kenfack, pers. comm.), probably plesiomorphic features.

Rather surprisingly, molecular data also place Paradrypetes (ex Euphorbiaceae) here (e.g. Davis et al. 2005a), strongly supported as sister to Cassipourea (Wurdack & Davies 2008: only one species from each tribe included). Paradrypetes has a rather unexpected combination of characters and is highly apomorphic (see above).

Classification. Schwarzbach and Ricklefs (2000) suggested that three tribes be recognized for the three major clades that were apparent in their phylogeny of the family.

Previous Relationships. Rhizophoraceae have often been associated with Myrtales (Cronquist 1981) or Myrtanae (Takhtajan 1997), largely because of their vestured pits, opposite leaves, and inferior ovary (e.g. Cronquist 1981; Takhtajan 1997), and they have sometimes also included or been closely associated with (Takhtajan 1997) Anisophylleaceae, here in Cucurbitales.

[Irvingiaceae + Pandaceae] / pandoids: leaves two-ranked, at least on plagiotropic axes; lamina vernation involute; flowers small; K connate basally; anthers basifixed; ovule 1/carpel, apical, pendulous, epitropous; fruit indehiscent; exotesta and endotegmen tanniniferous.

Age. The divergence of these families is estimated at (107.1-)91.2(-70.5) m.y. in Xi et al. (2012b: Table S7). Although Davis et al. (2005a) did not recover this clade, the two families were both in isolated positions in his analysis, and he dated their stem-group ages to somewhere between 119-97.5 m.y.aago

Evolution. Divergence & Distribution. The rate of diversification of this clade - it contains ca 25 species - may have decreased (Xi et al. 2012b).

Economic Importance. Embryos of both Panda and Irvingia are rich in fats and are much used locally.

IRVINGIACEAE Exell & Mendonça   Back to Malpighiales

Irvingiaceae

Trees; ellagic acid, myricetin +; vessel elements with simple perforation plates; nodes ?multilacunar; (sclereids +); stomata paracytic, veins vertically transcurrent; lamina margins entire, secondary veins strong, rather close and subparallel, tertiary veins also ± parallel and at right angles to the secondary veins, stipules intrapetiolar, deciduous; inflorescences racemose, branched, axillary or terminal; pedicels basally articulated; K cochlear; C protective in bud, cochlear or quincuncial, with 3 traces; A (9) 10, latrorse, filaments [and style] folded in bud; pollen ± triangular [polar view]; nectary massive, annular, vascularized from staminal traces; G [(2) 5], G median (when 2) or opposite sepals, style single, stigma subcapitate-papillate, ?type; cotyledons large, cordate.

4[list]/12: Irvingia (7) - two groups below. Africa, Madagascar; South East Asia to W. Malesia (map: from Harris 1996). [Photo - Fruit]

1. Allantospermum Forman

Vessel/tracheid pits minute, half bordered; petiole bundles arcuate (plus adaxial-annular); fruit a septicidal/part loculicidal capsule with columella.

1/2. Madagascar, West Malesia.

2. Klainedoxa Engler + Irvingia J. D. Hooker

Secretory canals +; epidermal mucilage cells +; petiole bundle annular, (with inverted adaxial bundles in sheath); stipules very long and ensheathing terminal bud; ovules ± sessile, attachment broad, funicle thick, micropyle bistomal, outer integument 2-3 cells across, inner integument 3-4 cells across, parietal tissue 3-4 cells across, (nucellar cap +, weak), epidermis at nucellar apex with radially elongated cells, suprachalazal zone massive, placental obturator +, hypostase 0; embryo sac becomes long; fruit a 1-seeded berry, 1- or 5-seeded drupe, or samara; hilum long [Irvingia], K deciduous or not; outer (esp.) and inner integuments multiplicative, testa vascularized, exotegmen fibrous/tracheidal, the rest ± collapsed; endosperm copious to 0; n = 13, 14, chromosomes 0.7-1.4 µm long; germination epigeal, phanerocotylar.

3/10. Africa; South East Asia to W. Malesia.

Evolution. Divergence & Distribution. Klainedoxa and Irvingia diverged (22.6-)11.8(-4.1) m.y.a. (Xi et al. 2012b: Table S7).

Chemistry, Morphology, etc. Keller (1996) suggests that the leaves are involute in bud; this should be confirmed.

Forman (1965) descibed the seeds of Allantospermum as pulling away from a basal arilloid process. Netolitzky (1926) is unclear about exactly where the fibrous layer is in the seeds of Desbordea and Klainedoxa, suggesting that the latter is exotestal, although Boesewinkel (1994) calls it exotegmic, which seems more likely.

See also Harris (1996: monograph) and Kubitzki (2013b) for general information, Forman (1965: Allantospermum), also Jadin (1901), Rojo (1968) and van Tieghem (1905a: stomata anomocytic?), all anatomy, Nooteboom (1967: esp. chemistry), van Welzen and Baas (1986: foliar anatomy), Weberling et al. (1980: stipules), Link (1992c: nectary), and Tobe and Raven (2011: stamen, ovules and seed: Irvingia alone); details of floral orientation are taken from Eckert (1966).

Phylogeny. Relationships are [Allantospermum [Klainedoxa + Irvingia]] (Byng et al. 2016: support good).

Previous Relationships. All over the place, both in early molecular studies and in morphological studies - see introduction to the order. Prior to xii.2015, Allantospermum was in Ixonanthaceae...

PANDACEAE Engler & Gilg, nom. cons.   Back to Malpighiales

Pandaceae

Trees to shrubs; chemistry?; cork?; vessels in radial multiples, vessel elements with scalariform (and simple - Galearia) perforation plates; rays 2-9 cells wide; sieve tubes with non-dispersive protein bodies; pericycle also with sclereids; druses and crystals +; petiole bundles D-shaped to (incurved-)arcuate; stomata various, cuticle waxes 0; leaves spiral and reduced on orthotropic axes, lamina with a single vein running into the opaque persistent tooth apex, one stipule higher than the other on the stem; inflorescences various; plant dioecious; K free to ± connate, C valvate or imbricate, petals usu. thick, hooded to flat; nectary 0; staminate flowers: stamens = and opposite sepals, 10, or 15, in one or two series, connective produced or not; pistillode +; carpellate flowers: staminodes 0; G [2-6], style 0, stigmas spreading, laciniate or entire; ovule (straight - Panda), outer integument 3-5 cells across, inner integument 3-5 cells across, nucellar cap ca 6 cells across, obturator 0/+; fruit a 2-5-seeded drupe, stone surface often irregular; exotegmen tracheoidal, (many layered - Panda); endosperm ?development, +, cotyledons incumbent, thin and flat, oily; n = 15.

3[list]/15: Microdesmis (10). Tropics, Africa to New Guinea (map: in part from Léonard 1961; van Welzen 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006).

Age. Crown-group Pandaceae are (72.7-)47(-23.3) m.y.o. (Xi et al. 2012b: Table S7).

Chemistry, Morphology, etc. Panda smells like onions. Microdesmis has punctate leaves. The plagiotropic branches have been confused with compound leaves, especially in the derived Galearia and Panda; the stipules may be asymmetrically placed, as in Panda. If the pedicels are articulated, they are articulated only at the very base.

For general information, see Forman (1966), Radcliffe-Smith (2001), van Welzen (2011) and Kubitzki (2013b), Hegnauer (1969: chemistry), Nowicke (1984) and Nowicke et al. (1998: pollen), Stuppy (1996) and Vaughan and Rest (1969), both seed anatomy, and Tokuoka and Tobe (2003: ovules and seeds) - mostly as Euphorbiaceae.

The embryology, etc., of the family are little known.

Phylogeny. What is known about wood anatomy suggests that Galearia and Panda are close, while pollen suggests that Galearia and Microdesmis are close (van Welzen 2011). The relationships [Microdesmis [Galearia + Panda]] are strongly supported by molecular data (see Xi et al. 2012b), in line with wood anatomical variation.

Classification. For a checklist and bibliography, see Govaerts et al. (2000, vol. 4).

Previous Relationships. Pandaceae were included in Euphorbiaceae until quite recently, e.g. Govaerts et al. (2000) and Radcliffe-Smith (2001), but they differ from even the uniovulate taxa (Peraceae and Euphorbiaceae s. str.) in several respects, including their indehiscent fruits. Rays of Euphorbiaceae are only 1-5 cells wide (Hayden & Hayden 2000); Pandaceae usually lack obturators, while Euphorbiaceae have them - another difference. Dicoelia (Euphorbiaceae - Dicoelieae) and Galearia both have stamens in depressions in the petals. However, Dicoelia has a low, thin-walled testa, a massive exotegmen, and a moderately thickened mesotegmen (Stuppy 1996), and belongs in Phyllanthaceae (Kathriarachchi et al. 2005).

Engler had trouble with Panda, mistaking its plagiotropic branches for compound leaves, so he described it first as a species of Burseraceae, then as a species in Sapindaceae, and after he recognized his mistake, he was still unclear as to its relationships and placed it in a monotypic Pandales (Forman 1966).

[Ochnaceae [[Bonnetiaceae + Clusiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]]]: biflavones +; indumentum poorly developed; stomata paracytic; C widely spreading/reflexed; contorted, (protective in bud); A many, basifixed; pollen grains usu. small [<30µm in diameter]; nectary 0; (G [5+]); ovules many/carpel, lacking parietal tissue, endothelium +; fruit a septicidal or -fragal capsule; endosperm at most slight.

Age. The crown age of this clade is (106.7-)101.5(-96.4) m.y.a. (Xi et al. 2012b: Table S7), ca 100.9 m.y. (Tank et al. 2015: table S1, S2), around 150, or even 185 m.y. (Bissiengou et al. 2015b), or (124.9-)120.6, 115.4(-104.2) m.y. (Ruhfel et al. 2016: app. S9).

Evolution. Divergence & Distribution. Several of the characters above are suggested as possible synaporphies for Ochnaceae by Schneider et al. (2014a). Optimization of characters like ovule number and styles free (= styluli +)/fused is difficult.

Chemistry, Morphology, etc. It is quite common for the calyx to be small relative to the corolla in bud (e.g. Matthews et al. 2012 for Ochnaceae), so the corolla has taken over the protective function for the bud, although in taxa like Calophyllum and Clusia the bud is at first completely enclosed by the sepals. Pollen grains in general are quite often small, but there is substantial variation in the [[Bonnetiaceae + Clusiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]] clade (Furness et al. 2013b, c.f. 2012).

Classification. Van Tieghem (1902) early thought that on balance Clusiaceae s.l. and Ochnaceae might be close, largely because of the polystemony of the former and also of some of the latter.

OCHNACEAE Candolle, nom. cons.   Back to Malpighiales

Pits vestured; mucilage cells/canals +; branching from previous flush; lamina with secondary and tertiary venation well developed; pedicels articulated; stamen development centrifugal; (pollen with endexine thickened around apertures ["costate"]); micropyle often zig-zag; K persistent in fruit; endosperm +.

27/495 - seven groups below. Tropical, esp. Brazil.

Age. Bell et al. (2010) date crown group Ochnaceae at (60-)45(-28) m.y.a.; (43-)39, 36(-32) m.y. is the estimate in Wikström et al. (2001: note topology) and (90.5-)77.8(-83.5) m.y.a. in Xi et al. (2012b: Table S7).

1. Ochnoideae Burnett

Ochnoideae

Isoflavonoids +; stem with cortical vascular bundles; (vessel elements with scalariform perforation plates); vessel/parenchyma pitting unilaterally compound; nodes also multilacunar; (sclereids +); pericycle of small isolated fibre bundles; petiole bundle annular, (several, arcuate); leaves 2-ranked; lamina with secondary veins strong and close, and/or with parallel tertiary veins, stipules fimbriate or not, (intrapetiolar); flowers (3-)5(-10)-merous, monosymmetric in bud; K almost scarious; A (5-many), anthers (locellate), porose (not), filaments abruptly narrowed at anther junction, shorter than the anthers; (short) androgynophore +, G (1-)5(-15), stipitate, opposite sepals, when 3 median member adaxial, style not branched, stigma ± punctate; ovules with endostomal micropyle; antipodals persistent; filaments persistent in fruit, anthers abscising; ovules many/carpel; seeds winged; endotesta with small crystalliferous cells; endosperm +, (embryo curved).

27[list]/495. Tropical, esp. Brasil (map: from Kanis 1968, 1971; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Australia's Virtual Herbarium xii.2012; Brummitt 2007 [America]).

Age. Crown-group Ochnoideae are estimated to be (74.6-)69.5(-63.5) m.y.o. (Bissiengou et al. 2014a).

1A. Testuleeae Horaninow

Lamina with secondary veins distant, brochidodromous, margin entire; bracteole 1; flowers 4-merous, monosymmetric; androecium adaxial, A 1, staminodes +, two thirds connate; G [2], placentation parietal; capsule inflated.

1/1: Testulea gabonensis. West tropical Africa.

[Luxemburgieae [Ochneae + Sauvagesieae]]: lamina with secondary veins closely parallel.

Age. The crown age of this clade is (72.4-)53(-38.9) m.y.o. (Xi et al. 2012b: Table S7).

1B. Luxemburgieae Horaninow

Venation closely parallel; flowers obliquely monosymmetric, monosymmetry developing early; androecium adaxial, anthers connate or not, porose, deciduous after anthesis, filaments ± connate, (staminodes small, outside fertile A); pollen exine with small perforations, ± smooth; placentation ± parietal, stigma commissural; (carpels pulling away acropetally and opening adaxially); G [3]; n = ?; ?germination.

2/22; Luxemburgia (18). Venezuela and Brazil.

Age. Crown-group Luxemburgieae are estimated to be (29.6-)20.1(-11.1) m.y.o. (Bissiengou et al. 2014b).

Synonymy: Luxemburgiaceae van Tieghem

[Ochneae + Sauvagesieae]: (pith chambered); (lamina with secondary veins distint); pollen with striate-rugulate exine.

1C. Ochneae Bartling

Root phellogen ± superficial [Ochna]; vessel/parenchyma pitting not unilaterally compound; (petiole with inverted medullary bundle and subepidermal fibres); leaves two-ranked, (stipules semi-intrapetiolar - Ouratea); flowers polysymmetric; (inner edge of petal enveloping stamens in pairs); (A ob/diplostemonous), stamen development centripetal, (anthers dehiscing by long slits), (filaments longer than anthers); (pollen 3-celled); G [2-]5-10[-15], postgenitally connate [± apocarpous], style gynobasic, hollow or not, branched, transmitting tissue variously arranged, stigmas expanded (not); ovule one/carpel, (campylotropous), apotropous, integument single [= 2 fused, except sometimes at tip], 7-17 cells across, (micropyle straight, often endostomal, outer integument 3-4 cells across, inner integument 2-3 cells across - Ochna), pachychalazal, vascularized by raphal bundles, hypostase + (/0?); embryo sac with antipodals enlarged; fruit indehiscent, nut-like (drupe), receptacle enlarged, (K enlarged, wing-like - Lophira); seeds not winged; testa with vascular bundles, endotesta lacking small crystalliferous cells, fibrous exotegmen 0; endosperm 0; cotyledons massive, variously arranged, (unequal); germination commonly hypogeal; n = 10, 12-14.

9/390: Ouratea (inc. Gomphia: 200), Ochna (paraphyletic?: 85), Campylospermum (50). Tropical, especially Brazil. [Photo - Flower, Flower, Fruit.]

Age. Crown-group Ochneae are estimated to be (48.4-)36.3(-22.5) m.y.o. (Bissiengou et al. 2014b).

Fossil fruits identified as Ochninae have been found in North Dakota in deposits of Late Palaeocene age perhaps around 58 m.y.a. (Ickert-Bond et al. 2015b).

Synonymy: Gomphiaceae Schnizlein, Lophiraceae Loudon

1D. Sauvagesieae de Candolle

(Herbs); (medullary vascular bundles +); (colleters +); leaves spiral, (compound - Rhytidanthera), lamina vernation conduplicate-flat, (venation very closely parallel), base ± decurrent; monosymmetry developing late, involving A and G (flowers polysymmetric); (K with outer members smaller than the rest), (C with 3 traces); (androecium with positional monosymmetry at anthesis), A 5, 10 (many, centrifugal), obdiplostemonous, (anthers deciduous after anthesis), (dehiscence apical or by long slits), staminodes +, petal-like (forming a cone, staminodes contorted or connate) or not, 0; (pollen exine with small perforations); G [2, 3, 5], when 3, median member adaxial, ovary finely ridged, (placentation parietal; laminar), style (0), (stigma shortly lobed), (lobes commissural); (ovules >2/carpel), outer integument ca 2 cells across, inner integument ?3-4 cells across; (fruit a drupe); (seeds not winged); exotesta of large cells, ± detached, entotesta with crystalliferous cells; germination epigeal; n = 19 [one count].

16/82: Sauvagesia (40). Pantropical, only 2 spp. in Africa, most South American.

Age. The age of crown-group Sauvagesieae is estimated to be (49.4-)41.8(-29.7) m.y. (Bissiengou et al. 2014b).

Synonymy: Euthemidaceae van Tieghem, Sauvagesiaceae Dumortier, Wallaceaceae van Tieghem

[Medusagyne + Quiinoideae]: leaves opposite; flowers unisexual; anthers relatively short (<2 x longer than broad], thecal septum massive, persistent; ovary with longitudinal ridges, styluli +, ovary roof well developed, stigmas expanded ["suction-cup-shaped"]; ovules 2/carpel, superposed, inner integument 3-4 cells across, nucellar endothelium +; K not persistent in fruit.

Age. The age of this clade is (89.1-)72.3(-54.9) m.y. (Xi et al. 2012b: Table S7) or (77.5-)64.7(-42.6) m.y. (Bissiengou et al. 2014b).

2. Medusagynoideae Reveal

<i>Medusagyne</i>

Plant tanniniferous; phloem stratified; true tracheids +; nodes 5:5 + 2 phloic bundles; cristarque cells 0; petiole bundles many, arcuate, variously oriented; stomata anomocytic, cuticle waxes 0; plant glabrous; buds perulate; lamina venation very reticulate, stipules 0, colleters +; inflorescence terminal, ?cymose, plant andromonoecious; K basally connate, C with 3 traces; A spiral, from 5 trunk bundles; orbicules numerous; pollen porate, exine protruding at the pores, onci +, basal layer of exine massive, endexine not lamellate, intine lamellate; pollen surface finely striate, striae intertwined; G [16-25], adnate to central axis, ridges ± interrupted, without vascular bundles, stigmas capitate, ?type; ovules 2-5/carpel, outer integument 3-4 cells across, inner integument 3-4 cells across, "weakly crassinucellate", funicles long; fruit verrucose, deeply ridged, carpels pulling away acropetally and opening adaxially, columella persistent; seeds winged, wings with several cell layers; exotesta slightly thickened; endosperm ?development, thin; n = ?

1[list]/1: Medusagyne oppositifolia. Seychelles, very rare.

Synonmy: Medusagynaceae Engler & Gilg, nom. cons.

3. Quiinoideae Luersson

Quiinoideae

Trees mycorrhizae 0; cork?; (vessel elements with scalariform perforation plates); true tracheids +; (silica bodies +); petiole bundle annular, often complex; lamina with strong, close secondary venation, tertiary venation closely parallel, at right angles to secondary veins, stipules pubescent; flowers small [5> mm in diameter]; (hypanthium +); K 4-5, pubescent, C 4-5(-8), usu. imbricate; A basally connate or not, (adnate to the base of the C), (subdorsifixed), thecae distinct; pollen exine with small perforations; (androgynophore 0); G (strongly ridged, ridges with vascular bundle), stigma type?; ovules basal, apotropous or epitropous, outer integument 4-7 cells across; fruit striate-somewhat ridged when dry, exocarp with lacunae; seeds 1-4, unwinged; coat ?; endosperm development?, cotyledons massive; n = ?

4[list]/46. Tropical America (map: from Schneider et al. 2002).

Age. The crown age of this clade is (38.7-)18.1(-4.3) m.y.o. (Xi et al. 2012b: Table S7) or (27.2-)19.1(-11.7) m.y.o. (Bissiengou et al. 2014b).

3A. Froesia Pires

Cristarque cells 0; phloem fibres 0; leaves compound, lamina margins entire; flowers ?perfect; G 3, free, stigma punctate; ovules collateral; fruit follicular; endosperm 0.

1/3. Tropical South America.

3B. The Rest.

(Lianes); phloem fibres +; (leaves compound), lamina margins entire to deeply lobed, (venation paxillate), stipules also interpetiolar, large, ± persistent; plant (cryptically) dioecious; G [2-13], stigmas obliquely expanded; (ovules 1-4/carpel); fruit ± berry-like; seeds hairy; (endosperm 0).

3/43: Quiina (31), Lacunaria (8-12). Tropical America. [Photo - Flower, Fruit.]

Synonymy: Quiinaceae Engler, nom. cons.

Evolution. Divergence & Distribution. The diversification rate in Medusagynoideae may have slowed down (Xi et al. 2012b). Indeed, throughout this family there is substantial clade size imbalance [1 [[4 + 18] [[5 + 77] [2 + 388]]]] [1 [3 + 49]].

The very long stem of Ochnaceae, over 70 m.y. by some estimates, could reflect extinction at the K/P boundary, although the length of that stem suggests ages for angiosperm evolution as a whole that are perhaps unlikely. Bissiengou et al. (2014b) suggest that Ochnaceae originated in America, the ancestors of Medusagyne, now restricted to the Seychelles, perhaps getting where they did via extensive migration over the North Atlantic land bridge via India. Ocean crust separating India and the Seychelles started to form ca 63.4 m.y. old (Collier et al. 2008).

A number of "features of systematic interest", "possible synapomorphies", etc., listed in bold by Matthews et al. (2012) have been placed tentatively at their appropriate hierarchical levels. Schneider et al. (2014a) suggest numerous apomorphies throught the family, which I have tried to follow. however, I have not placed monosymmetric flowers as an apomorphy for Ochnoideae (with subsequent reversals), mainly because the flowers are monosymmetric in three different ways.

Pollination Biology & Seed Dispersal. Buzz pollination is common/prevalent in Ochnaceae, and although the anthers have an endothecium, it is sometimes restricted to the area around the anther pore or pores. In Sauvagesieae a cone formed by petaloid staminodes closely surround the fertile stamens (dehiscence varies from pores to longitudinal slits); pollen comes out of the apex of the cone, which functions as a pore, when the flower is buzzed (Kubitzki & Amaral 1991). There may have been reversal from dehiscence by pores to dehiscence by slits (Amaral 1980; Amaral & Bittrich 2004, 2013).

Chemistry, Morphology, etc. Sauvagesia lacks vestured pits; two other genera in Ochnoideae are recorded as having them (Jansen et al. 2001). Godoya has stratified phloem. There are mucilage cells or mucilage channels throughout the family that are to be found in various places in the plant, and the plants sometimes have a watery exudate.

There is considerable variation in floral morphology in Ochnaceae-Ochnoideae. Sauvagesia has numerous linear staminodes, five petal-like staminodes opposite the petals, and five stamens opposite the sepals. The antesepalous primordia of Ochna (Ochnoideae-Ochneae) show centripetal androecial development (Pauzé & Sattler 1978), while the androecia of members of the other tribes have centrifugal development (Amaral & Bittrich 1998). Zygomorphy is largely the result of the unequal later development of the androecium, but in Philacra and Luxemburgia it is evident early in development (Amaral & Bittrich 1998). Lophira has unequally accrescent sepals, two members forming wings (there are only two carpels, each with many ovules, and the testa is thin). Placentation is often axile, but it can be laminar, as in Wallacea, or parietal, as in Schuurmansia (Amaral & Bittrich 2013).

There is also variation in the ovule, etc., of Ochna, alternatively, some reports must be incorrect. Chikkannaiah and Mahalingappa (1974) suggest that there is no endothelium, although the nucellar epidermis seems to take over that function (but see Endress et al. 2012). Batygina et al. (1991, p. 222) show Sauvagesia erecta as having a much enlarged endotesta with thick walls.

For further information on Ochnoideae, see Amaral (1991), Kanis (1968), Matthews et al. (2011) and Amaral and Bittrich (2013), all general, Hegnauer (1966, 1989: chemistry), van Tieghem (1903c: root anatomy), Decker (1966: Luxemburgieae) and Dickison (1981), both anatomy, van Tieghem (1902: general, esp. embryo, 1904 and references), Ronse De Craene and Bull-Hereñu (2016: androecium), Baum (1951: gynoecium), and Narayana (1975) and Guádès and Sastre (1981), both embryology,

In Medusagyne the upper ovules are ascending and epitropous, the lower ovules descending and apotropous (Batygina et al. 1991; Doweld 1998b). For a comparison of the fruit dehiscence of Medusagyne with that of some Ochnaceae, particularly some Sauvagesioideae, see Fay et al. (1997a); the anatomy of the fruits is similar to that of Caryocaraceae (Dickison 1990a).

Additional information on Medusagyne is taken from Dickison and Kubitzki (2013: general), Beauvisage (1920: anatomy), Robinson et al. (1989: morphology), Dickison (1990a, 1990b: morphology and anatomy), and Matthews et al. (2012: floral morphology).

The venation of the leaves of Quiinoideae is very distinctive, although not that dissimilar from that of other Ochnaceae, and it was studied in detail by Foster (1952 and references). Veinlets ending free in the mesophyll can be few or even absent. The stomata are described as being paracytic by Schneider et al. (2002).

For general information, see Kubitzki (2013b) and Schneider and Zizka (2014), for wood anatomy, see Gottwald and Parameswaran (1967), and for many details of floral morphology, see Matthews et al. (2012).

In both Quiinoideae and Medusagyne some of the ovules in each carpel abort. For pollen of the Ochnaceae s.l., see Furness (2013b).

Phylogeny. There is good molecular support for a monophyletic Ochnaceae s.l., e.g. Fay et al. (1997a), Nandi et al. (1998), Savolainen et al. (2000a), Chase et al. (2002) and Korotkova et al. (2009), although relationships between the three main clades that make up the family were less clear. However, Xi et al. (2012b: as families) found moderate (75% ML bootstrap; 1.00 p.p.) support for a [Medusagynoideae + Quiinoideae] clade, support is weaker in Wurdack and Davies (2009) and not terribly strong in Schneider et al. (2014a). The tribes and their relationships are all well supported in the study by Schneider et al. (2014a: 4 plastid loci + ITS; see also Bissiengou et al. 2014b). Bissiengou et al. (2014a) examined relationships within Ochneae, and although support was sometimes not very good, Campylospermum may be polyphyletic.

Elvasia (Ochnoideae-Ochneae) is morphologically very distinct: it has congenital carpel connation, an ovary with commissural lobes, terminal, shortly branched style with punctate stigmas, and non-vascularized integument, but it is clearly embedded in Ochneae (see also Schneider et al. 2014a). Within Quiinoideae, Froesia is sister to the other genera (Schneider et al. 2006, esp. 2014a, see also Schneider et al. 2002 for a morphological phylogeny; Wurdack & Davies 2009). Relationships among the other three genera are unclear.

Both Quiinoideae and Medusagyne are particularly poorly known embryologically, etc..

Classification. Including Ochnaceae, Medusagynaceae and Quiinaceae in Ochnaceae s.l. is an optional arrangement in A.P.G. II, and they have much in common; Ochnaceae s.l. are recognized in A.P.G. III (2009). The tribal classification above is that of Schneider et al. (2014a); they also describe subtribes.

Previous relationships. Diegodendron was included in Ochnaceae by Cronquist (1981), it is here placed in Malvales as Diegodendraceae (see also Amaral 1991).

Medusagyne is morphologically very distinctive. Comments on the species cover of Medusagyne at the Royal Botanical Gardens, Kew, ca 1985: "c.f. Actinidia. - Would be much better placed in Guttiferae or Hypericaceae - !!!!! - this plant allied to Myrtales. - Nonsense! - oh yes it is!" Hardly surprisingly, it was placed in a monotypic Medusagynales (Theanae) by Takhtajan (1997) and generally associated with Theales (e.g. Cronquist 1981); the latter was already such an heterogeneous group that the further inclusion of practically anything made little difference to its description.

Thanks. For discussion, and for comments on relationships within Ochnoideae, I am grateful to Maria Amaral and Volker Bittrich.

[[Bonnetiaceae + Clusiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]] / clusioids: flavones, flavonols, (ellagic acid), biphenyls, xanthones and dimeric xanthones, polyisoprenylated benzophenones, acylphloroglucinol derivatives, quinones +; vessel elements with simple perforation plates; schizogenous canals or cavities + [plant with exudate]; nodes 1:1; cristarque cells 0; stomata paracytic; leaves opposite, with colleters, lamina margins entire, stipules 0; inflorescence cymose; A fasciculate, fascicles opposite C; G opposite sepals [check], or median member adaxial; micropyle exostomal; exotegmen with low, lignified, sinuous anticlinal cell walls; embryo ± fusiform.

Age. This node can perhaps be dated to the Cenomanian (104-)94, 89(-87) m.y.a. (Davis et al. 2005a: note topology), (91-)89.5(-88.4) m.y. (Xi et al. 2012b: Table S7), around 148-110 m.y. (Bissiengou et al. 2015b), (116.9-)110.6, 102.9(-92.3) m.y. (Ruhfel et al. 2016: app. S9), or as little as 54-45 m.y.a. (Wikström et al. 2001).

Evolution. Divergence & Distribution. Ruhfel et al. (2016) looked at distribution patterns in the whole clade, observing that most of the numerous disjunctions they observed, some forty nine in all, were best explained by dispersal rather than Gondwanan-age vicariance-type events - thus there were no fewer than eleven dispersals to, but none from, Madagascar, for example. They also noted that their estimates of clade ages varied depending on where the the problematic fossil Paleoclusia was placed, whether as the most recent common ancestor of Clusiaceae or that of [Bonnetiaceae + Clusiaceae]. Estimated ages using the former position were older, sometimes, as with the crown-group age of Clusiaceae, the age estimates of the two calibrations showed no overlap (Ruhfel et al. 2016).

There are several potential morphological synapomorphies for the clade (see Ruhfel et al. 2013 for some ancestral state reconstructions). Variation in seed/diaspore size is considerable (see also Moles et al. 2005a).

Chemistry, Morphology, etc. For a summary of the chemistry of the group, see Crockett and Robson (2011); exactly where on the tree particular classes of secondary metabolites are to be placed will depend on more detailed sampling. Xanthones are uncommon elsewhere in seed plants, being known from Gentianaceae, some Moraceae, etc.. The xanthones of Podostemaceae are similar to those both of Gentianaceae (in their -6-0-glucosides) and of Clusiaceae (in their isoprenyl substitutions). Benzophenone has the formula (C6H5)2CO.

Given the likely phylogenetic relationships above, anatomical studies of Bonnetiaceae are needed to clarify the apparent absence - or near absence - of secretory tissues there. Takhtajan (1993) describes the pith of Bonnetiaceae as having secretory canals, as in Clusiaceae, but c.f. Baretta-Kuipers (1976).

Furness (2012) summarized the palynolgical variation - considerable - in this clade; some characters were optimised on an outline tree, but there was not much obvious phylogenetic signal (see also Furness 2014 for pollen of Medusagyne).

Phylogeny. Morphological data in particular (most of the features above) initially seemed to suggest a grouping of [Elatinaceae + Bonnetiaceae + Clusiaceae/Hypericaceae], seed anatomy and gross morphology of Elatinaceae and some Hypericaceae in particular being similar (e.g. see versions 4 and earlier). This was not a monophyletic group in Savolainen et al. (2000a), indeed, Ploiarium is there even placed in Malvales (but see Wurdack & Davis 2009), although testa anatomy, etc., are strongly against such a position. Analyses in Chase et al. (2002) weakly linked Elatinaceae and Bonnetiaceae with Clusiaceae + Podostemaceae. Evidence now suggests that Elatinaceae are sister to Malpighiaceae (Davis & Chase 2004; Davis et al. 2005a; Tokuoka & Tobe 2006; Wurdack & Davis 2009), and some morphological data support this. Bonnetiaceae link with Clusiaceae s.l. in morphological phylogenetic analyses (e.g. Luna & Ochoterena 2004: Hypericaceae not included).

Relationships within this clade were initially unclear (see also Soltis et al. 1999b; Gustaffson et al. 2002; Davis et al. 2005b), although Wurdack and Davis (2009) and particularly Ruhfel et al. (2011, 2013, see also Xi et al. 2012b) have confirmed the paraphyly of the old Clusiaceae. Relationships are [[Bonnetiaceae + Clusiaceae] [Calophyllaceae [Hypericaceae + Podostemaceae]]], and support is generally quite strong, although that for the [Bonnetiaceae + Clusiaceae] clade is the weakest (Xi et al. 2012b; Ruhfel et al. 2013). The branch leading to Podostemaceae is rather long. Meseguer et al. (2014a: nuclear markers) found that Podostemon, the only Podostemaceae they examined, was sister to Vismia, although support was not strong.

Classification. The old Clusiaceae (see versions 8 and before) were strongly paraphyletic, so continuing to include all the genera that used to be include there, and making Cluisceae monophyletic, would entail the inclusion of Bonnetiaceae, Hypericaceae and Podostemaceae - and the latter has one of the most distinctive morphologies of all flowering plants. For the "price" of recognizing Podostemaceae, we have five coherent and moderately easy recognizable clades.

[Bonnetiaceae + Clusiaceae]: root cork superficial; hypocotyl/radicle long [cotyledon:hypocotyl + radicle ratio ca <0.2].

Age. The age for this node is (89.6-)82.1(-69.6) m.y. (Xi et al. 2012b: Table S7), around 93.5 m.y. (Tank et al. 2015: table S2), or (114.6-)106.6, 91.5(-89.8) m.y. (Ruhfel et al. 2016: app. S9).

BONNETIACEAE Nakai   Back to Malpighiales

Bonnetiaceae

Shrubs; anthraquinones +, polyisoprenylated benzophenones, biphenyls, biflavones 0; (nodes 3<:3<); schizogenous cavities 0 [plant lacking exudate?]; hypodermal mucilage cells +; plant glabrous; leaves spiral, lamina vernation supervolute, margins minutely toothed by setae, petiole short; C protective in bud; (androecium not obviously fasciculate - Bonnetia); tapetal cells binucleate; G [3-5], style long, hollow, or style branches ± separate, stigma surface rounded-papillate; ovule bistomal, outer integument ca 3 cells across, inner integument ca 2 cells across, suprachalazal zone ca 2/3 length of ovule; cotyledon:hypocotyl + radicle ratio (<0.5 the embryo); n = 11 [Ploiarium], ca 150 [Bonnetia cubensis].

3[list]/35: Bonnetia (30). Cambodia, Malesia (mostly Western), Cuba, South America. [Photo - Flower, another Flower.]

Age. The crown age of this clade is (66.8-)52.6(-35.7) m.y.o. (Xi et al. 2012b: Table S7) or (86-)59.2, 52(-31.7) m.y. (Ruhfel et al. 2016: app. S9).

Chemistry, Morphology, etc. Bonnettia s.l. has tri- or multilacunar nodes, a mucilaginous epidermis, a foliar endodermis, and foliar sclereids; Archytaea and Ploiarium have unilacunar nodes and lack the mucilaginous epidermis, foliar endodermis and sclereids (Dickison & Weitzman 1996). The absence of any secretory system should be confirmed. Keller (1996) described the leaf vernation as being involute.

Bonnetia also often has 3-trace petals while the bracetoles sometimes have only a single trace (Dickison & Weitzman 1998). For Archytaea, Wawra de Fernsee (1886) shows a floral diagram in which both the five carpels and the stamen fascicles are drawn opposite the calyx.

For vegetative anatomy, see Beauvisage (1920), for chemistry, see Hegnauer (1969, as Theaceae) and Carvalho et al. (2013: Bonnetia), for some embryology, see Prakash and Lau (1976), for chromosome numbers, see Oginuma and Tobe (2013), and for a general account, see Weitzman et al. (2006).

Phylogeny. Relationships are [Bonnetia [Archytaea + Ploiarium]] (e.g. Xi et al. 2012b; Ruhfel et al. 2016).

Previous Relationships. Savolainen et al. (2000b) found that Ploiarium was placed within Thymelaeaceae. Morphologically and anatomically this position would seem rather unlikely - probably the leaf was from Gonostylus (Thymelaeaceae), which grows in the same area.

CLUSIACEAE Lindley, nom. cons. // GUTTIFERAE Jussieu, nom. cons., nom. alt.   Back to Malpighiales

Clusiaceae

Trees or shrubs; isoflavones, diterpenes; (vessel elements with scalariform perforations); exudate usu. in (branched) canals; petiole bundle arcuate to annular; lamina vernation often flat (conduplicate), margins entire, (base forming intrapetiolar hood-shaped structure); flowers (3-)4-5(-8)-merous; K and C usu. decussate; A (5-), connate or not, (anthers extrorse), (with small glands), filaments as stout as anthers; G [2-5(-16)], often opposite petals, style short [shorter than ovary], stigmas expanded, wet; seeds few-many, large; embryo chlorophyllous or white, cotyledons minute [cotyledon:hypocotyl + radicle ratio <0.1].

14 [list]/800 - three groups below. Throughout the tropics (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Gustaffson et al. 2007; Fang et al. 2011).

Age. The spread of crown ages of this clade is (72.4-)52.9(-30.4) m.y. (Xi et al. 2012b: Table S7), around 51-42 m.y.a. (Bissiengou et al. 2015b), or as much as (92.8-)91.1, 63.6(-52.2) m.y. (Ruhfel et al. 2016: app. S9).

An interesting and well-preserved late-Cretaceous fossil ca 90 m.y.o., Paleoclusia chevalieri, from New Jersey, U.S.A., is possibly assignable to Clusiaceae (Crepet & Nixon 1998; see also Friis et al. 2011). The seeds are described as being arillate, but the position of the aril is unlike that of extant Clusiaceae (it is adjacent to the seed, rather than surrounding it), and it may be an aborted seed (Ruhfel et al. 2013). If used in calibrations, where it is placed on the tree affects ages of the whole group (see above).

1. Clusieae Choisy

(Plants lianes), (epiphytes); plant dioecious; (C 0); androecium not obviously fasciculate, (anthers locellate), (sporangia annular); ovary with a roof, (ovule 1/carpel), styluli distinct; ovules 2-many/carpel, (micropyle bistomal), outer integument 2-6 cells across, inner integument 3-7 cells across, chalaza quite massive; seed arillate, aril vascularized or not; testa and tegmen somewhat multiplicative; germination phanero(crypto-)cotylar, epigeal (hypogeal).

5/480: Clusia (300-400), Tovomita (60), Chrysochlamys (55). New World tropics. [Photo - Staminate flower, Fruit.]

Age. Crown-group Clusieae are (32.8-)21.7, 20.5(-11.4) m.y. (Ruhfel et al. 2016: app. S9).

[Garcinieae + Symphonieae]: (paired "stipular glands" on the stem); pollen at least 4-aperturate; style +; fruit indehiscent, baccate; (testa and endocarp ± fused); seed coat complex, outer integument vascularized, multiplicative, exotegmen usu 0; germination crypto(phanero-)cotylar, hypogeal (epigeal), radicle reduced (not).

Age. The crown ages of this clade are around (56.6-)49.3, 44.1(-42.3) m.y. (Ruhfel et al. 2016: app. S9).

2. Garcinieae Choisy

(Buds perulate); plant dioecious; (androecium not obviously fasciculate), (filaments thinner than anthers); placentation basal or parietal, style usu. short; ovule 1 or many/carpel, apotropous, outer integument 4-8 cells across, inner integument 2-3 cells across, (outer integument ca 10 cells across, inner integument ca 22 cells across - Allanblackia), (integument single, 18-20 cells across), chalaza not massive, (parietal tissue ca 5 cells across), (nucellus protruding up micropyle); (fruit septicidal); (exotegmen +).

2/270: Garcinia (240). Tropical, esp. Old World.

Age. The age of crown-group Garcinieae is some (31.3-)21.1, 9.8(-11.5) m.y. (Ruhfel et al. 2016: app. S9).

Synonymy: Cambogiaceae Horaninow, Garciniaceae Bartling

3. Symphonieae Choisy

Buds perulate; (flowers single); C contorted; anthers extrorse, (2-)5-40 mm long, much longer than broad; style (relatively long), branched (not), stigma porose, punctate; ovules 4-8/carpel, (micropyle endostomal), outer integument 10-22 cells across, inner integument 10-15 cells across, chalaza massive; (exotegmen massively developed).

7/48: Symphonia (23). Tropical, few mainland Africa.

Age. Crown-group Symphonieae are around (46.6-)44.3, 44.1(-42.3) m.y.o. (Ruhfel et al. 2016: app. S9).

Evolution. Divergence & Distribution. The around 750 species in Garcinieae and Clusieae, about 93% of the whole family, have diverged within the last 25 m.y. or so (Ruhfel et al. 2016: fig. 1).

Ecology & Physiology. Garcinia is one of the five most diverse genera in West Malesian l.t.r.f. (Davies et al. 2005); its members are mostly rather small trees. In the New World, the speciose Clusia includes epiphytes and stranglers many of which are more or less leaf succulents, and a number grow at elevations up to 3500 m (Gustafsson et al. 2007). Furthermore, a number of species in the C. minor and C. flava groups (see Gustafsson & Bittrich 2002) have strong to weak crassulacean acid metabolism (CAM) (Holtum et al. 2004; Lüttge 2008), and CAM has evolved twice or more in species of Clusia from Panama alone (Gehrig et al. 2003). The development of CAM may be promoted by phosphorus deficiency; in species of Clusia like C. pratensis CAM is facultative (Winter & Holtum 2014; Lüttge 2008). (Whether or not the plant is mycorrhizal also affects the plant's phosphorus and carbon metabolism - Maiquetía et al. 2009.) Barrera Zambrano et al. (2014) discuss CAM and C3 photosynthesis in Clusia in the context of its leaf anatomy, although that doesn't seem to be very distinctive. Clusia, shrubby to tree-like and often an inhabitant of lowland tropical rainforest, differs from most other CAM species which are small, either epiphytes (of course, Clusia is often an epiphyte) or plants of dry conditions, and quite often annuals (for major foci of CAM photosynthesis, see Orchidaceae, centrosperms, etc.; Lüttge 2008). For the general ecology of Clusia, see papers in Lüttge (2007).

Pollination Biology. Bittrich et al. (2006) summarize information about the role of oils, resins, etc., in the pollination of the family; see also Amaral et al. (2016). Variation in the androecium in Garcinia and Clusia in particular is extreme. For additional details of androecial morphology in Garcinia and its immediate relatives, see Sweeney (2008, 2010), Leins and Erbar (1981) and Leal et al. (2012); the nectary is unlikely to be staminodial. Little is known about pollination in that genus.

Stamens in Clusia may be fused or free, the filaments are often massive, with canals in which resins are produced and a vascular system that can be quite complex, sometimes forming a ring (Sá-Haiad et al. 2015), the anthers can be locellate and thecate or athecate, or there is an outer annular sporangium surrounding a small central spherical sporangium (C. valerioi: Hochwallner & Weber 2006), and so on. The endothecium is locally absent to about three cell layers across, and this affects how the anther dehisces (see also Sá-Haiad et al. 2015; Amaral et al. 2016). In Clusia, resins (almost pure polyisoprenylated benzophenones mixed with fatty acids) are a common floral reward (Porto et al. 2000; Nogueira et al. 2001), and plants may also produce oils to reduce the viscosity of the resins (Porto et al. 2000). Floral resins are involved in pollination in about half the genus, as well as in the Clusia look-alike, Clusiella (Calophyllaceae) (Gustafsson & Bittrich 2002; Bittrich et al. 2006; Gustafsson et al. 2007; Sá-Haiad et al. 2015). Floral resin production has evolved three or four times or so, but it has also been lost at lest twice (Gustafsson et al. 2007). Depending on the species, resin and pollen may be mixed or presented separately (Amaral et al. 2016). Euglossine and especially stingless Trigona (meliponine) bees have been observed at Clusia flowers (Bittrich & Amaral 1986; Porto et al. 2000; Bittrich et al. 2006; Martins et al. 2007; Amaral et al. 2016), while the cockroach Amazonia platystylata may pollinate C. aff. sellowiana (Vlasáková et al. 2008). Interestingly, species of Clusia growing at higher altitudes, where bees are less common, produce nectar as a floral reward (Armbruster 1984). In general, resins are an uncommon floral reward in angiosperm flowers, but see also Dalechampia (Euphorbiaceae) and Maxillaria (Orchidaceae).

In the American Symphonia globulifera pollen is suspended in a distinctive oil which is picked up by hummingbirds and then deposited in a droplet that exudes through the pore at the tip of the stylar branches; the droplet and the pollen it contains is then sucked back into the pore (Bittrich & Amaral 1996; Bittrich et al. 2013). All other Symphonieae have similar stigmas, and so the pollination mechanism is likely to be the same throughout the tribe; bird pollination is known in other American Symphonieae like Moronobea and Platonia (Bittrich et al. 2013 for references).

Fragrant oils are produced in the stout filaments of the flowers of Tovomita, and these attract male euglossines. The composition of the fragrances in three different species growing in the Ducke Nature Reserve was found to be quite different (Noguiera et al. 1998).

Chemistry, Morphology, etc. The distinctive exudates of Garcinia have been called xanthics (Lambert et al. 2013). For resins, see e.g. Porto et al. (2000) and Bittrich et al. (2006); whether the benzophenones are polyisoprenylated or both polyisoprenylated and benzoylated may have taxonomic significance in Clusia.

Roots of Clusia, at least, may have superficial phellogen, as is fairly common in epiphytic taxa in general. Genera like Dystovomita and Garcinia have distinctive basal intrapetiolar hood-shaped structures whose development needs study; see Cruz et al. (2015) for the stipular nature of apparently similar structures in Metrodorea (Rutaceae).

Hochwallner and Weber (2006) described the androecium of Clusia valerioi as being fasciculate, but this is not obvious from the illustrations. Puri (1939), Leal et al. (2012) and Tobe and Raven (2011) described the ovules as being bitegmic, while Corner (1976) and Asinelli et al. (2011) described them as being unitegmic. However, variation in ovule, seed, and fruit in Clusiaceae in general is considerable and poorly understood and would repay a broad and careful survey.

For chemistry, see Hegnauer (1966, 1989), for floral morphology of the distinctive Clusia gundlachii, see Gustafsson (2000), for that of other Clusiaceae, see Mourão and Beltrati (1995) and Mourão and Marzinek (2009), and for general information, see Stevens (2006c).

Phylogeny. Clusieae are a well-supported clade clearly sister to the rest of the family (e.g. Ruhfel et al. 2016). However, the relationships of Symphonieae and Garcinieae are less clear, although they are provisionally separated here; there is no strong evidence for their reciprocal monophyly. Thus Gustaffson et al. (2002) found that Garcineae were embedded in Symphonieae, Ruhfel et al. (2011) did recover a monophyletic Symphonieae, but there was no support for a monophyletic Garcineae, they were branches of a comb, while Ruhfel et al. (2016) recovered both as monophyletic.

The relationship between Allanblackia, with its numerous ovules per carpel, and Garcinia s.l., with but a single ovule per carpel, are unclear, and the former may be derived from the latter, and there is an African clade made up of Allanblackia and some species of Garcinia (Gustafsson et al. 2002; Sweeney 2008; Ruhfel et al. 2011, 2013, 2016). Less problematically, the old Tripetalum and Pentaphalangium are to be included in Garcinia. Within Clusieae, Dystovomita is sister to the rest of the tribe and Tovomita is polyphyletic (e.g. Ruhfel et al. 2016). There is good support for an monophyletic Clusia, and many of the classicial sections are turning out to be monophyletic, but relationships between these sections are less clear (Gustafsson et al. 2007). Within Symphonieae, Symphonia is sister to the other genera (Rufel et al. 2016).

Classification. Clusia is to include genera like Renggeria, Decaphalangium, etc., previously segregated from it (Gustafsson et al. 2007)..

[Calophyllaceae [Hypericaceae + Podostemaceae]]: exudate usu. in pale yellowish glands (unbranched canals).

Age. This node has been dated at (57-)54, 45(-42) m.y. (Wikström et al. 2001), (73-)61, 45(-31) m.y. (Bell et al. 2011), (88.7-)82.2(-73.6) m.y. (Xi et al. 2012b: Table S7), around 91.3 m.y. (Tank et al. 2015: table S2), or even older, (113.8-)106, 98.7(-87.4) m.y. (Ruhfel et al. 2016: app. S9).

CALOPHYLLACEAE J. Agardh    Back to Malpighiales

Calophylloideae

Trees or shrubs; (vessel elements with scalariform perforations); lamina vernation often flat, (paired "stipular" glands at the leaf base), (colleters 0); (plant dioecious); flowers 4-5-merous, C (contorted), (protective in bud), (0-)4-5(-8); A not obviously fasciculate, (connate), anthers often with complex or simple glands; (placentation apical, basal), style usually long, stigmas much expanded to punctate, wet; (fruit a berry or drupe); seeds 1-many; (exotegmen 0); embryo chlorophyllous or white, cotyledons huge [cotyledon: hypocotyl + radicle ratio >5 [Calophyllum, Mesua, etc.], or smaller; germination phanerocotylar, epigeal, or cryptocotylar, hypogeal.

13[list]/460: two groups below. Throughout the tropics (map: in part see Stevens 1980 - blue is Calophyllum inophyllum; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).

Age. Crown-group Calophyllaceae are around (72.6-)57.6(-40) m.y.o. (Xi et al. 2012b: Table S7) or (93-)61.9, 56.4(-30.9) m.y.o. (Ruhfel et al. 2016: app. S9).

1. Endodesmieae Engler

secondary veins closely parallel; G (?1); ovule 1/carpel

2/2. West Africa.

2. Calophylleae Choisy

(leaves spiral, two-ranked), lamina vernation often flat (conduplicate; supervolute - Kielmeyera); (anthers locellate - Haploclathra); G [2-5]; (ovules 2-few/carpel), outer integument 20-30+ cells across, inner integument 2-3 cells across [Calophyllum], or integument single, ca 26 cells across [Mammea]; (testa multiplicative - Old World Clade).

11/458: Calophyllum (190), Kayea (70), Mammea (70), Kielmeyera (50). Throughout the tropics (map: in part see Stevens 1980 - blue is Calophyllum inophyllum; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower, Flower.]

Age. The crown-group age of Calophylleae is only (42.9-)31.8, 29.5(-19.4) m.y. (Ruhfel et al. 2016: app. S9).

Evolution. Divergence & Distribution. Although Calophylleae are far more diverse than Endodesmieae, they have a very long stem and have diverged only within the last 35 m.y. or so (Ruhfel et al. 2016).

The recent discovery of Calophyllum in southwest Mali, mainland Africa (= C. africanum), but apparently related to the New World C. antillanum, is biogeographically perplexing (Cheek & Luke 2016).

Ecology & Physiology. Calophyllum has unusually dense secondary veins compared to those of the 484 other species of angiosperms studied (Sack et al. 2012); some Ochnaceae will come close.

Pollination Biology. Buzz pollination occurs in Kielmeyera, while the distinctive cup-shaped anther glands more common on the related Caraipa are believed to secrete fragrances (Bittrich et al. 2006).

Chemistry, Morphology, etc. Although all species of Calophyllum have opposite leaves when adult, a few species have seedlings with alternate leaves (Stevens 1980).

Marila asymmetralis, alone in the clusioids, has obliquely monosymmetric flowers. The androecial (and gynoecial) morphology of Endodesmia and Lebrunia needs study; is it fasciculate (Ruhfel et al. 2103)? The glands on anthers of genera like Caraipa are large, paired and crateriform, perhaps because the contents have been removed, while in other genera like Kayea they are small and rounded. As in Clusiaceae, variation in ovule and seed morphology and anatomy is poorly understood; most data on ovule morphology come from Old World taxa.

For chemistry, see Hegnauer (1966, 1989, as Guttiferae), for some anatomy, see Beauvisage (1920), general information, see Stevens (2006c, as Clusiaceae), for fruits and seeds, see Mourão and Beltrati (2000), and for the distinctive foliar fibres of many species of Mammea, see Dunthorn (2009).

Phylogeny. Endodesmia is sister to the rest of the family (Lebrunia has not been sequenced), which otherwise separates into largely Old and New World clades, although these are not always well supported (Ruhfel et al. 2011, 2013, 2016). Clusiella is embedded in the latter clade (see also Gustaffson et al. 2002; Rufel et al. 2016). Its seeds and vegetative anatomy (including the deep-seated phellogen of the root) are consistent with this position, although the flowers are a little odd, since they do indeed look like those of Clusia. Also in the New World clade, there is a group of largely alternate-leaved genera that form a clade (Ruhfel et al. 2013, 2016); these genera (e.g. Kielmeyera, Caraipa) also have capsular fruits, often with quite large, winged seeds, and their embryos have large cotyledons with cordate bases. Kayea and Mesua, until quite recently considerd to be congeneric, occur on the two main branches in the Old World clade (e.g. Ruhfel et al. 2016)

Previous Relationships. Many Theaceae also have spiral leaves, capsular fruits, winged seeds, and flowers with many stamens. Alternate-leaved Calophyllaceae seemed superficially to be similar and so used to be placed in that family, more or less "intermediate" between Theaceae and Guttiferae, groups that turn out not to be closely related at all (c.f. Baretta-Kuipers 1976).

[Hypericaceae + Podostemaceae]: stigma surface rounded, with papillae.

Age. Divergence between Podostemaceae and Hypericaceae may have occurred as early as the Cenomanian, (106.5-)97.6, 90.9(-79.9) m.y. (Ruhfel et al. 2016: app. S9), (82-)76, 72(-66) m.y.a. (Davis et al. 2005a), ca 75 m.y.a. (Tank et al. 2015: Table S2), (78.4-)69.7(-59.3) m.y.a. (Xi et al. 2012b: Table S7), or as recently as (56-)43, 42(-26) m.y.a. (Bell et al. 2010) or still more so, (42-)40, 36(-34) or (28-)26(-24) m.y.a. (Wikström et al. 2001).

Evolution. Divergence & Distribution. The morphology of Podostemaceae is so highly derived that finding synapomorphies with Hypericaceae is difficult.

HYPERICACEAE Jussieu, nom. cons.   Back to Malpighiales

Hypericaceae

Small trees to shrubs; lignans, flavones, flavonols, (ellagic acid) +; stem cork pericyclic; polyderm widespread; petiole bundle arcuate (with wing bundle(s)); lamina vernation?; dark glands also present; K quincuncial, C (imbricate), (protective in bud); A (5-15), fasciclodia + (not), A development centrifugal, anthers dorsifixed, often with simple glands; styluli + (± connate), (stigma surface not rounded-papillate); ovules usu. many, (micropyle also exostomal), (zig-zag), outer integument ca 2 cells across, inner integument 2-7 cells across; seeds (1-)many; (exotestal cells in vertical lines), (exotegmen 0); embryo chlorophyllous or white, cotyledons moderate in size (to 80% of the length of the embryo).

9[list]/700. World-wide (map: from Hultén & Fries 1986; Meusel et al. 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]

Age. Meseguer et al. (2013: rooting?) suggested an age of (66-)53.8(-43) m.y. for crown Hypericaceae, (63-)53.7(-42.5) m.y. is the spread in Xi et al. (2012b: Table S7), (62.7-)52.3(-45) m.y. in Nürk et al. (2015), or (93.3-)77, 71.5(-56) m.y. (Ruhfel et al. 2016: app. S9).

For the fossil record of the family, both pollen and seeds, see Meseguer and Sanmartin (2012). Seeds of the fossil Hypericum antiquum (see Budantsev 2005: p. 110, 111) are not particularly uniquely hypericaceous, and a comparison with H. virginianum shows rather different cell types in the two, while the electron micrographs of the latter seem different yet again; c.f. also Elatine, some Nymphaea, Passifloraceae s.l., etc., for similar seeds.

1. Vismieae Choisy

C adaxially pubescent; stamen fascicles 3, staminodial fascicles 3; G [5]; fruit fleshy [berry or drupe]; n = ?10.

2-3/150. Vismia (55), Harungana (50). South America and Africa + Madagsacar.

Age. Estimates of the age of crown-group Vismieae are around (32.7-)19.6(-10.2) m.y.o. (Nürk et al. 2015) or (60.9-)44.3, 40.7(-28.3) m.y. (Ruhfel et al. 2016: app. S9) - barely overlapping.

Age. The age of the clade [Vismieae + Hypericeae] is (86.9-)69, 63.8(-49.6) m.y. (Ruhfel et al. 2016: app. S9).

[Cratoxyleae + Hypericeae]: fruit dry.

Age. This node is ca 40 m.y.o. (Nürk et al. 2015).

2. Cratoxyleae Bentham & J. D. Hooker

(C with adaxial basal nectariferous scale); stamen fascicles 3, staminodial fascicle 3; G [3], (with secondary septae); (ovules 2

2/7. Madagascar, tropical Southeast Asia-western Malesia.

Age. Crown-group Cratoxyleae are (41.1-)27.5(-11.2) (Nürk et al. 2015) or (70.4-)46.7, 43,7(-20.8) m.y.o. (Ruhfel et al. 2016: app. S9).

3. Hypericeae

Often herbaceous-subshrubs; vessel elements many [75-ca 500/mm2], short [<225 µm long, not Thornea] and narrow [<81 µm across]; (flowers 4-merous); C contorted; stamen fascicles 4-5, variously organised, staminodial fascicles 0 (3); G [2-5], (placentation parietal); fruit septicidal, (baccate); seeds (winged), (carunculate); endosperm with chalazal cyst; n = 6-12, etc..

1/500<. Especially northern hemisphere, in the tropics ± montane.

Age. Crown-group Hypericum is estimated to be (37-)34.9(-34) m.y.o. (Meseguer et al. 2013), (33.3-)25.9(-19.6) m.y.o. (Nürk et al. 2015), or (52.2-)39.7, 37.3(-26.1) m.y.o. (Ruhfel et al. 2016: app. S9).

Synonymy: Ascyraceae Plenck

Evolution. Divergence & Distribution. Meseguer et al. (2013, 2014b; see also Nürk et al. 2015) discuss diversification of the genus in detail, integrating past distributions and past ecological preferences with the present, and they suggest that the ancestor of Hypericaceae may have been African, while the stem lineage of Hypericum itself was in the holarctic region by 50-35 m.y.a., depending on the models used. Nürk et al. (2015) thought that that diversification in Hypericum could be explained by a late Eocene niche shift as the stem clade became adapted to cooler conditions, only some 15 m.y. later did diversification rates in the genus increase, in part triggered by cooling temperatures ca 14 m.y.a. and in part by dispersal (twice) into South America, orogenesis in various parts of its range also contributing to the rate shifts. There are major Old and New World clades of Hypericum; the African H. lalandii is well embedded in the latter - probably long distance dispersal - although Africa was thought to be home of ancestors of the genus (Meseguer et al. 2013, q.v. for more details). Diversification of the ca 70 páramo species has been dated to (5.6-)3.8(-2.3) m.y. and has been accompanied by extensive variation in flower size, etc., the plants ranging from prostrate shrublets to shrubs up to 6 m tall (Nürk et al. 2014). Hypericum has also diversified in alpine habitats elsewhere (Hughes & Atchison 2015 and references). For more dates within Hypericum, see Meseguer et al. (2013) and Nürk et al. (2014, 2015)

Ecology & Physiology. The chirality of the contorted corolla varies within an individual in Hypericum, but it seems to have little effect on pollination (Diller & Fenster 2014, ).

Like other bat-dispersed plants in the New World, Vismia tends to be a member of early successional communities (Muscarella & Fleming 2008). It dominates succession on old pastures, forming dense and persistent stands partly because of its root suckers (Mesquita et al. 2001).

Plant-Animal Interactions. Production of hyperforins (acylphloroglucinols, present in pale glands) and hypericins (phototoxic anthraquinones, present in dark glands) increased in Hypericum perforatum when eaten by generalist herbivores, but not by specialists (Sirvent et al. 2003).

Seed Dispersal. Fruits of New World Vismia are an important food for phyllostomid bats such as Carollia (Lobova et al. 2009). The bats are fast feeders, ingesting the fruits and voiding the seeds in their faeces. Resin and seeds are collected from Vismia fruits by Melipona bees in the Neotropics and used to construct nest entrances, etc. (Roubik 1988).

Bacterial/Fungal Associations. The naptha-dianthrone hypericin may be synthesized by an endophytic fungus close to Chaetomium (Kusari et al. 2008).

Chemistry, Morphology, etc. Hypericin, common here, is a red-colored derivative of anthraquinone. Details of the system of canals and spherical translucent reddish (schizogenous) or black (solid) glands in the plant, and what these structures secrete, are poorly understood (Nürk et al. 2012 and references). For the secretory structures in the vegetative parts of Hypericum, see in particular Curtis and Lersten (1990), Sirvent et al. (2003) and Lotocka and Osinska (2010).

For chemistry, see Hegnauer (1966, 1989, as Guttiferae) and Crockett (2012: Hypericum), for the anatomy of Cratoxylum, etc., see Baas (1970), for the wood anatomy of Hypericum s.l., see Gibson (1980), for androecial development, etc., see Robson (1974 and references: fascicle/fasciclode number), Leins and Erbar (1991, 2010), Leins (2000) and Ronse de Craene and Smets (1991e: Harungana), for ovules, see Guignard (1893) and Nagaraja Rao (1957), for fruits and seeds of Vismia, see Mourão and Beltrati (2001), and for seeds of Hypericum, see Robson (1981) and Meseguer and Sanmartin (2014). For some general information, see Stevens (2006c).

Phylogeny. The basic relationships within Hypericaceae are sometimes recovered as [Cratoxyleae [Vismieae + Hypericeae]] (e.g. Ruhfel et al. 2016), however, Nürk et al. (2015) found the relationships [Vismieae [Cratoxyleae + Hypericeae]].

Within Vismieae, Harungana and the African Vismia rufescens form a clade with the American Vismia examined; the other African Vismieae studied formed a sister clade (Ruhfel et al. 2011, 2013; Xi et al. 2012b). Nürk and Blattner (2010) discussed relationships and evolution in Hypericum in an analysis of morphological characters; the groupings they found had little support. Ruhfel et al. (2011) found some support for an expanded Hypericum, including Thornea. In a much more extensive study of Hypericum, Nürk et al. (2012: ITS only; see also Pílepic et al. 2011) found that Thornea was sister to Hypericum, but support for that position was not strong. In the analysis of Meseguer et al. (2013: four genes, inc. ITS), Thornea was a member of a basal polytomy, Triadenum was clearly to be included in Hypericum (see also Ruhfel et al. 2011; Meseguer et al. 2014), and some of the sections that Nürk et al. (2012) had found to be monophyletic were here paraphyletic. Santomasia was not included in these analyses. More recently, Nürk et al. (2015) has recovered a largely similar set of relationships, but again, support for the basal branchings was not strong. For diversification of South American Hypericum, see Nürk et al. (2014).

Classification. Generic limits need attention, with those of Hypericum and Harungana in particular probably needing to be expanded (Ruhfel et al. 2009, esp. 2011; c.f. in part Stevens 2006c). For a sctional classification of Hypericum, see Robson (2012) and references; Robson (2016) adjusted this somewhat to take on board molecular findings on relationships, unthought of when he began his studies.

PODOSTEMACEAE Kunth, nom. cons.   Back to Malpighiales

Annual (perennial) herbs of fast-flowing water; polyisoprenylated benzophenones 0, quinones 0; plant ± thalloid, stem root and leaf often not distinguishable, plant attached to substrate by haptera, basic construction sympodial; roots photosynthetic, (dorsiventrally flattened), exogenous (endogenous), (apical meristem 0), adventitious roots producing shoots; shoots endogenous, [also at least sometimes flowers], branching extra-axillary; cork?; vessels usu 0; ?resin cells + [glands/canals 0]; epidermal cells with SiO2 bodies and chloroplasts; cuticle waxes 0; when leaves present spiral, opposite, 2- or 3-ranked, leaf base broad or not, "stipules" petiolar or 0; (flowers solitary); (flowers monosymmetric); P +, uniseriate; ?androecial arrangement, A 1-many (2 whorls, inner extrorse), filaments often basally connate (connective prolonged); pollen microechinate, infratectum granular; when G = P, opposite, style + (0), stigma linear; ovules (2-few/carpel), integuments develop simultaneously [?level], outer integument 2(-4) cells across, inner integument ca 2 cells across, (embryo sac protruding), nucellus amoeboid before fertilization; embryo sac monosporic, from the subchalazal spore, tetranucleate [Apinagia type], polar nuclei degenerate; capsule ribbed, about the same size as the ovary, pedicels elongating; exotesta thick-walled, often mucilaginous, (exo- and) endotegmen ± lignified; no double fertilization, embryonic suspensor haustorial; cotyledons large; root developing from hypocotyl; n = 10.

Tristichoideae

48[list]/280 - three subfamilies below. Usually tropical, esp. America.

Age. The age of crown-group Podostemaceae is around (89.4-)80.1, 74.5(-64.3) m.y. (Ruhfel et al. 2016: app. S9).

1. Tristichoideae (Willis) Engler

Xanthones?; primary roots producing shoots, (root 0), (root cap 0); stem (flattened), with determinate branches, (branch systems complanate, laterally connate); stomata?; P 3, connate; A (1-)3, anthers sagittate; pollen pantoporate, in tetrads (?not); G [3]; hypocotyl 0.

3/14-20. India and Southeast Asia to Australia, Tristicha trifaria in Africa and America (map: from van Royen 1953; Cusset & Cusset 1988a; Kito & Kato 2004; Kato 2009).

Age. The age of crown-group Tristichoideae is ca (70.1-)56.9, 52.8(-38.6) m.y. (Ruhfel et al. 2016: app. S9).

Synonymy: Philocrenaceae Bongard, Tristichaceae J. C. Willis

Weddellinoideae

[Weddellinoideae + Podostemoideae]: radicle/primary root 0; G [2].

Age. The age of this clade is (76.8-)66.1, 62(-49.9) m.y. (Ruhfel et al. 2016: app. S9).

2. Weddellinoideae Engler

Plant with scales; root-born shoots 0; flowers single, terminal; P (4) 5 (6), 1-veined; A 5-25, anthers X-shaped; pollen ?development, lacking spinules, rugulate, ?infratectum?; ovary with apical septum having recurrent dorsal bundle, stigma single, globose; capsule not ribbed; tegmen [?layer] thick walled; hypocotyl +.

1/1: Weddellina squamulosa. N. South America (map: from van Royen 1953).

3. Podostemoideae (Warming) Engler

Shoot apical meristem 0 [cryptic embryonic meristem], shoot growth determinate; apical meristems of root on the underside of the thallus, roots foliose or ribbon-like; ("laticiferous" tubes +); stomata 0, "epidermal" cells with dimorphic chloroplasts; "leaves" ± endogenous [initiated as a shoot meristem], often 2-ranked, ensiform, but bifacial, (digitate), (some leaves dithecous [double-sheathed, one sheath on both sides]), (leaves with Podostemoideaeaxillary branches, not dithecous - Thelethylax), base sheathing [?all}, (stipulate); flowers or groups of flowers enveloped by a non-vascularized spathella, (spathella of non-terminal flower open - Diamantina), (flowers monosymmetric), (flowers inverted in bud - some African/Madagascan taxa); P 2-25, often 2-3 on one side, (minute), lobes narrow, sometimes replaced by stamens; A 1-3(-many), often sagittate, (extrorse); (microsporogenesis successive [tetrads tetragonal]), pollen (in dyads, ?tetrads), (a)calymmate, 3(-5)-colpate; G also [3(-7)], (ovary with apical septum having recurrent dorsal bundle), (unilocular), gynophore + (0), style short, branches long, (2 styluli - Diamantina); ovule with outer integument that develops first, (apex of nucellus exposed); (embryo sac bisporic [Polypleurum and Podostemon types]); plumule reduced, (plumule 0), (cotyledon 1); (hypocotylar root exogeneous); (n = 14). Floral Diagram.

45/260: Apinagia (50: perhaps paraphyletic, see Philbrick et al. 2001). Pantropical (map: from van Royen 1951; van Steenis 1972; Kato 2009). [Photo - Marathrum Flower]

Age. Crown-group Podostemoideae are some (63.9-)53.3, 49.7(-40.3) m.y.o. (Ruhfel et al. 2016: app. S9).

Synonymy: Marathraceae Dumortier

Evolution. Bacterial/Fungal Associations. Although there have been suggestions that Podostemaceae are attached to rocks by means of a special glue that they produce, it is more likely that it is materials in a biofilm produced by associated cyanobacteria that attach the plant to the substrate. There are hooked hairs on the lower side of the thallus that stick to the cyanobacterial filaments and associated biofilm. Indeed, these cyanobacteria may even produce nitrate that is used by the plant; Podostemaceae usually grow in oligotrophic rivers flowing over gneiss or granite, being absent in rivers over limestone (Jäger-Zürn & Grubert 2000).

Pollination Biology & Seed Dispersal. Some Podostemaceae self pollinate, the pollen tubes growing through the tissue of the flower to the ovules (Sehgal et al. 2009).

For germination and establishment, see Grubert (1970, 1976); mucilage from the testa firmly attaches the seed to a rock.

Vegetative Variation. Interpretations of the plant body of Podostemaceae, the "thallus", vary greatly The thallus can be thought of as a very highly modified but ultimately fairly conventional plant body (Jäger-Zürn 2005) or as a structure incomparable with anything else in plants, with saltational evolution invoked to explain how the very different and distinctive morphologies in the family have evolved (Koi & Kato 2010). Since Podostemaceae are sister to Hypericaceae, detailed studies of the latter may provide clues for the evolution of the growth of the former, particularly building on the developmental studies of e.g. Katayama et al. (2010, 2013).

Podostemaceae with ribbon-like roots have opposite branching, those with a crustose or foliose growth form have endogenous shoots born singly on the upper surface. The evolution of the remarkable flattened roots of some Podostemoideae and Tristichoideae, which lack caps but have meristematic regions on both sides, from the more ordinary-looking roots found in Weddelinoideae and some other Tristichoideae has been carefully documented by Koi et al. (2006). The exogenous or superficial origin of roots of some Podostemoideae is unusual, since roots are normally endogenous, being initiated inside the pericycle; Cladopus has both exogenous and endogenous lateral roots (Rutishauser & Pfeifer 2002). Whatever their origin, roots often have root caps.

The apex of the stem has a tunica-corpus construction. There is some controversy over whether normal axillary branching occurs or not (e.g. Rutishauser et al. 2005; Jäger-Zürn 2009a). Some taxa have shoots arising endogenously in the cortex (e.g. Moline et al. 2007). In the dithecous leaves of Podostemoideae the leaf bases have two concave sheaths facing in opposite directions and with a flower or branch bud in the axils of each; these leaves usually terminate growth of the axis that bears them (Rutishauser et al. 2003); for the optimisation of these dithecous leaves on a phylogeny of Podostemoideae, see Moline et al. (2007: note the adaxial position of the prophyll of the axillary dithecal vegetative shoot illustrated). Jäger-Zürn (2009b) also depicts the dithecous leaf as being adaxial on the axillary shoot that bears it. Interesting, the determinate ramulus system of Tristichoideae also involves the initial development of one or two cataphylls, the first (or only) cataphyll may be adaxial in position (Fujinami et al. 2013); there a distinction is made between cataphylls and scale leaves, although Terniopsis, sister to the rest of the subfamily, which is supposed to form a pair of leaves (?cataphylls) on all branches before the "ordinary scaly leaves" is not shown in their Fig. 6 as having such leaves. Fujinami and Tmaichi (2015) put the evolution of flattened shoots in Tristichoideae in a phylogenetic context.

Katayama et al. (2010, see also 2013) found from gene expression patterns in two Podostemoideae that it is almost as if a determinate "leaf" caps the indeterminate stem, new leaves/branches developing endogenously from the base of the "leaf". Since separation of the young "leaves" is by cell death, they will lack an epidermis, hence, perhaps, the absence of stomata in the subfamily - although they might be found on the flowers, in which there is more normal development (e.g. Katayama et al. 2008). The "epidermal" cells have dimorphic chloroplasts; smaller chloroplasts are found against the outer periclinal walls and much larger normal-looking chloroplasts against the inner periclinal walls, a condition known only from this subfamily (Fujinami et al. 2011, 2015).

Chemistry, Morphology, etc. Grubert (1976) noted distinctive contents in cells of young plants of several Podostemaceae. For SiO2 bodies, see Machado da Costa (2011).

The nature of the spathella is unclear. Unlike bracts in Podostemoideae examined, its development is that of a "typical organ of leaf homology" (Katayama et al. 2010, see also Katayama et al. 2008), although Eckardt and Baum (2010) suggest more specifically that it is calycine. However, there can be more than one flower per spathella so it cannot be simply calycine. Some species of Dalzellia (Tristichoideae) have a cupule at the base of the pedicel that is formed by leafy shoot axes (Mathew et al. 2001).

Tristicha - A 1, adaxial, median carpel abaxial? (Schnell 1998). The position of the stamens may suggest an obliquely monosymmetric flower (Cusset & Cusset 1988b), while Razi (1955; see also Endress & Matthews 2006a) described the flowers of Zeylanidium olivaceum, which have a spathella, two stamens and two carpels, as being monosymmetric. There is sometimes an apical meristem in the vegetative body of Podostemoideae and the spathella may be produced by the connation of two foliar structures (Jäger-Zürn 2005b). The outer integument develops early and the nucellus protrudes beyond the inner integument. The plasmodial nucellus has been described as a pseudo-embryo sac. Tobe and Raven (2011) describe the tegmen as being unspecialised.

There is considerable variation (and a corresponding amount of controversy) over the development of the embryo sac in particular, perhaps especially in Weddellina (see e.g. Battaglia 1971; Arekal & Nagendran 1975, 1977a, b; Nagendran et al. 1976; Murguía-Sánchez et al. 2002; Sehgal et al. 2011a). Is it mono- or bisporic, and does it have 3, 4 or 5 cells at maturity? However, there is general consensus that there is no double fertilization, the single polar nucleus degenerating (Sehgal et al. 2011b). During development of the embryo, the nucellus becomes plasmodial (different pathways are involved) and helps in the nutrition of the embryo (see Jäger-Zürn 1997).

Although the embryo usually lacks a plumule and radicle, these were reported for Malaccotristicha sp. (Kita & Kato 2005), and the seedling of Zeylanidium olivaceum has a hypocotyl; Koi et al. (2012b) discuss seedling evolution in the family. More information is needed on embryo morphology (but see Koi & Kato 2010).

Much information is taken from Rutishauser (1997), also Cook and Rutishauser (200), general; see also Hegnauer (1969, 1990), Contreras et al. (1993) and Kato et al. (2005), all chemistry, Graham and Wood (1975), Barlow (1986: roots), Cusset and Cusset (1988a), Rutishauser and Huber (1991), both Tristichoideae, Lobreau-Callen et al. (1998: pollen), Rutishauser and Grubert (1993 [Mourera], 2000 [Apinagia]), Passarelli (2002: pollen), Suzuki et al. (2002: seedlings), Sehgal et al. (2002: seeds, etc.), Ameka et al. (2002: general), Koi and Kato (2003: roots, 2007: hypotheses on nature of shoots and leaves), Jäger-Zürn (2003: apical septum, 2005b: interpretation of the thalloid plant body, 2007: shoot apex; 2011: possible new characters), Rutishauser et al. (2004: Diamantina), Rutishauser and Moline (2005: emphasis on "homology"), Jäger-Zürn et al. (2006: microsporogenesis), Sehgal et al. (2007: organ identity), Jäger-Zürn (2008: Thelethylax), Kato (2008: general), Thiv et al. (2009: African Podostemoideae), Ghogue et al. (2009: Djinga, morphology), Koi and Kato (2010: vegetative body, Hydrodiscus et al.), and Grob et al. (2007b: growth, etc., of Thelethylax) and de Sá-Haiad et al. (2010: Podostemon: floral morphology).

Phylogeny. The basic phylogenetic structure of the family is [Tristichoideae [Weddellinoideae + Podostemoideae], all clades having very strong support (Kita & Kato 2001; see also Kita 2002: phylogeny and morphology; esp. Koi et al. 2012a; Ruhfel et al. 2016).

See Moline et al. (2007) for the phylogeny and evolution of African Podostemoideae, Koi and Kato (2010) that of Asian Podostemoideae, and Khanduri et al. (2015: Indian members of the family, also a morphological matrix). In New World Podostemoideae morphological analyses allowed the recovery of a few small generic clades, but molecular data resolved quite a number of nodes (Tippery et al. 2011). The recently-described Diamantina appeared to be sister to all other Podostemoideae (Ruhfel et al. 2009), although that genus was not studied by Tippery et al. (2011), who found Podostemon and a paraphyletic Mourera as successively sister to the rest, while Diamantina was sister to the other members of one of the two major clades into which the subfamily was resolved in Ruhfel et al. (2016) - Mourera belonged to that clade, Podostemon to the other. Koi et al. (2012a: very good sampling) confirmed the position of Diamantina, although support was weak; further large scale structure in Podostemoideae mostly had very little support, and monophyly of genera seems to be almost a foreign concept there.

Koi et al. (2009) discussed the phylogeny of Tristichoideae (and described a distinctive new genus), while Koi et al. (2012a) found groupings in Tristichoideae to be well supported and the genera to be monophyletic (see also Ruhfel et al. 2016: Terniopsis sister tpo the other genera).

Classification. Many genera are monotypic, the morphology of the thallus being so bizarre. For generic limits in some African Podostemoideae, see Thiv et al. (2009).

Previous Relationships. Prior to molecular work, systematists were largely at a loss as to where the relationships of Podostemaceae were to be found. The micropylar suspensor haustorium seemed like that of Crassulaceae, perhaps suggesting a link between the two families (e.g. Les & Philbrick 1996; Ueda et al. 1997a), or isolated in its own order in Rosidae (Cronquist 1981), etc.. Indeed, Podostemaceae have sometimes been placed apart from all other angiosperms (e.g. Cusset & Cusset 1988b).

Possible clade.

[[[Lophopyxidaceae + Putranjivaceae], Caryocaraceae, [Centroplacaceae [Elatinaceae + Malpighiaceae]], [Balanopaceae [[Trigoniaceae + Dichapetalaceae] [Euphroniaceae + Chrysobalanaceae]]]] [[Humiriaceae [Achariaceae [[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]]]] [[Peraceae [Rafflesiaceae + Euphorbiaceae]] [[Phyllanthaceae + Picrodendraceae] [Ixonanthaceae + Linaceae]]]]: ovules 2/carpel, apical, pendulous, epitropous.

Evolution. Divergence & Distribution. Although ovule number can be optimised to this node, both the position and orientation of the two ovules varies...

[[Lophopyxidaceae + Putranjivaceae], Caryocaraceae, [Centroplacaceae [Elatinaceae + Malpighiaceae]], [Balanopaceae [[Trigoniaceae + Dichapetalaceae] [Euphroniaceae + Chrysobalanaceae]]]] / Clade 3 of Xi et al. (2012b): outer integument 5-7 cells across, inner integument 5-6 cells across.

Age. The spread of ages for this clade is (111.4-)107, 102.3(-95.8) m.y. (Xi et al. 2012b: Table S7).

[Lophopyxidaceae + Putranjivaceae] / putranjivoids: stomata paracytic; hairs unicellular; pedicels at most barely articulated; flowers imperfect; sepals not enclosing gynoecium in bud; staminate flowers: stamens ± basifixed, pistillode +; carpellate flowers: staminodes 0; style ± 0; ovules with inner integument much thicker than the outer, endothelium +, parietal tissue +, funicular-placental obturator +; fruit indehiscent, 1-seeded.

Age. Lophopyxidaceae and Putranjivaceae may have diverged in the Cretaceous at end-Coniacian or thereabouts ca 85 m.y.a. (Davis et al. 2005a) or (35.8-)34.2(-33.1) m.y. (Xi et al. 2012b: Table S7).

Chemistry, Morphology, etc. For detailed studies of the floral morphology of these two families, see Matthews and Endress (2013); much information is taken from this account.

Phylogeny. Davis et al. (2005a) found a strong association between this family pair, and they may in turn be associated with the group of families with parietal placentation. However, the position above has strong support in Xi et al. (2012b).

LOPHOPYXIDACEAE H. Pfeiffer   Back to Malpighiales

Lophopyxidaceae

Lianes, climbing by leaf tendrils; chemistry?; secondary thickening anomalous, with included phloem; vessel elements with simple perforation plates; phloem stratified; pith pentagonal; nodes ?; petiole bundles arcuate and with wing bundles; branches with prophyllar bud at base; leaves spiral; plant monoecious; inflorescence branched, ultimate units clusters; flowers with slender pedicels, small; K connate basally, valvate, C small, shorter than K, cordate or reniform nectary glands adnate to C; staminate flowers: stamens = and opposite sepals; carpellate flowers: nectary glands connate at the base; G [(4) 5], opposite petals, ovary ridged, stigmas subulate, adaxially channelled; ovules with outer integument 3-5 cells across, inner integument 5-10 cells across, ?"weakly crassinucellate", suprachalazal zone long; fruit a 5-winged samara, K persistent; seed coat?; endosperm ?development, +, cotyledons long; n = ?

1[list]/1: Lophopyxis maingayi. Malesia to the Solomon and Caroline Islands (map: from Sleumer 1971b).

Evolution. Divergence & Distribution. The diversification rate in Lophopyxidaceae seems to have slowed down (Xi et al. 2012b).

Chemistry, Morphology, etc. Sleumer (1971b) described the tendrils both as being leaves and also bud-bearing branches; the ultimate spirally-recurved portion does seem to be foliar.

For general information, see Kubitzki (2013b), for ovule morphology, see Mauritzon in Sleumer (1942).

Lophopyxis is poorly known.

Previous Relationships. Lophopyxidaceae were included in Celastraceae by Cronquist (1981) and Hutchinson (1973), and in Celastrales by Takhtajan (1997).

PUTRANJIVACEAE Meisner   Back to Malpighiales

Putranjivaceae

Trees; cucurbitacins [triterpenes], glucosinolates, biflavonoyls +; cork?; vessel elements with scalariform perforation plates; petiole bundles elliptic; leaves two-ranked, (lamina with veins running into opaque deciduous teeth, or spines); plant dioecious; inflorescence fasciculate; (K with single trace), C 0, 4-5(-7); nectary + or 0; staminate flowers: A (2-)3-20(-many), (extrorse), (with pseudopit); carpellode?; carpellate flowers: (staminodes 0); G [(1-)2-4(-9)], (style very short, branched), stigmas large, often flap-like, bifid, ?type; ovules (micropyle exostomal), outer integument 3-9 cells across, inner integument 6-14 cells across, (integument single, 6-9 cells across - Drypetes macrostigma), parietal tissue 1-2 cells across, disintegrating early, suprachalazal zone long to short, hypostase massive; megaspore mother cells 2-3; fruit a drupe; testa vascularized, exomesotesta sclereidal, tegmen ± multiplicative, 6-24 or more cells thick, exotegmic cells sclereidal, flat-lying; endosperm copious; n = (19) 20 (21).

3[list]/210: Drypetes (200). Tropical, esp. Africa and Malesia (map: from FloraBase 2005; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006; Andrew Ford, pers. comm.). [Photo - Flower, Fruit]

Evolution. Divergence & Distribution. Some analyses suggest that the diversification rate in Putranjivaceae increased (Xi et al. 2012b).

Pollination Biology. Glucosinolates make the flowers of Drypetes smell very strongly indeed, and they are produced consitutively; bees, wasps and beetles have been recorded visiting Drypetes natalensis (Johnson et al. 2009c).

Plant-Animal Interactions. Perhaps not surprisingly, caterpillars of pierid butterflies have quite often (23/2690 records) been recorded eating Putranjivaceae (see also Brassicales and Fabaceae) - nothing so far is known about Lophopyxidaceae - species of the Indo-Malesian Appias subgenus Catophaga (albatrosses) feeding more or less indiscriminately on Drypetes (Putranjivaceae) and Capparaceae (Yata et al. 2010). In Drypetes natalensis, at least, constitutively-released isothiocyanates are part of the floral odour, but what exactly they do is unclear (Johnson et al. 2009a).

Chemistry, Morphology, etc. Older literature is under Euphorbiaceae. For general information, see Levin (2013), for chemistry, see Hegnauer (1966, 1989), for wood anatomy, Hayden and Brandt (1984: like that of Aporosa, etc. [= Phyllanthaceae]), for embryology and seed anatomy, see Singh (1970) and Stuppy (1996).

Phylogeny. Tokuoka and Tobe (1999, 2001) included Lingelsheimia here, but it has a tegmen 3-4 cells thick and a vascularized testa and it is to be placed in Phyllanthaceae (see Kathriarachchi et al. 2005).

Classification. For a checklist and bibliography, see Govaerts et al. (2000).

Previous Relationships. Putranjivaceae have usually been included in Euphorbiaceae (as by Webster 1994b, in Phyllanthoideae), but can be distinguished i.a. by their chemistry, embryology, and fruit. They are certainly not to be placed with the rest of the glucosinolate families in Brassicales (e.g. Rodman et al. 1997, 1998).

CARYOCARACEAE Voigt, nom. cons.   Back to Malpighiales

Caryocaraceae

Trees to shrubs; ellagic acid, triterpenoid saponins + [Caryocar]; vessel elements with simple (scalariform) perforations; nodes 5 or more:5 or more; petiole bundles incurved arcuate, irregularly annular, etc.; pericyclic sheath little lignified; branched sclereids +; cuticle waxes as smooth to irregular platelets; colleters +; leaves opposite [Caryocar] or spiral, trifoliolate, leaflets ± articulated, (margins entire), stipellate or not, stipules ± intrapetiolar [Anthodiscus] or inter-intrapetiolar; inflorescences terminal, racemose(-corymbose); pedicels articulated, bracts 0; flowers large [>5 cm across], (6-merous); K imbricate, (small, ± connate, lobed - Anthodiscus), C protective in bud, with 3 traces, connate below, or forming a deciduous calyptra; A many, connate at base and adnate to C, (in 5 bundles), filaments long, tuberculate/vesiclulate towards apex, anthers basifixed, inner stamens staminodial; nectary at base of staminodia/0 [Anthodiscus]; G [4-6 - Caryocar] [8-20], placentation basal, styluli +, impressed, arising together, with 2 vascular bundles, stigmas punctate-impressed; ovule 1/carpel, basal, erect, campylotropous to anatropous, sessile [attachment broad], micropyle endostomal, outer integument 2-3 cells across, inner integument 3-4 cells across, (unitegmic, integument 4-5 cells across - Anthodiscus), parietal tissue?, epidermal cells of nucellar apex radially elongated, nucellus below embryo sac massive, obturator 0; fruit a drupe, (pericarp with radiating fibres - Caryocar), stone separating into 1-seeded units; seeds reniform, hilum large; coat undistinguished, testa vascularized, aerenchymatous or not, exotegmen?; endosperm type?, at most thin, (hypocotyl very large, oily, spirally-twisted - Anthodiscus); n = 23.

2[list]/27: Anthodiscus (18). Tropical America, esp. Amazonia (map: from Prance & Freitas da Silva 1973). [Photo - Flower, Flower, Fruit.]

Age. Crown-group Caryocaraceae are (57.2-)55.8(-54.8) m.y.o. (Xi et al. 2012b: Table S7).

Evolution. Pollination. Both genera are pollinated by bats (Fleming et al. 2009).

Chemistry, Morphology, etc. Prance and Freitas da Silva (1973) described Anthodiscus as lacking stipules.

Dickison (1990c) described details of the complex floral vasculature and other floral features; in Anthodiscus each stylulus receives a vascular bundle from adjacent carpels and so is presumably commissural, while the styluli of Caryocar are vascularized from single carpels. The androecium may form a ring primordium (Ronse de Craene & Smets 1992b).

See Hegnauer (1964, 1989, the latter also under Lecythidaceae) and Chisté and Mercadante (2012) for chemistry; the fruits of both genera are used as fish poisons.

For general information, see Prance (20130, and for vegetative anatomy, see Beauvisage (1920).

All in all, the family is rather poorly known, especially embryologically.

Previous Relationships. Both Cronquist (1981) and Takhtajan (1997) included Caryocaraceae in Theales.

[Centroplacaceae [Elatinaceae + Malpighiaceae]] / malpighioids: pedicels articulated; K persistent in fruit.

Age. The ages of this clade are (109.4-)102.1(-93.3) m.y. (Xi et al. 2012b: Table S7) or ca 90.3 m.y. (Tank et al. 2015: table S2, younger than next node up).

Phylogeny. for relationships in this area, see W. Zhang et al. (2009a, 2009b, 2010) and Wurdack and Davis (2009); Xi et al. (2012b: = malpighioids) found that support for the inclusion of Centroplacaceae in this clade was only weak (63% ML bootstrap; 0.51 PP).

CENTROPLACACEAE Doweld & Reveal   Back to Malpighiales

Centroplacaceae

Trees; inflorescence branched; A 5, opposite sepals; style branches widely diverging, stigmas little expanded; ovules collateral; fruit a loculicidal capsule, seed one/loculus, with [?]exostomal aril; exotegmic cells laterally compressed, thick-walled; embryo short; n = ?.

2[list]/6. West Africa, Indo-Malesia.

Age. The crown age of this clade is around (94.3-)63.7(-35.1) m.y. (Xi et al. 2012b: Table S7).

1. Centroplacus Pierre

Chemistry?; cork?; vessel member perforations?; sclereids +; stomata anisocytic; leaves two-ranked, stipules cauline; plant dioecious; flowers small; nectary outside A, lobed, lobes alternating with K; staminate flowers: anther dehiscence oblique-apical, connective well developed; pollen psilate, perforate; pistillode +; carpellate flowers: C 0; staminodes +, minute; G [3], placentae swollen; ovules subapical, ?morphology, obturator 0; fruit also septicidal, opening from the base; exotestal cells rather tall, outer wall thickened, mesotegmic cells flattened, at right angles to exotegmen, endotegmen ± thick-walled.

1/1: Centroplacus glaucinus. W. Africa (blue on map above: from Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006).

2. Bhesa Arnott

Chemistry?; (cork mid-cortical); vessel elements with scalariform perforation plates; paratracheal parenchyma +; nodes 5:5; calcium oxalate as crystals [?always]; petiole with bundles forming a U or flattened-annular, 2-3 medullary bundles, (also wing bundles); stomata laterocylic; leaves spiral, lamina vernation conduplicate, margins entire, tertiary venation closely scalariform, petiole ± pulvinate apically, stipules almost encircling the stem, colleters +; inflorescence racemose; C contorted; A extrorse to introrse; pollen finely striate; nectary lobed or not; G [2]; ovules basal, apotropous, micropyle exostomal, outer integument 6-8 cells across, inner integument 4-5 cells across, hypostase +; fruit loculicidal; aril sheet-like; exotegmic cells massive, exotegmic cells laterally compressed tracheidal; germination epigeal.

1/5. Indo-Malesia (red on map above: from Ding Hou 1962).

Evolution. Divergence & Distribution. Xi et al. (2012b: some analyses) found that diversification rate in this clade slowed down.

Bacterial/Fungal Associations. Bhesa is reported to be ectomycorrhizal (Smits 1994).

Chemistry, Morphology, etc. The ribbon-shaped exotegmic cells of Bhesa are longer than those of Centroplacus, and its integument is much thicker. The endostome of Centroplacus is lignified and more or less protruding.

For general information, see Kubitzki (2013b): Bhesa is often under Celastraceae, see Pierre (1894), Ding Hou (1962) and Wurdack and Davis (2009), genearl information, for seed and vegetative anatomy of B. ceylanica, see Jayasuriya & Balasubramaniam 3107, for seeds of B. robusta, see Corner (1976). Centroplacus is often in Euphorbiaceae: see Forman (1966) and Radcliffe-Smith (2001), both general, Stuppy (1996: seed anatomy and good discussion), and Tokuoka and Tobe (2001: seed anatomy, ?Euphorbiaceae-Phyllanthoideae).

Studies of the embryology, etc., of both genera are much needed.

Phylogeny. In a molecular study by Wurdack et al. (2004) Centroplacus was associated with Pandaceae, although with very little support, however, in Davis et al. (2005a) it was separate from Pandaceae and weakly associated with Ctenolophonaceae. L.-B. Zhang and Simmons (2006) found that Bhesa fell among the few Malpighiales they included in their analysis of Celastrales, and Ken Wurdack (pers. comm.) suggested that a position around about here may be appropriate.

Classification. Recognising the two genera as a single family seems most reasonable, although they are quite distinct in their gross morphology.

Previous Relationships. Centroplacus glaucinus has been placed in Pandaceae (Takhtajan 1997; Mabberley 1997), but Webster (1994b) and Radcliffe-Smith (2001) included it in Euphorbiaceae, but only with hesitation and with little certainty as to where it should be placed within the family.

Bhesa was distinctive in morphological analyses of Celastraceae, in which it used to be included (Simmons & Hedin 1999; Matthews & Endress 2005b), if sometimes with some doubt (e.g. Pierre 1894 [he thought it might be in a separate family]; Metcalfe & Chalk 1950; Ding Hou 1962). Its huge stipules, distinct styles, vessels with scalariform perforation plates, etc., were somewhat out of place there, although Celastraceae were so heterogeneous that a strong case could not be made for its removal. The seed coat, with its massive exotegmic cells, is also very different, as are its pentalacunar nodes.

[Elatinaceae + Malpighiaceae]: vessel elements with simple perforation plates; sieve tube plastids lacking starch and protein inclusions; leaves opposite, with glands[?], (lamina margins entire); inflorescence cymose; flowers with inverted orientation [odd petal adaxial]; nectary 0; when G 3 median member adaxial, ?integument; fruit septifragal; endosperm slight; x = 6.

Age. Malpighiaceae and Elatinaceae may have separated some (113-)98, 89(-85) m.y.a. (Davis et al. 2005a), ca 93.7 m.y.a. (Tank et al. 2015: table S2), or (99.9-)86.1(-72.9) m.y.a. (Xi et al. 2012b: Table S7).

Evolution. Divergence & Distribution. Depending on the interpretation of variation, both the evolution of monosymmetric flowers and flowers with an inverted orientation can be pegged to this node (W. Zhang et al. 2009a, 2010: see also the discussion after Malpighiaceae).

Chemistry, Morphology, etc. For the foliar glands and resin and latex production in Elatinaceae and Malpighiaceae, neither well understood, see Vega et al. (2002) and Davis and Chase (2004). Vega et al. (2002) suggested that the laticifers of Galphimieae might be a symplesiomorphy with those of Euphorbiaceae, however, laticifers are not even an apomorphy of that family, which anyhow is not immediately related to this group (see below); I know nothing of the composition of the latex of Malpighiaceae.

For variation in seed size, see Moles et al. (2005a).

Phylogeny. Support is strong for the sister-group relationship between Malpighiaceae and Elatinaceae (e.g. Davis & Chase 2004; Tokuoka & Tobe 2006; Korotkova et al. 2009; Wurdack & Davis 2009; Wang et al. 2009; Xi et al. 2012b, etc..

ELATINACEAE Dumortier, nom. cons.   Back to Malpighiales

Elatinaceae

Herbs to subshrubs of moist/wet habitats; flavonols, ellagic acid +; plant resinous; (cork from inner cortex); nodes 1:1; mucilage cells +; leaves with colleters, stipules scarious; ?pedicel articulation; flowers (single), (2-)5-6-merous, K connate (free), (with an apical "gland"), C contorted or imbricate; stamens = and opposite sepals, or 2x K; tapetal cells binucleate; (pollen grains tricellular - Elatine); G [2-5], opposite sepals, stigma papillate; ovules many/carpel, (not vascularized), micropyle bistomal, zigzag, outer integument 2-3(-5) cells across, inner integument 2-3 cells across, parietal tissue 1-4 cells across, suprachalazal zone at least initially long [Bergia]; megaspore mother cells several; fruit a capsule; seeds ± curved; exotestal cells in vertical lines, exotegmen with low lignified sinuous anticlinal cell walls; embryo ± fusiform; n = (9, 18, 20); duplication of CYC genes.

2[list]/35: Bergia (25), Elatine (10). Worldwide, most tropical, not arctic (map: from Meusel et al. 1978; Frankenberg & Klaus 1980; FloraBase 2006; Popiela et al. 2012).

Age. Crown-group Elatinaceae are (76.3-)48(-25.1) m.y.o. (Xi et al. 2012b: Table S7).

Chemistry, Morphology, etc. Eichler (1878) draws three-merous flowers of this family with the odd sepal abaxial, i.e., in the monocot position, and W. Zhang et al. (2010: Supplement 1) consider that this orientation also occurs in flowers of the 5-merous Bergia texana. Kubitzki (2013b) recorded the ovules as being epitropous; they are shown as being apotropous in the literature that I have seen. Friesendahl (1927) thought that the mesotegmen was lignified in Elatine while Dathan and Singh (1971 and references) recorded the seed coat of Bergia as being exotegmic.

For general information, see Kubitzki (2013b); for embryology, see also Kajale (1940a), Raghavan and Srinivasan (1940a) and Tobe and Raven (1983b: summary).

Synonymy: Cryptaceae Rafinesque

MALPIGHIACEAE Jussieu, nom. cons.   Back to Malpighiales

Malpighiaceae

Lianes to trees; (inulin +), ellagic acid 0; (cork ?near endodermis); secondary thickening often anomalous, (interxylary phloem +); pits vestured; (nodes 1:1); petiole bundle arcuate; cuticle waxes as rosettes; stomata usu. paracytic; branching from current flush; hairs unicellular, ± T-shaped, surface rough; leaves glands common, abaxial or petiolar, stipules cauline, intrapetiolar and hooded or petiolar; inflorescence various; flowers monosymmetric (polysymmetric); 4 or 5 K with pairs of large abaxial oil glands (0 - esp. Old World taxa), C clawed, often crumpled in bud, often fringed, one adaxial-lateral often different to the others; A (2; = and opposite sepals) 10, obdiplostemonous, (15), often basally connate; tapetal cells multinucleate; G [3(-5)], styles +, (style single), stigma dry; ovule 1/carpel, apical, pendulous, epitropous, micropyle exo/endo/bistomal, (apex of nucellus exposed), outer integument 2-4 cells across, inner integument 3-6 cells across, parietal tissue 10< cells across, nucellar beak +, (epistase +), hypostase +, (suprachalazal area massive), (pachychalazal); megaspore mother cells 1-several, embryo sac tetrasporic, 16-nucleate [Penaea type], (bisporic, 8-nucleate); K and A often persistent in fruit, (K accrescent, wing-like); fruit separating into mericarps, or indehiscent; exotegmen 0; endotegmic cells (elongated), lignified; (endosperm pentaploid), chalazal endosperm haustoria +, (embryo spirally coiled), cotyledons incumbent; duplication of CYC genes.

68[list]/1250 - two groups below. Tropical and subtropical, especially American (map: C. C. Davis, from Arènes 1957; Anderson 2011; Australia's Virtual Herbarium xii.2013). [Photo - Flower, Flower, Fruit.]

Age. The age of crown-group Malpighiaceae has been estimated at (39-)36, 32(-29) m.y. (Wikström et al. 2001), 75-64 m.y. (Renner & Schaefer 2010), or ca 68 m.y. (Davis & Anderson 2010); ages of (69-)59.8(-52.5) m.y. were suggested by Xi et al. (2012b: Table S7).

The earliest fossils attributable to Malpighiaceae are from the Northern Hemisphere in the later Eocene Claiborne Formation in Tennessee, U.S.A.; the deposits are ca 34 m.y. old (Taylor & Crepet 1987: Eoglandulosa; see also Friis et al. 2011).

1. Byrsonimoideae W. R. Anderson

(Articulated laticifers + - Galphimieae); style subulate, stigma terminal; (exotegmen fibrous - Thryallis); (fruit baccate); (hypocotyl ± 0); n = 6.

Byrsonima (150). American Tropics.

2. Malpighioideae Burnett

(Monofluoroacetates +); (leaves spiral, stipules 0 - Acridocarpus); pollen globally symmetric [4-polyporate]; (G [2], inferior - Acridocarpus), style various, stigma usu. not terminal, asymmetrically capitate; (integument 1, 3-5 cells across - Janusia); fruit winged, (bristly), (unwinged); n = (9) 10.

Heteropterys (120), Stigmaphyllon (105), Banisteriopsis (90), Bunchosia (55), Mascagnia (50), Malpighia (40). Tropical and subtropical, especially the Americas.

Evolution. Divergence & Distribution. The rate of diversification may have increased in Malpighiaceae (Xi et al. 2012b). An origin of the family in South America during the Late Cretaceous has been suggested, with several - it now appears to be nine - subsequent migration/dispersal events to the Old World followed by the loss of oil secretion by the sepals in the taxa involved (Davis et al. 2002a, b, 2004; esp. Davis & Anderson 2010; see also below). Malpighiaceae in Mexico are very diverse in seasonally-dry tropical forest, and this is because of the numerous (over 30) dispersal events from the south as much as subsequent diversification of these clades in Mexico. Initially animal-dispersed clades (more l.d.d.) were involved, but there was an increase in wind-mediated dispersal events in the mid-Miocene ca 24 m.y.a. when connections with South America were established (Anderson 2013; Willis et al. 2014 [see also B. Bremer & Eriksson 1992]; Bacon et al. 2015a, c.f. Proc. National Acad. Sci. U.S.A. 112(43): E5765-E5678; Montes et al. 2015: geology re-evaluated).

Ecology. Malpighiaceae are one of the three ecologically most important groups of lianes in the New World tropics, around 400 species being lianescent (see also Bignoniaceae-Bignonieae and Sapindaceae-Sapindoideae: Gentry 1991; additional information in Angyalossy et al. 2015).

Pollination Biology. New World members of the family are noted for having oil flowers, a trait that is probably plesiomorphic in the family. Oil is secreted by paired glands, epithelial elaiophores, on the backs of the sepals. Several genera of Apidae and solitary Centridini (Epicharis, Centris: paraphyletic, see below) are pollinators. Centridini bees have tufts of hairs on four legs that the insects use to get the oil from the glands on the sepals (Martins et al. 2014), at the same time holding on to the flower by grasping the narrow base of the adaxial banner petal with their mandibles; this banner petal is often distinctively coloured, and may change colour as it ages (Renner & Schaefer 2010 and references). Note that flowers of New World Malpighiaceae have a "monocot" orientation, the flower being rotated 36o, and so the odd petal, the banner petal, is adaxial (W. Zhang et al. 2010). At least some species with apparently yellow flowers - yellow flowers are common in the family - are bee UV-green (Papadopulos et al. 2013). Bezerra et al. (2009) discussed the pollination networks formed by bees and plants, and found them to be very resilient to the loss of species of either (see also Mello et al. 2012: 75 bee and 64 malpig spp.), although activities of the bees on flowers other than those of malpigs were not discussed. Trigonid bees visit the flowers of New World malpigs for pollen (Anderson 1979), and some taxa are buzz pollinated (Sigrist & Sazima 2004). Davis et al. (2014b) note that the floral morphology of these New World oil-secreting taxa is not very variable, even if there are many species there; they attribute this to stabilizing selection rather than some kind of inherent developmental stasis.

The flowers of some Oncidiinae orchids mimic (both Batesian and Müllerian mimicry) those of Malpighiaceae (see esp. Papadopulos et al. 2013). The orchids may even provide distinctive fatty acids as a reward that are similar to those of Malpighiaceae (Reis et al. 2007 and references); the mimicry unit of the orchid is formed largely by the labellum, with the column being visually similar to the malpighiaceous banner petal. Other Oncidiinae have a distinctive shiny green nectary-look alike on the labellum, which may otherwise be white. In addition to the calyx glands, Malpighiaceae may have small glands, osmophores, on the fimbriate margins of the petals, as well as glands on the anther connectives, but these have a less clear role in pollination (Possobom et al. 2015).

Cardinal and Danforth (2013) suggested that Centradini (Centris 230 spp.; Epicharis 35 spp.) and Tetrapedia bees which take oil from Malpighiaceae, evolved in the Late Cretaceous, 87-52 and 92-66 m.y.a. respectively, and these ages and the family ages above are broadly consistent. Martins et al. (2014a; see also Hedtke et al. 2013) found Centradini to be paraphyletic, Epicharis diverging (102-)91(-79) m.y.a. and Centris (95-)84(-72) m.y.a., about contemporaneous with Xi et al.'s (2012b) estimate of the stem-group age of Malpighiaceae of (100-)86(-73) m.y. (75-60(-32) m.y.a. above), and broadly consistent with some kind of co-evolutionary story. Crown ages of Epicharis are (39-)28(-18) m.y.a. and of Centris (58-)44(-36) m.y.a., rather younger than most family ages. Fossils of Eoglandulosa warmanensis from the Eocene Claiborne Formation in Tennessee, U.S.A., and ca 34 m.y.o. show the distinctive paired glands on the sepals (Taylor & Crepet 1987; Friis et al. 2011). Details of the evolution of the association between the bees and malpigs are currently unclear.

In Galphimia brasiliensis the subbasal glands on the lamina margins have the same anatomy as small glands on the sides of the sepals towards the base, both secreting oil (Castro et al. 2001). However, Lobreau-Callen (1989) recorded the leaf/bracteole glands of G. bracteata as producing sugars.

Oil is secreted by New World taxa only. There are about 150 species of Old World Malpighiaceae, relatively few compared to the New World, but they show much more variation in basic floral morphology, and this is associated with the adoption of different pollinators and pollination mechanisms. Their flowers may be radially symmetrical and/or have a "normal" floral orientation for a core eudicot with the odd petal abaxial (W. Zhang et al. 2010), and this has happened independently in the separate clades (Davis et al. 2014b); there are 9 separate dispersal events to the Old World (see above). The calyx glands may secrete nectar (Vogel 1974, 1990; Ren et al. 2013), although in most pollen is the only obvious reward (Davis & Anderson 2010). The anthers may be porose or have slits, and the flowers are on occasion mirror images and have a single stamen much larger than the rest (Ren et al. 2013). The flowers tend to be more or less polysymmetric, the petals are less strongly clawed, and the style branches are longer and more widely spreading (Davis & Anderson 2010 for illustrations).

Self-fertilization is common in species of Gaudichaudia, Janusia and relatives. Here pollen tubes grow from the indehiscent anther through the tissues of the flower to the embryo sac (Anderson 1980; X.-F. Wang et al. 2011). Apomixis - nucellar polyembryony - is common, and embryo sac development and reproduction in general is very variable; as Johri et al. (1992: p. 450) noted "failure of fertilization is a common feature of Malpighiaceae".

Genes & Genomes. There have been duplication(s) of CYC genes, and CYC2 genes are expressed only in the adaxial part of the flower in monosymmetric Malpighiaceae. However, details of exactly when gene duplication occurred and what changes in pattern of gene expression there have been are unclear (W. Zhang et al. 2010). Polysymmetry is associated with changes in the expression of the CYC2 gene, and these differed in each case of the evolution of polysymmetry studied (Zhang et al. 2013).

Chemistry, Morphology, etc. Acridocarpus has spiral, exstipulate leaves. Some species of Stigmaphyllon have leaves with palmate venation and toothed margins; some taxa, especially when young, have almost fimbriate lamina margins, albeit distantly so (the fimbriae are ca 4 mm long). Stipules are very diverse, being petiolar in Hiraea and cauline in many vines and also in Malpighia; in the latter genus they may be lobed or toothed.

The flowers of Acridocarpus have an inferior ovary with only two fertile carpels. Although Lorenzo (1981) suggested that the nucellar beak was produced by periclinal divisions of the epidermal cells, i.e., it would technically be a nucellar cap, the cell wall patterns do not suggest this.

Testa anatomy may repay investigation. In Mascagnia macrodisca there is a layer of thin-walled, slightly elongated cells with brown contents over a layer of more or less isodiametric, lignified cells with somewhat more thickened and straight anticlinal walls, the latter layer having a "frosted" appearance; the origin of these cell layers is not known (pers. obs.). Given that the main protective part of the propagule is not the seed coat, testa and tegmen are likely to be more or less reduced. In Banisteriopsis there is vascular tissue in the testa, and the seed is more or less exotestal (Silva & Trombert 2008). Endotegmic fibres may be quite conspicuous (Silva & Trombert 2006), but since fibres in other Malpighiales are exotegmic and Elatinaceae also have exotegmic seeds (but see above), what is going on in Malpighiaceae is unclear.

Some information on chemistry is taken from Hegnauer (1969, 1989: iridoids have been reported from Stigmatophyllum) and Lee et al. (2012: monofluoroacetates); for embryology, etc., see also Stenar (1937), A. M. S. Rao (1941 and references), Subba Rao (1980), and Souto and Oliveira (2005, 2008), for fruit and seed is taken from Takhtajan (2000), and seedlings from Barbosa et al. (2014). C. Anderson et al. (2006 onwards) provide vast amounts of general information, especially phylogeny and nomenclature, and links to papers, on the whole family.

Phylogeny. Information on relationships within the family is taken from Davis et al. (2001) and Cameron et al. (2001); within Malpighiodeae, for the most part well-supported branches including Acridocarpus, McVaughia, Barnebya, Ptilochaeta, [Bunchosia, Tristellateia] and Hiraea (these are the main genera in the clades) are successively sister to the remaining taxa. A recent study by Davis and Anderson (2010: four genes, all genera sampled) returned the same set of relationships, and with good support; there are many other well-supported clades. Within Byrsonimoideae, relationships are [Galpimia group [Acmanthera group + Byrsonima group]] (Davis & Anderson 2010).

Previous Relationships. Malpighiaceae were included in Vochysiales by Takhtajan (1997) and in Polygalales by Cronquist (1981).

[Balanopaceae [[Trigoniaceae + Dichapetalaceae] [Euphroniaceae + Chrysobalanaceae]]] / chrysobalanoids: hairs simple [unicellular always?]; ovules collateral, micropyle bistomal, outer integument >5 cells across, inner integument >5 cells across, nucellus evanescent by maturity, endothelium +; endosperm at most slight, embryo chlorophyllous.

Age. This node can be dated to (106)100(-95.5)/(95-)90(-88.5) m.y. (Davis et al. 2005a), (94.9-)83.5(-74.8) m.y. (Xi et al. 2012b: Table S7), ca 76 m.y. (Tank et al. 2015: table S2), (83-)71-70(-58) m.y. (Bell et al. 2010), or (62-)59, 57(-54) m.y. (Wikström et al. 2001).

Evolution. Divergence & Distribution. Polarization problems again: Fruit plesiomorphically a drupe, with transitions sot septicidal capsule, or fruit types apomorphies for individual families...?

Chemistry, Morphology, etc. Tobe and Raven (2011) suggested that there is a multiplicative inner integument; although it is thick, it does not usually become thicker after fertilization. There is insufficent information to know if a vascularized testa might be an apomorphy for the clade.

For a comparison of general morphology within the clade, see Litt and Chase (1999), for floral morphology in particular, see Matthews and Endress (2006a); for ovule position, see Merino Sutter and Endress (2003), and for pollen, see Furness (2013b).

Phylogeny. For relationships, see especially Litt and Chase (1999). This group (= chrysobalanoids: Xi et al. 2012b) has held together strongly in subsequent studies.

BALANOPACEAE Bentham & J. D. Hooker, nom. cons.   Back to Malpighiales

Balanopaceae

Trees; ellagic acid?, prob. tanniniferous; vessel elements long [usu. 1,000 µm<], with scalariform perforation plates; parenchyma diffuse; sclereid nests with rhomboidal crystals in bark; rhomboid crystals +; petiole bundle?; (cristarque cells in leaf); buds perulate; cuticle waxes 0 (platelets); stomata usu. laterocytic; leaves spiral, lamina tooth ?type, stipules minute; plant dioecious; staminate plants: inflorescence catkinate; P +, uniseriate, of small teeth; A (1-)3-6(-14), anthers much longer than filaments; pollen 3-5-colpate, microechinate, exine columellate-granulate; pistillode common; carpellate plants: inflorescence fasciculate; flowers with cupule made up of spirally arranged bracts; P 0; staminodes 0; G [(2)], styles long, once or twice bifid, stigma adaxial on styles, ?type; ovules subbasal, apotropous, facing laterally, outer integument 5-7 cells across, inner integument 5-9 cells across, parietal tissue ca 2 cells across; fruit a drupe, with 2-3 stones; testa vascularized, persistent, cell walls not much thickened; endosperm ?type, slight, embryo large, cotyledons cordate; n = 20 (21); germination epigeal, phanerocotylar, cotyledons with single adaxial papilla.

1[list]/9. S.W. Pacific, especially New Caledonia (map: from van Steenis & van Balgooy 1966). [Photo - Fruits © Andrew Ford, CSIRO.]

Evolution. Divergence & Distribution. Some analyses suggest that the diversification rate in Balanopaceae decreased (Xi et al. 2012b).

Chemistry, Morphology, etc. The leaves are often described as being dimorphic (Carlquist 1980; Cronquist 1983), but they are no more so than in many plants that have perulate buds.

Pollen descriptions in Feuer (1991) and Herendeen et al. (1995) differ somewhat.

For general information, see Carlquist (1980) and Kubitzki (2013b); Batygina et al. (1991) provide details of testa anatomy, Merino Sutter and Endress (2003) of the floral morphology of carpellate flowers.

Previous Relationships. Relationships of Balanopaceae were for long problematic. Cronquist (1983) compared their wood anatomy with that of Hamamelidaceae, Balanopales were included in Daphniphyllanae by Takhtajan (1997), while Merino Sutter and Endress (2003) found that many features of the female flowers were consistent with a position in Malpighiales, Balanopaceae perhaps being somewhat similar to Euphorbiaceae s.l..

[[Trigoniaceae + Dichapetalaceae] [Euphroniaceae + Chrysobalanaceae]]: vessel elements with simple perforation plates; vestured pits +; mucilage cells +; stomata paracytic; lamina margins entire, (flat surface glands or glandular hairs +); pedicels articulated; flowers obliquely monosymmetric; K basally connate, with epidermal mucilage cells, quincuncial, 2 outer members shorter; fertile stamens abaxial, ± connate, anthers with a little pit where the filament joins, connective well developed abaxially with endothecium continuous there, staminodes adaxial; G with longitudinal furrows, unicellular unlignified hairs +, style +, stigmas commissural; ovules with zig-zag micropyle, outer integument 2-5 cells across, inner integument 3-8 cells across, parietal tissue?, obturator +.

Age. This node can be dated to (53-)50, 41(-38) m.y. (Wikström et al. 2001) and (72-)60, 59(-46) m.y. (Bell et al. 2010).

Chemistry, Morphology, etc. Matthews and Endress (2008), q.v. for much information, elaborate the floral morphology of this clade and suggest synapomorphies for its members.

Previous Relationships. Including these four families in Chrysobalanaceae s.l. was optional in A.P.G. II (2003), and specimens of Chrysobalanaceae and Dichapetalaceae are quite often misidentified as the other family (G. T. Prance, pers. comm.), however, the families are kept separate by Prance and Sothers (2003a) and A.P.G. III (2009).

[Trigoniaceae + Dichapetalaceae]: (vessel elements with scalariform perforations); petiole bundle arcuate; lamina with strongly looping secondary veins; inflorescences cymose; K with mesophyllar mucilage cells; nectary with lobes or scales, semi-annular [staminodial?]; ovary and lower style completely synascidiate; outer integument <5 cells across; testa multiplicative.

Age. The age of this node may be (43-)40(-37), (32-)29(-26) m.y. (Wikström et al. 2001), (66-)50, 48(-34) m.y. (Bell et al. 2010), ca 57 m.y. (Tank et al. 2015: table S2), or (71.4-)59.7(-47.4) m.y. (Xi et al. 2012b: Table S7).

TRIGONIACEAE A. Jussieu, nom. cons.   Back to Malpighiales

Trigoniaceae

Trees or lianes; helical thickening in ray and axial parenchyma; wood fluorescing [1 sp]; parenchyma in apotracheal bands; branched sclereids +; (nodes with split laterals); hairs unicellular, T-shaped or not; leaves opposite, spiral or two-ranked, lamina with dense whitish hairs below (not), stipules interpetiolar [when leaves opposite]; (inflorescence racemose - Isidodendron); C contorted, adaxial-lateral petal basally spurred or saccate [the standard], plicae in abaxial + abaxial-lateral petals form the keel, or these petals saccate; A 5-13, filaments ± connate, fertile stamens 4-9, adaxial, endothecial cells extending over the back of the connective, staminodes 0-6; pollen 3-5-porate; nectary of 1 or 2 [and then each to 3-lobed] glands at base of standard (glands on base of staminodes - Isododendron); G [(4)], median member adaxial, placentation also parietal, stigma capitate to slightly trilobed, papillate; ovules 1-10/carpel, (apotropous), (micropyle endostomal); outer integument 2-3 cells across, inner integument 4-6 cells across, whole inner integument endothelial; fruit a septicidal capsule, valves opening internally, central fibrous strands persisting, (hairs from endocarp- Trigoniastrum), or samara; seeds (winged), (long-hairy); tegmen also multiplicative, exotesta with thickened outer walls, with long lignified hairs or not, endotegmic cells tanniniferous, walls slightly thickened; endosperm +/0, development?; cotyledons large; n = ca 10; germination epigeal, phanerocotylar.

5[list]/28: Trigonia (24). Central and South America, Madagascar (Humbertiodendron), W. Malesia (Trigoniastrum) (map: from van Steenis 1949c; Lleras 1978). [Photo - Flower.]

Age. Crown-group Trigoniaceae can be dated to (49.6-)31.6(-12.6) m.y. (Xi et al. 2012b: Table S7 - sampling).

Chemistry, Morphology, etc. Trigonia has opposite leaves, interpetiolar stipules, and split lateral vascular bundles; lamina glands are not obvious. The bracts of Trigoniastrum are more or less glandular, with large glands on the abaxial surfaces, Trigonia has stalked glands variously on pedicels or petioles and margins of bracts and leaves, while Humbertiodendron has concave marginal glands towards the base of the leaf blades.

For floral morphology, I follow the interpretations of Warming (1875) and Eichler (1878) rather than that of Cronquist (1981). Schnizlein (1843-1870: fam. 233) draws the flowers as being more or less vertically monosymmetric, while the orientation shown by Schatz (2001) is difficult to work out; in the latter it appears that the corolla may be quincuncial. Warming (1875) showed the nectary glands as being part of the androecial whorl; Lleras (1978) describes them as being "disc glands". In any event, the androecium at least sometimes seems to have more than 10 stamens. Testa anatomy is similar to that of Linaceae, but the two are not immediately related.

Some general information is taken from Lleras (1978), Takhtajan (2000), Fernández-Alonso et al. (2000) and Bittrich (2013); see Hegnauer (1973) for chemistry, Carlquist (2012c) for some wood anatomy, and Mauritzon (1936) and Boesewinkel (1987) for embryology, etc..

Previous Relationships. Trigoniaceae were included in Vochysiales by Takhtajan (1997), while Cronquist (1981) placed them in Polygalales.

DICHAPETALACEAE Baillon, nom. cons.   Back to Malpighiales

Dichapetalaceae

Trees or lianes; (monofluoroacetates, pyridine alkaloids +); sieve tubes with non-dispersive protein bodies; parenchyma ± paratracheal; pericyclic sheath interrupted; fibres common; branching from current flush; hairs warty[?]; leaves spiral, (lamina with flat abaxial glands), stipules fimbriate or not; inflorescence epiphyllous, from petiole, (not); flowers small [<6 mm across], (polysymmetric), (4-merous); C (connate), petals bifid (unlobed), (3 small entire petals forming a "lip" - Tapura), drying black; nectary a ring, or bilobed lobes opposite petals; stamens 5, opposite sepals, (3 + 2 staminodes), (connate), (adnate to C), (anthers without pits); (pollen <30µm), aperture fastigiate; G [(2-4)] (inferior), (styluli +), stigmas ± punctate, wet, papillate; ovules pendulous, outer integument 3-5 cells across, inner integument 6-8 cells across, hypostase 0, funicular obturator +; fruit a flattened drupe, 1(-3, then often lobed) locular, (loculicidal capsule); 1 seed/loculus, (arillate); testa vascularized, only enlarged tanniniferous (divided) exotestal cells and remains of vascular bundles persist, exotegmen 0; embryo (orange), oily; n = (?10) 12, 1-2 µm long.

3[list]/165: Dichapetalum (130). Pantropical, few in Malesia (map: see Prance 1972b; Leenhouts 1957a; van Steenis 1963; Heywood 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006). [Photo - Flower, Photo - Fruit.]

Age. This node can be dated to (36-)20.7(-6.8) m.y. (Bell et al. 2010 - inc. Tap).

Evolution. Divergence & Distribution. Some analyses suggest that the diversification rate in Dichapetalaceae may have increased (Xi et al. 2012b).

Chemistry, Morphology, etc. Dichapetalum at least has fluoracetic and related acids in its seed oils and is often very poisonous as a result (e.g. Badami & Patil 1981; Lee et al. 2012); it also contains the cytotoxic dichapetalins, tetracyclic triterpenes (Long et al. 2013: also in Phyllanthus!). The petiole bundles are arcuate above the insertion of the inflorescence.

The flowers of Tapura in particular are quite complex (Prance 1972b). Some species of Dichapetalum are reported to have arils (Prance 2013).

Some information is taken from Prance (1972b, 2013); see also Hegnauer (1966, 1989) for chemistry, Barth (1896) for petiole anatomy, Punt (1975) for pollen morphology, and Boesewinkel and Bouman (1980) for ovule and seed.

Previous Relationships. Dichapetalaceae were placed in Celastrales by Cronquist (1981) and in Euphorbiales by Takhtajan (1997).

Synonymy: Chailletiaceae R. Brown

[Euphroniaceae + Chrysobalanaceae]: hypanthium +, nectary on inside; C clawed, with lignified hairs; embryo ?colour.

Age. The age of this node is around (74.9-)66.2(-60.3) m.y. (Xi et al. 2012b: Table S7), ca 86 m.y. (Bardon et al. 2012), ca 53.5 m.y. (Tank et al. 2015: table S2), or (56.8-)49.2(-42.3) m.y. (Bardon et al. 2016).

Chemistry, Morphology, etc. Whether or not this clade has a spur in the floral cup is a matter of perspective; I prefer to interpret the flower in many Chrysobalanaceae as having the gynoecium adnate to one side of the hypanthium rather than being spurred as may appear to be the case in a l.s. of the flower. Hairs have been found in the ovary loculi in flower, but they are not apparent in the capsule, even if it has not yet opened (pers. obs.).

EUPHRONIACEAE Marcano-Berti   Back to Malpighiales

Euphroniaceae

Tree; parenchyma ± aliform-confluent; petiole bundles annular or arcuate, (not joining immediately with stele); cortical and foliar sclereids +; hairs unicellular; hypodermis mucilaginous; leaves spiral, lamina with revolute vernation, white tomentose below; inflorescence terminal; bracteoles 0; C 3 [abaxial-lateral and abaxial C absent], contorted; stamens 4-7, in two groups, adnate to C, filaments basally connate, staminodes one long, abaxial-lateral, retrorsely pilose, between the stamen groups, and 4-5 small, appearing dentate; G with median carpel adaxial, stigma clavate; ovule apotropous; fruit a septicidal capsule, columella persisting; seeds winged, 1/carpel, coat?; endosperm development?; n = ?

1[list]/1-3. The Guyana Shield, South America (map: from Steyermark 1987).

Evolution. Divergence & Distribution. Some analyses suggest that the diversification rate in Euphroniaceae decreased (Xi et al. 2012b).

Chemistry, Morphology, etc. Lleras (1976) suggested that the (long) staminode of Euphronia was in the position of the fertile stamen of Vochysiaceae (that was a time when the two were thought to be related), Marcano-Berti (1995) that there is a staminal tube and four stamens of two different lengths. Prance and Sothers (2003) in a table comparing the four families note that Euphronia lacks a disc.

Some information is also taken from Warming (1875) and Kubitzki (2013b), both general, Barth (1896: general anatomy), and de Pernia and ter Welle (1995: wood anatomy), and some more data come from Euphronia guianensis: Colonnello-Medina 712, vegetative anatomy.

Ovule morphology, etc., of Euphronia is still very poorly known.

Previous Relationships. Euphronia has been included in Trigoniaceae (Airy Shaw 1966; Hutchinson 1973; Takhtajan 1997) or Vochysiaceae (Cronquist 1981; Lleras 1978, Mabberley 1997). However, Euphronia and Trigoniaceae differ in a number of features, including those of wood anatomy (see Lleras 1976 for a table) and other aspects of vegetative anatomy (e.g. Trigoniaceae lack the mucilaginous hypodermis of Euphronia: Sajo & Rudall 2002) and are not sister taxa.

CHRYSOBALANACEAE R. Brown, nom. cons.   Back to Malpighiales

Chrysobalanaceae

Trees or shrubs; trihydroxyflavonoids, distinctive unsaturated fatty acids in the seeds +, ellagic acid 0; trunk often with red exudate; (cork ± deep-seated); true tracheids +; wood siliceous, with SiO2 grains; parenchyma in apotracheal bands; nodes 5:5; petiole vasculature annular, often with medullary plates, etc., wing bundles +; branching from previous flush; (foliar sclereids +); leaves often two-ranked, lamina vernation (flat-)conduplicate, abaxial surface often with flat glands, esp. near base, (margins toothed), (stipules petiolar or intrapetiolar); inflorescence various; (flowers almost polysymmetric); (C 0); A (2-)5-many, usually long-exserted, abaxial members only/best developed, filaments (connate), (coiled in bud), (staminodes adaxial); tapetal cells 2-nucleate; pollen (4-colporate), angled in polar view; usu. only abaxial carpel developed, (loculus divided), (all three carpels fertile), often borne on side or top of tube, style ± gynobasic, stigma punctate to 3-lobed; ovules ± basal, erect, outer integument 5-12 cells across, inner integument 5-12 cells across, (micropyle not zig-zag); megaspore mother cells several, embryo sac lacking antipodals; fruit a 1-seeded drupe, medium-sized to large, (germination plus or lines), endocarp densely hairy (not); (seed ruminate), testa (multiplicative), vascularized, undistinguished or mesotestal, exotesta collapsed-fibrous, (tanniniferous), tegmen multiplicative; n = 10, 11; germination cryptocotylar, hypogeal.

18[list]/530: Licania (220), Hirtella (107), Couepia (70), Parinari (39). Pantropical, especially American (map: from van Balgooy 1993; Prance & Sothers 2003a, b; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006). [Photo - Flower.]

Age. The age of crown-group Chrysobalanaceae may be Palaeocene, around 59-58 m.y. (Bardon et al. 2012), rather older, some (74.9-)66.2(-60.3) m.y. (Xi et al. 2012b: Table S7, Atuna and the rest), or as young as (37.3-)33.4(-30.2) m.y. (Bardon et al. 2016).

Evolution. Divergence & Distribution. For the fossil record of Chrysobalanaceae, see Jud et al. (2016); modern genera had evolved and the family as a whole was widely distributed by the early Miocene.

Chrysobalanaceae are possibly Old World in origin, probably moving from the paleotropics to the neotropics whether by long distance dispersal or the North Atlantic land bridge, and most of the diversity in the family is in a neotropical clade whose arrival there is dated to ca 29.5 m.y.a., mid Oligocene, although most diversification within this clade is Miocene and younger (Jud et al. 2016; Bardon et al. 2016); the age of thecrown neotropical clade in Bardon et al. (2012) is (57-)47(-40) m. years. The net rate of diversification was overall higher in the neotropics than the palaeotropics, despite also having a higher extinction rate. The driver of all this is unclear, particularly since the family is found in lowland habitats and Africa has often been thought of as the area likely to have a higher extinction rate (Bardon et al. 2012).

Ecology & Physiology. Chrysobalanaceae are common in terms of both numbers of species and individuals with stems at least 10 cm d.b.h. in the Amazonian tree flora, but they do not have a disproportionally high number of common species (ter Steege et al. 2013).

Seed Dispersal. For seed dispersal, generally by animals, see Prance and Mori (1983).

Plant-Animal Interactions. For the association between Amazonian Hirtella species of section Myrmecophila and their obligate ant associates, Allomerus spp., see Rico-Gray and Oliveira (2007) and Ruiz-González et al. (2011); the ant cultivates an ascomycete fungus whose hyphae strengthen the ant galleries within which the ants lurk, coming out to ambush their prey. However, the ant domatia drop from older leaves of H. myrmecophila, otherwise A. octoarticulata would eat the inflorescences, effectively sterilizing the plant (Izzo & Vasconcelos 2002).

Chemistry, Morphology, etc. Chrysobalanaceae, rich in silica, contribute notably to the pool of phytoliths (Piperno 2006). Syllepsis is uncommon both here (Keller 1994), and probably more generally in the whole group of five families.

Cronquist (1981) suggested that the pollen grains might also be colpate.

For more information, see Prance (2013) and Prance and White (1988: nicely illustrated), both general, Hegnauer (1973, 1990: chemistry), Badami and Patil (1981: seed fatty acids), Morvillez (1918: petiole vasculature), Tobe and Raven (1984: embryology), and LaFrankie (2011: field characters).

Phylogeny. A recent molecular study (Yakandawala et al. 2010) yielded support for the monophyly of the genera but poor resolution of deeper relationships, and suggested that groupings apparent in earlier morphological "taximetric" studies (Prance et al. 1969; Prance & White 1988) should be reexamined; the situation remained largely unchanged in the study by Bardon et al. (2012), with practically no support for relationships along the backbone of the tree. Licania may be wildly para/polyphyletic, and Hirtella and Coupeia, especially the latter, are also not monophyletic (Sothers et al. 2014; for problems with the first two genera, see also Bardon et al. 2016). There is some support for Atuna being sister to the rest of the family, perhaps in a clade with one or two other taxa including Kostermanthus (Bardon et al. 2012; see also Wurdack & Davis 2009), although basal relationships were unclear in Sothers et al. (2014: Atuna not included), Maranthes and Parinari perhaps being near basal. Bardon et al. (2016) found the poorly-kmown Kostermanthus alone to be sister to the rest of the family

Classification. See Prance (1989: New World Taxa), and Prance and Sothers (2003a, b: world monograph), but genera are beginning to be reworked (Sothers et al. 2014: Coupeia).

Previous Relationships. The flowers of some Chrysobalanaceae look rather like those of Prunus, and Chrysobalanaceae and Rosaceae were often considered to be close (e.g. Cronquist 1981; Takhtajan 1997), either recognized as separate families but placed more or less adjacent in the sequence, or Chrysobalanaceae might even be included as a subfamily of Rosaceae. However, there are numerous differences between them (see table in Prance 1972a).

Synonymy: Hirtellaceae Horaninow, Licaniaceae Martynov

[[Humiriaceae [Achariaceae [[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]]]] [[Peraceae [Rafflesiaceae + Euphorbiaceae]] [[Phyllanthaceae + Picrodendraceae] [Ixonanthaceae + Linaceae]]]] / Clade 1 of Xi et al. (2012b): ?

Age. This node is estimated to be (111.8-)107.9(-104.5) m.y.o. (Xi et al. 2012b: table S7), 48.3 or 40.3 m.y.o. (Xue et al. 2012, only Salicaceae and Euphorbiaceae included), or (111.8-)107.9(-104.5) m.y.o. (Xi et al. 2012b: Table S7).

[Humiriaceae [Achariaceae [[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]]]]: endosperm persistent.

Age. This node is around (110-)10.7(-101.6) m.y.o. (Xi et al. 2012b: table S7) or some 105.8 m.y. (Tank et al. 2015: table S2).

HUMIRIACEAE A. Jussieu, nom. cons.   Back to Malpighiales

Humiriaceae

Trees; ellagic acid +; cork subepidermal; vessel elements solitary, with scalariform perforation plates; true tracheids +; vestured pits +; sieve tube plastids with protein crystals and starch; nodes 5-lacunar; petiole bundles annular, with wing bundles; rhombic calcium oxalate crystals +; mucilage cells frequent; stomata anomocytic (paracytic - Vantanea); branching from previous flush; leaves often two-ranked, lamina vernation involute, tooth ?type, (margins entire), petiole short, stipules small or 0; inflorescence cymose; K connate, at least at base, quincuncial, C (quincuncial/cochlear), (with 3 traces - Vantanea); A 10-30 (50< - Vantanea), filaments ± connate at least basally, with interdigitated hairs higher up, forming a tube, (obdiplostemonous), thecae with each sporangium dehiscing separately [Vantanea], or sporangia 4 or 2, separate, connective broad, prolonged; pollen exine usu. microreticulate; nectary from base of filaments to base of G, prominent, raised, annular; G [(4-7)], opposite sepals (petals - Humiria), style undivided, stigma capitate, ± lobed/radiate, ?type; ovules 1(-2 superposed)/loculus, (with 5 traces), epitropous, micropyle exo(endo)stomal, outer integument 2-3 cells across, inner integument 2-3 cells across, parietal tissue 3-6 cells across, nucellar cap +, endothelium 0; fruit a drupe, stone operculate, 1-3(-5)-seeded, surface sculpted, with "resin" cavities; exotestal cells thick-walled, lignified, tegmen multiplicative [ca 5 cells thick], cross layer of fibres beneath exotegmen; endosperm copious [?always], perisperm +, slight, embryo somewhat curved, green; n = 6.

8[list]/50: Vantanea (16), Humiriastrum (12). Tropical America, W. Africa (Saccoglottis, also American) (map: from Thorne 1973; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower, Fruit.]

Age. This node is estimated to be (32.1-)20.7(-10.4) m.y.o. (Xi et al. 2012b: table S7).

Evolution. Divergence & Distribution. Herrera et al. (2010, see also 2014a) rejected all fossils placed in this family other than some from South America, and they suggested that Humiriaceae originated there.

If the family phylogeny is confirmed (see below), the family characterization above will change considerably; Vantanea in particular is very distinctive morphologically.

Seed Dispersal. The fruits are dispersed by bats or by water, empty cavities in the stone affording bouyancy.

Chemistry, Morphology, etc. Although D. A. Link is sometimes cited as the author of a paper on the nectaries of Humiriaceae, and he promised such a paper himself, it seems never to have appeared. Some species of Saccoglottis have stamens each with 3 anthers opposite the sepals (Herrera et al. 2010).

Some information is taken from Herrera et al. (2010) and Kubitzki (2013b), both general, Mauritzon (1934d: ovules), Herrera et al. (2014a: summary of what is known about wood anatomy), Narayana and Rao (1977 and references: floral morphology), Boesewinkel (1985a: ovule and seed), Bove and Melhem (2000: pollen).

Phylogeny. Morphological phylogenetic analyses suggested that Vantanea was sister to the other Humiriaceae; it has many stamens in three or more whorls (Bove 1997). Herrera et al. (2010: more detailed morphological analysis of 40 characters) suggested that Vantanea and Humiria were successively sister to the remainder of the family, although support for this topology was weak; the [Humiria + the rest] clade had quincuncial corollas and 30 or fewer stamens with unilocular anthers, the stones often had "resin" cavities, etc.. Schizostemon was sister to the other three genera (including Vantanea) in a molecular analysis, but support was weak (Xi et al. 2012b).

Previous Relationships. Bove (1997) suggested that Ixonanthaceae were sister to Humiriaceae, both having ellagic acid, a "free" annular nectary encircling the ovary, and an undivided style with an entire stigma. Humiriaceae have also been linked with Linaceae and Erythroxylaceae, and thence to Geraniales (Narayana & Rao 1978b), or the three families together are placed in Linales (Cronquist 1981).

[Achariaceae [[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]]] / parietal clade: crystals in ray cells; sieve tubes with non-dispersive protein bodies; cuticle waxes usu. 0; (foliar glands +); pedicels articulated; nectary outside A; G with median member abaxial, placentation intrusive parietal; ovules several/carpel, nucellus massive; seeds arillate; endotegmen persistent; endosperm oily.

Age. This node has been dated to (72-)69, 65(-62) m.y. (Wikström et al. 2001), ca 99.2 m.y. (Tank et al. 2015: table S2), (114-)108(-104) m.y. (Davis et al. 2005a: note topology), (89-)81, 79(-74) m.y. (Bell et al. 2011: Ixonanthes also included!), and (104.6-)99.2(-93.1) m.y. (Xi et al. 2012b: Table S7).

Evolution. Divergence & Distribution. All six major clades in this group (Malesherbiaceae + Turneraceae + Passifloraceae = Passifloraceae s.l., a single clade) may have diverged in the Cretaceous-Albian 111-100 m.y.a., or a little later (Davis et al. 2005a, details are given for the individual clades), but ages are somewhat younger in Xi et al. (2012b). At the other extreme, Wikström et al. (2001) suggested that many of the clades do not diverge until (well) after 63 m.y. ago.

Plant-Animal Interactions. Larvae of butterflies such as Nymphalidae-Acraeinae and N.-Nymphalinae-Heliconiini, -Vagrantini and -Argynnini commonly eat members of this group (Ehrlich & Raven 1964; see also Arbo 2006; Simonsen 2006; Silva-Brandão et al. 2008; Nylin & Wahlberg 2008; etc.); this is also discussed under the individual families below. Some Acraeinae in particular may cue on the presence of the cyanogenic glucoside gynocardin in potential food plants, indeed, that larvae of Acraea horta, which normally ate leaves of the woody Kiggelaria africana, also ate herbaceous Achariaceae, prompted the successful search for that compound in the latter family (Steyn et al. 2002). Toxic compounds like gynocardin may be sequestered by the larva and passed on to the adult. Interestingly, given the relationships evident in Wurdack and Davis (2008), the distinctive cyclopentenoid glycosides may have to have evolved more than once, and or been lost.

Phylogeny. For relationships in this clade (= the parietal clade), which has strong support, see Xi et al. (2012b).

Chemistry, Morphology, etc. For cyclopentenoid cyanogenic glycosides, see e.g. Spencer and Seigler (1984, 1985b) and Spencer et al. (1984) and references. There is much information on seed anatomy in Takhtajan (1992) while Krosnick et al. (2006) briefly discuss the evolution of polyandry in this group - in some cases, at least, the numerous stamens form a single whorl. See Mauritzon (1936b) for some information on embryology and Furness (2011) for pollen development and ultrastructure.

Previous Relationships. It was commonly agreed that the old Flacourtiaceae presented major taxonomic problems. "Flacourtiaceae as a family is only a fiction; only the tribes are homogeneous" (Hermann Sleumer, a monographer of the family, in Miller 1975: p. 79) - it was indeed a fiction. Some of the old Flacourtiaceae are now in Achariaceae, a few in Lacistemataceae, while Flacourtiaceae-Berberidopsideae are in Berberidopsidales-Berberidopsidaceae and Aphloia is in Crossosomatales-Aphloiaceae. The name Flacourtiaceae is now no longer in use, and the remainder of this family is included in Salicaceae. Variation in chemistry, leaf teeth, floral morphology, and seed coat anatomy is largely correlated with this division.

When parietal placentation was considered to be a very important characters, other families with parietal placentation such as Caricaceae (Brassicales), Cucurbitaceae (Cucurbitales), etc., might also be grouped here - as the Parietales.

ACHARIACEAE Harms, nom. cons.   Back to Malpighiales

Achariaceae

Shrubs to trees; cyclopentenoid cyanogenic glucosides and/or cyclopentenyl fatty acids [gynocardin; tetraphyllin rare], ellagic acid [Kiggelaria] +; vessel elements with simple or scalariform perforation plates; fibres septate; axial parenchyma usu. 0; ray cells with scalariform perforations [?distribution]; petiole bundle annular, with two wing/adaxial strands, (inverted medullary plate - Lindackeria); ?stomata; leaves spiral or two-ranked, lamina margins entire (serrate), (stipules 0), petiole often geniculate; (plant dioecious); inflorescence spicate or cymose (fasciculate), (epiphyllous); K and C not in a simple alternating relationship, spiral or not, K 2-5, C 4-15 (3-4, connate - Acharieae), often in two series, (adaxial scales +); (nectary 0); A 5-many, opposite petals or irregularly inserted, initiation centripetal or simultaneous, (from a ring meristem), anthers basifixed, elongate (barely so - Chiangodendron), (dehiscing by pores), (locellate); pollen also tricolporoidate; G [2-10], median member?, style (short), branched or not, stigma capitate-peltate to punctate; ovules sessile [attachment to placenta broad], (1/carpel), (straight - Xylotheca, Hydnocarpus, Lindackeria, Scaphocalyx), micropyle endo- or bistomal or zigzag, outer integument 3-7 cell layers across, (lobed), inner integument 3-8 cell layers across, parietal tissue 4+ cells across, nucellar cap +, epistase +, ring/cap of tracheids in chalaza, funicle 0; (megaspore mother cells 2), embryo sac penetrating chalaza, forming a caecum below tracheids; fruit also a berry; (seed arillate); seed coat thick, vascularized [pachychalazal], testa multiplicative, (with crossing layers in middle - Pangium), (mesotesta with sclerenchyma, palisade layer, and sclereids - Scaphocalyx), endotesta lignified, cells sclereidal (radially elongated), tegmen multiplicative, exotegmic cells elongated, massive, sclereidal; endosperm copious, suspensor 0, embryo chlorophyllous; n = 10, 12, 23.

30[list]/145: Hydnocarpus (40). Pantropical. (map: from Sleumer 1954, 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. China 13. 2007; Khan et al. (2014); Serban Procheŝ, pers. comm. [Africa]; Andrew Ford, pers. comm. [Australia]). [Photos - Flower, Fruit, Fruit, Acharia tragodes - Leaves.]

Age. Check node. This node has been dated at (71-)59, 58(-44) m.y. (Bell et al. 2011: Ixonanthes also included!), (60-)57, 54(-51) m.y.a. (Wikström et al. 2001), and (86.2-)65(-48.2) m.y. (Xi et al. 2012b: Table S7, Hyd. Pang. Ach.).

[Acharieae + Pangieae]: ?

Age. This node has been dated to around (33-)23, 22(-12) m.y.o. (Bell et al. 2011).

1. Acharieae Bentham & J. D. Hooker

More or less herbaceous and viny; leaves palmately lobed (not Guthriea), stipules 0; flowers imperfect; C connate; antipetalous glands +; staminate flowers: A opposite K, anthers with swollen hairs, connective broad; pistillode 0; carpellate flowers: staminodes 0; style lobed; micropyle zig-zag; (embryo sac bisporic, [chalazal dyad], eight-celled [Allium-type]; fruit a capsule; seeds with pits or tubercules, sarcotestal and with stomata, testa not vascularized, exotegmen fibrous; n = ca 10.

2. Pangieae Clos

?

Evolution. Plant-Animal Interactions. The feeding behaviour of Acraeini butterfly larvae are consistent with the family limits adopted here (van Wyk in Dahlgren & van Wyk 1988; Steyn et al. 2002a, 2003 and references). Species of Ryparosa consistently produce glycogen-containing food bodies, and in a number there are associations of varying closeness with ants (Webber et al. 2007).

Chemistry, Morphology, etc. There are large and medium intervascular pits; the wood also has solitary pores and lacks tracheids (Miller 1975). Lindackeria has superficial cork cambium. Pollen variation is considerable (Wendt 1988), as is that in ovule development and seed coat anatomy (Dathan & Singh 1979; van Heel 1973, 1974, 1977, 1979; Steyn et al. 2002a, b, 2003).

Information is taken from Hegnauer (1966, 1989), chemistry, Datahan and Singh (1979: embryology), Endress and Voser (1975: floral development of Caloncoba), Lemke (1988), Gavrilova (1998: pollen), and Groppo et al. (2010: general); see also Judd (1997a), Van Wyk in Dahlgren and Van Wyk (1988: Acharieae) and especially Chase et al. (2002). Bernhard and Endress (1999) discuss androecial initiation. Much of the old literature is under Flacourtiaceae!

Phylogeny. For the circumscription of Achariaceae, see Chase et al. (2002) and Sosa et al. (2003): It includes Acharieae, Erythrospermeae (Erythrospermum - fibrous exotegmen), Pangieae (inc. Kiggelarieae), and Lindackerieae (Oncobeae minus Oncoba). The family is divided into three strongly-supported clades, [Hydnocarpus [Erythrospermeae + Lindackerieae]] [Pangieae, Acharieae, Ryparosa, etc.]], and support for monophyly of the family as a whole is strong, although Sosa et al. (2003) did not find much support for the last clade; Groppo et al. (2010) questioned some tribal limits in the family.

Classification. I have not followed the classification in Chase et al. (2002) since the four tribes recognised there do not map (in terms of monophyly) on to the tree.

Previous Relationships. The bulk of Achariaceae had almost universally been included in Flacourtiaceae s.l. until recently (e.g. Cronquist 1981; Takhtajan 1997).

Botanical Trivia. Immature fruits of Australian Ryparosa have the highest concentrations of cyanogenic glucosides known - 12 mg g-1 dry weight (Webber & Woodrow 2004).

Thanks. I thank Sue Zmarzty for comments.

Synonymy: Erythrospermaceae Doweld, Kiggelariaceae Link, nom. inval., Pangiaceae Hasskarl

[[Goupiaceae + Violaceae] [Passifloraceae [Lacistemataceae + Salicaceae]]]: stamens = and opposite sepals; G [3]; exotegmen of ± cuboidal cells.

Age. The age of this node is (69-)66, 63(-60) m.y. (Wikström et al. 2001: Goupiaceae sister to rest), (86-)79, 76(-71) m.y. (Bell et al. 2011: Goupiaceae not included), or (102.9-)97.1(-90.6) m.y. (Xi et al. 2012b: Table S7).

[Goupiaceae + Violaceae]: petiole with ± annular and wing bundles; cuticle waxes 0; connective ± developed apically; stigma proper ± punctate, receptive area small, appearing recessed/hollow.

Age. This node has been dated to (100.8-)92(-81.9) m.y.o. (Xi et al. 2012b: table S7) or around 96.2 m.y. (Tank et al. 2015: table S1, S2).

GOUPIACEAE Miers   Back to Malpighiales

Goupiaceae

Trees; plants Al-accumulators, ?chemistry otherwise; vascular cylinder and pith 4-5-angled; vessel elements with scalariform perforation plates; petiole with inverted medullary bundle; branched sclereids +/0; hairs thick-walled, with pitted bases; orthotropic axes lacking expanded leaves; leaves two-ranked, lamina tooth ?type, secondary veins actinodromous, 3ary veins scalariform; inflorescences umbellate, axillary, pedicel articulation?; C induplicate-valvate, long, apical part narrow, differentiated; nectary annular; connective stout, shortly prolonged, with long hairs; pollen with endexinal folds; G [5], opposite petals, placentation basal-axile, styluli short, adaxially channeled, on outer shoulders of carpels [ovary with roof], stigma type?; ovules few/carpel, ?morphology; fruit a berry; seeds not arillate, testa reticulate, both it and tegmen ca 3 cells across, exotegmen ridged, with 1 layer of ± laterally flattened sclereids, wall thickenings U-shaped; endosperm copious; n = ?

1[list]/2. Central and N. South America (map: from Tropicos xii.2010).

Evolution. Divergence & Distribution. Diversification in the Goupiaceae clade seems to have slowed down (Xi et al. 2012b).

Ecology & Physiology. Goupia glabra is a common and sometimes abundant member of the Amazonian tree flora, where it ranks #7 in terms of above-ground biomass and #10 in productivity (ter Steege et al. 2013; Fauset et al. 2015).

Chemistry, Morphology, etc. Kubitzki (2013b) thought that the node was unilacunar, but Hoyos-Gómez (2015) found that it was trilacunar, the lateral traces departing from the central stele well before the central trace. It is often suggested that only seedlings have dentate leaves, those of the adult being entire, but leaves of flowering specimens are frequently toothed.

If Takhtajan (2000) is correct in that there is a lignified endocarp, the fruit is technically a drupe.

For general information, inc. anatomy, see Hoyos-Gómez (2015) and Kubitzki (2013b); information on wood anatomy is taken from den Hartog and Baas (1978) and on pollen from Lobreau-Callen (1977, 1980) and Furness (2011).

The family is poorly known, especially embryologically.

Previous Relationships. Cronquist (1981) included Goupiaceae in Celastraceae, Takhtajan (1997) in Celastrales, A.-L. de Jussieu and others have placed it in Rhamnaceae. Furness (2011: pollen size) suggested that Goupiaceae were closest to the Lacistemataceae-Salicaceae clade.

VIOLACEAE Batsch, nom. cons.   Back to Malpighiales

Trees; vessel elements long to short with simple or long-scalariform perforation plates; petiole bundles arcuate; leaf teeth with a deciduous apex [Salicoid - ?level]; pedicels articulated; flowers weakly monosymmetric; K quincuncial; A with connective forming apical scales; K persistent in fruit; exotesta subpalisade to tabular, ± thickened, (mesotesta sclerenchymatous), endotesta usu. crystalliferous; exotegmen cells tracheidal, lignified, thickened on all walls.

34[list]/985. World-wide.

Age. This node is around (86.8-)72.9(-57.4) m.y.o. (Xi et al. 2012b: table S7).

Fusispermoideae

1. Fusispermoideae Hekking

Pith with thin-walled cells; nodes 5:5; petiole with an elliptical medullary bundle, phloem internal; ?stomata; C contorted; nectary annular, fleshy, 5-lobed, lobes alternating with A, filaments ± adnate to inner surface at indentations; anther thecae cordate/trapezoid, confluent apically?, connective as short paired fringed apical scales; capsule ca 3 mm long; seeds elongated, longitudinally winged, aril 0, ?exotegmen only moderately developed, of somewhat elongated cells; n = ?

1/3. Costa Rica, Panama, Columbia, Peru (Amazonas) (map: from S. Hoyos-Gómez, pers. comm.).

2. Violoideae Beilschmied

Violoideae

Nectary opposite A; connective lobed, as long as and broader than anther, ± free, margin entire or erose; (capsule with explosive dehiscence).

2A. ex Rinorea

Vessel elements?; nectary as thick semicircular lobes at base of A; anther connective subapical, thecae visible from abaxial side; style broadening subapically; ovule 1/carpel; n = ?

1/3. Costa Rica to Peru.

2B. The Rest.

(Annual to perennial herbs; lianes); plants often Al accumulators; cyclotide proteins +, tannins 0 [woody members?]; calcium oxalate often as crystals; (petiole bundles arcuate); stomata also para- or anisocytic; leaves spiral or two-ranked (opposite), lamina margins involute, colleters +, (stipules petiolar; lobed); flowers often strongly monosymmetric, (papilionoid); C quincuncial, abaxial C spurred or not; A (3), basally connate or not, nectariferous appendage on abaxial surface of filaments (on 2 abaxial A only), (filaments connate), anthers connivent, thecae (horizontal), obscured by connective from abaxial side, (connective ± 0); G [(2-5)], (when 5 opposite K), styles separate or style +, straight or curved, apex subcapitate, asymmetric or not, (stigma hollow); ovule (1/carpel), with zig-zag micropyle (endostomal), outer integument 2-4 cells across, inner integument ca 3 cells across, parietal tissue 2-3 cells across, nucellar cap ca 2 cells across, hypostase +; (fruit a berry, nut); seeds (winged), (not arillate/carunculate), (exotesta ± thick-walled, lamellate), (mesotesta sclerenchymatous), endotesta crystalliferous (not - Ionidium), (exo)tegmic fibre layer 1-3 cells across, endotegmen thick-walled, not lignified or elongated; embryo (small), green [Viola], cotyledons accumbent (oblique); n = (5-)6(7)8(-13+).

22-32/980: Viola (525), Rinorea (?230-250), Hybanthus (?120), Pombalia (42), Afrohybanthus (25+). World-wide; woody taxa esp. in the lowland tropics, especially the neotropics (map: from Hultén 1958, 1971; Hultén & Fries 1986; Hekking 1988; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Australia's Virtual Herbarium i.2013 - incomplete for South America). [Photo - Leonia, Alexis fruit and flowers, Viola.]

Synonymy: Alsodeiaceae J. Agardh, Leoniaceae A. L. de Candolle

Evolution. Divergence & Distribution. Marcussen et al. (2012, especially 2014) disentangle the complex reticulate history of the polyploid northern hemisphere species of Viola where reticulations as old as ca 29 m.y.a. have been detected; there have been 16-20 or more major alloplyploidization events. There is a radiation of Viola on Hawaii; these are also polyploids and include woody species, and their ancestry is to be sought in west North American species (Marcussen et al. 2012). The genus may have had its origin in Andean South America (Ballard et al. 1998), where the large section Andinum, perhaps one fifth of the genus and including some remarkable rosette- and tussock-forming species, is found along the Andes.

Van Velzen et al. (2015) optimized the evolution of a number of characters for African Rinorea.

Ecology & Physiology. Violaceae are notably common in terms of both numbers of species and individuals with stems at least 10 cm across in the Amazonian tree flora, and they are disproportionally common in the 227 species that make up half the stems in Amazonian forests (ter Steege et al. 2013). Rinorea is common and can dominate in the lower strata of African forests, and several species may grow together (van Velzen et al. 2015).

Metal hyperaccumulators are quite common in the family, and include both herbaceous and woody members (Brooks 1998 for a summary).

Pollination Biology & Seed Dispersal. Cleistogamy is widespread in Viola.

The largely temperate Viola is myrmecochorous (Lengyel et al. 2010), and myrmecochory, as well as dispersal by larger animals and by wind, also occurs in more tropical taxa.

Plant-Animal Interactions. Violaceae are the preferred food plants for the caterpillars of the majority of fritillaries, Nymphalidae-Argynnini (Simonsen 2006; Nylin et al. 2014). In Africa, perhaps half the species of Cymothoë (ca 75 spp., Nymphalidae-Limenitidinae) occur on Rinorea, Salicaceae and Kiggelariaceae also being reported as hosts; although individual species of butterfly and plant may be closely associated, the current geography of the two may differ from that in the past (McBride et al. 2009).

Genes & Genomes. Viola tricolor, the pansy, and the related V. arvensis were important subjects of early studies of genetics and speciation.

Chemistry, Morphology, etc. Inulin has been reported from Hybanthus (Beauvisage 1889); for cyclotides, widely distributed in the family, see Burman et al. (2010). From the description of the root of Ionidium (= Hybanthus) ipecacuanha by Beauvisage (1889), the cork cambium may be mid-cortical or superficial. Viola has storied cambium.

For information on the flowers of Fusispermum, see Cuatrecasas (1950) and Hekking (1984), the former describes the scales as being ventral appendages of the connective. Feng and Ballard (2005) suggested that even those Violaceae with polysymmetric adult flowers were monosymmetric earlier in development, so "flowers monosymmetric, at least in bud" may be an apomorphy for all/most of the family (see also Arnal 1946 for monosymmetry). The anthers and stigmas of many species are very complex (e.g. Kuta et al. 2012: Viola). In Anchietea and Decorsella the seeds mature exposed on the open carpels.

For general information, see Munzinger and Ballard (2003), Hoyos-Gómez (2015: basal pectinations) and Ballard et al. (2013). An unpublished thesis by Feng (2005) includes a phylogeny of the family and details of the floral development of seven genera. For chemistry, see Hegnauer (1970, 1990), for growth and branching patterns, see Hekking (1988), for seed anatomy, etc., see Singh (1963), Singh and Gupta (1967), and Dathan and Singh (1974), for embryology, etc., see Singh (1970), for pollen morphology, see Mark et al. (2012: pollen of Fusispermum has two size classes); see also Leins and Erbar (2010: flowers of Viola).

Phylogeny. There is good support for the relationships [Fusispermum [Rinorea apiculata group [Rinorea s. str. [[Viola etc.], [Leonia, etc.], [Melicytus, etc.]]]]] (Tokuoka 2008, see also Feng & Ballard 2005; Ballard et al. 2009; Wahlert & Ballard 2012; esp. Wahlert et al. 2014). The para-/polyphyly of Rinorea is well established, but some major polytomies make it difficult to clarify details of relationships much further. Viola is included in a well-supported clade the other members of which are woody and also have strongly monosymmetric flowers - with the exception of most species of Allexis, which is is sister to the rest of that clade; other taxa with strongly monosymmetric flowers are not immediately related (Wahlert et al. 2014). Hybanthus pops up all over the place in both the Leonia (the type of Hybanthus is there) and Melicytus, but unfortunately relationships in the latter clade are not well understood (Wahlert et al. 2014).

Bakker et al. (2006b), Wahlert and Ballard (2012) and in particular van Velzen et al. (2015) discuss relationships in the speciose African Rinorea, where the clade [R. ?exappendiculata + R. woermanniana] may be sister to the rest of the genus.

Classification. The current infrafamilial classification is insupportable, the large genus Hybanthus is to be cut up into nine genera, perhaps, and Rinorea is also to be divided. Ballard et al. (2013), Wahlert et al. (2014) and Flicker and Ballard (2015) have begun the process of dismemberment.

[Passifloraceae [Lacistemataceae + Salicaceae]] / salicoids: ?

Age. The age of this node may be around (66-)63, 60(57) m.y. (Wikström et al. 2001: Hymenanthera included), (100.5-)94.4(-87.5) m.y.o. (Xi et al. 2012b: table S7), or ca 98.8 m.y. (Tank et al. 2015: table S2).

Phylogeny. This clade has strong support in the analysis of Xi et al. (2012b).

PASSIFLORACEAE Roussel, nom. cons.   Back to Malpighiales

Cyclopentenoid cyanogenic glycosides and/or cyclopentenyl fatty acids + [esp. tetraphyllin], cyanogenic glycosides derived from valine and isoleucine +; (plant with unpleasant smell); (colleters +); leaves spiral, (foliar glands +); K + C forming a tube, corona or scales towards mouth of tube (0); styluli +; exotestal cells in vertical lines, endotestal cells massive, exotegmen sclereidal oblique-palisade, endotegmen persistent; endosperm persistent, oily; x = 7; biparental or paternal transmission of plastids, atpF intron lost.

27[list]/975. Tropical, esp. America and Africa, also warm temperate - 3 subfamilies below.

Age. This node has been dated to around (38-)36, 32(-30) m.y. (Wikström et al. 2001: [M + T] P]), (59-)47, 43(-32) m.y. (Bell et al. 2011: [T [M + P]]), and (80.3-)62.8(-47.7) m.y.o. (Xi et al. 2012b: table S7).

1. Malesherbioideae Burnett

Malesherbioideae

Herbaceous or subwoody; hairs conspicuous, multiseriate, often glandular; plant with unpleasant smell; tannins?; (cork cortical); vessel elements usu. with simple perforation plates; nodes also 1:1; lamina often deeply lobed, (margins entire), (stipules foliaceous or 0); K + C tube long, K valvate, ± petal-like, C valvate; androgynophore +; nectary at base; (G [4]), gynophore +, styles slender, stigmas capitate-clavate, ?type; ovule with large protrusion at chalazal end, micropyle endostomal; K + C tube persistent; seeds pitted, aril 0; endosperm type?

1/24. South America from Peru southwards, esp. N. Chile (map: see Gengler-Novak 2002). [Photo - Habit]

Synonymy: Malesherbiaceae D. Don, nom. cons.

[Turneroideae + Passifloroideae]: extrafloral nectaries + [often on stipules/petiole/base of lamina]; lamina vernation conduplicate; anthers long; tapetum amoeboid; aril ± raphal.

Age. This node has been dated to (66.8-)50(-35.5) m.y.o. (Xi et al. 2012b: table S7).

2. Turneroideae Eaton

Turneroideae

Herbaceous or woody; plant with unpleasant smell; ellagic acid 0; cortical vascular bundles [= leaf traces] common; vessel elements with simple (and scalariform) perforation plates; stomata various; hairs tufted/stellate; stipules 0 (+ - e.g. Erblichia); bracteoles often large; (flowers heterostylous),; (hypanthium +); glands or corona at mouth of K + C tube (0), C contorted, deliquescent; nectary near base of tube (on sepals; filaments); (G [2]), (half inferior), stigmas concave, often ± penicillate; (ovule 1/gynoecium, basal - Stapfiella), micropyle zig-zag, outer integument ca 2 cells across, inner integument 3(-4) cells across, (nucellar cap ca 2 cells across), parietal tissue 2-5 cells across, suprachalazal zone massive, hypostase +/0; K + C tube deciduous; aril (fimbriate); exostome persistent, testa with stomata; n also = 5 (13).

12/227: Turnera (143), Piriquetia (44). Tropical to warm temperate America and Africa (inc. Madagascar and Rodriguez I.) (map: from Wickens 1976; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Heywood 2007, in part; Arbo 2008; Thulin et al. 2012a - T. ulmifolia widely naturalized). [Photo - Flower.]

Age. Crown-group Turneroideae are dated to (42.5-)32.3(-42.5) m.y. (Thulin et al. 2012b) or (40.3-)27.8(-14.6) m.y. (Xi et al. 2012b: table S7).

Thanks. To M. M. Arbo for species numbers, etc..

Synonymy: Piriquetaceae Martynov, Turneraceae Candolle, nom. cons.

3. Passifloroideae Burnett

Woody; (lamina margins entire); flowers (3-)5-merous; K ± petal-like, corona of (1-)2-several rows of filaments or membranes (0), nectary ± on K + C tube; androgynophore +; (A basally connate), anthers versatile; G [(2-)3(-7)], stigma/s capitate; seeds flattened, surface not smooth, bony; exotesta cells not in lines; endosperm ruminate.

16/705. Tropics to warm temperate, especially Africa and America - two tribes below.

Age. Crown-group Passifloroideae have been dated to around (29-)27, 26(-24) m.y. (Wikström et al. 2001) and (42.6-)26.6(-11.6) m.y. (Xi et al. 2012b: table S7).

3A. Passifloreae de Candolle

Passifloroideae

Vines or lianes, climbing by simple branch tendrils; cyclopentenoid cyanogenic glycosides diverse, flavonols +, ellagic acid +/0, tannins 0; anomalous secondary thickening quite common; vessel elements with simple perforation plates; wood often fluorescing; supernumerary buds +; leaves (compound), lamina vernation conduplicate, (margins entire), secondary veins often palmate, glands common on petiole or on lamina surface; (plant dioecious), inflorescence cymose; (flowers monosymmetric); C (0, 1), corona of (1-)2-several rows of filaments or membranes (0), nectary ± on K/C tube, (A basally connate); tapetal cells binucleate; pollen to 12-colporate; (G [4]), (gynophore [and androgynophore] +), (stigmas divided - Adenia), with multicellular papillae; ovules with bistomal micropyle, zig-zag or not, outer integument 2-5 cells across, inner integument 3-5 cells across, parietal tissue 6-20 cells across, (nucellar cap ca 2 cells across), nucellus protrudes through micropyle, hypostase +, funicle often long; fruit a berry, (capsule - Passiflora section Xerogona); seeds hairy or not, often sculpted; testa multiplicative, sarcoexotestal, or exotesta palisade, endotesta crystalliferous, lignified or not; cotyledons accumbent; n = 6 (7) 9(-12); rpl22 gene transferred from chloroplast to nucleus [Passiflora].

10/715: Passiflora (565), Adenia (100). Tropics to warm temperate, especially Africa and America (map: from van Balgooy 1975; Fl. Austral. vol. 8. 1982; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Collection]

3B. Paropsieae de Candolle

Paropsieae

Trees or shrubs; vessel elements in multiples, with scalariform perforation plates; leaves reduced [orthotropic axes], two-ranked [plagiotropic axes], lamina with glands especially on margin and apex, (stipules 0); inflorescence racemose; androgynophore +; (A-30, partly connate); (pollen 6-porate); nectary 0 (annular); gynophore + (0); (style single - Barteria); (fruit dry, indehiscent); seeds scrobiculate; n = ?

6/ca 22: Paropsia 12. Tropical, esp. West Africa (map: from Sleumer 1970; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; de Vos & Breteler 2009).

Synonymy: Modeccaceae Horaninow, Paropsiaceae Dumortier, Smeathmanniaceae Perleb

Evolution. Divergence & Distribution. The rate of diversification may have increased in Passifloroideae or the [Turneroideae + Passifloroideae] clade (Xi et al. 2012b); Weber and Agrawal (2014) suggested that the evolution of extra-floral nectaries in Turnera was associated with an increase in diversification rates, while extrafloral nectaries may be a key innovation in Passiflora (Krosnick et al. 2011: see also below).

Thulin et al. (2012b) suggest that Mathurina, the only Turneroideae with wind-dispersed seeds, is older than Rodrigues Island, to which it is now restricted. The majority of genera of Turneroideae are African, but include only a few species; most species are New World, most in Turnera itself, and there are three or so links across the South Atlantic; biogeographical relationships, which can be summarized as [[New World -> movement to Old World] [New World (1 species) + Old World]], were obscured by the pre-2012 taxonomy (Thulin et al. 2012b).

For androgynophore evolution, see Tokuoka (2012).

Ecology & Physiology. About 625 species of Passifloroideae are vines/lianes of one sort or another (estimate derived from Feuillet & McDougal 2007; see also references in Schnitzer et al. 2015). For the considerable anatomical variation in Adenia as well as variation in life form - many species have more or less grotesquely swollen stem bases - see Hearn (2006, 2009a). Hearn (2009b) suggested that where vascular strands and associated parenchymatous storage tissue in root and/or stem developed varied in the plant, hence helping to generate the diversity of growth forms in the genus, and emphasized that transport, support, and storage functions in the plants were semi-independent, perhaps facilitating evolutionary change (Hearn 2013). Leaf morphology also varies considerably in Adenia

Pollination Biology & Seed Dispersal. A complex corona (with a similarly complex terminology) is partcularly conspicuous in Passiflora, and it is variously involved in nectary protection and presentation, tube formation, etc., and a more or less well developed K/C tube with some kind of corona is common in Passifloraceae as a whole. For the pollination of some 37 species of Andean Passiflora supersection Tacsonia by the long-billed hummingbird Ensifera ensifera, see Abrahamczyk et al. (2014: many support values low); the Tacsonia clade is dated to ca 8.4 m.y.a., Ensifera to about a million years more. Sazima and Sazima (1978) note that the bat-pollinated flowers of Passiflora mucronata become zygomorphic as the stamens move after the flowers opens (see also Endress and Matthews 2006a).

Floral mimicry between Turnera and Malvaceae in Argentina has been suggested (Benitez-Vieyra et al. 2007). Heterostyly is common in Turnera, Piriqueta and some other Turneroideae.

Myrmecochory occurs in Turnera (Lengyel et al. 2010), but numerous species of ants playing a variety of roles may be associated with species such as T. ulmifolia (Rico-Gray & Oliveira 2007 and references); wind dispersal may occur when the aril is fimbriate (Arbo et al. 2015).

Plant-Animal Interactions. The cyclopentenoid glycosides common in Passifloraceae may be sequestered by caterpillars feeding on the plants and perhaps used in defence and/or even as nitrogen sources; Achariaceae also have such glycosides.

Caterpillars of Heliconius butterflies (Nymphalidae) use Passiflora and its relatives as their main food (Fordyce 2010 for references and diversification rates). The plants show great variation in leaf morphology and foliar glands. Some of the glands are egg mimics (Vanderplank 2007 for references) and/or are epithelial extrafloral nectaries and may attract ants that defend the plants (Krosnick et al. 2011 for a summary). Butterflies lay eggs on plants that lack eggs, hence the egg mimicry. Heliconiine butterflies may have diversified on the foothills and lower slopes of the eastern Andes from Peru northwards (Rosser et al. 2012). Heliconius butterflies themselves are also closely associated with Psiguria (Cucurbitaceae) and relatives, and perhaps some other plants, which they pollinate; unusually, the pollen is a source of nutrients for the butterfly.

The larvae of some Acraeinae, also nymphalids, and also of brightly-coloured Notodontidae-Dioptininae (moths) are also often found on Passiflora (Miller 1992; Silva-Brandão et al. 2008), and at least the former are also found on Barteria. Turneroideae are the hosts of caterpillars of several genera of Nymphalidae, alternate hosts include Salicaceae, Passifloroideae, and Violaceae (Arbo 2006 and references).

Details of the association between the African ant-plant Bartera fistulosa and the ant Tetraponera aethiops are given by Dejean et al. (2008). The evolution of this association, which involves all four species of Barteria and both specialist and generalist species of ants, is complex (Peccoud et al. 2012), and it is ascomycete fungi inhabiting the domatia that are an immediate source of nitrogen for the ant (Blatrix et al. 2012).

Genes & Genomes. For the PEP subunit α rpoA gene in Passiflora, see Blazier et al. (2016).

Species of Turneroideae have biparental or paternal transmission of plastids, as may also species of Passifloroideae (Shore et al. 1994).

Chemistry, Morphology, etc. Cyanogenic glycosides in this family are diverse and have a variety of precursors, both protein and non-protein amino acids (Miller et al. 2006 for references). See also Spencer and Seigler (1985a: Malesherbioideae), Spencer et al. (1985: Turneroideae) and Spencer and Seigler (1984, 1987, and references: Passifloreae).

Do the sieve tubes have non-dispersive protein bodies? Anatomically, the old Flacourtiaceae-Paropsieae (Barteria, Paropsia, etc.) and Passifloreae (Chase et al. 2002) are rather similar, indeed, the major variation in Passifloroideae seems to be associated with habit - lianes versus trees (Ayensu & Stern 1964). Passiflora and its immediate relatives have stem collenchyma, cymose inflorescences, and branches developing from an accessory (superposed) bud; accessory buds are common in taxa that have axillary tendrils with non-basal prophyllar buds. In Passifloreae these prophyllar buds may produce additional tendrils, hence branched tendrils, or flowers. There is debate as to whether the tendril is the pedicel of a terminal flower or the ?axial terminus of the inflorescence (Prenner 2014).

Cronquist (1981) suggested that Malesherbioideae lacked stipules. In species of Passiflora with strongly bilobed leaves, vernation may be modified conduplicate: The blade makes a V with an inverted V at the end of each arm. The tendril is an axillary shoot and flowers - single, or 3-flowered cymes - can arise from the prophyllar buds on it. For the floral and extrafloral nectaries of Passifloraceae, see Krosnick et al. (2008a, b, 2011). The latter are anatomically quite different from the former (i.a. they lack nectarostomata) and the CRABS CLAW gene is not expressed in them (Krosnick et al. 2008a), and so they are arguably not "homologous".

For a survey of floral morphology in Turneroideae, see Arbo et al. (2015); some species of both Turnera and Piriqueta have epiphyllous flowers. Monosymmetric flowers, with stamens, etc., adaxially positioned, are found in species of Passiflora like P. ampullacea, and at least sometimes here the odd sepal is abaxial (Macdougal 1994: there are also four carpels); P. unipetala has but a single petal in the adaxial position. Although the tubular flowers of Passifloraceae s.l. are often described as having a hypanthium, the floral tube is nearly always formed from calycine and corolline elements only. For floral morpholoigy in Passiflora subgenus Decaloba, see Krosnick et al. (2006).

A little is known about the development of the complex series of fimbriae and membranes at the base of the androgynophore and in the throat of the KC tube in Passiflora. In subgenus Passiflora at least, genes normally involved in stamen development are expressed in the centripetally developing fimbriae, although the limen, a rim structure at the base of the androgynophore protecting the nectar, is from this point of view an organ sui generis (Hemingway et al. 2011). These fimbriae are unlikely to be staminodia (Prenner 2014: P. lobata). Claßen-Bockhoff and Meyer (2016) also discuss the development of the corona, and Bernhard (1999) looks at similar structures here and in other Passifloreae.

The styles of Malesherbioideae are shown as being commissural by Schnizlein (1843-1870: fam. 198). For a discussion on aril development, see Kloos and Bouman (1980); although the aril is often described as funicular, they incline to call it raphal.

Adenia seems rather different from other Passifloroideae, perhaps being more like the two other subfamilies, as in having an only moderately developed corona and tricolporate pollen (e.g. see Feuillet & MacDougal 2006). Adenia also has a nectary often made up of separate glands, a hollow style, and its stigma lacks multicellular papillae (Bernhard 1999a, c), in addition, it may be dioecious, it lacks an androgynophore but may have a gynophore, its stamens are sometimes connate, and some species have a true hypanthium (de Wilde 1971b).

For general information on Passifloroideae, see de Wilde (1971b, 1974), Feuillet and MacDougal (2006) and de Vos and Breteler (2009: Paropsieae), for chemistry, see Hegnauer (1969, 1990), for anatomy, see Harms (1893), for branching and growth, see de Wilde (1971a) and Cremers (1974), for stipules, see Dahlgren and van Wyk (1988), for floral morphology, see Bernhard (1999: Passifloreae), for pollen, see Presting (1965) and Spirlet (1965), carpel orientation of Passifloreae is taken from Le Maout and Decaisne (1868) and Schnizlein (1843-1870: fam. 197), for embryology, etc., see Raju (1956a) and Singh (1970), for arils, see e.g. Pfeiffer (1891), Kapil et al. (1980).

For floral anatomy of Passiflora, see Puri (1947), and for floral morphology, see Endress (1994b), for a general account of the genus, see Ulmer and MacDougal (2004). Hansen et al. (2006) discuss chromosome number evolution, n = 12 may be the basal number; see also de Melo and Guerra (2003) and Mayrose et al. (2010).

Some information on Turneroideae is taken from Raju (1956b), Vijayaraghavan and Kaur (1967), and Gonzalez and Arbo (2013), all embryology and seed, Arbo et al. (2015: esp. seeds, diversity of arils), Hegnauer (chemistry), González and Arbo (2005: anatomy) and Gonzalez et al. (2012: Adenoa, general), and Arbo (2006: general account).

General information on Malesherbioideae is taken from Ricardo S. (1967: the micropyle is endostomal) and Kubitzki (2006b); for chemistry, see Hegnauer (1969, 1990).

Embryologically Malesherbioideae are largely unknown.

Phylogeny. Turneraceae were weakly associated with Malesherbiaceae in Chase et al. (2002), the two being strongly associated with Passifloraceae. Although preliminary data seemed to suggest that a paraphyletic Passifloraceae might include Turneraceae and Malesherbiaceae (A.P.G. II 2003), Korotkova et al. (2009: only three taxa from the three families) found that Turnera and Passiflora were sister and with 98% jacknife support. For relationships in the clade that are the same as those shown above, see Tokuoka (2012) and Xi et al. (2012b).

Thulin et al. (2012b) disentangled relationships within Turneroideae, finding a largely Old World and a largely New World clade (see above). Relationships are [[Adenoa [Piriquetia + Turnera]] [Erblichia [African and malagasy clade]]] (see also Tukuoka 2012). Arbo and Espert (2009: morphological analysis, basally pectinate tree with little support) discuss the morphology and biogeography of Turnera; relationships suggested by a later study with 91 characters, including several from the seed, were rather different that those apparent in molecular analyses (Arbo et al. 2015).

For relationships within Malesherbioideae, see Gengler-Novak (2002, 2003).

Tokuoka (2012) clarified the phylogeny of Passifloroideae, only Paropsiopsis was not included. Paropsieae are monophyletic, with [Paropsia + Viridivia] being sister to the rest. Within Passifloreae relationships were [Adenia [Dilkea, Passiflora, etc.] [Basananthe, Deidamia, etc.]] (Thulin et al. 2012b). In earlier studies, e.g. Krosnick and Freudenstein (2005), the position of Adenia was unclear.

For a phylogeny of Passiflora, see Yockteng and Nadot (2004), Krosnick and Freudenstein (2005: also morphology), and Krosnick and Freudenstein (2006); Krosnick et al. (2013: inc. much information) discuss the phylogeny of Passiflora subgenus Decaloba. Hearn (2006) provides a phylogeny for Adenia.

Classification. Including Turneraceae and Malesherbiaceae in Passifloraceae s.l. was an optional arrangement in A.P.G. II (2003), and because of the basic similarity of the three families, they were placed in one by A.P.G. III (2009).

For a revision of Turnera, see Arbo (2008 and references). Passiflora includes Hollrungia and Tetrapathea (Krosnick & Freudenstein 2006); for a formal infrageneric classification of Passiflora, see Feuillet and Macdougal (2004).

Thanks. I am grateful to J. M. Macdougal for information.

[Lacistemataceae + Salicaceae]: anthers ellipsoid to subglobose; endosperm copious.

Age. This node has been dated to (60-)57, 53(-50) m.y. (Wikström et al. 2001), ca 91.1 m.y. (Tank et al. 2015: table S2), (108-)100(-96)/(96-)90(-89) m.y. (Davis et al. 2005a), (81-)73, 72(-64) m.y. (Bell et al. 2010), (94.2-)87.1(-80.5) m.y. (Xi et al. 2012b: table S7) and (73-)62(-53) m.y.a. (Percy et al. 2014).

LACISTEMATACEAE Martius, nom. cons.   Back to Malpighiales

Lacistemataceae

Trees; plants Al accumulators; chemistry?; vessel elements with scalariform perforation plates; sieve tubes?; petiole bundle D or deeply C-shaped, also wing bundles +; leaves two-ranked, (lamina entire); inflorescence raceme-like to densely spicate (flowers 3/node); flowers small; P +, uniseriate, cup-like, (1-)4(-6); A 1, the thecae ± separated and even stipitate; (G [2]), median member adaxial, style branches short, ?stigma; ovules 1-2/carpel, apical, funicles thick, long, ovule type?; fruit a 1(-3)-seeded capsule; ?aril; testa fleshy or not; embryo (short), with foliaceous cotyledons; n = 22, chromosomes 0.9-2.3 µm long.

2[list]/14. Greater Antilles (Jamaica), Mexico southwards, not in Chile (map: from Sleumer 1980).[Photo - Flower, Fruit]

Age. Crown-group Lacistemataceae are around (49.3-)19.8(-2.6) m.y.o. (Xi et al. 2012b: table S7, inc. Los.).

Chemistry, Morphology, etc. The inflorescence may be derived from a more elborate form with determinate branches. Chirtoiü (1918) described the flower as having 4-5 free perianth parts and an irregularly lobed , annular nectary. The presence of an aril in Lacistemataceae needs to be confirmed (see also Corner 1976). Sleumer (1980) records an aril in Lacistema, but a fleshy seed coat for Lozania. In Lozania there appear to be long "hairs" inside the fruit which perhaps support the dangling seed; these hairs are thick-walled but unlignified cells that may be derived from the funicle (see also Casearia, Salicaceae). The embryology, etc., of the family remain largely unknown

Additional information is taken from: Lozania - Riviere 270 (anatomy), Gentry et al. 22231 (fruit); Lacistema - Aymard & Delgado 6882 (fruit), Rimachi Y. 11201 (anatomy - stomata tending to anisocytic). See Young (2007 onwards: Lacistemataceae website, focus is on species, nomenclature, etc..

Phylogeny. Lacistemataceae did not cluster with the rest of Salicaceae and Kiggelariaceae in an early study by Savolainen et al. (2000a), although they were probably in this area (Chase et al. 2002; see also D. Soltis et al. 1999, 2000). Davis et al. (2005a) place them as sister to Salicaceae s.l. (61% bootstrap, 1.0 posterior probability), as do Korotkova et al. (2009: slightly higher jacknife); as might be expected, they lack salicoid teeth.

Classification. See Sleumer (1980: as Flacourtiaceae-Lacistemeae) for a monograph.

SALICACEAE Mirbel, nom. cons.   Back to Malpighiales

Salicaceae

Shrubs to trees; cocarcinogens, (cyclopentenoid cyanogenic glycosides and/or cyclopentenyl fatty acids [gynocardin], ellagic acid) +, tanniniferous; cork?; vessel elements with simple or scalariform perforation plates; petiole bundle arcuate or annular with wing bundles; stomata ?; leaves two-ranked, lamina vernation supervolute-curved or involute, (margin entire), (venation palmate), (glands +), (stipules 0); inflorescence various; flowers 3-6-merous, (hypanthium +); K (0-)3-8(-15), often valvate, (basally connate; corona +), nectary extrastaminal, often lobed; A 1 to many (fasciculate, opposite petals), anthers (extrorse), (linear); G [2-5], (placentation axile), styles separate or fused; ovules anatropous, micropyle usu. bistomal and ± zig-zag, funicle short; fruit also a berry (drupe); (embryo chlorophyllous); n = 9, 10-12, 19.

55[list]/1010. Pantropical, also temperate (but few in the Antipodes) to Arctic (map: from Sleumer 1954; Meusel et al. 1975; Sleumer 1980; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower, Fruit.]

Age. Crown Salicaceae have been dated to (50-)47, 40(-37) m.y. (Wikström et al. 2001), (71-)63, 61(-55) m.y. (Bell et al. 2010), or (87-)79.2(-72.8) m.y. (Xi et al. 2012b: table S7).

1. Samydoideae Reveal

(Heartwood brown, rays wide, visible - Irenodendron); lamina often punctate or lineate, teeth theoid; (inflorescence fasciculate); hypanthium +; P +, uniseriate, 3-7, basally connate, C 0; nectary on base of P; A 3-many, initiated simultaneously, (filaments closely adpressed, forming a tube), staminodes/nectary glands alternating with or adaxial to stamens; tapetal cells 2-4-nucleate; styles fused or free apically; embryo sac straight, outer integument ca 2 cells across, inner integument ca 2 cells across, hypostase + [Casearia]; (embryo sac protruding into micropyle); (seed squeezed from fruit, aril vascularized - Casearia); exotegmen cells laterally flattened, crystalliferous.

14/245: Casearia (180). Pantropical, especially South America.

Age. Crown-group Samydoideae (Cas., Lunania) are (38.8-)37.4(-36.3) m.y.o. (Xi et al. 2012b: table S7).

Synonymy: Bembiciaceae R. C. Keating & Takhtajan, Prockiaceae Bertuch, Samydaceae Ventenat, nom. cons.

[Scyphostegioideae + Salicoideae]: lamina with a small vein proceeding into the tooth, where it expands, the apex of the tooth being a variously coloured spherical gland or stout hair [salicoid teeth].

Age. The age of this node is (78.7-)68.9(-59.8) m.y. (Xi et al. 2012b: table S7).

2. Scyphostegioideae Reveal

Scyphostegia

Vessels in radial multiples, with simple (and scalariform) perforations; rays mostly uniseriate; petiole bundle annular and with adaxial mass of xylem and phloem becoming adaxial inverted plate of vascular tissue; stomata paracytic; plant dioecious; inflorescences terminal, branched, long-lived, bracts large, overlapping, tubular, pedicels not articulated; P petal-like, not differentiated [= T 3 + 3], connate; staminate flowers: nectary as lobes opposite A; A 3, opposite inner whorl of T, connate, extrorse; pollen ?tricolpate; carpellate flowers: G [8-13], placentation basal, style 0, stigmas ray-like, with an opening in the middle; ovules with much elongated micropyle, ?exostomal, outer integument 2-3 cells across, lobed, inner integument 3-4 cells across, nucellar cap +, persistent, funicle +; fruit a fleshy capsule with lignified commissural valves; seeds with aril from funicle/outer integument; exotesta +, hairy; endosperm slight, perisperm +, very scanty; n = 9.

1/1: Scyphostegia borneensis. Borneo, not the southern part. [Photo - Flower, Leaf, Inflorescence.]

Synonymy: Scyphostegiaceae Hutchinson, nom. cons.

3. Salicoideae Arnott

(Plant deciduous); benzoylated glycosides, etc. +, (cyanogenic glycosides + - Banara); (nodes 2:2 - some Azara); (leaves spiral, opposite); (plant dioecious/monoecious); (inflorescence densely spicate), terminal or axillary; (C 0), (more than K - e.g. some Scolopieae); A initiation centrifugal; (pollen inaperturate - Populus); G [2-5(-13)], (inferior - Homalium), (stigmas flabellately divided); (ovule straight), (micropyle exostomal - Idesia; endostomal - Oncoba), (outer integument lobed - Caloncoba), outer integument 2-5 cells across, inner integument 3-5 cells across, (integument 1, 3-4 layers across - Salix), (nucellar cap +), (hypostase +), funicle (long),( 0); (embryo sac ± protruding into the micropyle), (sac bisporic [chalazal dyad], eight-celled: Allium-type); (seeds with funicular hairs - Salix); (exotesta alone - Salix), (testa vascularized, sarcotesta +, endotesta palisade - Oncoba); (endosperm 0 - Salix); n =.

41/735: Salix (450), Homalium (150), Xylosma (85), Scolopia (37), Banara (31). Worldwide, but only Saliceae cold Temperate/Arctic, few Australia, not New Zealand.

Age. Crown Salicoideae, or somewhere around there, are (36-)33, 26(-23) m.y.o. (Wikström et al. 2001), (55-)51, 50(-47) m.y.o. (Bell et al. 2010), (65.1-)58(-51.3) m.y.o. (Xi et al. 2012b: table S7 - see below) or (58-)52(-48) m.y.o. (Percy et al. 2014).

Synonymy: Flacourtiaceae Richard, Homaliaceae R. Brown, Poliothyrsidaceae Doweld

Evolution. Divergence & Distribution. Boucher et al. (2003) described Pseudosalix, a ca 48 m.y.o. Eocene fossil from North America, which is morphologically intermediate between Salix and more florally conventional Salicaceae, with a terminal, branched inflorescence and flowers with well developed sepals; Populus is known from deposits of about the same age.

Diversification in Scyphostegioideae seems to have slowed down (!: Xi et al. 2012b: as Scyphostegiaceae).

Ecology & Physiology. Salix and Populus are often ectomycorrhizal and grow with other ectomycorhizal trees in boreal forests. Salix itself is a major component of the biomass in tundra ecosystems (Chapin & Körner 1995); with almost 70 species growing in the Arctic, it is the second largest genus there (Elven et al. 2011).

A single clone of Populus tremuloides is recorded as covering 43.6 ha and has around 47,000 stems (DeWoody et al. 2008.

Metal hyperaccumulators (nickel) are notably common in members of the family growing in New Caledonia (Brooks 1998 for a summary).

Pollination Biology. Populus is dioecious and wind-pollinated.

Plant-Animal Interactions. Boeckler et al. (2011) discuss the anti-herbivore properties of the phenolic glycosides, salicinoids, characteristic of Salix and its immediate relatives, and sometimes be up to 30% of dry weight (Pentzold et al. 2014 and references). Nevertheless, a number of insects and fungi are associated with them, thus around 34 species of Phyllonorycter leaf-mining moths (Lepidoptera-Gracillariidae-Phyllocnistinae) are found on Populus and Salix in the Holarctic region (Lopez Vaamonde et al. 2006). Caterpillars of Atella (Nymphalinae) fed on the old Flacourtiaceae and Salicaceae (Ehrlich & Raven 1964) as do several Vagrantini (Nylin et al. 2014), while some Notodontidae moths (Miller 1992) show similar host patterns. The amount of condensed tannins in the leaves may vary greatly, but the implications of this for plant defence are unclear (Barbehenn & Constabel 2011).

There has been a remarkable radiation - 400-500 species - of euurine sawflies (Hymenoptera-Tenthredinidae-Nematinae), mostly gallers but also folding or rolling leaves, on Salix and Populus, although they have yet to be recorded from other Salicaceae. Leaf folding appears to be the primitive condition, and the sawflies show considerable host specificity (Roininen et al. 2005; Nyman et al. 1998, 2006 and references); high diversity and high host specificity are not commonly correlated in Lepidoptera, at least (Menken et al. 2009). Unlike other galls, sawfly-induced galls result largely from stimuli provided by the ovipositing wasp, which may inject fluids into the plant, rather than from the activities of the larvae, so the galls assume their mature forms before the eggs hatch (Redfern 2011).

Bacterial/Fungal Associations. Salix and its immediate relatives enter into a variety of associations with both ectomycorrhiza1 and endomycorrhizal fungi, and dark septate endophytes have also been found on them (e.g. Gardes & Dahlberg 1996; Van der Heijden 2000; Becerra et al. 2009). Tedersoo et al. (2013) found a strong correlation between host and ECM community composition and species richness in Salix and Populus - and in a small sample of less closely related hosts. Melampsora spp. are found on Salix, M. idesiae on Idesia (Holm 1979).

Genes & Genomes. A genome duplication in the common ancestor of Salix and Populus, the salicoid duplication, has been dated to 65-60 m.y. (Tuskan et al. 2006); it will be interesting to know if other Salicaceae s.l. have it. This duplication has also been dated to (36.3-)34.7(-32.6) m.y.a., although the oldest fossils known (of Populus) are 47.4 m.y.o. (Vanneste et al. 2014a and references; see also above); Jiang et al. (2013) followed the fate of duplicated genes. Note that Murat et al. (2015b) date a duplication in Populus to 17-7 m.y.a., overall chromosome number changes in Salicaceae being x = 12 → 24 → 19 (Populus). Populus has lost the PHYC gene (Matthews 2010 and references); again, the phylogenetic extent of this loss is of interest.

The [Salix + Populus] clade is dioecious, and an X/Y sex determination system has evolved at least three times (twice in Populus) in the clade, maybe within the last 7-6 m.y. - although the whole clade is at least 25 m.y.o. (Geraldes et al. 2015).

Salix in particular is notorious for its extensive interspecific hybridisation. The closely-related Populus balsamifera and P. trichocarpa introgress at contact zones and are estimated to be ca 75,000 y.o. from nuclear data - and 6-15 m.y.o. from chloroplast data - perhaps chloroplast capture from a ghost lineage (Huang et al. 2014)? DNA barcoding failed spectacularly in Salix, and although 2-7 plastid genome regions were examined, only 1 of 71 species was successfully barcoded (Percy et al. 2014, q.v. for explanations).

Chemistry, Morphology, etc. Banara is the only genus reported to have cyanogenic glycosides, but it is well embedded within Salicaceae (Chase et al. 2002). The perforation plates of the tracheary elements are more or less simple and the intervascular pits are small. Xylosma, Flacourtia, etc., have groups of large sclereids in the phloem (Zahur 1959). Xylosma and some Casearia seem to have unilacunar nodes. Leaf traces arise an internode below the leaf they innervate in Hasseltia.

Branching in Casearia is phyllanthoid, the orthotropic axes having spirally arranged and reduced leaves while the plagiotropic branches are sylleptic and have fully-expanded and two-ranked leaves. Salicoid leaf teeth are quite variable, but all have secretory palisade cells over parenchyma and are well supplied by vascular tissue, especially xylem (Wilkinson 2007); is the salicoid tooth basically colleter-like? Thadeo et al. (2008; see also Thadeo & Meira 2009) discuss the similarity between leaf teeth and foliar nectaries in Salicaceae, in particular the foliar nectaries of Prockia crucis that secrete fructose, glucose, sucrose, etc. Nectaries at the base of the lamina in two species of Populus differed markedly. In one they were persistent, with continuous nectar flow, while in another, large amounts of nectar were produced over a short time and cell death occurred, but new nectaries could be produced (Escalante-Pérez et al. 2012). Abatia has opposite leaves with at most very small stipules and marginal glands at the base of the lamina. There are also taxa with pli-nerved leaf blades and foliar glands in Salicaceae - this is a vegetatively rather heterogeneous clade.

For inflorescence development in catkinate Salicaceae and genera like Idesia, see Cronk et al. (2015). The valvate perianth members of Abatia are basally connate and bear many filamentous processes, and the flowers lack a nectary. In those species that have a nectary, its morphology is very variable. It is often made up of a number of lobes, and these may be intrastaminal. It has been claimed that the nectary of Salix represents a perianth member, but Alford et al. (2009) suggest that it is like that of other members of the family; there are receptacular nectaries adaxial to the stamens in taxa in the clade sister to [Salix + Populus]. Indeed, in Poliothyrsus the nectary is outside the stamens and is on the bases of the valvate perianth members. Elongated embryo sacs occur in both Salicaceae and old Flacourtiaceae (Steyn et al. 2005a), indeed, the embryo sac more or less protrudes into the micropyle in Archevaletaia (Maheshwari 1950). Corner (1976) described the micropyle of Scyphostegia as being exostomal. The exotegmen of Dovyalis consists of ribbon-like cells.

Much older literature is under Flacourtiaceae: See Lemke (1988), Alford and Dement (2015: Samydoideae), Judd (1997a) and Chase et al. (2002), all general information, Hegnauer (1973, 1990, also 1966, 1989), Spencer and Seigler (1985b) and Chai (2009), all chemistry, Miller (1975: wood anatomy), Bernhard and Endress (1999: androecial initiation), Gavrilova (1998: pollen), and Narayanaswami and Sawhney (1959) and Steyn et al. (2004, 2005a, b), all ovule and seed development, summary in latter paper) and van Heel (1977, 1979: testa anatomy). For Scyphostegia, see Metcalfe (1954: anatomy), van Heel (1967a: flowers and fruits) and Hutchinson (1973: different interpretations of the gynoecium).

Phylogeny. Chase et al. (2002) greatly clarified the phylogenetic situation in the old Salicaceae-Flacourtiaceae area (see also Judd 1997a; Nandi et al. 1998; T. Azuma et al. 2000; Savolainen et al. 2000a), although sampling within tribes still needs to be extended. Casearia, which lacks salicoid leaf teeth and has apetalous flowers with a nectariferous area on the basal-adaxial surface of the perianth tube, is sister to the rest of Salicaceae, although support for this position is weak (Chase et al. 2002; Xi et al. 2012b, c.f. D. Soltis et al. 1999, 2000). Trichostephanus (Trichostephaneae) was not assigned to any family (Chase et al. 2002), but in lacking petals and in having a disc at the base of the calyx it is like Casearia (Samydeae).

In gross morphology Oncoba is remarkably like other members of the erstwhile Oncobeae, but they differ in chemistry, leaf tooth type, and stamen initiation and are now in Achariaceae-Lindackerieae; Oncoba itself is perhaps to be assigned to Flacourtieae. Xi et al. (2012b) found the relationships [Flacourtia + Prockia] [Poliothyrsis + Salix and relatives]].

For relationships of Salix and its immediate relatives, see Leskinen and Alström-Rapaport (1999). Relationships are [Microhasseltia, etc. [[Salix + Populus] [Olmediella [Bennettiodendron + Idesia]]]; characters like hairy seeds, sepals deciduous in fruit, loss of corolla, and dioecy are apomorphies at various levels within this clade (Alford et al. 2009). For a phylogeny of Salix, see T. Azuma et al. (2000) and Chen et al. (2010).

Classification. Chase et al. (2002) provide a detailed tribal classification for the clade: Abatieae, Bembicieae, Prockieae (inc. Banareae), Oncobeae (Oncoba only), Homalieae, Saliceae, Samydeae (Casearieae), Scolopieae, and Scyphostegieae. These tribal limits may well have to be adjusted, thus Saliceae will probably have to be expanded, Flacourtieae are polyphyletic, etc. The classification is only partly adopted here pending more detailed sampling. Alford (2003) recognised three families for the New World genera previously included in Flacourtiaceae - in addition to Achariaceae, Berberidopsidaceae and Lacistemataceae.

Generic limits in the Casearia group neeed attention (Samarakoon et al. 2010).

Previous Relationships. It had been observed in the past that Salicaceae s. str. and Flacourtiaceae-Idesieae were close, despite the catkins of the former (summary in Chase et al. 2002) - they both have similar, distinctive leaf teeth, phenolic-type compounds such as salicin, etc. (Miller 1975), and rusts and caterpillars, perhaps keying in on chemical characters, show similar distributions (e.g. Meeuse 1975; see above). However, in the Englerian system Salix was often kept with the wind-pollinated Amentiferae, not at all close to Flacourtiaceae, a family that was also recognised at the time and which encompassed the bulk of Salicaceae above and also Achariaceae, etc.; see also Gilg's (1914) emphatic rejection of Hallier's suggestion that there might be a link between Idesia (Flacourtiaceae) and Salicaceae. Cronquist (1981) placed Salicaceae in a monofamilial order, but next to his Violales.

Thanks. I am grateful to S. Zmarzty for comments.

[[Peraceae [Rafflesiaceae + Euphorbiaceae]] [[Phyllanthaceae + Picrodendraceae] [Ixonanthaceae + Linaceae]]] / Euphorbioids: fruit a part-septicidal + loculicidal capsule/schizocarp; cotyledons longer and broader than radicle.

Age. This node has been dated to (74-)71, 69(-66) m.y. (Wikström et al. 2001), ca 82.8 m.y. (Tank et al. 2015: table S1, S2) and (111.3-)106.9(-103.1) m.y. (Xi et al. 2012b: table S7).

Evolution. Divergence & Distribution. Lee et al. (2011) found that genes involved in oxygen and radical detoxification clustered at this node, but Populus and Bruguiera were the only other members of Malpighiales in their study.

On strict parsimony grounds the distinctive fruits of Euphorbiaceae, etc., could be a synapomorphy for the whole clade or acquired twice, in any case, they have been lost several times within Euphorbiaceae s. str., etc..

Phylogeny. See Xi et al. (2012b: Rafflesiaceae not included) for the composition of this clade (= euphorbioids) and relationships within it.

[Peraceae [Rafflesiaceae + Euphorbiaceae]]: vessel elements with simple perforation plates; flowers small, imperfect; G [3], styles ± separate; ovule 1/carpel, nucellar cap + [unknown in Peraceae]; fruit with outer pericarp often separating from the woody layer, valves falling off, central column persistent; seeds large, micropylar caruncle + (0).

Age. The age of this node is (103.8-)97.2(-87.1) m.y. (Xi et al. 2012b: table S7).

Evolution. Divergence & Distribution. Note that all the features mentioned above are lost in Rafflesiaceae, clearly a very derived group. This one clade includes the extremes of flower size in angiosperms. Pseudanthia have evolved ca 4 times, and in Euphorbia, for example, a single stamen represents the staminate flower. In Rafflesia, on the other hand, the flower can be up to 1.5 m across (e.g. Barkman et al. 2008).

Seed Dispersal. Esser (2003b) emphasized that over 50% of Malesian Euphorbiaceae s.l. were zoochorous, notably more than in other tropical areas.

Chemistry, Morphology, etc. For pseudanthial bracts in Peraceae and Euphorbiaceae, see Gagliardi et al. (2016. The exotegmen in Rafflesiaceae is described as having U-shaped thickenings, and the exotegmen of some Peraceae can also look U-shaped in transverse section (see illustrations in Tokuoka & Tobe 2003).

Phylogeny. Barkman et al. (2004a) sequenced the mitochondrial gene, matR, of Rafflesia and found a strong association with Malpighiales (see below for previous placements of Rafflesiaceae). Although sampling within Malpighiales (only three taxa with parietal placentation were studied) and other rosids was poor, Barkman et al. (2004) noted that the flowers of Rafflesia could be interpreted as having a number of features in common with those of Passifloraceae, including a corona (called a diaphragm by students of Rafflesiaceae), androgynophore, parietal placentation (but this is common in echlorophyllous parasites), etc., but as Nickrent et al. (2004a) pointed out, the "homology" of these structures needs careful examination. Davis and Wurdack (2004: two nuclear, one mitochondrial [matR] genes), with considerably more extensive sampling, confirmed the inclusion of Rafflesiaceae in Malpighiales, favouring a position closer to Ochnaceae, Clusiaceae and their relatives. Although tenuinucellate ovules are common there, too, it is quite common for holoparasitic taxa to lack parietal tissue in their ovules. A position of Rafflesiaceae in or near Malpighiales was common in the analyses described by Nickrent et al. (2004a). Most recently, Davis et al. (2007), using largely mitochondrial genes, exemplars of all families of Malpighiales, three of the four genera of Peraceae, Chaetocarpus only excluded, and several Euphorbiaceae, including Cheilosioideae, placed Rafflesiaceae within Euphorbiaceae and with quite good support (see also Wurdack & Davis 2009).

Classification. Merino Sutter and Endress (1995) argue for a rather broadly delimited Euphorbiaceae (inc. both Phyllanthaceae and Putranjivaceae), Huber (1991) for a narrower circumscription, with the biovulate taxa (Phyllanthaceae, Picrodendraceae, Putranjivaceae) being considered to be closer to Linales s. str., while Meeuse (1990) also suggested that the family should be split - into eleven families. There is no molecular evidence yet for a broadly delimited Euphorbiaceae (unless Linaceae et al. were to be included), yet Euphorbiaceae s. str, Phyllanthaceae and Picrodendraceae all have a similar and rather distinctive capsule, etc. (see also Merino Sutter et al. 2006).

Indeed, molecular analyses by Wurdack and Chase (2002), and especially by Wurdack et al. (2005, see also Tokuoka 2007) and Xi et al. (2012b), suggested that substantial changes were needed to the groupings that had been recognised in the family. The reclassification they proposed is followed here, with the interpolation of Rafflesiaceae (see Davis et al. 2007) and the associated recognition of Peraceae. Splitting Peroideae from the other Euphorbiaceae s. str. - which actually makes the latter more homogeneous in fruit and testa anatomy - and keeping Rafflesiaceae seems reasonable, there being little enthusiasm for including a Rafflesioideae within an already large Euphorbiaceae.

Euphorbiaceae

PERACEAE Klotzsch   Back to Malpighiales

Peraceae

Shrubs to trees; petiole bundles interrupted arcuate to annular, complete annular, (also with medullary plate and wing bundles); stomata?; leaves spiral, lamina vernation involute, margins entire, venation pinnate, stipules (large), small or 0; plant dioecious (monoecious); (coloured inflorescence bracts +); staminate flowers: C (clawed), (0 - Pera); nectary lobes opposite K (0 - Pera); A 2-8, (?androgynophore, extrorse, opposite C - Clutia); pistillode + (0); carpellate flowers: (K 0, C 0 - Pera)); staminodes 0; stigma bilobed (trumpet-shaped - Pera); ovule with both integuments 3-6 cells across; fruit septa membranous and without visible vascularisation, (valves connected at base), perianth [when present] persistent; seeds carunculate or arillate, very shiny; exotesta palisade, lignified, endotesta crystaliferous, exotegmen tracheoidal, oblique, (palisade - Pogonophora); endosperm copious; n = 18, chromosomes 0.5-1.1 µm long.

5[list]/135: Clutia (75), Pera (40). Pantropical, probably not East Malesia (one doubtful report) (map: inaccurate, see van Welzen 1994).

Age. The age of this node is (93.4-)63.5(-32.1) m.y. (Xi et al. 2012b: table S7 - Pog Per Clu).

Evolution. Seed Dispersal. Myrmecochory may predominate in this clade (Lengyel et al. 2009).

Chemistry, Morphology, etc. Neither wood anatomy nor pollen morphology are distinctive (Nowicke et al. 1998; Hayden & Hayden 2000), however, members of Peraceae are variously described as having lysigenous radial canals in the wood, laticiferous cells, or elongated cells with brown contents.

The highly reduced flowers of Pera are surrounded by coloured inflorescence bracts; a pseudanthium of sorts. Pogonophora has adaxially barbellate petals. Style branches are variable in this group, being very short to longer and bifid. The seeds are described as having arils by Tokuoka and Tobe (2003). The anatomy of the seed coat of Peraceae is distinctive compared to that of Euphorbiaceae s. str. - this from an earlier version of /APweb/: "Tokuoka and Tobe (2003) note some Acalyphoideae with a distinctive seed coat anatomy - a more or less tracheoidal exotegmen - unlike that of all other Euphorbiaceae (minus Phyllanthaceae, etc). Interestingly, all the taxa involved belong to other families or are in Euphorbiaceae-Peroideae. These are sister to other Euphorbiaceae, and the distinctive exotegmen structure is more like that common in other Malpighiales. So it is possible that this is plesiomorphic, whereupon the palisade exotegmen of Pogonophora is a parallelism..." The seed coat anatomy of Trigonopleura is unknown.

For general information, see Webster (1984, 2013) and Radcliffe Smith (2001), for wood anatomy, see Hayden and Hayden (2000), and for pollen, see Nowicke et al. (1998); for seed coat anatomy, see Huner (1991) and Tokuoka and Tobe (2003).

Many details of anatomy, and in particular floral development, ovule morphology, etc., are poorly known.

Phylogeny. Tokuoka and Tobe (2006) question the inclusion of Pogonophora in this clade; indeed, if it is to be included and is sister to other Peraceae, then mapping seed coat evolution on the tree does become a bit tricky.

Classification. For a comprehensive checklist and bibliography, see Govaerts et al. (2000, in Euphorbiaceae).

Previous Relationships. Although Airy Shaw (1976) recognised Peraceae as separate from Euphorbiaceae, his Peraceae included only Pera, a genus long considered very distinctive within Euphorbiaceae, even if rarely separated from it. Esser (2003a) drew attention to the distinctiveness of the whole group.

[Rafflesiaceae + Euphorbiacaeae]: ?

Age. The age of stem Rafflesiaceae may be (109.5-)95(-83.1) m.y. (Bendiksby et al. 2010), however, it has also been estimated as (84-)65.3(-45.9) m.y. (Naumann et al. 2013).

RAFFLESIACEAE Dumortier, nom. cons.   Back to Malpighiales

Rafflesiaceae

Stem or root parasites, plant endophytic, ± filamentous, uniseriate, undifferentiated, vessel elements 0; stem, leaf and roots 0; shoot apex becomes evident by schizogenous separation of cells; sieve tube plastids lacking starch and protein inclusions; cuticle wax crystalloids 0; plant dioecious [other breeding systems?]; flowers single; bracts +; flowers medium-sized to huge, (perfect); P/T 5/10/16-lobed, ± biseriate, (valvate - Rhizanthes), floral tube a ring derivative, floral chamber +/0, [inner T/C connate, incurved - Rafflesia); diaphragm +, annular, incurved - Sapria; chamber 0 - Rhizanthes], (nectary on distal part of perianth - Rhizanthes); gynostemium +; staminate flowers: A 12-40, adnate to central column [pistillode, = gynostemium], extrorse, anthers sessile, porose, (polysporangiate); microsporogenesis successive, pollen inaperturate, atectate; pistillode +; carpellate flowers: staminodes +; ovary inferior, nectary at base of style, carpel margins closed by postgenital fusion and secretion, placentation laminar-parietal, loculi irregular, schizogenous, gynostemium short, stigma on outer margin or underside of disc-shaped structure; ovules very many/carpel, parietal tissue 0, inner integument ca 2 cells across, micropyle (exo-)endostomal, nucellar epidermis persists; antipodal cells ephemeral or not; fruit baccate, splitting; caruncle 0, seed in two parts, that covered by the testa not enveloping the embryo, exotegmic cells cuboidal, with U thickenings; endosperm initially nuclear [Rafflesia], slight, proembryo only; n = 11, 12.

3[list]/20: Rafflesia (16). S. China, Assam, Bhutan, Thailand, W. Malesia (map: from Meijer 1997). [Photo - Flower.]

Age. The age of crown-group Rafflesiaceae has been estimated at (95.9-)81.7(-69.5) m.y.a. (Bendiksby et al. 2010; see also Barkman et al. 2008).

Evolution. Divergence & Distribution. If Sapria split off from other Rafflesiaceae ca 81.7 m.y.a. (Bendiksby et al. 2010) there must have been a major reorganization of the plant body in less than 15 m.y. after the Rafflesiaceae and Euphorbiaceae s. str. clades diverged; holoparasitism must have been established by then. This also raises the issue of when lowland tropical rainforest evolved. Today it is the preferred habitat of Rafflesiaceae as well as many echlorophyllous myco-heterotrophic taxa such as Burmanniaceae, Thismiaceae (Dioscoreales), Gentianaceae-Voyrieae (Gentianales), etc.. However, the dates in Naumann et al. (2013, q.v. for discussion), with the stem age being around 65.3 m.y.a., suggest a rather different scenario. Bendiksby et al. (2010, q.v. for more dates; see also Barkman et al. 2008) suggested that diversification within the genera of Rafflesiaceae did not begin until very much after the origin of the clade. Rhizanthes and Rafflesia may have separated ca 37 m.y.a. (Naumann et al. 2013), while crown-group Rafflesia may be a mere (15.1-)11.8(-9.2) m.y.o., and this is the oldest of the crown-group ages suggested - perhaps there was an extinction event immediately prior to this.

P. Chen et al. (2011b: HPD) suggest ages of (65.3-)50.6(-36.4) m.y. for stem Tetrastigma, (49.3-)36.9(-25.7) m.y. for the crown group, well before diversification of Rafflesia; ages in Lu et al. (2013) are somewhat older, at (67.7-)57.4(-47.4) and (59.4-)47.6(-36.4) m.y. respectively. However, if the whole family is parasitic on Tetrastigma, there could be an interesting timing problem. Fruits of crown-group Vitaceae from the Deccan Traps have been dated to around/a little before the K/C boundary ca 66 m.y.a. (Manchester et al. 2013).

Ecology & Physiology. Rafflesia - Rafflesiaceae in general - are parasitic on species of Tetrastigma (Vitaceae), an association that may have evolved more than once (P. Chen et al. 2011a). Furthermore, although some of the mitochondrial genes that have moved into Vitaceae place as sister to Vitaceae, others group with Cucurbitaceae and even Daucus (Apiaceae). This may suggest that the hosts of Rafflesiaceae may have been rather different in the past (Xi et al. 2013a). The parasite obtains all its nutrients from the host.

The vegetative plant body of Rafflesiaceae is endophytic, and Wurdack and Davis (2009) suggested that it might be derived from laticiferous tissue, however, the common ancestor of Euphorbiaceae and Rafflesiaceae is unlikely to have had laticifers. The endophyte is quite inconspicuous, almost filamentous, and the cells are undifferentiated (Nikolov et al. 2014b).

Pollination Biology & Seed Dispersal. The flowers of at least some Rafflesiaceae are thermogenic (Seymour 2001) and pollination, where known, is by flies, the flowers looking and smelling rather like a rotting carcass and the pollen being presented in the form of a slurry, as occurs in other fly-pollinated flowers (Bänziger 2004; Davis et al. 2008; Nikolov et al. 2014a; see also Jürgens et al. 2013 for this syndrome). The ca 79-fold increase in flower size during the evolution of stem-group Rafflesiaceae over a period of ca 46 m.y. may be linked to the adoption of sapromyophily; size increase in the subsequent ca 60 m.y. was much more modest (Davis et al. 2007, 2008). However, in a more extensive study of Rafflesia, Barkman et al. (2008) suggested that there had been very considerable changes in flower size even within the last 12 m.y. or so, the age of crown group Rafflesia, with repeated both considerable increases and moderate decreases in flower size. A\The ancestral flower size was (very approximately) 29 cm across (Barkman et al. 2008), and the largest flowers are about 1 m across (R. arnoldii) while those of R. consueloae are the smallest at around 10 cm across, although the perianth lobes are erect (Galindon et al. 2016).

The seeds are embedded in ?placental tissue and the fruits may be eaten by rats (Bänziger 2004).

Genes & Genomes. Davis and Wurdack (2004) found that the sequence of the mitochondrial gene nad1B-c In Rafflesiaceae strongly suggested a relationship with Vitaceae; the presence of this gene in Rafflesiaceae they reasonably thought was caused by horizontal gene transfer from Vitaceae. Similarly, Barkman et al. (2007) suggested that there had been a transfer of the mitochondrial atp1 gene from host to parasite. Xi et al. (2012a) showed that slightly over 2% of the nuclear genome may be involved, some Tetrastigma genes functioning in their new host, and even in a number of vertically transmitted Rafflesia genes, codon usage was Tetrastigma-like, perhaps facilitating the close association of the host and endophytic parasite. This is certainly the closest integration of host and parasite genome so far known in land plants. Xi et al. (2013a) confirmed this gene movement, which was more extensive than was previously thought; 24-41% of the mitochondrial genes examined had moved from host to parasite, probably by homologous recombination, and again these genes seemed still to be functional.

Molina et al. (2014) thought that the entire chloroplast genome in Rafflesia lagascae, at least, had been largely lost (see Bellot & Renner 2015 for discussion). Those gene fragments that could be detected lacked open reading frames, they were not expressed in floral bud tissues, and a third of them had sequence similarities with Tetrastigma genes; any chloroplast remnants might be in the nucleus (see also Krause 2015).

Chemistry, Morphology, etc. The plant is tanniniferous (Gottlieb et al. 1989). Although there are stomata in Rafflesia, they are clearly abnormal, having three or more guard cells (Cammerloher 1920).

There has been much debate as to what the perianth and the diaphragm/annulus (the latter forming a floral chamber) of the flowers of Rafflesiaceae might represent, although this has largely been cleared up by Nikolov et al. (2013, 2014a). Sapria can be interpreted as having a biseriate perianth (the spreading lobes of the flower), the annular diaphragm in the middle is a corona of sorts (perhaps rather similar to such structures in Passifloraceae); it arises where the expression of B and C genes changes (Nikolov et al. 2013: morphological and gene-expression studies). However, in Rafflesia the tubular structure below the diaphragm seems to have an inner and outer portion, suggesting that the spreading lobes represent the outer portion and are the calyx/outer perianth whorl and the diaphragm the inner portion or the connate corolla/inner perianth whorl (also D. Boufford, pers. comm.), while a rim at the base of the tube/around the gynostemium is the annulus. Rhizanthes lacks a diaphragm, but its perienth tube clearly has an inner and outer portion, and a slight bump on the perianth is probably where a fragmented annulus has become adnate to the perianth. Thus Nikolov et al. (2013) showed that the tubular structure found in all three genera develops in different ways in all three genera - in Rafflesia it is a K/C tube alone and in Sapria and Rhizanthes there is a K/C tube, but formed in different ways in the two, and the annulus is involved.

The ovary loculi develop by cell separation, unique in flowering plants, and the apex of the floral shoot becomes evident in a similar fashion (Nikolov et al. 2014a).

Furness and Rudall (2004) note a very distinctive combination of microsporogenesis and pollen morphology for the family; for pollen morphology, see also Blarer et al. (2004). The outer integument, when present, is one cell layer thick, but it is not easy to interpret the ovule (see Solms-Laubach 1874; Ernst & Schmid 1913 for more details). Although the funicle is bent, the integument is not adnate to it; in taxa with a single integument, there is a swelling on the chalaza, perhaps an indication of the other integument.

During germination of some Rafflesia, at least, the seed is anchored onto the host by sticky endosperm tubules and also the embryonal primary haustorium, the whole thing looking rather like a T4 bacteriophage (Arekal & Shivamurthy 1976).

For additional information, see Harms (1935), Meijer (1993), Nais (2001: superb photographs), the Parasitic Plants website (Nickrent 1998 onwards) and Heide-Jørgensen (2008), all general, Takhtajan et al. (1985: pollen), Bouman and Meijer (1986: seeds, 1994: ovules and seeds).

Phylogeny. Relationships within Rafflesiaceae are [Sapria [Rhizanthes + Rafflesia]] (Davis et al. 2007).

Previous Relationships. Rafflesiales of some authors included a number of other echlorophyllous, parasitic groups such as Cytinaceae (here Malvales), Hydnoraceae (Piperales-Aristolochiaceae), Apodanthaceae (Cucurbitales), and Mitrastemonaceae (Ericales). Many early and more recent authors have sought an affinity between Rafflesiaceae and taxa like Aristolochiacaeae (references in Takhtajan 1997), perhaps in part because of a belief that the pollen of the former had only a single aperture, as did that of Aristolochiaceae; there is a gynostemium of sorts and extrorse anthers in both. Cocucci and Cocucci (1996) saw connections of Rafflesiaceae first with Apodanthaceae and then with Annonaceae.

Thanks. To Lachezar Nikolov, for helpful discussions on floral morphology.

EUPHORBIACEAE Jussieu, nom. cons.   Back to Malpighiales

Euphorbiaceae

Trees or shrubs; (Al-accumulators); cucurbitacins [triterpenes], (polyacetylenes), ellagitannins [geraniin and mallotussic acid], lectins [hemagglutinins], cocarcinogens [phorbol ester diterpenes] +; cork also outer cortical (pericyclic); vessel elements often in multiples, (with scalariform perforation plates); (pits vestured); sieve tubes with non-dispersive protein bodies; (nodes also or 5 or more:5 or more); petiole anatomy very variable, often ± annular, etc.; (epidermis silicified); stomata various; leaves spiral, two-ranked or opposite, lamina vernation variable, venation pinnate, margins entire or single veins running into opaque persistent tooth, paired abaxial subbasal glands +/0 (also elsewhere), petioles often apically pulvinate, stipules (0), with axillary colleters; P/K (2-)3-6(-12), (connate); nectary ± annular (0), outside A; staminate flowers: A introrse; pistillode 0; carpellate flowers: staminodes 0; G [(2) 3(-many)], median member usu. abaxial, style (short), branched or not, stigmas prominent, often branched or with adaxial furrow, dry or wet; micropyle exo(bi)stomal, nucellar beak +, placental obturator +; exotegmen sclereids laterally flattened, oblique [Malpighian cells, "palisade"]; endosperm usu. copious, embryo chlorophyllous or not; n = (5-)9(-11+).

218[list]/6,745 - four groups below. Pantropical, also (cool) temperate (map: see Meusel et al. 1978, Canada not very accurate). [Photo - Flower, Flower, Fruit, Fruit.]

Age. Estimates for the crown group age of the family are ca 102 m.y. (van Ee et al. 2008) and (94.7-)89.9(-81.2) m.y. (Xi et al. 2012b; Table S7 - check).

Cheilosoideae

1. Cheilosoideae (Müller Arg.) K. Wurdack & Petra Hoffmann

Petioles pulvinate;; plant dioecious; C 0; staminate flowers: A 5-12; pollen echinate; carpellate flowers: style bifid; (G [2]), outer integument 8-10 cells across, inner integument 8-12 cells across; seeds not carunculate; testa vascularized, exotesta fleshy; endosperm +, ?embryo morphology; n = ?

2/7. Burma, Malesia (map: from van Welzen 1994).

Synonymy: Cheilosaceae Doweld

[Acalyphoideae [Crotonoideae + Euphorbioideae]]: (herbs, lianes); (diterpenoids, inc. phorbol esters +); (leaves opposite); plant monoecious or dioecious; C 0, 3-8; pistillode 0/+; outer integument 6-10 cells or so across; (fruit indehiscent), caruncle +/-.

Age. This node is around (90-)86.4(-81) m.y. (Xi et al. 2012b; Table S7, Acalypha + Suregada).

2. Acalyphoideae Beilschmied

(Herbs); (nodes 1:1 + split laterals); (lamina palmately compound); (venation palmate); (P one-trace); staminate flowers: A 2-many, (connate); (tapetum amoeboid), cells 2-4-nucleate; pollen grains (tricolpate), (inaperturate), etc., (tricellular); carpellate flowers: styles unbranched to multifid (Acalypha); (micropyle zig-zag), outer integument 3-6(-16) cells across, inner integument 3-24 cells across, nucellar cap ca 8 cells across [Micrococca], nucellar beak +/0, hypostase +, obturator +; (embryo sac tetrasporic, 12-16 celled - Penaea type); (testa vascularized), (outer 2 layers persistent), exotegmen radially elongated, palisade, slightly curved; (endosperm 5-10-ploid), cotyledons longer and broader than radicle; n = 9-12.

99/1865: Acalypha (430), Macaranga (260), Tragia (170), Dalechampia (120), Mallotus (115), Claoxylon (80), Bernardia (>50), Ditaxis (45). Pantropical.

Age. Crown-group Acalyphoideae may be (101.6-)92.6(-84.2) m.y.o. (Cervantes et al. 2016).

Synonymy: Acalyphaceae Menge, Mercurialaceae Berchtold & J. Presl, Trewiaceae Lindley.

[Crotonoideae + Euphorbioideae]: laticifers +; pollen grains (tricellular - ?level), (inaperturate).

3. Crotonoideae Beilschmied

(Herbs), (deciduous); cyanogenesis via the valine/isoleucine pathway; laticifers articulated or not; hairs often stellate or lepidote; (lamina palmate; abaxial paired lamina glands pale); (K connate), staminodes +, secretory, opposite P/K; staminate flowers: A 3-many, (connate), (filaments 0); pollen inaperturate, with supractectal processes attached to muri with short and irregular columellae [Croton-type pollen], or colpate, or porate; carpellate flowers: (G -20 - Hura); (micropyle endostomal), outer integument 4-8 cells across, inner integument (8-)18-25 cells across, nucellar beak +; micropylar megaspore functional; seeds arillate or not, often pachychalazal; (sarcotesta +), (exotesta palisade, endotestal cells ± palisade, thin-walled, slightly lignified), tegmen vascularized, exotegmen cells elongated periclinally, quite stout; (perisperm +, slight), (endosperm with chalazal haustorium); (100+ bp deletion in trnL-F spacer); n = (9-10) 11 (12, 14).

68/2050: Croton (1300+), Jatropha (180), Manihot (100), Trigonostemon (95), Cnidosculus (75). Pantropical, some warm temperate.

Synonymy: Crotonaceae J. Agardh

4. Euphorbioideae Beilschmied

Annual to perennial herbs, (thorny/spiny) stem succulents to trees; laticifers not articulated; (nodes 1:1); (starch grains much elaborated - Euphorbieae); monoecy common; (inflorescences pseudanthia; P 0; nectaries on inflorescence bracts - Euphorbieae); staminate flowers: A not covered by P, (extrorse); A 1-20(-80); (pollen grains tricellular); nectary 0; (G alt. with 3 P - Excoecaria); outer integument 3-6 or 8-22 cells across, inner integument 3-7(-22) cells across, parietal tissue 5-16 cells across, nucellar beak +/0, (postament +); testa (mucilaginous), (vascularized), tegmen (vascularized), (two layers of tegmic sclereids, fibres between); n = 6-11.

39/2810: Euphorbia (2420), Gymnanthes (45), Excoecaria (40), Mabea (40). Pantropical, extending (mostly Euphorbia) into temperate regions.

Synonymy: Bertyaceae J. Agardh, Hippomanaceae J. Agardh, Ricinaceae Martynov, Ricinocarpaceae Hurusawa, Tithymalaceae Ventenat, Tragiaceae Rafinesque

Evolution. Divergence & Distribution. A Mallotus/Macaranga-like plant has been found in deposits from New Zealand that are about 23 m.y. old - this clade is not currently known from the island (Lee et al. 2010).

Diversification within Acalyphoideae occurred within the last ca 70 m.y. (Davis et al. 2005a). Some estimates for the divergence of Macaranga and Mallotus are as early as (79.1-)63.8(-63.3) m.y.a., and Van Welzen et al. (2014a) suggested that the two showed general congruence in their dispersal patterns, crown group ages of the two being ca 32.7 and 34.3 m.y. respectively. The stem and crown group ages for the large genus Croton (Crotonoideae) are ca 55 and ca 40 m.y. respectively (van Ee et al. 2008).

Divergence within Euphorbieae may have begun (63.5-)48.9(-40.5) m.y.a. (Bruyns et al. 2011); see below for dates for divergence within the very speciose Euphorbia. There seems to be but a single origin of the distinctive cyathium that is an apomorphy for the genus (Park & Backlund 2002; Wurdack et al. 2005), and although it characterises a very species-rich clade, diversification may also be associated with the evolution of a variety of distinctive life forms, seed dispersal mechanisms, and CO2 concentrating mechanisms (see below). For fruit and seed morphology in subgenus Esula, see Pahlevani et al. (2015), and for the biogeographic implications of relationships in the genus, see e.g. Dorsey et al. (2013) and Riina et al (2013). Subgenus Chamaesyce has undergone notable diversification on Hawaii where trees growing in mesophytic forest have evolved (Y. Yang et al. 2009, 2012; Yang & Berry 2011b).

See Tokuoka (2007) for seed and ovule evolution.

Ecology & Physiology. "Euphorbiaceae", i.e. including Phyllanthaceae, Putranjivaceae, etc., are often the second most abundant family in tropical rainforests in South-East Asia and Africa (Gentry 1988); Euphorbiaceae s. str. are common in Amazonian forests and they have a disproportionally high number of the common species with stems at least 10 cm across (ter Steege et al. 2013).

Both growth patterns and carbon fixation pathways show much diversity in Euphorbia. Even Euphorbia s. str. (i.e. not including Chamaesyce, etc.) alone was extremely variable (Keller 1996), but with the inclusion of Chamaesyce and other segregate genera (e.g. Horn et al. 2009a, 2012) there is yet more diversity. Basic relationships within the genus are [Esula [Rhizanthium (= Athymalus) [Euphorbia + Chamaesyce]]] (for subgeneric names, see Bruyns et al. 2011, also below).

Diversification in Euphorbia is estimated to have begun over 42.5 m.y.a. (van Ee et al. 2008: subgenus Esula not included; see also Horn et al. (2012). Other estimates are (47.2-)36.6(-29.0) m.y.a. (Bruyns et al. 2011) and (54.7-)47.8(-41.0) m.y. (Horn et al. 2014, q.v. for more ages). Divergence within the largely succulent subgenera Athymalus and Euphorbia is rather more recent, (38.2-)28.1(-22) and (39.6-)29.9(-22.5) m.y. respectively, with much speciation in the latter subgenus in particular occuring within the last ca 13 m.y. or so (Bruyns et al. 2011).

The evolution of the annual habit and the cactiform growth form are associated with much speciation (Horn et al. 2009a, 2010b). The annual habit, common in Euphorbia subgenera Chamaesyce and Esula, has evolved eight times or more in subgenus Esula alone (Frajman & Schönswetter 2011; Riina et al. 2013; see also Peirson et al. 2014). Stem succulence in Euphorbia - some are quite massive stem succulents (see below: Vegetative Variation) - is associated with the evolution of a monopodial growth form and axillary inflorescences (Horn et al. 2012, 2014; see also Dorsey et al. 2013); these plants are cactus-analogues of drier areas throughout Africa and into India and even beyond (Steinmann & Porter 2002; Bruyns et al. 2006, 2011). Succulent species of Euphorbia are a particularly prominent component of the winter rainfall vegetation of the Succulent Karoo of south west Africa (Nyffeler & Eggli 2010b). Plants of subgenus Euphorbia in Madagascar that are chamaephytes, with tuberiform structures and succulent leaves, grow in the drier, but not particularly warmer, areas, although cactiform species surprisingly showed no particular environmental correlations there (Evans et al. 2014). Xeromorphism of one form or another has evolved ca 14 times in the genus (Horn et al. 2012). All told, some 850 species belonging to all four subgenera are succulents, and succulence has evolved ten times or so, and in subgenera Athymalus and Euphorbia the succulent habit is particularly common, both subgenera lacing annuals (Horn et al. 2010b; Bruyns et al. 2011; Morawetz & Riina 2011; Dorsey et al. 2013; see Eggli 2002 for an enumeration of taxa).

Most of the ca 350 species of subgenus Chamaesyce section Anisophyllum carry out C4 photosynthesis. This probably originated a single time here and section Anisophyllum is the largest C4 clade in the eudicots (Y. Yang & Berry 2011a; Yang et al. 2012; Horn et al. 2014). Some C4 species grow in the more arid parts of Africa and are also succulents. Species growing on Hawaii form a distinctive woody radiation and include some of the largest C4 plants anywhere, some being trees up to 9 m tall that grow in mesic forests (Pearcy & Troughton 1975; Robichaux & Pearcy 1984: see Winter 1981 for slightly larger C4 Chenopodioideae); Horn et al. (2012) discuss how the tree habit might evolve in a clade in which all branches are basically plagiotropic. This Hawaiian clade appears to have evolved from within a small clade of weedy annuals now found in Southern USA, Mexico, and the Caribbean (see also Yang et al. 2009); hybridisation is involved in their origin, and it is also known from elsewhere in the C4 clade (Yang & Berry 2011b).

The C4 clade, predominantly herbaceous, probably evolved in drier areas of North America, and it is sister to the small subsection Acutae from southwest North America which includes C4, C3, and C2 herbs, although only species with the two latter kinds of photosynthesis have been sequenced (Y. Yang & Berry 2011a, esp. b; Yang et al. 2012). T. Sage et al. (2011) described C2 photosynthesis in subsection Acutae, and they noted that E. angusta, with C3 photosynthesis, had some anatomical similarities with C2 and C4 taxa. Horn et al. (2012) emphasize that it is not simply the evolution of the C4 pathway, but also the adoption of a plagiotropic branching habit, etc., that may have made this clade successful, as well as its movement from the Old to the New World (see also Yang & Berry 2011b).

Given the prevalence of succulence in Euphorbia and its association with drier habitats, it is not surprising that CAM is also quite common. Horn et al. (2014) looked at diversification in the genus in the context of CO2 concentration mechanisms, and found that perhaps 7 of the at least 17 independent acquisitions of CAM photosynthesi (five in Africa-Madagascar) and the single acquisition of C4 photosynthesis showed increased diversification rates. The former changes occured in the context of drying climates after the Mid-Miocene ca 14 m.y.a. (estimates of the crown ages of the clades are (15.9-)11, 5.6(-2.5) m.y.a.) and ancestors of these CAM clades were more or less woody plants, and in the Old World they had axillary inflorescences (Horn et al. 2014). The origin of C4 photosynthesis may have been somewhat earlier, the crown age being (20.2-)15.3(-10.5) m.y.a., and aridity may not have been a driver (Horn et al. 2014), however, estimates of the age of origin of the pathway vary, some being as recent as (13.1-)10.4(-7.3) m.y. (Christin et al. 2011b).

All 28 species of Cuban Leucocroton (= Croton s.l.) are reported to accumulate nickel (Reeves et al. 1996).

Pollination Biology & Seed Dispersal. Flowers of Euphorbiaceae are generally small, and pseudanthia have originated more than once (and also in Peraceae), and in Dalechampia and some species of Euphorbia inflorescence bracts may be very large and brightly coloured. Euphorbia, with some 2,400+ species, is by far the biggest clade with pseudanthia (= cyathia). Cyathia are surrounded by bract-like structures that vary considerably in shape and colour, and some or all of these also have conspicuous nectaries. Several species of oligolectic pollinators may visit a single species of Euphorbia, overall, there may be hundreds of species of insect visitors (Ehrenfeld 1979). New World species of Euphorbia that used to be segregated as Pedilanthus (= Euphorbia subg. Euphorbia sect. Crepidaria) have distinctive red, spurred, monosymmetric cyathia pollinated by birds, a "key innovation" (Cacho et al. 2010). The jury is out, but there aren't many species in this clade...

The ca 115 species of Dalechampia (Acalyphoideae) also have remarkable pseudanthia which have evolved independently of thos of Euphorbia. Here female megachilid, euglossine and stingless Trigona (meliponine) bees visit the "flowers" for triterpenoid resins that they use to build their nests (resin is a very uncommon reward in flowering plants, see Armbruster 1984, 1993, 1996); a few male euglossines collect fragrances. The resin has secondarily become used for defence in some species of Dalechampia, probably its original fuction, and there is a reversal in the arrangement of the staminate flowers (Armbruster et al. 2009b). In some Madagascan Dalechampia there is buzz pollination (linked to paedomorphy), itself derived from generalized pollination, in turn derived from resin flowers - and perhaps generalized pollination is derived from buzz pollination, although the former may have but a single origin (c.f. support values: Armbruster et al. 2013a).

Pollination by thrips (Thysanoptera) is particularly common in myrmecophytic species of Macaranga (Fiala et al. 2011); 24/29 species may be so pollinated, based on floral morphology, about double the frequency when compared with non-myrmecophytic species of the genus growing in the West Malesian localities that Fiala et al. visited.

Interfloral protogyny is common in Euphorbiaceae, perhaps associated with the fact that female flowers are often borne towards the base of the infloreacence, and so might be expected to open first (see Bertin & Newman 1993).

Seed dispersal is initially usually by the explosion of the capsule, the seeds being hurled quite some distance - in Hura crepitans, the sand-box tree, the seed has an escape velocity of up to 252 kph and it is hurled up to 45 m (Swaine & Beer 1977). In addition, some seeds have nutritive elaiosomes (e.g. Rössler 1943) which facilitate further local dispersal of the seeds, especially by ants. Around 2,300 species in the family, especially in Euphorbia, are likely to be myrmecochorous (Lengyel et al. 2010). Elaiosomes of one sort or another have evolved ca 13 times in Euphorbia (Horn et al. 2012), and include many of the ca 480 species of subgenus Esula (Riina et al. 2013, see also Peirson et al. 2014 for photographs). A number of species of Euphorbia subgenus Chamaesyce section Anisophyllum in particular have a testa that becomes mucilaginous when wetted (Grubert 1974; Jordan & Hayden 1992).

Plant-Animal Interactions. Caterpillars of nymphalid butterflies are quite common on Euphorbiaceae (Ehrlich & Raven 1964), e.g. caterpillars of the ca 340 species of Biblidinae are found on Dalechampia and Tragia (Euphorbioideae: DeVries 1987; Wahlberg et al. 2009; Nylin et al. 2014). Caterpillars of the spectacular Uraniinae moths are found on Endospermum, Omphalea and Suregada, also Euphorbioideae, throughout the tropics (Lees & Smith 1991); the first two are rather closely related, the position of the last is unclear (Wurdack et al. 2005). It would be interesting in this context to clarify both Euphorbiaceae phylogeny and Uraniinae host plant preferences.

In Malesia about 29 species of fast-growing, large-leaved Macaranga are ecological analogues of the New World Cecropia (Urticaceae); for a phylogeny, see Bänfer et al. (2006) and also Blattner et al. (2001) and Davies et al. (2001: mymecophily perhaps evolved more than once, but support values low). Food bodies (Beccarian bodies) and extra-floral nectaries provide food for ants (Camponotus and especially Crematogaster spp.) that have an obligate association with the plants, living in their stems which are either hollowed out by the ant or become hollow as the stem ages; myrmecophytism seems to have evolved more than once here (Hatada et al. 2001 for references; Feldhaar 2003a, b). A whole complex of adaptations in Macaranga is involved, for instance, whether the stems are waxy, or not (not all ants can run up waxy stems), whether the food bodies on the stipules are exposed or protected, and whether or not there are extrafloral nectaries on the lamina margins, and these are variously correlated (Federle & Rheindt 2005). The age of the association with Crematogaster subg. Decacraema was estimated at less than 7 m.y., and suggested co-speciation of the two partners (Itino et al. 2001b; see de Vienne et el. 2013), although the aging of the association was rather vague; Itino et al. (2001a and references) thought that an association with coccids, which also provide carbohydrates for the ants, represented the original condition for the ant-plant association. On the other hand, Ueda et al. (2008) offered an age of 20-16 m.y. for the ant-plant association (see also Chomicki & Renner 2015), the association with Coccus scale insects being only 9-7 m.y. old. Other organisms are involved in this association. These include bacteria that live off material in colony rubbish dumps in M. bancana, for example, that are in turn eaten by rhabditid nematodes that are possibly in turn eaten by the ants; nematodes (?and bacteria) may move from colony to colony with the queen ants (Maschwitz et al. 2016). Arhopala (a lycaenid) caterpillars may be found in the domatia, and they eat ant larvae but are not attacked by the ants, rather, the products of a tentacle-like gland that is extruded by the caterpillar calm the ants (Maschwitz et al. 1984).

Bacterial/Fungal Associations. Although latex might a priori seem to protect the plant in some way, a diversity of bacteria and fungi (mean: 44 and 21 species repectively) were found growing in latex of cultivated Euphorbia (Gunawardana et al. 2015). Perhaps some of these were endophytes, but between-species variation was great (up to seven fold), and what is actually going on in this system is unclear.

Complex maytansinoids, ansamycin antibiotics, that are likely to be synthesized by fungal endophytes or other plant associates, are found in Trewia (Acalyphoideae: Cassady et al. 2004 for references). The fungus Uromyces pisi causes Euphorbia cyparissias to form nectar-producing pseudoflowers that facilitate transmission of the fungus spermatia (Pfunder & Roy 2000).

Vegetative Variation. Succulence in Euphorbia is of various types. The plants may have variously articulated or simply pencil-like stems, the latter as in some species of subgenus Chamaesyce, or they may be medusoid, with relatively slender but succulent branches radiating from a stout central axis. The plants may also be spiny in various ways. Thus in subgenus Euphorbia there are spine shields, there are also stipular spines, as well as spines in the stipular position that are not actually vascularized, and branched or simple thorns, which may also do duty as inflorescences (see e.g. Park & Jansen 2007; Carter 2002, esp. illustrations; Bruyns 2010). Bruyns et al. (2011) describe in detail the different forms of stem succulence found in the genus, and they note that in a number of species of subgenus Euphorbia the branches become permanently differentiated; orthotropic axes will not develop from plagiotropic branches.

The whole plant body of some species of Euphorbia-Chamaesyce-Anisophyllum can be compared with the inflorescence of other species of the genus. The seedling apex aborts after the production of a single pair of leaves, and several axillary shoots showing complex determinate and unequal branching patterns produce the adult plant (Hayden 1988).

Genes & Genomes. The diterpenoid-synthesizing genes form a cluster - except in Manihot (King et al. 2014). A genome duplication in that genus has been dated at (42.1-)40.4(-38.7) m.y.o. (Vanneste et al. (2014a).

Chemistry, Morphology, etc. Phorbol esters in the [Crotonoideae + Euphorbioideae] clade in particular are very diverse; for the biosynthesis of these and other diterpenes, see King et al. (2014). Cyanogens can be derived from nicotinic acid or valine/isoleucine (Seigler 1994). Latex and cocarcinogens are both apparently restricted to Euphorbioideae and Crotonoideae; for the composition of Euphorbia latex, see references in Gunawardana et al. (2015). Distinctive fatty acids in the seed oils are quite common in the family (Badami & Patil 1981); for lectins, see Vandenborre et al. (2011).

The thickness of first-order roots in the family ranges from 1009.6 μm in Endospermum chinense to 72.6 μm in Macaranga sampsonii, spanning the extremes of the measurements made on 96 species from southern China (Kong et al. 2014). Laticifers in Euphorbiaceae are discussed by Rudall (1987, 1994a) and Wiedenhoft et al. (2009); see also Vitarelli et al. (2015) and the cautionary comments in Wurdack et al. (2005). Biesboer and Mahlberg (1981) describe the complex morphology of the starch grains found in the latex of Euphorbia and laticifer evolution there. Prismatic crystals in wood parenchyma and/or ray cells are common, but these also occur in Putranjivaceae and Picrodendraceae, which used to be included in Euphorbiaceae s.l. (Hayden 1994). Stipules may be lacking in species of Euphorbia subgenus Esula (Riina et al. 2013), and 1:1 nodes have been reported from the genus (Sehgal & Paliwal 1974: also somewhat improbable 2:2 nodes). Claoxylon has distinctively rough leaves when dry because of the styloids in their tissues (Kabouw et al. 2008). Vitarelli et al. (2015) discuss the considerable variety of foliar secretory structures in Croton and its near relatives. In addition to recording colleters, the paired basal glands on the lamina (the two have some underlying similarities), etc., they suggest relationships between cells in the lamina filled with secretions ("idioblasts") and short secretory trichomes, whose occurrence is mutually exclusive, and in both of which the secretion is some kind of lipid. Extending the survey would be good... Feio et al. (2016) examine the variety of secretory structures in other species of the genus, i.a. recording colleters from inside the flower.

The cyathium of Euphorbia is best interpreted as a modified cymose inflorescence with a single, terminal, carpellate flower (see the basically similar arrangement in Jatropha, etc.). Details of its development are provided by Prenner and Rudall (2007), and although they thought that the morphological nature of both the cyathial glands and the petal-like bracts surrounding the cyathium was unclear (see also Hoppe 1985 and Prenner et al. 2008b), the glands, at least, may be modified commissural stipules (Steinmann & Porter 2002) or derived from involucral bracts (Gagliardi et al. 2016), not necessarily different ideas. "Floral" genes may be expressed in the cyathium as a whole (Prenner et al. 2011).

Vascularization of the ?staminodial nectary in Croton and its near relatives varies; a secretory staminodial nectary may be a high-level apomorphy around there (De-Paula et al. 2011), but it can be difficult to understand possible homologies of floral structures in Astraea (= Croton s.l.: c.f. De-Paula et al. 2011). Prenner et al. (2008a) described the development of the distinctive androecium of Ricinus with its branched stamens; these are not cauline as had been suggested. Some Euphorbiaceae are reported to have two vascular traces supplying each ovule (Venkata Rao & Ramalkshmi 1967). Johri and Kapil (1953) noted that the vascular tissue in ovules of Acalypha indica proceeded one third the way up the nucellus. The projecting nucellus in Codiaeum variegatum, at least, seems to result from periclinal divisions of the epidermal layer of the nucellus, the nucellar cap, although in Euphorbia less striking projections seem to be the result of divisions of the underlying nucellar cells (Bor & Kapil 1975 and references). Mennega (1990) suggested that the subdermal initiation of the inner integument separated Euphorbiaceae from other families.

Van Welzen (1994) described Neoscortechinia (Cheilosoideae) as having a thin, red aril, but no aril was mentioned by Tokuoka and Tobe (2003) or Tokuoka (2007).

For general information on Euphorbiaceae, see Webster (1967, 1994a, b - also other papers in Ann. Missouri Bot. Gard. 81. 1994 - and 2013), Radcliffe-Smith and Esser (2001: generic descriptions, etc.), Esser (2001), and Eggli (2002: succulent species), while Hegnauer (1966, 1989), Evans and Taylor (1983: phorbol esters), Jury et al. (1987), Beutler et al. (1989, 1996) discuss chemistry. see also Hayden and Hayden (2000: wood anatomy of Acalyphoideae), Westra and Koek-Noorman (2004: wood end-grain), Mennega (2005: wood anatomy of Euphorbioideae), Cervantes et al. (2009: leaf anatomy of some Acalyphoideae), Fiser Pecnikar et al. (2012: leaf anatomy of Mallotus and relatives) and Maity (2014: split laterals in Mallotus). See also Tokuoka and Tobe (1993: general embryology); for embryology, ovules and seeds in Crotonoideae, see Rao (1976) and Tokuoka and Tobe (1998), in Euphorbioideae, Pammel (1892), Venkateswarlu and Rao (1975), Bor and Bouman (1975), Tokuoka and Tobe 2002), in Acalyphoideae, Kapil (1960) Nair and Abraham (1963), and Tokuoka and Tobe (2003), and in general, see Schweiger (1905) and Landes (1946). See Merino Sutter and Endress (1995: floral morphology), De-Paula and Sajo (2011: anthers and ovules in Croton), Singh (1969), and Stuppy (1996), both seed anatomy. For pollen morphology of Crotonoideae in particular, see Lobreau-Callen et al. (2000), for that of Acalyphoideae s.l., see Nowicke and Takahashi (2002) and references, for that of Acalypha, see Sagun et al. (2006), for that of Plukenetieae and Euphorbieae, see Suárez-Cerbera et al. (2001), for that of Euphorbioideae, see Park and Lee (2013: Pimeleodendron, etc., distinct), and also Matomoro-Vidal et al. (2015: function). See Hans (1973) for chromosomes.

Phylogeny. Neoscortechinia and Cheilosa are strongly supported as being sister to the rest of the family (Wurdack et al. 2005; Tokuoka 2007; Xi et al. 2012b). "There is no support for a monophyletic Crotonoideae s.l. Instead, there are four distinct lineages (Adenoclineae s.l., Gelonieae, and articulated and inaperturate crotonoids)" (Wurdack et al. 2005: p. 1413) sums up the major problem along the spine of the family, indeed, Tokuoka (2007) found that Adenoclineae and Gelonieae, with a thinner outer integument and unvascularized testa and tegmen, formed a paraphyletic grade at the base of the family (minus Chelisioideae), albeit this topology had little support. Crotonoideae were monophyletic, again with little support, Acalyphoideae and Euphorbiacaeae were monophyletic, but with more support (Tokuoka 2007).

There are number of distinctive features in the Crotonoideae as broadly construed, but there is as yet no strong evidence that the subfamily is monophyletic (see the C1-5 clades in the tree above, the C1-2 clades are the same as in Wurdack et al. 2005). Many features in the subfamilial characterization above are synapomorphies either for individual clades or groups within them; for indtance the trnL-F spacer deletion is a feature of part of Crotonoideae s. str.. Crotonoideae s. str., the C1-2 clades, may expand from this minimalist circumscription as details of phylogenetic relationships are clarified, and for the most part they have petals, distinctive inaperturate pollen with supratectal processes ("crotonoid pollen"), and the tegmen is usually vascularized. The pollen of Suregada (Crotonoideae: C1 clade) is pantoporate and it also lacks columellae. The large genus Croton is being actively studied by Berry and collaborators (see Berry et al. 2005; van Ee et al. 2008, 2011, 2015; van Ee & Berry 2009; Riina et al. 2009, 2010; Caruzo et al. 2011 for phylogenies, dates, biogeography, and more).

Although Acalyphoideae in the old sense are paraphyletic, the great bulk of the subfamily is included in a strongly-supported clade, Acalyphoideae s. str., and Cervantes et al. (2016) suggest that Erismanthus is sister to all other Acalyphoideae examined. Several tribes are para- or polyphyletic as currently delimited, perhaps most notably Acalypheae, members of which are in six clades in the tree recovered by Cervantes et al. (2016). Wurdack et al. (2005) discuss groupings in the subfamily in some detail. Slik et al. (2001: morphology), Sierra et al. (2006, 2010 and references [the latter with symmetric resampling values and both qualitative and quantitative variation used]), Kulju et al. (2007a, b) and van Welzen et al. (2014a) evaluate the phylogeny of the Macaranga-Mallotus complex ("Acalypheae"); there are three main clades, and in Mallotus s. str. in particular some small, segregate genera are embedded. Cardinal-McTeague and Gillespie (2016) looked at relationships within the monophyletic Plukenetieae (not so much at Dalechampia, for which see Armbruster et al. 2013a, esp. 2009b), where Tragia in particular was found to be very para/polyphyletic; there was not that much correlation between phylogeny and pollen morphology.

Within Euphorbioideae, Stomatocalyceae may be sister to the rest; they often have extrorse anthers and the testa is at least sometimes vascularized. For a phylogeny of Euphorbia, see Molero et al. (2002: Macaronesian taxa), Bruyns et al. (2006), Park and Jansen (2007), Zimmermann et al. (2010) and Wurdack et al. (2011). The last three authors found that subgenus Esula was sister to the other subgenera, although not always with very strong support - relationships are [Esula [Rhizanthium (= Athymalus) [Euphorbia + Chamaesyce]]] (see also the extensive study by Bruyns et al. 2011; Horn et al. 2012). Sampling was initially poor, however, this has steadily improved. Some characters are particularly common/important within the subgenera, although there is very extensive homoplasy. A few of the major characters are [Esula (annuals, cyathium with 4 glands) [Athymalus (cyathium with 5 glands, inflorescences sometimes lateral, plants succulents) [Euphorbia (inflorescences often lateral, plants succulents) + Chamaesyce (annuals, C4 photosynthesis, leaves often opposite)]]] (Horn et al. 2012, q.v. for references and many more details).

For relationships in the leafy Euphorbia subgenus Esula in particular, with a considerable number of north temperate taxa, see Frajman and Schönswetter (2011) and Riina et al. (2013); the position of E. lathyris is unclear, but it may be sister to the rest of the subgenus. See also the summary in Geltman et al. (2011) and the study or relationships in the New World section Tithymalus by Peirson et al. (2014). For relationships in the Old World subgenus Athymalus, in which the only Malagasy species, E. antso, is sister to the rest, see Morawetz and Riina (2011) and Peirson et al. (2013). For relationships in the mostly New World subgenus Chamaesyce, see Y. Yang and Berry (2007, 2011) and Yang et al. (2012), and for those in the large subgenus Euphorbia, see Dorsey et al. (2011, 2013). See also above for cyathia, growth forms, succulence, thorns and spines, and photosynthetic pathways.

Classification. For a comprehensive checklist and bibliography of the family, now dated, see Govaerts et al. (2000). Wurdack et al. (2005) discuss morphology, groupings and relationships in the family in considerable detail.

Cardinal-McTeague and Gillespie (2016) discuss generic limits in Acalyphoideae-Plukenetieae and Kulju et al. (2007a) and Sierra et al. (2007) those in the Macaranga-Mallotus area, and for an outline of the classification of the speciose Macaranga, see Whitmore (2008). For a sectional classification of Croton, see van Ee et al. (2011, 2015: Australian sections). For information on Euphorbia, see EuphORBia (Esser et al. 2009) and there is a developing inventory, etc., of the genus, at Tolkin (Riina & Berry 2012), but not if you use Internet Explorer only... Euphorbia is best broadly circumscribed, so including the whole of the Euphorbiinae of Webster (1994b), i.e. genera like Chamaesyce, Pedilanthus, Monadenium, Synadenium, etc., and is well characterized by its cyathium (e.g. Bruyns 2010 and references); Y. Yang et al. (2012) provide a classification of Euphorbia subgenus Chamaesyce, Riina et al. (2013) that of subgenus Esula, Dorsey et al. (2013) that of subgenus Euphorbia, and Peirson et al. (2013) of subgenus Athymalus.

Previous Relationships. Cronquist's Euphorbiales included Simmondsiaceae (Caryophyllales here), Pandaceae (elsewhere in Malpighiales) and Buxaceae (Buxales), whilst Takhtajan's (1997) Euphorbianae included Pandaceae and Dichapetalaceae (elsewhere in Malpighiales), as well as Thymelaeaceae (Malvales) and Aextoxicaceae (Berberidopsidales), but these groups clearly have little to recommend them.

Botanical Trivia. Croton has got nothing to do with the cultivated croton, which is Codiaeum.

Thanks. I am grateful to Hajo Esser for comments and to Ken Wurdack for help with the generic synonymy.

[[Phyllanthaceae + Picrodendraceae] [Ixonanthaceae + Linaceae]]: stomata paracytic; ovules 2/carpel.

Age. Estimates of the age of this node are (108.6-)102.5(-94.8) m.y. (Xi et al. 2012b; Table S7).

[Phyllanthaceae + Picrodendraceae] / Phyllanthoids: Lamina margins entire; flowers small; anthers extrorse (introrse); micropyle bistomal, parietal tissue 10 or more cells across, obturator +, nucellar beak + [= parietal tissue protruding through micropyle]; fruit with outer layer often separating from the woody layer, valves falling off, central column persistent; endosperm copious; x = 13.

Age. Estimates for the age of this node are (101.6-)94(-86.5) m.y. (Xi et al. 2012b; Table S7), ca 94.8 m.y. (Tank et al. 2015: table S2), or the Cretaceous-Albian 111-100 m.y.a. or a little later - (114.0-)108.1(-105.8)/(101.9-)97.1(-95.6) m.y.a. (Davis et al. 2005a).

Evolution. Divergence & Distribution. Merino Sutter et al. (2006) suggest additional possible similarities between the two families.

Chemistry, Morphology, etc. Pre-2005 references to Euphorbiaceae may contain information about this clade. For general information, see Webster (1994a, b, 2013), see also Radcliffe-Smith and Esser (2001: description of genera), Hegnauer (1966, 1989) and Jury et al. (1987), all chemistry, see also Schweiger (1905: ovules and seeds).

Phylogeny. The clade [Phyllanthaceae + Picrodendraceae] had only very slight support in a rbcL analysis, although the two families have morphological similarities (Wurdack et al. 2004). Support is stronger (75% bootstrap, 1.0 posterior probablility) in a recent 4-gene analysis (Davis et al. 2005a; see also Tokuoka & Tobe 2006; Korotkova et al. 2009) and even stronger in Soltis et al. (2011). Thus the two are probably sister taxa.

PHYLLANTHACEAE Martynov   Back to Malpighiales

Phyllanthaceae

Trees, shrubs, (deciduous), (herbs); (plants Al accumulators); cyanogenesis via the tyrosine pathway, tropane, piperidine and pyrrolizidine alkaloids, cucurbitacins [triterpenes], nonhydrolysable tannins [geraniin] +, ellagic acid 0; cork?; (axial parenchyma 0); (mucilage cells [epidermis] +); (stomata anisocytic); lamina vernation involute or conduplicate; (plant dioecious); K 2-8(-12), often basally connate, C (0, 3-)5(-9), (small); nectary extrastaminal, ± annular and/or variously lobed, (0, central); staminate flowers: A 2-35; pollen surface reticulate; (pistillode +); carpellate flowers: (staminodes +); G 1,[2-5(-15)], styles usu. bifid, stigmas with adaxial furrow, wet; ovules with outer integument 2-many cells across, inner integument 2-3(-10) cells across, placental obturator +; fruit a septicidal capsule/schizocarp; seeds large; (vascular bundles in testa), tegmen 2-5(-20) cells thick, exotegmic cells (radially-elongated), ribbon-like; (endosperm 0), (embryo chlorophyllous); n = (6-9, 11, 14).

59[list]/2330. Pantropical, but esp. Malesia, some temperate (map: from Webster 1970, 1984, 1994a, etc.; Wickens 1976; Frankenberg & Klaus 1980; FloraBase 1.2011 - note, as of xii.2012 similar, but very different from Australia's Virtual Herbarium; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006). Two subfamilies below. [Photo - Flower.]

Age. Estimates for the crown group age of the family are (93.7-)81.2(-58.8) m.y. (Xi et al. 2012b; Table S7).

1. Phyllanthoideae Beilschmied

(Plant monopodial), growth continuous; vessel elements with simple ["Glochidion"] perforation plates; (nodes 1:1); leaves on orthotropic axes reduced, spiral, on plagiotropic axes two-ranked; plant mon- or dioecious; inflorescence fasciculate; staminate flowers: A distinct to connate; pollen (to 16-colporate), (colpi diploporate), (inaperturate), (surface spiny - Croizatia); carpellate flowers: G [2-6(-15)]; (ovules hemitropous); (fruit indehiscent); (embryo curved), (cotyledons ± plicate).

38/1680: Phyllanthus s.l. (1270), Cleistanthus (140), Bridelia (50). Tropical to Temperate.

Synonymy: Porantheraceae Hurusawa

2. Antidesmatoideae Hurusawa

Plant growth rhythmic; (pits vestured - Bridelieae); (sieve tubes with non-dispersive protein bodies - Bischofia); vessel elements with scalariform [Aporosa] perforation plates; epidermal cells tanniniferous; leaves spiral, (trifoliolate, margins toothed, teeth deciduous - Bischofia), petiole pulvinate apically; plant dioecious (monoecious); inflorescence with axis; C often 0; staminate flowers: (A connate basally); tapetal cells 2-3-nucleate; carpellate flowers: G 1[2-5], (stigma plumose); fruit often indehiscent; (seeds carunculate - Celianella).

21/451: Antidesma (150), Aporosa (90), Uapaca (60), Baccaurea (50). Tropics and subtropics.

Synonymy: Antidesmataceae Loudon, Aporosaceae Planchon, Bischofiaceae Airy Shaw, Hymenocardiaceae Airy Shaw, Scepaceae Lindley, Stilaginaceae C. Agardh, Uapacaceae Airy Shaw

Evolution. Divergence & Distribution. Lachnostylis (Phyllanthoideae), a small Cape genus, seems to be a relict element there, being dated to as much as 97 m.y.a. (Warren & Hawkins 2006), while the distribution of the Baccaurea group (Antidesmatoideae) may initially have been affected by drift events ca 80 m.y.a. (Haegens 2000); these clade ages should be re-examined. Phyllantheae (Flueggea, Glochidion, etc.) are dated to around 51.8 m.y. (van Welzen et al. 2015). For the possible (post-)Miocene E->W dispersal of Bridelia across the Indian ocean, see Li et al. (2009), and for diversification of Breynia s. str., with around 85 species, perhaps linked with pollination mode (Epicephala moths) and limestone habitats, see van Welzen et al. (2015).

Ecology & Physiology. 18/37 species (and one hybrid) of Cuban Phyllanthus growing on serpentine soils are reported to accumulate nickel, while in New Caledonia 14/76 species tested are accumulators (there are some 110 species on that island - see Reeves et al. 1996; Brooks 1998). Phyllanthus balgooyi, growing on ultramafic rock in Sabah, Malaysia, has around 16% by weight of nickel in its phloem sap, the second highest concentration known in angiosperms; normally nickel is found in the epidermis when it accumulates (Mesjasz-Przbylowicz et al. 2016).

Uapaca can locally dominate the vegetation in eastern Madagascar, while on the African mainland it is often a component of Detarieae-dominated woodlands and savannas (White 1983). It is an early successional species in the latter habitat, and acts almost a a nurse tree to other ectomycorrhizal species, all having similar mycorrhizal fungi (Högberg & Piearce 1986; see also Ducousso et al. 2008).

Pollination Biology. Pollination mutualisms involve the moth Epicephala (Gracillariidae) in some 500+ species of Breynia sect. Breynia and Glochidion (Kato et al. 2003; Kawakita & Kato 2004a, b, 2006; Kawakita et al. 2004; Svensson et al. 2010); the plants involved are all part of Phyllanthus s.l. (see below). Flowers in which the moth lays eggs may lose all their seeds to the growing caterpillars, but the moth pollinates more flowers than those on which it oviposits. This mutualism seems to have evolved several times, perhaps some time after the initial divergence of the clades in which mutualisms are found - 55.2-33.4 m.y.a. (plant) versus 35-20 m.y. (moth) ago - and it has also been lost (Kawakita & Kato 2009; Kawakita 2010). Ages seem to be in a bit of a muddle (or I am), crown-group Glochidion being only (13-)5.6(-1.6) m.y.o. (van Welzen et al. 2015; q.v. for discussion; ?sampling). Interestingly, Phyllanthus s.l. has speciated on the high islands of southeastern Polynesia, probably mostly within the last 5 m.y. (Hembry et al. 2013). Any phylogenetic congruence between moth and plant appears to break down rather comprehensively here (Hembry et al. 2013), host shifts, not straight coevolution=cospeciation being involved, and different species of plants can share the same pollinator, or a single species of plant may be pollinated by more than one species of moth (Hembry 2015). Two species of Epicephala moths pollinated two species of Phyllanthus in southern China, and the species of Phyllanthus may be sister taxa but the two moths are not (diffuse coevolution: J. Zhang et al. 2012). The system is complex: Male and female flowers may produce different scents, and female flowers may even change their scent after pollination, perhaps to avoid other visits of the moth and the consequent possible loss of all their seeds to caterpillars (Svensson & Okamoto 2015). Aside from all this, one wonders how both plant and pollinator are able to get from island to island together.

Bacterial/Fungal Associations. The ectomycorrhizal fungi of Uapaca group with those from Fabaceae (Högberg & Piearce 1986; Tedersoo et al. 2014a), perhaps reflecting the fact that the two may grow in the same communities. ECM and arbuscular mycorrhizae may occur together (Ba et al. 2012).

Vegetative Variation. Phyllanthoid branching occurs in many, but not all, species of Phyllanthus s.l. (Kathriarachchi et al. 2006). The orthotropic axes have reduced, spirally-arranged leaves and the plagiotropic axes usually have two-ranked, photosynthetic leaves and flowers in the axils of those leaves. The plagiotropic axes are often of more or less limited growth, and those of P. acidus, for example, are short-lived and lack flowers, so being the functional equivalent of compound leaves; the flowers themselves are borne on short branches lacking photosynthetic leaves and which arise from separate axillary buds on the main axes. Some Caribbean species are yet more modified. Thus the plagiotropic lateral branches of P. epiphyllanthus bear 2-ranked cladodes, each in turn bearing flowers and fruits in 2-ranks in the axils of reduced scale-like leaves.

Chemistry, Morphology, etc. The only record of cocarcinogens is from one species of Antidesma (Beuteler et al. 1989). Wood anatomy is variable (Hayden & Brandt 1984) and the nodes are quite often unilacunar (Thakur & Patil 2002).

The inflorescence of Uapaca is a pseudanthium. The pollen is very variable in Phyllanthus in particular (Webster 1956). The outer integument is variable in thickness. The fruit type of the ancestor of Phyllanthaceae is unclear (Kathriarachchi et al. 2005). The exotegmen is most often described as being ribbon-like or tracheoidal. However, Hymenocardieae (Didymocistus, Hymenocardium) have a collapsed tracheoidal exotegmen and large tanniniferous endotegmic cells; do they belong here (Tokuoka & Tobe 2001)? - yes, say Wurdack et al. (2004) and Kathriarachchi et al. (2005).

For additional information, see Radcliffe-Smith and Esser (2001) and Webster (2013), both general, also León Enriquez et al. (2008: architectural variation), Mennega (1987: wood anatomy), Westra and Koek-Noorman (2004: wood end-grain), Levin (1986: leaves), Schweiger (1905: ovules), Tokuoka and Tobe (2001: ovules and seeds), Z.-G. Zhang et al. (2012: floral morphology of Phyllanthus) and Hans (1973: chromosomes). For pollen, see Köhler (1965), Webster and Carpenter (2008) and Chen et al. (2009), both Phyllanthus, and Sagun and van der Ham (2003: Flueggeinae), also Matomoro-Vidal et al. (2015). For a monograph of Baccaurea and relatives, see Haegens (2000), and of Aporosa, see Schot (2004).

Phylogeny. Wurdack et al. (2004: also morphology), and Samuel et al. (2005: two gene analysis) discuss general phylogenetic relationships. Kathriarachchi et al. (2005: five-genes; see also Hoffmann et al. 2006; Xi et al. 2012b) divide the family into two main clades, one largely with fasciculate inflorescences (it includes Lingelsheimia, sometimes previously associated with Putranjivaceae, and Dicoelia, ditto with Pandaceae), see Phyllanthoideae above, and the other (including Hymenocardieae) tanniniferous, see Antidesmatoideae above (see also Xi et al. 2014b). Croizatia has previously been associated with genera included in Picrodendraceae, although it differs in several morphological features; it is here placed in Phyllanthaceae (see Wurdack et al. 2004; Wurdack 2008)

For the phylogeny of the Phyllanthus area, see Kathriarachchi et al. (2006), Lorence and Wagner (2011), and Pruesapan et al. (2008, 2012), for that of Poranthereae, see Voronstova et al. (2007). Cleistanthus is polyphyletic (Li et al. 2009).

Classification. Govaerts et al. (2000: as Euphorbiaceae) provide a checklist and bibliography, but this is now dated - e.g. see Vorontsova and Hoffmann (2008) for genera in Phyllanthoideae-Poranthereae, while Hoffmann et al. (2006) provide the phylogenetic classification followed here.

The limits of Cleistanthus will have to be adjusted, and most species will need a new name (Li et al. 2009), while the large genus Phyllanthus is paraphyletic, and I would broaden it to include Glochidion (some 300 species), Breynia, Sauropus (70 spp.), etc. (Kathriarachchi et al. 2006; Lorence & Wagner 2011; c.f. Pruesapan et al. 2008, 2012; van Welzen et al. 2014b). However, phylogenetic relationships are still not well enough understood to make the needed changes.

Previous Relationships. Phyllanthaceae include most of the old Euphorbiaceae-Phyllanthoideae, minus Drypetes and relatives, for which see Putranjivaceae.

PICRODENDRACEAE Small, nom. cons.   Back to Malpighiales

Picrodendraceae

Trees or shrubs; picrotoxanes +, otherwise chemistry?; cork?; mucilage cells [epidermis] + (0); subsidiary cells piggy back [on top of guard cells]; hairs unicellular or unbranched-uniseriate; leaves spiral, stipules petiolar, cauline, with axillary colleters, or 0; plant dioecious; staminate flowers: P 4; A 4; pollen oblate, echinate to verrucose; nectary between or inside A; pistillode +/0; carpellate flowers: ?staminodes; P (3-)4-8(-13); G (2-)3(-5), (style +), stigmas stout, entire, sometimes swollen, dry (wet); ovule with outer integument 5-6 cells across, inner integument 3-6 cells across, nucellar cap +, (nucellar beak +), hypostase +, funicular obturator +, with hairs; (fruit indehiscent); seeds carunculate (caruncle 0), vascular bundle branching in chalaza; exotegmic cells cuboid or fibrous.

24[list]/96 - three groups below. Mostly tropical (map: from Webster 1994a; van Welzen & Forster 2011; FloraBase i.2012 - approximate). [Photo - Picrodendron Fruit © A. Gentry.]

Age. Estimates for the age of crown-group Picrodendraceae are (92.9-)78(-72) m.y. (Xi et al. 2012b; Table S7).

1. Podocalyceae G. L. Webster

Vessel element perforations various; petiole thickened at both ends; stomata anomocytic; staminate flowers sessile, in clusters; pollen 4 zoniporate.

1/1. Podocalyx loranthoides. Amazonia.

[Caletieae + Picrodendreae]: vessel elements with simple perforation plates; ?nodes; (leaves opposite), (2-ranked); P to 13; (styles branched); seeds often carunculate.

2. Caletieae Müller Argoviensis

Often monoecious; A to 30, (connate basally); pollen ± spherical, zono- to pantoporate; (ovule with endostomal micropyle - Austrobuxus); (n = 12 - Pseudanthus).

14/68: Austrobuxus (20). Largely Australia, New Caledonia, few Malesian.

Synonymy: Androstachyaceae Airy Shaw, Micrantheaceae J. Agardh, Paivaeusaceae A. Meeuse, Pseudanthaceae Endlicher

3. Picrodendreae (Small) G. L. Webster

(Lamina palmate, or with secondary venation ± palmate), (margins toothed [teeth with deciduous apex]); A to 50; pollen 4-7-zono(panto-)porate (5-8-brevicolporate - Picrodendron); (exotegmen palisade, subprocumbent, mesotegmen ± thickened, endotegmen 2-layered, with banded thickenings - Oldfieldia); (endosperm ruminate, cotyledons plicate - Picrodendron).

9/27. Africa, America, S. India and Sri Lanka; tropical and warm temperate.

Evolution. Ecology & Physiology. The New World Piranhea may dominate flooded forests (Connell & Lowman 1989).

Seed Dispersal. Myrmecochory occurs in the majority of the species of the family (Lengyel et al. 2009, 2010).

Vegetative Variation. Leaves are very variable here. Genera like Oldfieldia have opposite, palmately-compound leaves, and in Podocalyx, although the leaves are simple, the petioles are swollen at both ends. Lamina margins are usually entire, but there are minute glands on the margins of Austobuxus while the margins of are strongly serrate. A number of taxa have very small leaves ca 1 cm long or less, and these are sessile and trifoliolate in Micranthemum. Stipules are often minute, but in Androstachys they are large, intrapetiolar and enclose the bud.

Chemistry, Morphology, etc. Podocalyx probably has trilacunar nodes (e.g. leaf scars on Aracá Inventory TF-2-20).

Picrodendron may have a perianth of two whorls (Hakki 1985), or perhaps it is modified quincuncial.

Additional information is taken from Radcliffe-Smith and Esser (2001: genera, etc.), Wurdack et al. (2004), van Welzen & Forster (2010), and Webster (2013), all general, Westra and Koek-Noorman (2004) and Hayden (1977, 1994), all wood anatomy, Levin and Simpson (1994: pollen), Huber (1991) and Tokuoka and Tobe (1999: seed anatomy), and Merino Sutter et al. (2006: morphology of carpellate flowers).

The family is poorly known.

Phylogeny. See Wurdack et al. (2004) and Xi et al. (2012b) for the phylogeny reflected in the classification above; the relationships are well supported.

Stuppy (1996) noted that both Picrodendron and Oldfieldia were rather different from other taxa included in his Oldfieldioideae, and he compared the latter with Meliaceae because of similarity in seed characters. However, both genera are firmly in Picrodendraceae-Picrodendreae.

Two other genera have been associated with this group in the past. Paradrypetes is probably to be included in Rhizophoraceae, although it is like Podocalyx in particular in wood anatomy and pollen morphology (Levin 1992). Croizatia (see Levin 1992) is also odd, with 5 petals, an extrastaminal nectary and style with distinct branches, and it lacks the distinctive pollen of the family; it is here placed in Phyllanthaceae.

Classification. For genera, see Euphorbiaceae-Oldfieldioideae (Webster 1994b). Govaerts et al. (2000) provides a checklist and bibliography (as Euphorbiaceae).

Previous Relationships. Picrodendraceae are the old Euphorbiaceae-Oldfieldioideae (see Webster 1994b).

[Ixonanthaceae + Linaceae] / Linoids: cristarque cells +; lamina vernation involute; C contorted; ovules epitropous, with endothelium, parietal tissue 2-5 cells across, hypostase +, placental obturator +; endosperm scanty, cotyledons large.

Age. Linaceae may have diverged from other Malpighiales in the Cretaceous-Albian 111-100 m.y.a. (Davis et al. 2005a); (103.4-)90(-73.6) m.y. is the spread in Xi et al. (2012b; Table S7) and (87.9-)78.6(-73.6) m.y. in Schneider et al. (2016).

Phylogeny. This family pair has strong support (Xi et al. 2012b).

Chemistry, Morphology, etc. For foliar anatomy, see van Welzen and Baas (1984).

IXONANTHACEAE Miquel, nom. cons.   Back to Malpighiales

Ixonanthaceae

Trees; ellagic acid, myricetin 0; vessel elements with simple perforation plates; mucilage cells 0; cuticle waxes as variously arranged platelets; petiole bundle annular (with medullary bundle) or arcuate; (foliar sclereids +); branching from previous flush; leaves spiral, lamina vernation involute, (margins entire), stipules cauline; inflorescences corymbose, axillary; (pedicels articulated); K usu. basally connate, (C imbricate); A [and style] folded in bud, 5, opposite sepals [no staminodes], 10, obdiplostemonous, -20 [in triplets opposite K]; pollen with supratectal spines; nectary between bases of and adnate to filaments, unvascularized, or ± adaxial, vascular tissue from stamen traces; G [(2) 5], (carpels subdivided), style undivided, slender, stigma capitate or discoid; ovule micropyle bistomal, (outer integument very long, expanded), suprachalazal zone massive, (obturator hairy); fruit valves opening adaxially as well, K and C persistent; seeds basally winged, or aril arising between the hilum and micropyle, (= wing - Ochthocosmus); endotegmen with sinuous anticlinal cell walls; (endosperm 0); n = 14, chromosomes 0.4-1.1 µm long; germination.

3[list]/21. Pantropical (map: from Aubréville 1974; Kool 1988; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).

Age. Estimates of the crown group age of Ixonanthaceae are (75.4-)51.9(-26.6) m.y. (Xi et al. 2012b; Table S7) and (74.3-)48.7-)17.5 m.y. (Schneider et al. 2016).

Evolution. Divergence & Distribution. Ixonanthaceae may have diverged in the Cretaceous-Albian 111-100 m.y.a. (Davis et al. 2005a: c.f. topology).

Chemistry, Morphology, etc. The stamens opposite the petals in Ixonanthes are paired, but arise from a single trace (Narayana & Rao 1966). Narayana (1970) depicted a tegmen ca 4 cells thick the innermost layer of which is an endothelium.

See also Forman (1965, but not Allantospermum), Kool (1988) and Kubitzki (2013b), all general, Nooteboom (1967: esp. chemistry), Weberling et al. (1980: stipules), Link (1992c: nectary), and Rao and Narayana (1965) and Narayana and Rao (1978a), both embryology, etc., for more information. Kool (1980) revised Ixonanthes.

Much remains unknown in this family.

Phylogeny. Relationships in Xi et al. (2012b) are [Ixonanthes [Cyrillopsis + Ochthocosmos]] - support strong (see also Byng et al. 2016). Schneider et al. (2016) found that I. icosandra was sister to the rest of the family, although other relationships were as just mentioned.

Previous Relationships. The circumscription and relationships of Ixonanthaceae have been particularly unclear (see introduction to the order). Allantospermum (now Irvingiaceae) was included here prior to xii.2015.

LINACEAE Perleb, nom. cons.   Back to Malpighiales

Cork?; vessel elements with simple or scalariform perforation plates; true tracheids +; petiole bundle(s) arcuate; epidermal wax crystals as parallel platelets; branching from previous innovation; lamina tooth ?type, petiole short; pedicels articulated; (flowers distylous); K quincuncial, C (trace single), postgenitally connate above base, caducous; nectary outside A; A basally connate, basally adnate to C, anthers basifixed; tapetum binucleate; pollen grains tricellular, starchy; G [2-5], opposite petals, or median member adaxial, style more or less divided, stigmas ± capitate; ovule (1/carpel), micropyle endostomal (bistomal), parietal tissue 4-6 cells across, endothelium +, obturator +; (megaspore mother cells several); fruit often septicidal, K persistent; tegmen strongly multiplicative; endosperm with chalazal haustorium, variable, (embryo slightly curved), cotyledons large.

Ca 7[list]/300 - two groups below. World-wide.

Age. Crown Linaceae have been dated to (47-)36, 35(-23) m.y. (Bell et al. 2010); McDill and Simpson (2011, q.v. for more details, as in Bell et al. 2010: Irvingiaceae sister to Linaceae) suggest that crown group divergence was in the early Caenozoic (range 82-43 m.y.); (54.8-)39.5(-28.9) m.y. is the age in Xi et al. (2012b; Table S7) and (51.6-)43.9(-37.7) m.y. in Schneider et al. (2016).

1. Linoideae Arnott

Linoideae

Annual to perennial herbs (shrubs); ellagic acid 0; vessel elements with simple perforation plates; rays uniseriate; (nodes 1:1 - Linum); cristarque cells uncommon; epidermis mucilaginous; leaves opposite or spiral, (lamina margins entire), (stipules 0); K ± equal, C clawed, protective in late bud; (nectary at base of C or A); A 5, opposite sepals, alternating with staminodes; pollen 3-many colpate, many colporate, or pantoporate, surface ± intectate, verrucate or echinate; G ([2-4]), loculi usu. divided, stigma unifacial, wet or dry; ovules with outer integument 2(-3) cells across, inner integument 3-12 cells across, parietal tissue 0, hypostase?, (lateral tissue scanty), (obturator with papillae); (2-seeded mericarps also splitting along false septae, units opening adaxially); seeds often mucilaginous, exotesta with outer walls massively thickened, cross cells beneath exotegmen; endosperm with xyloglucans, (helobial), embryo chlorophyllous [Linum]; n = 6, (8), 9, (11-18, etc.).

4/240: Linum (200). Worldwide, but esp. N. temperate and subtropical (map: from Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Diderichsen & Richards 2003; Flora of China vol. 11. 2008; McDill et al. 2009). [Photo - Flower]

Age. McDill and Simspon (2011) suggested that crown group divergence of Linoideae is Eocene in age, while (41-)39.2(-37) m.y. is a similar age suggested by Schneider et al. (2016).

2. Hugonioideae Hooren & Nooteboom

Hugonioideae

Trees or shrubs, often lianes with branch grapnels; ellagic acid?; vessel elements with scalariform perforation plates; sclereids +; stomatal accessory cells usu. lignified (not Indorouchera), lobed beneath the guard cells; leaves spiral or two-ranked, (stipules pectinate); (flowers tristylous); K often unequal, C at most slightly clawed, often yellow, (0); A 10, of two lengths, (obdiplostemonous); (pollen inaperturate); (G with 1 of 3 loculi better developed than others/fertile), (opposite K), styles impressed; ovule with micropyle endostomal [Roucheria], outer integument 2-3 cells thick, inner integument 3-12 cells thick, obturator with papillae; fruit a drupe or with mericarps; seed with an at most slight arillode, testa multiplicative, mesotesta with sclerotic cells, endotesta lignified, exotegmen barely lignified or tegmen obliterated; (endosperm copious); n = 6, 12, 13.

3/61: Hugonia (40). Pantropical (map: from van Hooren & Nooteboom 1984a; Jardim 1999; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; McDill et al. 2009). [Photo - Flower]

Age. McDill and Simspon (2011) suggested that crown-group Hugonioideae are Oligocene-Miocene in age, although Schneider et al. (2016) suggested a late Miocene age of a mere (13.5-)7.6(-2.9) m. years.

Synonymy: Hugoniaceae Arnott

Evolution. Ecology & Physiology. Hesperolinon (= Linum s.l.) is notably diverse on the serpentine soils of the western United States (Schneider et al. 2016).

Pollination Biology and Seed Dispersal. Heterostylous flowers are scattered in Linoideae, and tristyly is reported from at least some Hugonioideae (Meeuse et al. 2011), but whether heterostyly is an apomorphy for Linaceae is unclear; breeding systems have certainly been labile (Thompson et al. 1996; McDill et al. 2008, 2009). In Linum suffruticosum, at least, heterostyly involves positioning of anthers and stigmas so that pollen is placed on the insect in quite different places (dorsally, ventrally) by the anthers of the flowers of the different morphs (Armbruster et al. 2006).

A number of Linoideae have myxospermous seeds (references in Western 2012).

Economic Importance. Seeds of flax (Linum usitatissimum) have been used for oil, etc., for about 10,000 years (Vaisey-Genser & Morris 2003); linen is made from stem fibres.

Chemistry, Morphology, etc. Ellagic acid is not reported from Linoideae, but members of this subfamily are largely herbaceous. Flat vernation is reported from Linum narbonense by Cullen (1978), other taxa may be conduplicate. Bracts and bracteoles have a single vascular trace ().

Tirpitzia bilocularis has a corolla tube over 2 cm long. The "staminodes" may lack any vascularization (Al-Nowaihi & Khalifa 1973). Tobe and Raven (2011) suggest that the inner integument is multiplicative. In Hugonioideae, only half of the ovules may develop and produce seeds. Guignard (1893) drew the ovules of Linum as having a single parietal layer of cells; at the base of the embryo sac there was a persistent narrow column of cells, while Boesewinkel (1980a) also suggested there might on occasion be a single layer of parietal cells and a nucellar cap two cells accross. Note that septicidal dehiscence, presumably liberating pyrenes, may occur in Linoideae (Spichiger et al. 2002).

For general information on the family and its possible segregates see Robertson (1971: Linoideae), van Hooren and Nooteboom (1984, 1988a), Jardim (1999: New World Hugonioideae) and Dressler et al. (2013); see also Hegnauer (1966, 1989: chemistry), Schmidt et al. (2010: lignans, in most Linum alone), van Welzen and Baas (1984) and Kumar (1977), both anatomy, Cremers (1974: growth in Hugonia), L. L. Narayana (1964, 1970) and Narayana and Rao (1966, 1969, 1978a), all embryology, floral anatomy, etc., and Schewe et al. (2011: floral development in Linum.

Phylogeny. McDill et al. (2009: focus on Linoideae) oulined phylogenetic relationships in the family; Linoideae may be monophyletic, but support is from posterior probabilities only; the status of Hugonioideae is unclear. However, in the more extended sudy of McDill and Simpson (2011) Linoideae are well supported, although Linum is paraphyletic and its current sectional limits need adjusting, Hugonioideae are monophyletic, but still lacking strong support. Schneider et al. (2016) recovered both subfamilies with good support. Within Hugonioideae, Hugonia was paraphyletic and included Philbornea and Indorouchera; the Australian H. jenkinsii was sister to the combined clade (Schneider et al. 2016).

Classification. The topology suggested by McDill and Simpson (2011) and Schneider et al. (2016) necessitate nomenclatural adjustments. It is best to expand Linum; certainly, Cliococca must go, and if there is a desire to maintain Hesperolinon (it does have a sectional name in Linum), then another four or five genera will be needed. Generic limits around Hugonia are also difficult.

Previous relationships. For an early detailed discussion on relationships of Linaceae, then thought to be a "central" family, see Hallier (1923). Linaceae have been linked with Erythroxylaceae (the two have even been included in the same family) and Humiriaceae, and thence to Geraniales (e.g. Narayana & Rao 1978b), or the three families together are placed in Linales (Cronquist 1981); see also Boesewinkel and Geenen (1980)