EMBRYOPSIDA Pirani & Prado

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

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

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


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

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


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


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


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


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


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


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


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


Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open, pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [], dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.

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

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tectum reticulate-perforate, 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.


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; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).

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


[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.




[SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]: flavonols +; vessel elements with simple perforation plates; (cambium storied); petiole bundle(s) annular; style +; inner integument thicker than outer; endosperm at most scanty.

Age. Suggestions for the age of this node are (88-)71(-63) m.y. (N. Zhang et al. 2012; see also Xue et al. 2012), (102-)96(-90) and (80-)76(-72) m.y. (H. Wang et al. 2009), ca 98.25 m.y. (Magallón & Castillo 2009), around 93.6-89.9 m.y. (Naumann et al. 2013), about 103.5 m.y. (Hohmann et al. 2015), ca 111 m.y. (Foster et al. 2016: q.v. for details) or (117-)111.5(-106) m.y. (Muellner-Riehl et al. 2016) .

Evolution. Genes & Genomes. Based on a study of the genome of Arabidopsis, De Bodt et al. (2005, see also Maere et al. 2005) suggest there was a duplication of the whole genome some 109-66 m.y. before present, although given the uncertainty over the dating of this duplication and relationships within rosids, exactly where the duplication should go on the tree is unclear. Placing it at this node is one possibility.

For integument thickness, a possible apomorphy, which, however, reverses, and its condition is unclear in Huerteales, etc., see Endress and Matthew (2006a).

Phylogeny. Relationships between the malvid clades have been somewhat uncertain. The clade [Malvales + Sapindales] was sister group to Brassicales (Soltis et al. 2000; Peng et al 2003: both weak support; Bell et al. 2010), and Endress and Matthews (2006) noted that there are some features perhaps more common in these first two families than elsewhere in this affinity. Other studies suggest that [Malvales + Sapindales] may be sister to [Brassicales + Huerteales] (Soltis et al. 2007a: support weak for the latter pair; Bell et al. 2010). Although Bausher et al. (2006) in an analysis of whole chloroplast genomes found strong support for the clade [Brassicales + Malvales], only one species from the three larger orders and no Huerteales were included (but see also S.-B. Lee et al. 2006: sampling even more exiguous; Jansen et al. 2007; Moore et al. 2007; Muellner-Riehl et al. 2016). There was also some support for this topology in analyses by Savolainen et al. (2000) and Hilu et al. (2003). Alford (2006), when describing his Gerrardinaceae, found that Huerteales (Perrottetia not included), Brassicales and Malvales formed a tritomy, the combined group being rather poorly supported as sister to Sapindales, while Worberg et al. (2007b, 2009) recovered the relationships [Sapindales [Huerteales [Brassicales + Malvales]]], with strong support, and they found that each of the four orders was monophyletic. In studies including the mitochondrial matR gene, although the malvid clade was recovered, relationships within it were unclear (Zhu et al. 2007). I follow Worberg et al. (2009).

SAPINDALES Berchtold & J. Presl  Main Tree.

Interesting secondary compounds, ethereal oils, myricetin +; (secretory cells/tissue +); mucilage cells +, with swollen layered inner periclinal walls [position in plant varies]; branching from previous innovation, petioles leaving a prominent scar; leaves spiral, odd-pinnately compound, leaflets opposite, vernation conduplicate; A 2x K, (± obdiplostemonous); tapetal cells polyploid; (pollen exine distinctly striate); nectary well developed; G = and opposite petals, or 3, odd member adaxial, stigmatic head from postgenitally united free carpel tips; ovules few/carpel, epitropous, nucellar cap [?all]; exotegment not fibrous; (embryo chlorophyllous). - 9 families, 471 genera, 6,700 species.

Age. The age of crown-group Sapindales has been variously estimated as 117.4, 104.9, and 90.5 m.y. (Muellner et al. 2007: c.f. topology) or (110.5-)105(-99) m.y. (Muellner-Riehl et al. 2016).

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. Sapindales contain ca 3% eudicot diversity (Magallón et al. 1999) and show quite high diversification rates (Magallón & Castillo 2009).

Muellner-Riehl et al. (2016: Table S1) discusss dating in this clade - they provide dates for hundreds of nodes - in some detail. They prefered ages from analyses using three maximum constraints over those using one or no such constraints; ages in the latter case were ca 1.7-3 times those when three constraints were used - e.g. ca 441 versus ca 148 m.y. for the eudicot stem age... Their ages for families were older than those in earlier general studies that included Sapindales, but younger for the most part than studies that focussed on a single family (Muellner-Riehl et al. 2016: esp. Table 5).

For some embryological s.l. features possibly characterizing Sapindales, see Yamamoto et al. (2016), q.v. for cautions on numbers of nuclei in/polyploidy of tapetal cells.

Pollination Biology. There is notable variation in dichogamy here, see e.g. Bertin and Newman (1993), Routley et al. (2004).

Plant-Animal Interactions. Associated with the frequent accumulation of noxious secondary metabolites in Sapindales, specialised herbivores are found on many of this group. Thus the hemipteran Calophya eats largely Anacardiaceae, Burseraceae, Simaroubaceae and Rutaceae (Burckhardt & Basset 2000) - plus a couple of records from entirely unrelated families. A notable diversity of monoterpene synthase genes have been found in Sapindales studied, and the products of these genes may be involved either directly in plant defence, or indirectly by signalling to parasitoids of herbivores, but studies of these genes are currently only preliminary (Zapata & Fine 2013 and references). Galls are quite common, perhaps especially on Sapindaceae and Anacardiaceae (Mani 1964; see also Price et al. 1998).

Chemistry, Morphology, etc. Gums and resins occur in both the Rutaceae-Meliaceae-Simaroubaceae and Burseraceae-Anacardiaceae groups (Nair 1995).

Stratified phloem may be quite widespread (in some Meliaceae, Burseraceae and Simaroubaceae, at least: M. Ogburn, pers. comm.), also Sapindaceae. Teeth, when present, have a clear glandular apex broadening distally and with a foramen and two accessory veins (or one, the other going above the tooth: Hickey & Wolfe 1975). Stipular structures that vary in morphology are scatteerd through the order (Cruz et al. 2015 for examples and references), and these may be modified basal leaflet pairs; some have been described as pseudostipules or metastipules, the latter being defined as structures having the morphology of true stipules, yet there was good reason to believe that they were derived from pseudostipules... (Weberling & Leenhouts 1965).

Bachelier and Endress (2009) note some floral developmental features found widely in this clade, while Yamamoto et al. (2014: esp. Table S1) compare embryological features; for some details of embryology, see also Mauritzon (1936). Inconspicuous oblique monosymmetry may be common in the order, although many Sapindaceae, for example, are more strongly monosymmetric. The flowers are often imperfect, but since staminate and carpellate flowers have well-developed pistillodes and staminodes respectively, they can be difficult to distinguish. The rather uncommon feature of floral tubes that are formed by connate or closely adpressed and flattened filaments occur throughout Meliaceae, in a number of Rutaceae, and in Boswellia dioscorides (Burseraceae). Pollen with striate exine is scattered through the order. Septal cavities have been noticed in Cneorum (Rutaceae) and Koelreuteria (Sapindaceae), but they do not secrete nectar (Caris et al. 2006, c.f. septal nectaries in monocots).

Phylogeny. For general relationships, see Gadek et al. (1996), while Pell (2004) notes some deletions and insertions that may characterise groupings within the clade. Muellner et al. (2007) present a two-gene tree with quite good sampling; their results, albeit poorly supported, suggest the basal relationships in the tree here (also poorly supported in Soltis et al. 2011), and the position of Sapindaceae is unresolved (see esp. Muellner-Riehl et al. 2016). There was also a fair bit of resolution elsewhere, excepting an only moderately-supported sister group relationship between Meliaceae and Simaroubaceae (see also Koenen et al. 2015; Muellner-Riehl et al. 2016; but c.f. Gadek et al. 1996; Soltis et al. 2011: ?sampling). Relationships are somewhat different in Wang et al. (2009), but support was weak and sampling poor, and support was again mostly poor in M. Sun et al. (2016), although there was some support for a [Nitrariaceae + Biebersteiniaceae] clade sister to the rest of the order (see also Muellner-Riehl et al. 2016), while the relationships [Nitrariaceae [Biebersteiniaceae + The Rest]] in Z.-D. Chen et al. (2016) also had little support.

Molecular data had early placed Biebersteinia, ex Geraniaceae, in Sapindales, albeit with a long branch (Bakker et al. 1998). Its herbaceous habit is rather unusual for Sapindales, but its ethereal oils (no oxygenated sequiterpenes, high proportion of aliphatic hydrocarbons - Bate Smith 1973; Greenham et al. 2001), single ovule/carpel, etc., are all congruent with a position here.

Previous Relationships. In the past Bretschneideraceae and Akaniaceae (= Akaniaceae, see Brassicales here) have been associated with Sapindales, Bretschneidera in particular looking very like a member of Sapindaceae; at the time, the presence of myrosin cells in the former was not considered to be all that important (Cronquist 1981; Takhtajan 1997).

Includes Anacardiaceae, Biebersteiniaceae, Burseraceae, Kirkiaceae, Meliaceae, Nitrariaceae, Rutaceae, Sapindaceae, Simaroubaceae.

Synonymy: Rutinae Reveal - Acerales Berchtold & J. Presl, Aesculales Bromhead, Amyridales J. Presl, Aurantiales Link, Biebersteiniales Takhtajan, Burserales Martius, Cedrelales Martius, Citrales Dumortier, Cneorales Link, Diosmales J. Presl, Hippocastanales Link, Julianales Engler, Leitneriales Engler, Meliales Berchtold & J. Presl, Nitrariales Martius, Pteleales Link, Rutales Berchtold & J. Presl, Simaroubales Berchtold & J. Presl, Spondiadales Martius, Terebinthales Dumortier, Zanthoxylales J. Presl - Burseranae Doweld, Rutanae Takhtajan, Sapindanae Doweld - Aceropsida Endlicher, Aesculopsida Brongniart, Rutopsida Meisner - Rutidae Doweld

Biebersteiniaceae + Nitrariaceae]: ?.

Age. The age of this node (if it exists) is (107-)94.5(-79) m.y. (Muellner-Riehl et al. 2016).

BIEBERSTEINIACEAE Schnitzlein   Back to Sapindales


Rhizomatous perennial herbs; vessels?; nodes?; hairs glandular; leaves (2-3-compound), leaflets lobed, margins toothed, stipules +, petiolar, lobed or not; inflorescence racemose; C clawed, (denticulate); nectary glands opposite K; theca opening by single slit; tapetal cells up to 12-nucleate, nuclei fuse; pollen 3-celled, exine striate; gynophore +, short, G [5], styles separate, impressed, apically connate, stigma capitate; ovule 1/carpel, epitropous, initially apotropous, unitegmic, integument 4-5 cells across, (nucellar cap ca 2 cells across), nucellus apex exposed, parietal tissue 3-4 cells across, funicle massive, bent; embryo sac tetrasporic, 16-nucleate, 13-celled [Penaea type]; fruit a schizocarp, columella persisting, K ± accrescent; "exotesta" ± collapsed, "endotesta" lignified, cells polygonal; endosperm slight, pentaploid, embryo somewhat curved, cotyledons foliaceous, incumbent; n = 5.

1[list]/5. Greece to Central Asia (map: from Heywood 2007; Muellner et al. 2007). [Photos - Collection.]

Age. The age of crown-group Biebersteiniaceae is estimated as 63.3-54.8 m.y. (Muellner et al. 2007) or (77-)53.5(-33) m.y. (Muellner-Riehl et al. 2016).

Chemistry, Morphology, etc. At least some species of Biebersteinia are foul-smelling.

The ante-petalous stamens are longest. Takhtajan (1997) and Yamamoto et al. (2014) described the ovules as being unitegmic; however, Boesewinkel (1988, 1997) thought that the ovules were bitegmic and the micropyle was bistomal. Hence the apparent similarity of the seed coat of Biebersteinia and that of Vivianaceae (= Geraniales-Francoaceae-Vivianeae), especially when young, with both exotesta and endotegmen being tanniniferous (Boesewinkel 1988, 1997), need reevaluating There are distinctive changes in the ovule as it develops, and at the time of pollination the nucellus apex is exposed (Yamamoto et al. 2014).

Additional information is taken from Baillon (1874), Kunth (1912: general), Hegnauer (1989, as Geraniaceae: chemistry), Kamelina and Konnova (1989: embryology), Tzakou et al. (2001: fatty acids) and Muellner (2011: general).

Biebersteinia is little known.

Previous relationships. Biebersteinia has often been more or less closely associated with Geraniaceae (Geraniales) in the past (e.g. Cronquist 1981; Takhtajan 1997).

NITRARIACEAE Lindley   Back to Sapindales


Perennial herbs to shrubs; -carboline alkaloids +, ethereal oils?; cork in inner cortex; wood storied; nodes?; petiole bundle arcuate, with wing bundles; mucilage cells +, throughout plant or not; cuticle waxes 0 (platelets, rodlets); leaves fleshy, ?vernation, stipules +; inflorescence terminal, ± cymose; K (connate); C protects the flower in bud; A 15, with antepetalous staminal pairs, filament bases broad, flattened; (tapetal cells binucleate - Nitraria); nectaries antepetalous; G [2-4, 6], style long, stigma as commissural compital lines down part of its length, dry; ovules ?epitropous, micropyle zig-zag or bistomal, outer integument 2-4 cells across, inner integument 2-3 or 4-7 cells [which?] across, parietal tissue 2-4 cells across; fruit a loculicidal capsule, or 1-seeded drupe, mesocarp woody [Nitraria]; exotesta cells inflated or not, often mucilaginous; endotesta short palisade, or not, endotegmen ± fibrous [Peganum] or not [Tetradiclis]; (embryo chlorophyllous); n = 12.

3[list]/16. Usu. ± arid regions from North Africa to East Asia, also S.W. Australia and E. Mexico (map: from Brummitt 2007; modified by Frankenberg & Klaus 1980; Pan et al. 1999; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. Austral. vol. 26. 2013). [Photo - Flowers.]

Age. The age of crown-group Nitrariaceae is around 96.5, 86.1, or 57.7 m.y. (Muellner et al. 2007) or (84.5-)63(-42.5) m.y. (Muellner-Riehl et al. 2016).

1. Nitraria L.

(Plant with thorns); xylem parenchyma aliform-confluent; leaves often two or three/node, fleshy, (toothed or lobed), stipules scarious [?not associated with all leaves]; G opposite C, style short; ovules 1/carpel, apotropous; fruit a drupe; endosperm slight.

1/6. Europe to Asia, the Sahara, Australia.

[Peganum + Tetradiclis]: stomata in longitudinal bands of small cells; funicle long; endosperm copious.

2. Peganum L.

Mycorrhizae 0; raphides +, mucilaginous cells few; two adjacent leaves/node, or one leaf/node, blade deeply divided or not, stipules tiny; flowers leaf opposed; K valvate; ovules many/carpel; megaspore mother cells several [Peganum]; fruit a loculicidal capsule or berry; testa weakly multiplicative; n = ?

1/6. Europe to Asia, east Mexico.

Synonymy: Peganaceae Takhtajan

3. Tetradiclis M. Bieberstein

Plant annual; leaves spiral, fleshy, stipules small; flowers (3-)4-merous; A = and opposite K; nectary 0; G [4], each divided into three parts, placentation basal, placentae long, style ± basal, ± hollow, stigmatic ridges extend down expanded apical portion; ovules 6/carpel [4 ovules in central locellus, 1 each in lateral locelli]; fruit a loculicidal capsule [seeds in central locelli only released]; n = 7.

1/1: Tetradiclis tenella. Eastern Mediterranean to Central Asia.

Synonymy: Tetradiclidaceae Takhtajan

Evolution. Divergence & Distribution. Given the phylogeny of the family, the distinctive flowers and fruits of Tetradiclis may be derived.

Ecology & Physiology. Members of this family are often to be found in salt deserts.

Chemistry, Morphology, etc. The variation here is rather puzzling. Takhtajan (1997) says that stipules are absent in Tetradiclis; they are present, if small.

Bachelier et al. (2011) discuss floral morphology in detail, attempting to clarify features like androecial morphology that had been interpreted in various ways in earlier literature. The androecium of Peganum is described as being obdiplostemonous by Eckert (1966); the 15 stamens may be in groups of three opposite the sepals, or there may be paired stamens opposite the petals (Ronse Decraene & Smets 1991a, 1992, 1996a; Ronse Decraene 1992; Ronse Decraene et al. 1996). No endothelium has been recorded in members of Nitrariaceae (Kapil & Tiwari 1978), c.f. Zygophyllaceae s. str..

For general information, see Weberling and Leenhouts (1965), Hussein et al. (2009) and Sheahan (2011: as Nitrariaceae and Tetradiclidaceae); for chemistry, see Hegnauer (1973, 1990: as Zygophyllaceae), Sheahan and Cutler (1993) provide details of anatomy, Bachelier et al. (2011: nice study, all three genera) of floral morphology; for the embryology of Peganum, see Kapil and Ahluwalia (1963), and of Tetradiclis, see Kamelina (1994), for endosperm development, etc., see Batygina et al. (1985), and for seed anatomy, see Danilova (1996).

Phylogeny. Molecular data suggest the relationships [Nitraria [Tetradiclis + Peganum]] (Sheahan & Chase 1996; Savoilainen et al. 2000; Muellner et al. 2007; Muellner-Riehl et al. 2016; c.f. M. Sun et al. 2016 in part).

Previous Relationships. Nitrariaceae and Zygophyllaceae agree in general appearance, wood anatomy, and perhaps also chemistry (Nag et al. 1995). Indeed, the two families used to be placed in an expanded Zygophyllaceae (Cronquist 1981), while Takhtajan (1997) included the genera in Nitrariaceae as three separate families in his Zygophyllales. Zygophyllales-Zygophyllaceae here are not remotely close to Nitrariaceae, but their apparent similarities may be because both grow in dry and warm habitats.

[[Kirkiaceae [Anacardiaceae + Burseraceae]] Sapindaceae [Simaroubaceae, Rutaceae, Meliaceae]]]: wood silicified or with SiO2 grains +; tension wood +; persistent floral apex in the center of the gynoecium [?this level]; ovules 2/carpel, superposed, micropyle endostomal, inner integument elongated, S- or Z-shaped.

Age. Wikström et al. (2001) dated this node to (66-)62-57(-53) m.y. and Bell et al. (2010) suggested an age of around (75-)71(-70) m.y.; about 61.75 m.y. is the age in Naumann et al. (2013), ca 73.4 m.y. in Tank et al. (2015: Table S2), and (106.5-)102(-94.5) m.y. in Muellner-Riehl et al. (2016).

Evolution. Ecology & Physiology. All families in this clade (bar Kirkiaceae) include common trees at least 10 cm across in Amazonian forests and have at least one of the 227 species that make up half the stems in Amazonian forests (for a total of 24 species; ter Steege et al. 2013).

[Kirkiaceae [Anacardiaceae + Burseraceae]]: inflorescence thyrsoid [panicle of cymes]; flowers small [<1 cm across]; K ± connate; (pollen exine striate); G adnate to central receptacular apex, synascidiate, stigma with uniseriate multicellular papillae, wet; fruit a schizocarp, with 1 seed/carpel, endocarp well developed.

Age. The age of this node is somewhere around 93.6, 83.6 or 74.1 m.y. (Muellner et al. 2007), (127-)116(-105) m.y. (Weeks et al. 2014) or (103-)94.5(-85.5) m.y. (Muellner-Riehl et al. 2016).

Chemistry, Morphology, etc. Syllepsis is uncommon in this clade (Keller 1994). For some general information, see Bachelier and Endress (2008b).

KIRKIACEAE Takhtajan   Back to Sapindales


Tree or shrub, often with tuberous roots; ellagic acid +, Si in wood?; nodes?; petiole bundle with medullary bundles; glandular hairs with multiseriate stalk; cuticle waxes 0; stomata ?anomocytic; leaves ± opposite to spiral, leaflet margins serrate; plants monoecious; inflorescence subdichasial, ultimate branches monochasial; flowers 4-merous: K basally connate, decussate, initially valvate, then open, C with adaxial-basal glandular hairs; staminate flowers: stamens = and opposite sepals; pollen syncolpate; nectary broad, well developed; pistillode +; carpellate flowers: staminodes +; G [4 (8)], ?orientation, extra "loculus" ± developed, tip of receptacle apex convex, swollen, glandular, styluli closely adpressed, erect, finally spreading, apex postgenitally connate, stigmas ± punctiform; ovule usu. 1/carpel, micropyle bistomal, long [1/2 length of ovule], outer integument 2-3 cells across, inner integument 3-4 cells across; mericarps pendulous from columella; testa "very thin"; endosperm ?type, embryo curved; n = ?

1[list]/8. Tropical and S. Africa, Madagascar (map: from Brummitt & Stannard 2007).

Chemistry, Morphology, etc. The family is chemically unexceptionable, lacking distinctive secondary metabolites found elsewhere in the order (Mulholland et al. 2003). The wood of Pleiokirkia is reported to smell like honey (Schatz 2001).

The lower order inflorescence branches have carpellate flowers, while flowers on higher order branches are staminate (Bachelier & Endress 2008b). The endocarp of the fruit has elongated and variously oriented sclereids (Fernando & Quinn 1992).

For some information on anatomy, see Jadin (1901), and on chemistry, see Nooteboom (1967); for the floral morphology of Kirkia, see Bachelier & Endress (2008a, esp. b). For general information, see Muellner (2011).

Previous Relationships. Kirkiaceae were previously placed in (Cronquist 1983, but with some doubt) or near (Takhtajan 1997) Simaroubaceae, but they lack quassinoids and limonoids.

[Anacardiaceae + Burseraceae]: biflavonoids; silicification of wood prominent, (vessel elements with scalariform or reticulate perforations); phloem with vertical intercellular secretory canals; phloem surrounded by a light-coloured, sinuous, sclerenchymatous band [not easy to see]; glandular hairs with uniseriate stalks; cuticle waxes usu. 0; (plants dioecious); C little longer than K; (nectary extrastaminal); tapetal cells bi- (uni-, poly-)nucleate; central receptacular apex ± exposed in the center of the flower; ovule pachychalazal; fruit a drupe, operculate, endocarp cells in a mass, lignified, not oriented.

Age. Bell et al. (2010) suggested that the two families diverged (73-)64(-56) or (51-)50(-49) m.y.a., Tank et al. (2015: Table S1, S2) around 0/59.6 m.y., while Wikström et al. (2001) gave ages of (56-)51, 47(-42) m.y., Muellner-Riehl et al. (2016) ages of (97-)87.5(-78.5) m.y., and Weeks et al. (2014) ages of (121-)108(-95) m.y.; a mere 37.7 m.y. is the age in Naumann et al. (2013).

Fossils assignable to Burseraceae/Anacardiaceae are known from the early Eocene in England ca 50 m.y.a. (Collinson & Cleal 2001).

Evolution. Divergence & Distribution. Weeks et al. (2014) compared the path of evolution in Burseraceae and Anacardiaceae, clades of the same age and about the same size, noting the comparatively greater diversity of fruit morphologies and expanded climatic tolerances in the latter (see also Donoghue & Edwards 2014 for biome shifts).

Chemistry, Morphology, etc. Anacardiaceae like Pachycormus have thin, brown, flaking bark that looks quite like that of Burseraceae; the wood anatomy of the two is very similar (Daly et al. 2011).

The two families are palynologically indistinguishable. Bachelier and Endress (2009) discuss the floral morphology and anatomy of this clade in detail. The basic endocarp condition for [Anacardiaceae + Burseraceae] seems to be that of an unoriented mass of sclerified and often crystalliferous cells (Wannan & Quinn 1990), as found in Anacardiaceae-Spondiadoideae, and also in Buchanania, Campnosperma and Pentaspadon, included in Anacardioideae, as by Pell (2004: Campnosperma not sequenced), as well as in Burseraceae. An operculum may be derived twice in Anacardiaceae (Pell & Urbatsch 2001), but it is also found in fruits of Burseraceae and perhaps it, too, is plesiomorphic within the whole clade.

For chemistry, see Hegnauer (1964, 1989), for general developmental information, see Bachelier and Endress (2007a, especially 2008a, b).

ANACARDIACEAE R. Brown, nom. cons.   Back to Sapindales


Trees or shrubs; exudate resinous, black or becoming blackish; crystals in xylem; wood often fluorescing; pith loose, shining; nodes usu. 3:3; petiole with annular wing bundles; leaflets not articulated, margins toothed or not, base of petiole often swollen; breeding system various; flowers (3-)5(-7)-merous, protogynous; (stamens on nectary; nectary 0); (andro/gynophore +), styluli ± separate, terminal to gynobasic, (apex postgenitally connate), stigma capitate (lobed), dry; ovule 1/carpel, apotropous, ± anatropous, micropyle zig-zag (endostomal), funicle long, massive, ponticulus +; seed often ± pachychalazal, vascular bundles in this area, endotegmen usu. ± thickened, lignified; endosperm oily (and starchy), embryo often curved; n = 7-12, 14-16, 21.

80[list]/873. Tropical, also temperate (map: from Heywood 1976; modified by Barkley 1937; Fl. Austral. vol. 25. 1985; Wickens 1976; Meusel et al. 1978; Arbonnier 2002; Nie et al. 2009; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011). Two groups below, but this will almost certainly have to change. [Photo - Flower, Fleshy fruit, Dry fruits.]

Age. Estimates of ages of crown-group Anacardiaceae are 72.7, 65.2, and 54.8 m.y. (Muellner et al. 2007), (128-)97(-83) m.y. (Weeks et al. 2014) and (87-)75(-63.5) m.y. (Muellner-Riehl et al. 2016).

1. Spondiadoideae Takhtajan

Exudate often gums; (leaves simple); A obdiplostemonous; G (?1 - Solenocarpus)[2-)4-5(-12)], (style 1); ovule ± apical, (2/ovules carpel, one epitropous), hypostase +; exocarp thick), (endocarp crustose or cartilaginous), (operculum 0); exotestal cells (and hypodermis) thickened or not, ± persistent, tegmen ± 0, hypostase persistent, saddle-shaped.

20/138: Lannea (40). Tropical.

Synonymy: Spondiadaceae Martynov

2. Anacardioideae Takhtajan

(Vines; perennial herbs); exudate gums and resins, 5-deoxyflavonoids, also alkylcathechols and alkylresorcinols [phenols with unsaturated side chains - allergenic] +; (cork cortical); leaves (opposite), (simple); (flowers monosymmetric); K and/or C (0), K and C single trace [Toxicodendron]; A (1 [+ staminodes]), 5 [opposite sepals], 10 (many), (basally connate); G [3(-6)], (inferior), (highly) asymmetric, one carpel fertile (2 - Campnosperma), symplicate zone?, styluli gynobasic (style 1), stigma with multicellular papillae (punctate); ovule apical to basal, (unitegmic, usu. apically bifid), nucellus 5-20 cells across, (apex exposed - Pistacia), (ovule pachychalazal), funicle with "knees" and other outgrowths, (ponticulus +); (chalazogamy +); drupe often asymmetric, ± flattened, (K much accrescent, fruit a samara), (hypocarp developed); exocarp thin, epidermis lignified, endocarp with up to three layers of palisade lignified sclereids, internal to these a crystalliferous layer [= stratified], (not), (operculum 0); seed coat undifferentiated; (embryo chlorophyllous), (cotyledons folded - Mangifera).

60/735: Searsia (120), Semecarpus (72), Mangifera (68), Ozoroa (40[+]). Largely tropical, also temperate.

Synonymy: Blepharocaryaceae Airy Shaw, Comocladiaceae Martynov, Julianaceae Hemsley, Lentiscaceae Horaninow, Pistaciaceae Martinov, Podoaceae Franchet, Rhoaceae Sadler, Schinaceae Rafinesque, Vernicaceae Schultz-Schultestein

Evolution. Divergence & Distribution. For the early Caenozoic fossil history of what are now East Asian endemic Anacardiaceae, see Manchester et al. (2009) - Choerospondias has been found in Lower Eocene deposits of the London Clay. Middle Eocene deposits from Germany include fossils of the distinctive fruits of the New World Anacardium, with their much-swollen pedicels; the African Fegimanra, sister to Anacardium, also has swollen pedicels, although they are clearly different (Manchester et al. 2007b; Pell et al. 2011; Collinson et al. 2012 for this and other fossil records). Conversely, distinctive fruits that have been identified as the Old World Dracontomelon are known from the Late Eocene of Panama in deposits some 40-37 m.y. old (Herrera et al. 2012).

Weeks et al. (2014) emphasized the diversity of fruit dispersal types in the family, the extent of long distance dispersal, and they also noted that the ability to live in cooler (i.e. with some freezing) conditions has evolved in the family.

Pollination Biology & Seed Dispersal. Pistacia and Amphipterygium (see Julianaceae below) are both wind pollinated, dioecious, and have reduced flowers. Chalazogamy s.l. (technically, perhaps, funiculogamy - Gonzalez 2016) is known from Schinopsis, Pistacia, Toxicodendron, and Anacardium, the pollen tube moving into the ovule from the funicle via the ponticulus, an outgrowth of the funicle that bridges the gap between it and the chalaza (e.g. Martínez-Pallé & Herrero 1995; Bachelier & Endress 2009).

Disseminules of Anacardioideae are often modified in various ways for wind dispersal. The fruits may be adnate to broad bracts (Dobinea), or have a wing formed by the flattened peduncle of the inflorescence (Amphipterygium), much enlarged sepals (Parishia) or petals (Swintonia), or they may be ordinary samaras (Loxopterygium), while in Cotinus hairs on the pedicels help in the wind dispersal of the small, achene-like fruits. The evolution of these fruit types seems to be correlated with the adoption of drier habitats (Pell & Mitchell 2007). In Anacardium the fleshy swollen pedicel is part of the attractive unit.

Plant-Animal Interactions. Anacardiaceae are well known for the sometimes extremely violent allergenic reactions their exudates cause; catechols, resorcinols and other types of phenolic compounds - often in a mixture, as in urushiol - are involved. About a quarter of the genera, all Anacardioideae, have such compounds (Aguilar-Ortigosa et al. 2003; Aguilar-Ortigosa & Sosa 2004).

Aphids (Fordinae) that form distinctive galls are closely associated with species of Pistacia (Inbar 2009), the sometimes massive, spherical galls produce terpenes that dissuade goats, at least, from eating them (Rostás et al. 2013), and aphid galls form on other Anacardiaceae (Wool 2004). A gall-forming jumping psyllid plant louse, the hemipteran Calophya, is notably common on Schinus, and other psyllids occur on Anacardiaceae (Burckhardt & Basset 2000; Burckhardt 2005).

Chemistry, Morphology, etc. Schweingruber et al. (2011) emphasize the abundance of tension wood here. Branching in Anacardium may occur on the current flush.

Hardly surprisingly, wind-pollinated taxa often lack a disc, also petals. Mangifera has one or two stamens borne inside the nectariferous disc; normally the stamens are outside the nectary. In Anacardium a single large stamen is on an oblique plane of symmetry; the other smaller stamens are also fertile. More generally, the position of the carpel, when single, suggests that the flower is obliquely symmetric (Ronse de Craene 2010). In Anacardioideae the floral/receptacle apex is sometimes quite short (Bachelier & Endress 2009). In Schinopsis, Pistacia and Amphipterygium the ovules are unitegmic, etc. (Bachelier & Endress 2007b; Gonzalez 2016). Sometimes the second integument is represented by a small protrusion towards the apex of the otherwise single integument (e.g. Grundwag 1976; Robbertse et al. 1986). Ovule variation in the whole family is considerable; it needs to be put in a phylogenetic context. For infraspecific variation in style number - 1, 3 - see Gonzàlez and Vesprini (2010). The fruits are commonly described as drupes, but as is often the case, the origins of the various layers of the fruit wall do not correspond to those of a drupe in the strict sense (Gonzàlez & Vesprini 2010). The fruit often develops well before the seed, and the testa well before the embryo, so for some time the fruit appears almost empty (Copeland 1955, 1962).

For general information, see Ding Hou (1978), Pell et al. (2011) and Michell et al. (2006); Pell (2004) covered the morphology of the whole family in a phylogenetic context. For general chemistry, see Young (1976), for chemistry of Julianaceae, see Hegnauer (1966, 1989), for exudates, see Lambert et al. (2013), for wood anatomy, see Gupta and Agarwal (2008), for floral morphology, Wannan and Quinn (1991), for some embryology, see Grimm (1912), Copeland and Doyel (1940) and Copeland (1955), for fruit anatomy, Wannan and Quinn (1990), for ovules, fruit and seed, see von Teichman and van Wyk (1988 and references), and for seed anatomy, see von Teichman (1991, 1994, and references).

Phylogeny. Spondiadoideae-Spondiadeae and some Rhoeeae, including Pegia, Tapirira and Cyrtocarpa (see Aguilar-Ortigosa & Sosa 2004; Pell 2004) have been recovered as sister to the rest of the family. However, the situation is now rather complicated. Buchanania in some analyses is quite well supported as sister to other Anacardioideae (Aguilar-Ortigosa & Sosa 2004; Wannan 2006), consistent both with its chemistry, endocarp anatomy (it lacks a stratified endocarp), carpel number of 4-6, and different position of the fertile carpel, but its phylogenetic position is not fixed in other analyses (Pell & Mitchell 2007, c.f. abstract). Campnosperma, initially included in only one study (Chayamarit 1997: sampling limited, relationships different from those in other studies, no support values), has an endocarp similar to that of Buchanania and the fruit is sometimes two-locular; it was not sequenced by Pell (2004). Pell et al. (2011) suggested that Spondiadoideae may be polyphyletic, and Weeks et al. (2014) found that Spondiadoideae were paraphyletic, Campnosperma being between the two parts, Buchanania ending up sister to one of those parts, and Pentaspadon was sister to the whole family - however, support was not strong. M. Sun et al. (2016) also did not recover a monophyletic Spondiadoideae, and although relationships within a portion of the subfamily were quite well resolved, that portion did not include genera like Pegia and Spondias itself... On the other hand, Z.-D. Chen et al. (2016) found Spondias, Dracontomelon, and Buchanania to be in the same clade and sister to the rest of the family (moderate support) while relationships in Muellner-Riehl et al. (2016) are [[Spondias + Dracontomelon] [[Buchanania + Lannea, etc.] [other anacards]]].

In the remainder of the family, there are four main clades, with [Dobinaea + Campylopetalum] sister to the whole lot and support for the scaffolding quite good (Weeks et al. 2014). In the old Anacardioideae (Pell & Urbatsch 2000, 2001) wind-dispersed taxa do not form a single group (Pell & Mitchell 2007, also Muellner-Riehl et al. 2016, c.f. Pell & Urbatsch 2001).

For relationships within Rhus, from which the allergenic Toxicodendron has been excluded, see Yi et al. (2007) and Andrés-Hernández et al. (2014).

Classification. See Mitchell et al. (2006) for a list of genera and Pell et al. (2011) for a classification, etc., the latter included 21 genera in their polyphyletic Spondiadoideae. Buchanania and Campnosperma are included in Anacardioideae above, and this robs the subfamily of much in the way of apomorphies, but obviously the current classification is decidedly temporary. For the limits of Rhus, which seem best narrowly drawn (i.e., restricted to ca 35 species), see Yi et al. (2007 and references).

Previous Relationships. A number of anacardiaceous genera have highly reduced flowers and inflorescences, and in the past they have been segregated in separate families. These include Blepharocaryaceae, with their compact, involucrate inflorescences, Julianaceae, dioecious, the staminate flowers with extrorse anthers and carpellate flowers that lack a perianth but are surrounded by an involucre, and finally Podoaceae, with opposite leaves and carpellate flowers that also lack a perianth.

BURSERACEAE Kunth, nom. cons.   Back to Sapindales

Trees or shrubs; bark flaky, light grey; exudate colorless to white, resinous, ellagic acid +; pith cells heterogeneous; nodes usu. 5:5; sclereids in stem; indumentum very various; epidermis with mucilage cells; leaflets (with pellucid dots), ?vernation, margins toothed, petiolules and petioles often pulvinate; dioecy common; K induplicate-valvate, ± connate, C valvate; ventral carpel bundles fused bundles of adjacent placentae, style usu. short; ovules 2/carpel; fruit septifragal, with columella, stone with valves, K deciduous; (exotesta with shortly radially elongate but unthickened cells), endotesta lignified, ± tracheidal; embryo reserves hemicellulosic.

19[list]/755: four groups below. Tropical. [Photos - Leaf, Flower, Fruit.]

Age. De-Nova et al. (2012) dated crown-group Burseraceae to the early Palaeocene (69.7-)64.9(-60.3) m.y.a.; the estimate in Weeks et al. (2005: n.b. in text as the divergence between Anacardiaceae and Burseraceae) is (61.9-)60(-58.1) m.y.a., in Muellner-Riehl et al. (2016) it is (86.5-)75(-65) m.y., and in Weeks et al. (2014) the age is (106-)91(-78) m.y.a.; an age of 120 m.y. plus can be estimated from the discussion in Becerra (2005).

See Daly et al. (2011) for the fossil record of the family.

1. Beiselieae Thulin, Beier & Razafimandimbison

Plant deciduous; (vessel elements with scalariform perforation plates); leaf base much swollen, persistent, its apex/base of rhachis shriveling, forming a spine; G [9-12], symplicate zone short, ovary strongly furrowed, style ± 0; ovules superposed; pericarp splitting septifragally, columella strongly ribbed, pyrenes apically winged, between the ribs; cotyledons entire; n = 13.

1/1: Beiselia mexicana. Michoacan, Mexico (Map: in blue below).


[Garugeae [Bursereae + Protieae]]: (plant deciduous); oleoresins with mono- and bicyclic monoterpenes, triterpenes with ursane and oleanane components; (pith cells not heterogeneous); petiole bundle with medullary strands, (not); snail glands + [curled ± uniseriate glandular hairs]; (lamina margins entire); (K with single trace); A (apparently in a single whorl); (pollen psilate); G [(2-)3-5], (one carpel developing), symplicate zone well developed, receptacle enclosed by the gynoecium; ovules collateral, campylotropous, outer integument 3-5 cells across, inner integument 3-4 cells across, (integument 1, ca 5 cells across, apically bifid), parietal tissue 5-20< cells across, nucellar cap 1-30 cells across (?0); pyrenes usu. with pericarpial pseudo-aril, mesocarp quite frequently splits down loculicidal radius, or fruit indehiscent, seeds embedded in ± fleshy pericarp; drupe often angled; vascular bundle in outer integument; cotyledons straight to variously folded, entire to palmately lobed.

18/754. Tropical, but esp. America and N.E. Africa (map: from Rzedowski 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; D. C. Daly, pers. comm.).

Age. The crown-group age of this clade can be dated to (60.2-)58(-55.8) m.y. (Weeks et al. 2005), (72-)63(-55) m.y. (Muellner-Riehl et al. 2016) or (66.5-)63.4, 54.2(-48.8) m.y. (Fine et al. 2014), but some estimates, at (116-)98, 92.7(-74.8) m.y., are older (Becerra et al. 2012), and yet older in Becerra (2003, 2005).

2. Garugeae Marchand

(Cork cambium deeper - Santiria); (petiole bundle with medullary bundles); (leaves deciduous), (leaflets not pulvinate), ("stipules" +, petiolar or cauline, laciniate to entire); dioecious, or flowers perfect; flowers often 3-merous, (hypanthium +); (C connate); (A connate - Canarium); (pollen striate); fruit often not dehiscent, (pyrenes winged); if germination hypogeal, often phanerocotylar; n = 13, 22-24.

11/275: Canarium (120), Dacryodes (70). Tropical, esp. Old World.

Age. Crown-group Garugeae are estimated to be (54.5-)45.6(-36.9) m.y.o. (Federman et al. 2015) or (Muellner-Riehl et al. 2016).

[Bursereae + Protieae]: ?

Age. The age of this node can be dated to (66.8-)63.2, 48.6(-46) m.y. (Fine et al. 2014) or (67.5-)59.5(-52) m.y. (Muellner-Riehl et al. 2016).

3. Bursereae de Candolle

(Petiole bundle arcuate - Commiphora); (plant thorny - Commiphora); leaves usu deciduous; plant (polygamo-)dioecious; pollen colpi short; (pyrenes winged), (pseudaril +); n = 12, 13.

3/286: Commiphora (185), Bursera (110). Tropical America, Africa, 150 species Commiphora from Africa.

Age. Crown-group Bursereae may be around (58.5-)52.5(-47.5) m.y.o. Muellner-Riehl et al. 2016).

4. Protieae Marchand

C induplicate-valvate, (connate); (stamens = and opposite sepals); n = 11.

3/140: Protium (130). Mostly neotropical, a few Madagascar and Malesia

Age. Crown-group Protieae can be dated to (43.2-)32.6, 25.7(-18) m.y.a. (Fine et al. 2014) or (40-)24.5(-11.5) m.y.a. (Muellner-Riehl et al. 2016).

Synonymy: Balsameaceae Dumortier [?where]

Evolution. Divergence & Distribution. Dates for the split between Bursera and Commiphora vary from ca 120 to ca 60 m.y.a. - c.f. Becerra (2005) and Becerra et al. (2012); with the earlier age, distributions could be affected by continental drift; De-Nova et al. (2012) dated the split between Bursera and Commiphora to (59.0-)54.7(-50.6) m.y. ago. Weeks and Simpson (2007) suggested that divergence of Commiphora from the clade now represented by the E. Asian B. tonkinensis occurred some 53-42 m.y.a. in the Eocene; Commiphora itself did not diversify until 32.3-23.2 m.y.a., Neogene aridification of Africa occurring more or less at that time. Crown-group Commiphora may be (45.8-)36.6(-47.4) or (32.3-)27.8(-22.3) m.y.o. (Gostel et al. 2016 and Weeks & Simpson 2007 respectively), but Gostel et al. (2016) suggest that diversification began around 9.5 m.y. later, there being a very long branch above C. lasiodiscus. There are four quite separate clades of Commiphora on Madagascar, indeed, the Malagasy C. lasiodiscus is sister to the rest of the entire genus (Gostel et al. 2016). De-Nova et al. (2012) thought that crown group Bursera was ca 49.4. m.y.o., although diversification within the genus did not really get going until (23-)20 m.y.a, and Becerra et al. (2009) suggested that Bursera, speciose in the seasonally-dry, tropical forests of Mexico, had diversified most within about the last 25 m. years. De-Nova et al. (2012) estimated the age of most species of Bursera in these Mexican forests at ca 7.5 m.y. - more or less as predicted for species in such forests (Pennington et al. 2009; Dick & Pennington 2011).

Weeks et al. (2005), Weeks and Simpson (2007: much detail) and Weeks et al. (2014) discuss the complex biogeographic relationships within Burseraceae, the latter emphasizing the paucity of biome shifts in the family and the importance of Miocene radiations in both Protieae and Bursereae. Federman et al. (2015) suggest that Canarium arrived in Madagascar drifting in ocean currents from the Southeast Asian region only about 8.4 m.y.a.; diversification in Madagascar, where the genus is now a prominent and speciose component of the rainforest forest, happened only around about 6 m.y.a. or so.

Ecology & Physiology. Burseraceae are a notable component of the Amazonian forests, and include a disproportionally large number of the common tree species with stems at least 10 cm across (ter Steege et al. 2013). Fine et al. (2014 and references) have studied the diversification of the Protieae, an important element of neotropical forests, in some detail; this began well before the uplift of the Andes. 35 species of Burseraceae, mostly Protium, in the western Amazon largely separated out ecologically, preferring either fertile clay, white sand, or terrace soils (Fine et al. 2005); differentiation of secondary metabolites may also be involved - see also below.

Bursereae, very largely made up of Bursera and Commiphora, are predominantly denizens of drier forests in the New World and Africa-Madagascar. In Mexico, Becerra et al. (2009) noted that some 85% of the some 100 species of Bursera, often quite narrowly distributed, were to be found in seasonally-dry tropical forests. De-Nova et al. (2012) suggested that there had been nine shifts to xerophytic scrublands there, seven to oak forests, and one to tropical forests; overall they discussed the habitat preferences of the genus in terms of niche conservatism.

Seed Dispersal. Burseraceae are one of the three most important food sources (the others are Lauraceae and Arecaceae) for specialized avian frugivores (Snow 1981). The fruits of Malagasy Canarium are quite large for the genus and are dispersed by large lemurs, most of which have recently been made extinct (Federman et al. 2016).

Plant-Animal Interactions. For possible coadaptive relationships between Burseraceae, especially Bursera itself, and herbivorous chrysomelid beetles (Blepharida) and how the latter deal with the toxic terpene-containing resins the plants contain, see Becerra (1997, 2003 and references) and Becerra et al. (2001: particularly interesting). Becerra (2003) suggested that the two had been co-evolving for about 100 m.y., although other estimates for the age of the family (see above) suggest that this figure is very much an over-estimate. In species that have a squirt defence there is toxic material under pressure in their tissues, which, when perforated, is ejected up to 2 m in distance; such species have a rather simple terpenoid-based exudate (Becerra et al. 2009). Locally, species of Bursera tend to be chemically more dissimilar than would be expected at random (Becerra 2007). Overall chemical diversity in Bursera has increased with time/speciation, if dropping off when considered from a per speciation point of view, and terpene variation seems to have become a matter of permuting combinations of chemicals in the local ecological context (Becerra et al. 2009).

Zapata and Fine (2013) found there were 3-5 copies of monoterpene synthase genes in Protium, one copy being very old, the other copies representing duplication events that occurred 50-70 m.y.a., before the diversification of Protieae (Fine et al. 2014). The evidence suggested that the products of these genes might have functions other than direct defence against herbivores, rather, they might attract predators and parasitoids of these herbivores (Zapata & Fine 2013).

Chemistry, Morphology, etc. Phytoliths are commonly produced by Burseraceae (Piperno 2006). The remarkable leaf bases of Beiselia are described by Forman et al. (1989); the axillary bud is borne on the base a little way from the stem. Some Burseraceae have foliaceous stipule-like structures; these are usually interpreted as being the reduced basal pair of leaflets of a compound leaf.

A few genera (e.g. Garuga) have a well-developed hypanthium; the disc is rarely extrastaminal (Triomma). The odd carpel is drawn as being abaxial in 4-merous Amyris (Schnizlein 1843-1870, fam. 244). Srivastava (1968) thought that the ovules of Bursera delpechiana were straight, but they do not appear to be so from his illustration. The embryo sac is often very deeply seated in the ovule, with up to 85 cell layers between it and the nucellar epidermis; the shape of the embryo sac at maturity is very variable (Wiger 1935).

For additional general information, see Lam (1931, 1932), Leenhouts (1956), and in particular, Daly et al. (2011). For some chemistry, see Khalid (1983) and Lambert et al. (2013: exudates), for pollen morphology, see Harley and Daly (1995: Protieae) and Harley et al. (2005: considerable variation), for embryology, Narayana (1960 and references), and for pseudaril anatomy, see Ramos-Ordoñez et al. (2013).

Phylogeny. The quite recently-described Beiselia is sister to the rest of the family (Clarkson 2002; Weeks et al. 2005; Thulin et al. 2008; etc.). This has considerable implications for character evolution; Beiselia also has several probably autapomorphic features.

Thulin et al. (2008) found that Protieae, Bursereae, and Garugeae (the latter including Canarium, etc.) all had strong support individually, but relationships between them were unclear; again, although Becerra et al. (2012) suggested the relationships [Canarieae [Protieae + Bursereae]], support for the position of Canarieae was not very strong (see also Federman et al. 2015; Muellner-Riehl et al. 2016: support quite strong).

In some studies Commiphora has been found embedded in Bursera, but with weak support (Weeks et al. 2005). Becerra et al. (2012) and De-Nova et al. (2012, but c.f. some analyses in the latter) found that a monophyletic Bursera was sister to Commiphora; what about B. tonkinensis? For relationships within Commiphora, with several well-supported clades that do not correspond to previous infrageneric groupings, see Gostel et al. (2016). Canarium was polyphyletic in the analyses of Federman et al. (2015), although the great bulk of the genus formed a single clade, while Muellner-Riehl et al. (2016) questioned the monophyly of Bursera, Canarium and Dacryodes.

[Sapindaceae [Simaroubaceae, Rutaceae, Meliaceae]] (if a clade): anthers with a pseudo-pit; nucellar cap +, tapetal cells multinucleate, nuclei fusing to form polyploid mass; outer integument over five cells across; testa multiplicative.

Age. Wikström et al. (2001) dated this node to (61-)57, 55(-51) m.y.a., Magallón and Castillo (2009) suggested an age of around 70.7 m.y., Tank et al. (2015: Table S1, S2) an age of about 69 m.y., and Bell et al. (2010) an age of (70-)64(-57) or (54-)51(-49) m.y..

Chemistry, Morphology, etc. For an extensive tabulation of variation in anther, ovule and seed characters of this group, see Tobe (2011a).

SAPINDACEAE Jussieu, nom. cons.   Back to Sapindales


Woody; quebrachitol [cyclitol], toxic saponins, cyclopropane amino acids + [non-protein amino acid], ellagic acid 0 (+); cork also outer cortical; latex of sorts not uncommon; ring of sclerenchymatous tissue in bark; (vessel elements with scalariform perforation plates); (petiole bundle with cortical or adaxial bundles); (epidermal cells mucilaginous), cuticle waxes 0 (platelets, rodlets); leaves spiral, odd pinnate, leaflets articulated [check basal pectinations], vernation also conduplicate-plicate, margins serrate, colleters common; inflorescence paniculate, the flowers often in clusters, imperfect; pedicels articulated; flowers 5-merous, C clawed; nectary extrastaminal; A 8, hairy; (tapetal cells 1-3-nucleate); G [(2) 3(-6)], stigma strongly 3-lobed or not, dry or wet; ovules variously curved, sessile, campylotropous [?all], often apotropous, micropyle bistomal, outer integument thicker than the inner integument, parietal tissue 4-15 cells across (?0); fruit a loculicidal capsule; seed often pachychalazal; (tegmen multiplicative), testa vascularized, exotesta palisade (not), unlignified, (mesotestal cell walls thickened and lignified; endotesta crystaliferous), tegmen limited to radicular pocket, (exotegmen fibrous, lignified or not); endosperm 0, starchy, embryo curved, radicle in pocket formed by testa.

140[list]/1630: - four subfamilies below. ± World-wide. (map: from Herzog 1936; Meusel et al. 1978; Fl. Austral. vol. 25. 1985). [Photo - Flower, Fruit, Fruit.]

Age. Wikström et al. (2001) date crown-group Sapindaceae to (43-)39, 36(-32) m.y., Bell et al. (2010) suggested an age (53-)42, 41(-30) m.y., and Muellner-Riehl et al. (2016) an age of (96.5-)87.5(-77) m.y. - alternatively, it is mid Cretaceous and (very approximately) 116-98 m.y.o. (Buerki et al. 2010c). Crown and stem ages of 36 and 55 m.y.a. respectively were suggested by Quirk et al. (2012).

Fossils ascribable to Sapindaceae are known from the later Cretaceous (Coetzee & Muller 1984).

1. Xanthoceratoideae Thorne & Reveal

Phloem stratified; stomata anomocytic; buds perulate; leaves deciduous; flowers large [ca 2.5 cm across]; nectary with golden, horn-like glands alternating with C; pollen spiny; ovules 6-8/carpel, outer integument 6-8 cells across, inner integument 3-4 cells across, hypostase +, obturator 0; aril 0; mesotestal cell walls thickened, tegmen multiplicative, with inner layers thick-walled; germination epigeal; n = ?

1/1: Xanthoceras sorbifolia. N. China.

Synonymy: Xanthocerataceae Buerki, Callmander & Lowry

[Hippocastanoideae [Dodonaeoideae + Sapindoideae]]: pericyclic sheath of phloem fibres and stone cells; flowers often strongly obliquely or vertically [Aesculus] monosymmetric, (4-merous); (style hollow), (branched); ovules apotropous, funicular obturator +/-; (megaspore mother cells several); (fruit septicidal, a schizocarp with 1-seeded samaras); cotyledons spiral or not; germination hypogeal or epigeal.

Age. Wikström et al. (2001) dated this node to (36-)33, 29(-26) m.y., Bell et al. (2010) suggested that it was (46-)37, 35(-26) m.y.o. - alternatively, its age is mid Cretaceous between (very approximately) 116 and 98 m.y. (Buerki et al. 2010c), or somewhere in between, variously around 75.5, 65.8, or 58.8 m.y. (Muellner et al. 2007) or (91.5-)82(-72) m.y. (Muellner-Riehl et al. 2016).

2. Hippocastanoideae Dumortier

("Latex" +), (fructan sugars accumulated as isokestose oligosaccharides [inulins] - Aesculus), cyanogenic glucosides 0; (pericyclic sheath 0); cuticle wax crystalloids quite common [Acer]; stomata actinocytic (anomocytic); buds perulate (0); leaves opposite, palmate or simple, with palmate venation (odd pinnate), deciduous; (flowers large - Aesculus), (polysymmetric), protogynous; C (not clawed - Acer), (with appendages); A (5-)6-8(-12); (nectary - Acer); (style long-branched), stigma dry; outer integument 3-5 [Acer] or 8-10 cells across, inner integument 3-6 cells across - Handeliodendron), nucellar cap 8-10 cells across, (hypostase 0 - Handeliodendron); (aril + - Handeliodendron); (embryo chlorophyllous); n = 20.

5/143: Acer (126). North temperate, esp. China, Korea and Japan (Acer), some tropical and then usually montane.

Age. Wikström et al. (2001) dated crown-group Hippocastanoideae to (29-)26, 20(-17) m.y.o., Bell et al. (2010) to (37-)25(-14) m.y.o. - or they may be 83±20.5 m.y. old (Buerki et al. 2013b) or (77.5-)66.5(-60) m.y. (Muellner-Riehl et al. 2016).

Synonymy: Aceraceae Jussieu, Aesculaceae Burnett, Hippocastanaceae A. Richard, Paviaceae Horaninow

[Dodonaeoideae + Sapindoideae]: leaves usu. evergreen, even-pinnate, (bicompound; simple), leaflets opposite or not, (margins entire), (rachis winged); seeds often with chalazal/integumentary arils and sarcotesta, (dormancy physical, water gap near hilum).

Age. The age of this node may be mid Cretaceous between (very approximately) 116-98 m.y.a. (Buerki et al. 2010c) or (87.5-)77.5(-66) m.y.a. (Muellner-Riehl et al. 2016).

3. Dodonaeoideae Burnett

Cork pericyclic [Dodonaea]; stomata cyclocytic [Dodonaea]; C (0), petal appendages uncommon; A 5-many; ovule (1/carpel, pendulous), outer integument 8-10 cells across, inner integument 3-4 cells across; (seed arillate or with sarcotesta); n = 10, 12, 14-16.

22/145: Dodonaea (70). Pantropical-warm temperate, esp. Australia/Southeast Asia.

Age. Crown-group Dodonaeoideae are 80.5±12.75 m.y.o. (Buerki et al. 2013b) or (67.5-)59.5(-52) m.y.o.(Muellner-Riehl et al. 2016).

Synonymy: Dodonaeaceae Small

4. Sapindoideae Burnett

(Lianes, climbing by branch tendrils); (secondary thickening anomalous); stomata various; (stipules or petiolar pseudostipules +); C (0, 5+), with various ± complex appendages; A (4[Glenniea]-many); (pollen oblate, triporate - Serjania, etc.); ovule often 1/carpel, (epitropous), outer integument 4-12 cells across, inner integument 2-7 cells across; (antipodal cells persistent - Cardiospermum); fruit also a samara (indehiscent); seeds often arillate or with arillode or sarcotesta; (amyloid [xyloglucans] in seed - Cardiospermum); n = esp. 10-12 [climbers] and 14-16 [non-climbers]; chromosomes 0.62-4.36 µm long.

111/1340: Serjania (230), Paullinia (195), Allophylus (1-250), Guioa (65), Cupaniopsis (60), Talisia (42), Cupania (50), Matayba (50). Pantropical.

Age. The crown-group age of this clade has been estimated at (76-)63.5(-51) m.y. (Muellner-Riehl et al. 2016: Koelreuteria sister).

Synonymy: Allophylaceae Martynov, Koelreuteriaceae J. Agardh, Ornithrophaceae Martynov

Evolution. Divergence & Distribution. Cupaniopsis-type pollen is widespread in the fossil record, including from several sites in Africa, although Sapindaceae with such pollen are no longer to be found there (Coetzee & Muller 1984). Wehrwolfea, with striate pollen and a floral formula of K 4 C 4 A 10(?+) G 3-4, is known from the middle Eocene of western Canada (Erwin & Stockey 1990). For the early Caenozoic fossil history of what are now East Asian endemics, see Manchester et al. (2009).

For the biogeography of the family, in which much dispersal is involved, see Buerki et al. (2010c, 2013b). The subfamilies of Sapindaceae spread in the mid Cretaceous 116-98 m.y., initially from Laurasia, with South East Asia remaining an important area in the evolution of the family (Buerki et al. 2010c, 2013b).

Sapindaceae seem to have moved into New Caledonia ca 10 times or more, or there is yet a more complex pattern of movement to and from the island; the relatives of the Mauritian Cossinia pinnata (Dodonaeoideae) grow in the New Caledonian area (Buerki et al. 2012a). The very widespread Dodonaea viscosa has spread within the last two m.y. (Harrington & Gadek 2009). The split between Acer and Dipteronia has been dated to (98-)78(-63.5) m.y.a. (Renner et al. 2007b).

Ecology. Sapindaceae, along with Bignoniaceae and Fabaceae, are the major components of the viny vegetation of the Neotropics (e.g. Gentry 1991). The largely neotropical Paullinieae (Sapindoideae), with 8 genera including Serjania and Paullinia, contain one third of the species in the family, including around 470 species that are lianes or vines. Many of these have stems with unusual patterns of cambial origin and activity, including some species that develop several independent vascular cylinders (Tamaio & Angyalossy 2009; Angyalossy et al. 2015 and other references in Schnitzer et al. 2015). Vessel dimorphism - very wide and very narrow vessels - is common, perhaps ensuring rapid movement of water yet at the same time some protection against embolisms (Bastos et al. 2016 and references). The root anatomy of these vines shows similar dimorphism in vessel diameter but usually not the cambial variation of the above-ground parts of the same plant (Bastos et al. 2016).

Pollination Biology. Species of Acer like A. rubrum are known for having very labile breeding systems. Renner et al. (2007b) studied breeding systems in the genus and suggested that dioecy had evolved several times, and the sex of the flower may be determined by environmental cues.

Chemistry, Morphology, etc. Aesculus has large bud scales, Billia has naked buds, but both branch from the previous flush. "Ordinary-looking" stipules are known only from climbing species like Serjania, but leaflets looking like stipules (pseudostipules) occur elsewhere in the family.

Radlkofer (1892-1900) shows Serjania as having strongly obliquely symmetric flowers, with the odd gynoecial member abaxial on the plane of symmetry. The abaxial corolla member is absent, but the stamens are abaxial, the two adaxial(?)-lateral members being missing. The petals of Sapindaceae are often rather complex, and have a similarly complex set of terms used to describe them. In Acer, the samaras are shown as being oblique by Schnizlein (1843-1870), while Ronse de Craene (2010) depicts gynoecial orientation as varying within an inflorescence.

Brizicky (1963) reported that the ovules may be epitropous (see also Tanaka et al. 2016); those of Koelreuteria and other taxa are both epitropous (the lower ovule) and apotropous (the upper ovule) in the same loculus (Mauritzon 1936; Danilova 1996). Corner (1976) noted that the outer integument of Nephelium lappaceum was slightly thinner than the inner integument, and that there was a definite funicle in Aesculus, at least after fertilization. Tanaka et al. (2016) described how the ovule became campylotropous as an invagination developed in the raphal region; this also produced the radicular pocket characteristic of sapindaceous seeds.

The fruit can look like a follicle when only one carpel develops; dehiscence is, however, down the abaxial side and rudiments of other carpels are sometimes visible. In many Sapindaceae (and some Anacardiaceae) the pericarp grows much faster than the seed, so that what seem to be almost mature fruits can contain seeds that are still very small. Turner et al. (2009) document a water gap near the hilum in the hard seeds of Dodonaea. It has been suggested that the base chromosome number for Sapindaceae is x = 7 (Ferrucci 1989).

For general accounts, see Radlkofer (1890, 1933 to 1934, etc.) and Acevedo-Rodríguez et al. (2011), for chemistry, see Hegnauer (1964, 1966, 1973, 1989, 1990, also under Aceraceae and Hippocastanaceae), for wood anatomy, see Klaassen (1999) and Agarwal et al. (2005), for epidermal features, see Cao and Xia (2008) and Pole (2010), for floral morphology of Koelreuteria, see Ronse Decraene et al. (2000b), that of Handeliodendron, Cao et al. (2008), of Acer, etc., Leins and Erbar (2010), and for that of Xanthoceras, Zhou and Liu (2012), for nectaries, which may have three vascular traces, see Solis and Ferucci (2009) and Zini et al. (2014a), for endothecial thickenings, see Manning and Stirton (1994), for pollen, see Muller and Leenhouts (1976), for style morphology, see Lersten (2004), for embryology, Nair and Joseph (1960) and Tobe and Peng (1990), for chromosome numbers, Lombello and Forni-Martens (1998), for chromosome size, see Ferrucci (1989), for fruits of Paullineae, see Weckerle and Rutishauser (2005), for seeds, see Guérin (1901), van der Pijl (1955) and Turner et al. (2009: germination), and for genome size, Coulleri et al. (2014: not much correlation with anything).

Phylogeny. Preliminary studies suggested that Xanthoceras, with simply 5-merous, polysymmetric flowers (but eight stamens), ovules arranged in parallel (see also Magonia), and complex, golden nectaries borne outside the eight stamens, might be sister to all other Sapindaceae, general relationships being [Xanthoceras [[erstwhile Aceraceae + Hippocastanaceae] the remainder of the family]]] (see Klaassen 1999; Savolainen et al. 2000a; Soltis et al. 2007a). Subsequent two-gene studies (Harrington et al. 2005, 2009: information about secondary structure of ribosomal DNA, extensive sampling in Dodonaeoideae but no Sapindoideae) largely confirmed these results. Harrington et al. (2005) found that Xanthoceras was not sister to the rest of the family in single gene analyses, being somewhat embedded, but without strong support; it was only in the joint analysis that is was sister to all other Sapindaceae with 70% bootstrap and ³95% posterior probability (see also Buerki et al. 2010a, 2010b, support still very low; M. Sun et al. 2016; Muellner-Riehl et al. (2016). Early morphological analyses (Judd et al. 1994) suggested a rather different set of relationships.

For extensive phylogenetic studies of the family, see Buerki et al. (2009, 2010b: 81 and 104 genera respectively). Delevaya and Koelreuteria are successively sister to the rest of Sapindoideae (Buerki et al. 2013b), M. Sun et al. (2016) found Ungnadia to be sister to the rest of the subfamily, while Koelreuteria was in this position in the study by Muellner-Riehl et al. (2016: the two other genera not included). For the phylogeny of Acer, see J. Li et al. (2006), Renner et al. (2007b) and Li (2011), and for that of Dodonaea, see Harrington and Gadek (2010), and for relationships around Cupania, see Buerki et al. (2012a).

Classification. The phenetically distinctive Aceraceae and Hippocastanaceae are here included in Sapindaceae, with which they have much in common; Buerki et al. (2010b) prefered to recognize them (and Xanthoceras, as Xanthoceraceae [sic]) as families; for subfamilies, see Buerki et al. (2009). There is extensive polyphyly of the classically-recognized tribes (Buerki et al. 2010b), while generic limits in the Cupania group (Sapindoideae) are unclear (Buerki et al. 2012a).

Previous Relationships. Sapindaceae are chemically similar in some respects to Fabaceae, e.g. both have non-protein amino acids (for a summary, see Fowden et al. 1979), and both have compound leaves, their seeds may be arillate, etc., but they are not closely related.

[Rutaceae [Simaroubaceae + Meliaceae]: alkaloids, limonoids/protolimonoids +, pentanortriterpenes +; cuticle waxes 0; (leaves trifoliate), (simple); inflorescence branches cymose.

Age. Wikström et al. (2001) dated this node to (51-)47, 45(-41) m.y.a., while an age of ca 53.6 m.y. was suggested by Tank et al. (2015: Table S2) - note the topology in these two - and an age of (100-)93.5(-86.5) m.y. by Muellner-Riehl et al. 2016).

Chemistry, Morphology, etc. The triterpenoid limonoids (see Rutaceae), meliacins (Meliaceae), cneorids (Rutaceae), and quassinoids (Simaroubaceae) are biosynthetically related (e.g. Connolly et al. 1970; Evans & Taylor 1983; papers in Waterman & Grundon 1983; Waterman 1983, 1993) and often have a bitter taste. For additional details of the distribution of limonoids and protolimonoids, see Yin et al. (2009), and for trans-octadecanoic acids in seed oils, see Stuhlfauth et al. (1985).

For some information on carpel development, see van Heel (1983).

RUTACEAE Jussieu, nom. cons.   Back to Sapindales

Furanocoumarins, distinctive limonoids, tetranortriterpenes, flavones +; (vessel elements with scalariform perforation plates); libriform fibres +; wood often fluorescing; (nodes 1:1); (cuticle waxes platelets, rodlets, etc.); stomata various; schizogenous cavities +; (leaves simple), leaflets usu. prominently punctate, (subopposite), usu. articulated, vernation also flat, margins entire to crenate (serrate); flowers often perfect; (3-)5-merous; K (2-4), connate or free, C (0-4), often valvate?, (connate); A (2-many in a single whorl), obdiplostemonous, filaments ± flattened; (gynophore +); G (1 [2-)5(-many)], variously connate to almost free, style impressed to ± gynobasic, (stylar canals as many as carpels), (apex postgenitally connate), discoid or capitate, dry or wet; ovules 1-2/carpel, (apical), micropyle also bistomal, zig-zag, nucellar cap 2-6(-18) cells across; chalazal embryo sac haustorium +; seed with chalazal aperture in the sclerotesta at base or raphe [?Aurantioideae]; exotegmen tracheidal + (0); (endosperm +), (embryo curved); n = (7-)9(-11+).

161[list]/2070 - three groups below. Largely tropical.

Age. Bell et al. (2010) suggested that this node was (51-)40(-29) m.y.o.; however, other dates are (87-)82(-74) m.y.a. (Appelhans et al. 2012a), around 93.3, 82.1, or 72.9 m.y. (Muellner et al. 2007, see also 2006), (93.5-)84.5(-76.5) (Muellner-Riehl et al. 2016), (72.7-)62.7(-53.3) m.y.a. (Pfeil & Crisp 2008), or (43-)39, 37(-33) m.y.a. (Wikström et al. 2001), so there is quite a range with which to work.

1. Cneoroideae Webb


Woody; pyranochromones, (diterpenoid cneorubin; quassinoids; alkaloids [Dictyoloma]) +; schizogenous cavities 0 (+, e.g. Spathelia), oil cells commonly solitary; petiole bundle more or less cylindrical, of two opposed plates (arcuate - Bottegoa); stomata anomocytic to cyclocytic; solitary oil cells + (0), (schizogenous cavities 0); (leaves bicompound), (stipules and stipular thorns +); C valvate; A 4-5, (8-10 - Harrisonia), filaments ± flattened, with basal appendages; pollen reticulate, (tricellular - Cneorum); G (1-)3(-5), style with canals [Harrisonia]; ovules (-5/carpel), also apotropous, (becoming) campylotropous, micropyle endo-/bistomal, outer integument ca 2 cells across, inner integument 3-4 cells across, parietal tissue 4-5 cells across, hypostase +/0, obturator +; fruit a loculicidal capsule, or the carpels opening adaxially and separating laterally and from columella, a winged drupe, or follicle; [endo]testa multiplicative, exotestal cells large, outer walls thickened, endotestal cells small, thick-walled, with crystals, (oil cells +), exotegmen fibrous (not); n = ?

7/35: Spathelia (20). The tropics, also N. Australia and the Mediterranean (Map: from Appelhans et al. 2012a; Australia's Virtual Herbarium xii.2012; Fl. Austral. vol. 26. 2013).

Age. Crown Cneoroideae have been dated to (78-)74(-58) m.y.a. (Appelhans et al. 2012a) or (84.5-)67(-47) m.y.a. (Muellner-Riehl et al. 2016).

Synonymy: Cneoraceae Vest, Ptaeroxylaceae J.-F. Leroy, Spatheliaceae J. Agardh


[Amyridoideae [Rutoideae + Aurantioideae]]: dihydrocinnamic acid derivates, carboline alkaloids and canthinones [with tryptophane nucleus; ?level]; (exine striate); (ovules hemitropous, campylotropous), (apotropous), outer integument 3-10 cells across, inner integument 2-4(-6) cells across, parietal tissue (3-)5-12(-16) cells across; archesporium often multicellular; (exotesta mucilaginous) (map: from Meusel et al. 1978; Brummitt 2007; Groppo et al. 2012).

Age. The age of this node may be (56.8-)47.6(-36.4) m.y. (Pfeil & Crisp 2008), (73-)70(-62) m.y. (Appelhans et al. 2012a), (90-)74(-58) m.y. (Salvo et al. 2010: q.v. for more dates) or (83.5-)74.5(-66.5) m.y. (Muellner-Riehl et al. 2016).

2. Amyridoideae Arnott

Woody; quinolone and acridone [derived from anthranilic acid] or furo-pyranoquinoline and -pyranoquinoline alkaloids, (limonoids 0); (distinctive tracheal veinlet endings); (foliar sclereids +); oil cells also commonly solitary; (leaves opposite), (stipules intrapetiolar/hooded sheath - Metrodorea); flowers (vertically or obliquely monosymmetric), (4 merous); A (connate), (4), (2, with basal anther appendages, + 3 staminodes - Angostura alliance), (obdiplostemonous); ([andro]gynophore +); (G 2+), (opposite sepals - Zanthoxylum), (styluli [marginal] +), (connate only at apex); (obturator +); carpels separating in fruit, (seeds winged), (forcibly expelled with endocarp); exotesta often mucilaginous, irregularly palisade, lignified or not, or fibrous and lignified, (mesotesta sclerotic), (sarcoexotesta [spongy], lignified endotesta - Melicope, etc.), (mesotesta fibrous - Phellodendron), meso-/endotesta thickened [Zanthoxylum], exotegmen with crossed lignification bars, or not [Skimmia], (meso- and endo- tegmen tracheidal), (nucellar polyembryony +); n = (7-)8-9(-11).

113/1740: Melicope (235), Zanthoxylum (225), Agathosma (150 +), Boronia (150), Vepris (80), Acronychia (48), Conchocarpus (48), Zieria (45), Amyris (40). Pantropical, some (warm) Temperate. [Photo - Flower, Flower, Fruit.]

Synonymy: Boroniaceae J. Agardh, Dictamnaceae Vest, Diosmaceae Bartling, Diplolaenaceae J. Agardh, Flindersiaceae Airy Shaw, Fraxinellaceae Nees & Martius, Jamboliferaceae Martynov, Pilocarpaceae J. Agardh, Pteleaceae Kunth, Zanthoxylaceae Martinov

[Rutoideae + Aurantioideae]: Methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); (leaf rhachis winged), (leaflets alternate); C imbricate (valvate), clawed; G postgenitally united; micropyle bistomal, outer integument (3-)4(-6) cells across, inner integument (2-)3(-4) cells across; seed exotestal, (cells palisade), (mucilaginous), (endotesta thickened), (tegmen multiplicative), (exotegmen thickened).

Age. The age for this node is estimated to be some (76-)63(-50.5) m.y. (Muellner-Riehl et al. 2016).

3. Rutoideae Arnott

Perennial herbs to shrubs (trees); C (fringed - Ruta); (A obdiplostemonous); (G 1) postgenitally united, (gynophore +); fruit loculicidal-ventricidal (septicidal, with mericarps); (seeds reniform), (winged); n = (9), 10.

7/87: Haplophyllum (66). North (warm) temperate to tropical, some southern Africa, not the Antipodes or South America.

4. Aurantioideae Eaton

Shrubs to trees; methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); (leaf rhachis winged), (leaflets alternate); (A many); G postgenitally united; (ovules -many/carpel), (unitegmic, nucellus apex exposed, integument ca 5 cells across - Glycosmis), hypostase, obturator +, with hairs; fruit a ± dry berry with mucilaginous pulp directly from endocarp or multicellular hairs; (seed pachychalazal - Glycosmis), exotesta in part mucilaginous (not), fibrous, fibres laterally compressed, (with [multicellular] hairs), inner walls lignified, often fibrous, (testa sclereidal-fibrous - Atalanta), (exo, meso- and) endotesta with crystal-containing cells, exotegmen fibrous; endosperm 0, (chalazal haustorium/narrowing), (nucellar polyembryony +), cotyledons thick, not folded (not Micromelum); n/x = 9.

26/206: Glycosmis (50), Citrus (30). Indo-Malesia and the Pacific, also Africa.

Age. The age of crown-group Aurantioideae is estimated at (28.2-)19.8(-12.1) m.y.a. (Pfeil & Crisp 2008), ca 30 m.y.a. (Muellner et al. 2007) or (52-)40.5(-29.5) m.y. (Muellner-Riehl et al. 2016).

Synonymy: Amyridaceae Kunth, Aurantiaceae Jussieu, Citraceae Roussel

Evolution. Divergence & Distribution. For the early Caenozoic fossil history of what are now East Asian endemic Rutaceae, see Manchester et al. (2009); Gregor (1989) discussed Caenozoic fossil seeds.

For other dates of diversification within Rutaceae, especially Aurantieae, see Pfeil and Crisp (2008; c.f. in part Muellner et al. 2007); the family is relatively young, and distributions are unlikely to be much affected by continental drift (but c.f. Kubitzki et al. 2011; Hartley 2001a, 2001b; Ladiges & Cantrill 2007). Citrus probably moved from west to east Malesia and Australia some time in the Miocene/Pliocene (Schwartz et al. 2015).

Ca 250 species of Diosmeae are restricted to South Africa, largely to the Cape Floristic Region (Trinder-Smith et al. 2007). About 1/4 (400< spp.) of the species in the family are to be found in Australia (see Bayly et al. 2013b for a phylogeny), where most have narrow distributions; movement seems to have been from rainforest habitats to more sclerophyllous/xerophytic vegetation, but there were only four or five of these shifts (Bayly et al. 2013b). There is a major radiation of Melicope on Hawaii of some 50 species, and from Hawaii there seems to have been dispersal to the Marquesas Islands; the source area for the Hawaiian plants is likely to be in the general Australia-New Guinean region (Harbaugh et al. 2009b; Appelhans et al. 2014a). How Zieria arrived in New Caledonia is unclear (Z. chevalieri, sister to the rest of the genus, is the only species there), especially if the estimates of the age of Zieria of less than 20 m.y. are correct (Barrett et al. 2015 and references).

Appelhans et al. (2014b) suggested that the black shiny seeds common in the Acronychia-Melicope clade were a key innovation; the exotesta is edible (birds), and this clade has about 17x as many species as Tetracomia and the Euodia clade, successively its sisters.

Appelhans et al. (2011: many original observations!) plotted a number of morphological characters on the tree, focussing on Cneoroideae; the clade is morphologically quite heterogeneous - like the rest of the family. See also Bayly et al. (2013b) for morphology in Australasian members of the family.

Ecology & Physiology. Rutaceae have exceptionally diverse secondary metabolites, some of which (essential oils, coumarins, etc.) are similar to those in Apiaceae, Asteraceae, Papaveraceae, etc. (Hegnauer 1971; Kubitzki et al. 2011), while their alkaloids are like those found in some magnoliids - and are produced via nine or more different biosynthetic pathways. Thus 1-benzyltetrahydroisoquinoline alkaloids are found in a small group of related Rutoideae, and also in Papaveraceae (and a couple of other families), a distribution that has exercised phytochemists' imaginations in the past (Kubitzki et al. 2011).

Seed Dispersal. For black, shiny, fleshy seeds in the Acronychia-Melicope clade, see Bayley et al. (2013) and Appelhans et al. (2014b). Diosmeae (South African) and Boronia and relatives (Australian) both have seeds with elaiosomes that are endocarpial in origin and are dispersed by ants (Kubitzki et al. 2011; Bayley et al. 2013).

Plant-Animal Interactions. Caterpillars of Papilionidae-Papilionini butterflies are notably common on Rutaceae, about ca 1/3 of the records being from here, and 80% of the ca 550 species of Papilio will eat Rutaceae (Zakharov et al. 2004). Like the magnoliids, e.g. Aristolochiaceae, on which other Papilionidae are found, it is the alkaloids that attract the butterflies. Rutaceae may have been the original food plants for Papilio, since even those species which now eat Magnoliales will eat Rutaceae if they have to (Zakharov et al. 2004, but c.f. Fordyce 2010; see also Berenbaum & Feeney 2008; Simonsen et al. 2011; Condamine et al. 2011). Ehrlich and Raven (1964) noted that Papilio demodocus fed on Ptaeroxylon, which they thought belonged to Meliaceae - it is Rutaceae, so all is explained.

Economic Importance. For relationships in and around Citrus, see Carbonell-Caballero et al. (2015) and for the origin of limes and lemons, see Curk et al. (2016).

Chemistry, Morphology, etc. Rutaceae as circumscribed here are a variable group. For their diverse secondary metabolites, see Hegnauer (1971) and Kubitzki et al. (2011). Da Silva et al. (1988) surveyed the secondary metabolites, suggesting that an overhaul of the infrafamilial classification was in order. Adsersen et al. (2007) noted the value of prenylated acetophenones as a marker for Xanthoxyleae (inc. Melicope, etc.), and Braga et al. (2012) the distinctive dihydrocinnamic acid derivates common in Rutoideae.

Cruz et al. (2015) describe the development of a hood-shaped leaf base in Metrodorea from initially paired primordia and characterise it as stipular in nature; leaflets may arise directly from this hood-shaped structure (Kaastra 1977). Prickles of Zanthoxylum can be in the stipular position.

Rutaceae are particularly variable in flower and fruit (Boesewinkel 1980b). Peltostigma has a floral formula K3 C3 A9 G [?5], and looks almost lauraceous; Pilocarpus has an erect raceme and the calyx is reduced to a rim. Monosymmetry is scattered in the family, occurring in Dictamnus (relationships uncertain) and Erythrochiton, for example. Kallunki (1992) illustrates the flowers of Erythrochiton fallax as having the median sepal adaxial, but their exact orientation and how they are held in nature is unclear since the inflorescence can be pendulous and up to 1.5 m long. The flowers of Galipeinae (the Angostura alliance of Kubitzki et al. 2011), to which Erythrochiton (but not the tube-forming Correa) belongs, may have only two stamens plus staminodes, a connate corolla, filaments connate and forming a tube, or a tube formed by the serial adnation of filaments and petals; variation in gynoecial development is also considerable (Pirani & Menezes 2007; el Ottra et al. 2011, esp. 2013; Bruniera et al. 2015). Wei et al. (2011) thought that the plesiomorphic condition for Rutaceae was to have have five stamens.

Triphasia has G [3], the odd member being adaxial, and the same is true of Cneorum tricoccon, which has 3-merous flowers (see Caris et al. 2006 for floral development). Carpel (stylar) fusion may be postgenital (Gut 1966). Ovule development is notably variable (Mauritzon 1935b: Cneoroideae not included). Although anatropous ovules are common, various degrees of hemitropy and campylotropy occur, and of two ovules in a loculus, one may be apotropous and the other epitropous (Mauritzon 1935b), as in some other Sapindales. The micropyle maye be exo-, endo-, or bistomal or even naked, and in bitegmic taxa, either integument may be slightly thicker than the other (e.g. Corner 1976), although Mauritzon (1935b) suggests that the outer integument is often thicker - 3-10 cells across (outer) versus 2-4 cells across (inner). Nucellar cells above the embryo sac may be in series, and nucellar polyembryony is quite widespread (e.g. Mauritzon 1935b). The embryo sac can be relatively quite small relative to a massive nucellus - and on it goes. The endocarp divides periclinally during development (Hartl 1957) resulting in a pronounced layering of the mature capsule, especially in Rutoideae.

For general information, see van Wyk (in Dahlgren & van Wyk 1988: Ptaeroxylaceae), van der Ham et al. (1995), White and Styles (1966), and especially Kubitzki et al. (2011). For chemistry, see also Hegnauer (1973, 1990, also 1964, 1989 as Cneoraceae), Straka et al. (1976), Waterman and Grundon (1983), Mulholland et al. (2000, esp. Ptaeroxylaceae), and Yan et al. (2011: Harrisonia in particular), and for alkaloid chemistry, Waterman (1975, 1999). For wood anatomy of Cneoroideae, see Appelhans et al. (2012b: phylogenetic signal within the subfamily), for floral development, see Caris et al. (2006b: Cneorum), Zhou et al. (2002) and Wei et al. (2011), for floral orientation, see Eichler (1878), for gynoecial morphology, see Gut (1966), Endress et al. (1983), and Lersten (2004), for ovules of Harrisonia, see Wiger (1935), for ovules and testa, see Honsell (1954), Banerjee and Pal (1958), Johri and Ahuja (1957), Boesewinkel (1977, 1978a: see raphal vascular tissue, b), and Boesewinkel and Bouman (1978), and for fruit anatomy, see Brückner (1991). For the chalazal opening (?vascular bundle) in the seed, see Wilson (1998) and Hartley (2003); for seed anatomy in Rutoideae, see Gallet (1913). See also Straka (1976), Dahlgren and van Wyk (1988), van der Ham et al. (1995) and White and Styles (1966) for information about Cneoroideae.

Phylogeny. In a two-gene analysis, the [[Spathelia + Dictyoloma] [[Cneorum + Ptaeroxylum] Harrisonia]] clade was sister to all other Rutaceae (Chase et al. 1999), although the position of Harrisonia - sequences from only one gene - was somewhat unclear (see also Groppo et al. 2008, 2012). Spathelia (chromones) and Dictyoloma (C valvate) are a strong pair; secretory cavities are reported from them (Groppo et al. 2008). Jadin (1901) had noted that anatomically Harrisonia was rather different from other Simaroubaceae (in which it was then placed) in its heterogeneous pith and its lack of medullary secretory canals. Although it does not seem to have pellucid foliar gland dots, Fernando and Quinn (1992) found secretory cavities in the fruits while Waterman (1993) noted that the genus contained no quassinoids, which are unique to Simaroubaceae. Fernando et al. (1995) suggested that its removal to Rutaceae was justified on both molecular and morphological grounds. Razafimandimbison et al. (2010) found a weakly/moderately supported clade that included the old Ptaeroxylaceae and in which [Spathelia + Dictyoloma] were sister to the rest. Appelhans et al. (2011: denser sampling, five chloroplast genes, 2012a) again found this basic topology; support for the groups was strong, and within the two major clades in Cneoroideae, both strongly geographically circumscribed, in one Sohnreyia was sister to neotropical taxa and in the other Harrisonia sister to palaeotropical taxa (Appelhans et al. 2012a). Morton (2015) found the group to be paraphyletic and basal to the rest of the family, although it was not the focus of her study.

Recent work suggests that the basic relationships in the rest of the family are [Amyridoideae [Aurantioideae + Rutoideae]] (Groppo et al. 2012; Morton & Telmer 2014; Muellner-Riehl et al. 2016). For general relationships in the family, see also M. Sun et al. (2016) and Z.-D. Chen et al. (2016: Chinese taxa, quite good support). [Aurantioideae + [Chloroxylon, Boenninghausenia, Ruta, etc. (Ruteae plus!, = Rutoideae)]] form a poorly to well-supported clade (e.g. Morton et al. 2003; Groppo et al. 2008, 2012; Salvo et al. 2010; Appelhans et al. 2012a; Bayly et al. 2013b; Morton & Telmer 2014).

For relationships in the Irano-Turanian Haplophyllum (Rutoideae), which has colonized the Mediterranean area more than once, see Salvo et al. (2011) and Manafzadeh et al. (2011).

For relationships within Aurantioideae, see Pfeil and Crisp (2008) and Bayer et al. (2009). Clauseneae may not be monophyletic (Morton 2009, 2015); Glycosmis and/or Micromelum may be sister to other Aurantioideae (Groppo et al. 2012; Schwartz et al. 2015), and both have (1-)2 ovules/carpel and similar chromosome numbers (Mou & Zhang 2012). Murraya is very polyphyletic (Z.-D. Chen et al. 2016: Chineae taxa). For other relationships in Aurantieae/-oideae, see Morton (2009), and for relationships around Citrus, see Scott et al. (2000), Samuel et al. (2001), Araújo et al. (2003), Bayer et al. (2009) and in particular Carbonell-Caballero et al. (2015: chloroplast genomes) and Schwartz et al. (2015: Feroniella not in Citrus). Citrons group with the Australian Microcitrus and Eremocitrus, Fortunella links with Citrus madurensis, and Poncirus is then sister to the remainder of Citrus, at least its maternal parent is (Carbonell-Caballero et al. 2015).

Other genera in the family form a single clade within which the classical subfamilies other than Aurantioideae are variously mixed up. Hartley (e.g. 1981, 1997, 2001a, b) had early suggested some generic realignments in Malesian-Pacific Rutaceae that largely ignored the then-conventional subfamilies; this work has held up fairly well in molecular studies. Neither the large genus Melicope nor Acronychia are monophyletic (Appelhans et al. 2014b). Salvo et al. (2008, also 2010; Groppo et al. 2008, 2012) found that Dictamnus was widely separate from the other members that had been included in Ruteae, rather, it linked with Casimoroa and Skimmia (see also Morton & Telmer 2014; Morton 2015). Rutaceae not included in the previous three subfamilies formed a clade [Dictamnus et al. [[Pilocarpus + Ravenia] The Rest]]] (see Poon et al. 2007; Groppo et al. 2008, 2012; Salvo et al. 2010; Morton & Telmer 2014) or were part of a polytomy including them (Bayly et al. 2013b; Morton 2015). One large clade is mostly Old World-Oceanian in distribution, although it includes the Chilean Pitavia (Groppo et al. 2012). Flindersia and relatives have secretory cells in the stem only and septifragal capsules that are perhaps reminiscent of Meliaceae, but their furoquinoline alkaloids, schizogenous cavities, and subterete filaments are consistent with a position in Rutaceae. Euodia and relatives form another moderately to well supported clade (Salvo et al. 2010; Groppo et al. 2012) perhaps sister to a clade including most of the Australian taxa that were included in the old Boronieae (Bayly et al. 2013b; Morton 2015), and a [Zanthoxylum + Toddalia] clade (Groppo et al. 2012: support poor), in turn sister to the Flindersia group (Bayly et al. 2013b). For relationships in Boronia, see Bayly et al. (2015). A final clade (see e.g. Bayley et al. 2013b) includes the North American Ptelea, a largely African Diosmeae (for relationships, see Trinder-Smith et al. 2007), and a largely Central and South American Galipeinae (for relationships, see Kallunki & Groppo 2007: Bruniera et al. 2015: ten monotypic genera....). However, support for some of these groups, and of relationships between and within them, is still rather weak (Groppo et al. 2012; Bayly et al. 2013b; Morton & Telmer 2014). For relationships in the largely Australian Zieria, see Morton (2015) and Barrett et al. (2015); the latter found that the single New Caledonian species, Z. chevalieri, was sister to the rest of the genus, and that about one quarter of the morphological species appeared to be other than monophyletic.

Savolainen et al. (2000b) suggested that Lissocarpaceae should be included here, but a position in Ericales-Ebenaceae is now strongly supported (e.g. Berry et al. 2001).

Classification. Although Cneoroideae (also called Spathelioideae in some recent literature) form a fairly distinct group, inclusion within Rutaceae s.l. is reasonable (Groppo et al. 2008, 2012; Appelhans et al. 2011). Some of the fruit characters previously used to distinguish subfamilies in other Rutaceae are proving unreliable in delimiting major clades (e.g. see Hartley 1981; But et al. 2009), and tribal and subfamilial limits for the most part need overhauling (e.g. Salvo et al. 2008; Poon et al. 2008). For a tribal classification of Cneoroideae, see Appelhans et al. (2011), and for the beginnings of a classification of the rest of the family, I tentatively follow the subbfamilial framework suggested by Morton and Telmer (2014), although the sampling is rather slight (34 species, even if they do represent all subfamilies and tribes). Groppo et al. (2012) recognised only two subfamilies, Rutoideae being split into tribes, but the clades are the same (see also Muellner-Riehl et al. 2016).

Kubitzki et al. (2011) noted that a quarter of the genera in the family are monotypic. Beyond this, generic limits are difficult, especially around Citrus (Carbonell-Caballero et al. 2015 and references), as also in Galipeinae (Kallunki & Groppo 2007), Diosmeae (Trinder-Smith et al. 2007) and around Melicope (Appelhans et al. 2014b); the necessary nomenclatural changes are gradually being made.

Previous Relationships. Cronquist (1981) placed Cneoraceae in his Sapindales which included Rutales more or less as above and then some; Airy Shaw (1966) associated Kirkia with Ptaeroxylaceae, but with hesitation. Hegnauer (1990) included Ptaeroxylum in Meliaceae, although he noted it was chemically more similar to Rutaceae. Thorne (1992) included Harrisonia (ex Simaroubaceae), although no reasons were given.

Botanical Trivia. Ehrlich and Raven (1964) predicted, based on the caterpillars that ate it, that Ptaeroxylon would be found to have alkaloids - it has (e.g. Muscarella et al. 2008).

[Simaroubaceae + Meliaceae]: ?

Age. An age of (48-)44, 40(-36) m.y. for this node is suggested by Wikström et al. (2001) and of (96.5-)88.5(-81) m.y. by Muellner-Riehl et al. (2016).

SIMAROUBACEAE Candolle, nom. cons.   Back to Sapindales


Trees or shrubs; bark very bitter, quassinoids, carboline alkaloids and canthinones [with tryptophane nucleus], ellagic acid +; wood often fluorescing; (nodes multilacunar); pith conspicuous, medullary secretory canals common; sclereids common, oil cells uncommon; (stomata paracytic); leaflets not articulated, vernation also supervolute-curved, margins coarsely toothed to entire, (stipules petiolar); breeding system various; (pedicel articulated), flowers rather small, <1 cm across, (3-)4-6(-8)-merous; K connate or free; A (4, 5, opposite sepals); gynophore short and stout/0, G 1-5(-8), ± postgenitally connate [?level], style short, branches short, recurved, or separate, often ± basal, (apex postgenitally connate), stigmas ± recurved, ± pointed, with elongated receptive zone, dry; ovule 1(-2)/carpel, (hemitropous), micropyle zig-zag/endostomal, (inner integument very long, folded), outer integument 3-10 cells across, inner integument 2-8 cells across, parietal tissue 6-22 cells across, nucellar cap 2-7 cells across; carpels ± separate in fruit; seed (pachychalazal), with undistinguished testa or scattered lignified cells, endotesta often slightly lignified, tegmen crushed, (mesotegmen with reticulate thickenings); (endosperm with hemicellulose reserve), (perisperm +, thin); n = 8-13.

19-22[list]/110: Simaba (25). Largely tropical; a few (e.g. Ailanthus) temperate (map: from Nooteboom 1962; Heywood 1978; Thomas 1990; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; fossils of Ailanthus as black crosses, from Corbett & Manchester 2004 and Clayton et al. 2009, also Japan; fossils of Leitneria as blue crosses, from Clayton et al. 2009). [Photo - Flower, Fruit, Fruit.]

Age. Crown-group Simaroubaceae are dated to around the Cretaceous-Maastrichtian, a little more than 65 m.y.a. (Clayton et al. 2009), or a little older, (84.5-)74(-63) m.y.a. (Muellner-Riehl et al. 2016).

1. Picrasmateae Engler

(Plant all thorny; leaves scales); (stipules cauline); plant mon- or dioecious; fruits drupaceous mericarps.

3/22. Southern U.S.A. to Argentina, 2 spp. Southeast Asia-Malesia.

Age. Crown-group Picrasmateae are some (41-)23.5(-9) m.y.o. (Muellner-Riehl et al. 2016: Hol. + Cas.).

Synonymy: Castelaceae J. Agardh, Holacanthaceae Jadin, nom. inval.

2. The Rest: (leaves with flat surface glands), (stipules +, cauline - some Soulamea); A 10<, (obdiplostemonous); fruits 1-seeded drupelets or samaras; (endosperm with starch [Leitneria]).

Age. The age of this clade is variously suggested to be around 61.1. 52, or 47.5 m.y. (Muellner et al. 2007: inc. Soulamea) or (80.5-)70.5(-60) m.y. (Muellner-Riehl et al. 2016: inc. Picrasma), and the stem age of Ailanthus is about 23-21 m.y.a. (Pfeil & Crisp 2008).

Synonymy: Ailanthaceae J. Agardh, Leitneriaceae Bentham & J. D. Hooker, Soulameaceae Pfeiffer

Within "The Rest" is the clade

[Quassieae Baillon [Samadera + Simaroubeae Dumortier]]: (filaments with with lateral or basal-adaxial scales); (style long, with separate canals); (tissue below embryo sac massive, with central elongated cells - Samadera).

Synonymy: Quassiaceae Bertolini, Simabaceae Horaninow

Evolution. Divergence & Distribution. Most diversification of Simaroubaceae has been in the Caenozoic (Clayton et al. 2009). Despite (or because of?) the fairly good fossil history of the family in the northern hemisphere, the biogeographic hisory of Simaroubaceae is of considerable complexity with much dispersal (and some extinction) needed to explain the current distribution of taxa (Clayton et al. 2009, see also 2007).

Indeed, in the map above it is obvious that distributions of some genera in the past and the present are very different. Fossil Ailanthus is widespread in the Eocene ca 52 m.y.a.; it has not been recorded from the Palaeocene (Corbett & Manchester 2004; see also Clayton et al. 2009: the fossil history of Leitneria and Chaneya, the latter not certainly Simaroubaceae). Fruits identified as Leitneria, a genus now endemic to the U.S.A., have been found in eastern Siberia (Ozerov 2012).

I have put in some phylogenetic structure above because of its effect on our understanding of character evolution; the [Quassia [Samadera + Simarouba etc.]] clade has some distinctive features, but it is well embedded in the family, so these features are not family-level apomorphies.

Plant-Animal Interactions. Leaf webbing caterpillars of the yponomeutoid moth Attevidae are notably common here (Sohn et al. 2013).

Chemistry, Morphology, etc. The quassinoids, probably tetracyclic triterpenes, that are charactistic of and restricted to Simaroubaceae replace other limonoids (Waterman 1993; Vieira & Braz-Felho 2006).

The adult plant of Holacantha is basically a giant, intricately-branched branched thorn; the leaves are reduced to scales.

Although the carpels may seem more or less free, there is often only a single style. The gynoecium of Leitneria is described as having a single carpel with two ovules, of which only one is fertile (Tobe 2011a). Even in taxa with unitegmic ovules, the axis of the embryo and that of the micropyle are offset at a sharp angle, hence the latter can be thought of as being zig-zag. There are reports of other than porogamous fertilization in the family (c.f. Anacardioideae: Rao 1970).

For additional information, see Clayton (2011: general), for chemistry, see Hegnauer (1973, 1990, also 1966, 1989, as Leitneriaceae), and for other information, see Jadin (1901) and Boas (1913), both vegetative anatomy, Webster (1936: wood anatomy), Wiger (1935: embryology), Abbe (1974) and Tobe (2011a, 2013), inflorescence, floral morphology/anatomy and embryology of Leitneria, Endress et al. (1983: carpel morphology), and Fernando and Quinn (1992: pericarp anatomy).

Phylogeny. The overall relationships, [Picrasma etc. [Ailanthus [Soulamea, etc. [Nothospondias* [Picrolemma [Quassia* [Samadera* + Simarouba etc.]]]]]]] are are mostly quite well supported, although support for the position of first clade is not that strong and that for some nodes along the backbone (the genera that might move have an asterisk) could be improved (Clayton et al. 2007; see also M. Sun et al. 2016; Muellner-Riehl et al. 2016). Leitneria is well embedded in the family (Clayton et al. 2007) and has embryological similarities with Brucea, in the same clade (= [Soulamea, etc.]).

Gumillea (ex Cunoniaceae) may belong to Simaroubaceae, although the stamens do not appear to have scales and there are many ovules per carpel - the latter feature in particular is rather odd for any putative sapindalean plant. It has stamens alternate with the petals, so making membership in Picramniales unlikely (and ovule number also militates against this, too).

Classification. Note the demise of Leitneriaceae, the only family previously thought to be restricted to the continental U. S. A. - alack! For the dismemberment of Quassia, see Clayton et al. (2007).

Molecular data suggest the excision of Suriana and its relatives (see Fabales-Surianaceae), Harrisonia (Rutaceae), and Picramnia and Alvaradoa (Picramniales-Picramniaceae) (e.g. Fernando et al. 1995) from the old Simaroubaceae.

MELIACEAE Jussieu, nom. cons.   Back to Sapindales


Trees; tetranortriterpenes, flavones +, bark often rather bitter; secretory cells with resin, etc. +; nodes 5:5; (hairs stellate); leaves (even-pinnate), leaflets not articulated (articulated), (margins toothed); plants often dioecious, but flowers apparently perfect, (3-)5(-8)-merous; K not enclosing C [?level], often connate, (vascular trace single); A connate, 2 X C (5-30 in a single whorl); G (1) [2-6(-many)], postgenitally united, opposite C, hairy, stigma capitate or , wet; ovules ?anatropous, (micropyle (exo-)/bistomal), outer integument 2-5 cells across, inner integument 2-4 cells across, parietal tissue 3-9(-18) cells across, nucellar cap 3-5(-9) cells across, placental obturator common; megaspore mother cells often many; seeds often pachychalazal, coat vascularized, testa undistinguished but thick, endotesta crystalliferous, (tegmen multiplicative), (exotegmen fibrous [Trichilia, Swietenia]); embryo white; ?x = 6, 7.

50[list]/705 - 2 groups below. Pantropical, but largely Old World; plants of the lowlands (map: see Wickens 1976; Pennington 1981; FloraBase 2006; Flora of China 11. 2008; GBIF x.2009; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; Fl. Austral. vol. 26. 2013).

Age. Bell et al. (2010) suggested that the two subfamilies diverged (48-)39, 38(-27) m.y.a.; Muellner et al. (2007, see also 2006) thought that diversification within the family had begun considerably earlier, (98.5-)96, 73.5(-61.5) m.y.a., Koenen et al. (2015) gave ages of (91.5-)80.5, 59.5(-54) m.y., Muellner-Riehl et al. (2016) ages of (89.5-)79.5(-70) m.y., while Wikström et al. (2001) suggested another later date of (40-)36, 30(-26) m.y.a..

For fossil Meliaceae, see Mabberley (2011).

1. Melioideae Arnott

(Suckering shrublets); buds naked; (nodes 3:3); (leaves two-ranked - Turraea), (simple; bipinnate); C (-14; connate); (style hollow); ovules 1-3(-many)/carpel; fruit a loculicidal capsule, (berry, drupe, nut, inflated); seeds usu. with aril [funicular in Naregamia] or sarcotesta, (dry, winged - Quivisianthe); (embryo chlorophyllous - Trichilia, Nymania), (endosperm +); n = 8, 11, 12, 14, 15, 18 ... 140.

36/585. Aglaia (120), Dysoxylum (80), Guarea (75), Trichilia (70), Turraea (60), Chisocheton (50). Pantropical, but largely Old World.

Age. Diversification within Melioideae began (91-)78, 70(-58.5) m.y.a. (Muellner et al. 2006, 2007 - the latter a little bit older), (82-)70(-57.5) m.y.a. (Muellner-Riehl et al. 2016) or (83-)72.5, 54(-49) m.y. (Koenen et al. 2015).

Synonymy: Aitoniaceae R. A. Dyer, nom. illeg.

2. Cedreloideae Arnott

Buds perulate (naked - Capuronianthus); (leaves opposite); (C connate); (A at least partly free); (nectary 0); ovules (2 [Capuronianthus]) 3-many/carpel, collateral; fruit a septifragal capsule, valves falling off, columella persisting, (columella slight); seeds winged, (not winged, with massive woody or corky testa); n = 13, 18, 23, 25, 26, 28.

14/56: Cedrela (14). Pantropical, but largely Old World. [Photo - Flower, Fruit.]

Age. Diversification within Cedreloideae began (86-)75, 67.5(-58) m.y.a. (Muellner et al. (2006, 2007), (75-)65(-55) m.y.a. (Muellner-Riehl et al. 2016), or (59.3-)48.5, 38.6(-33) m.y. (Koenen et al. 2015).

Synonymy: Cedrelaceae R. Brown, Swieteniaceae E. D. M. Kirchner

Evolution. Divergence & Distribution. Muellner et al. (2006) discussed the biogeography of Meliaceae, suggesting its origin in Africa and subsequent dispersal. Koenen et al. (2015) also suggest an Old World origin for the family, and although one thinks of it as being characteristic of l.t.r.f., they suggest that its common ancestor was a deciduous tree of seasonal or montane habitats. Indeed, crown-group ages of rainforest clades in the family are a mere 23 m.y.o. (Late Oligocene/Early Miocene), their stem-group ages are Eocene and they may have been quite species rich in pre-Late Oligocene times, but with extinction then and subsequent diversification (Keunen et al. 2015).

For the biogeography of Aglaia, see Muellner et al. (2008b) and Grudinski et al. (2014a), the latter suggesting Oligocene-Miocene rather than Eocene diversification; movement was from West Malesia eastwards.

Ecology & Physiology. Although only a small family, Meliaceae make up 17% of all trees >10 cm d.b.h. in Sumatra (Mabberley 2011). Xylocarpus is a well-known mangrove genus; for some information, see articles in Ann. Bot. 115(3). 2015, also the mangrove habitat.

Pollination Biology & Seed Dispersal. Most Meliaceae have a well-developed floral tube which is formed by the connation of the filaments - a rather uncommon way of forming a tube. The pistillode in staminate flowers is well developed, the result being that staminate and carpellate flowers are very similar functionally, although the staminal tube in the former is often somewhat narrower. The whole apex of the style is commonly more or less massively swollen and is sometimes involved in secondary pollen presentation, as in Vavaea (Ladd 1994).

Animal dispersal is common in Meliodeae; for detailed studies of the dispersal of arillate-type seeds of Malesian Aglaia, see Pannell and Koziol (1987). Wind dispersal is common in Cedreloideae.

Plant/Animal Interactions. For the diversity of ant-attended extrafloral nectaries in Cedreloideae, especially Carapa see Kenfack et al. 2014).

Vegetative Variation. Munronia is ± herbaceous. Most species of Guarea (tropical America) and Chisocheton (Malesia), both Melioideae, have indefinitely growing leaves, although despite this distinctive similarity they are not much related (Koenen et al. 2015). In Guarea the apical part of the leaf is shoot-like in its gene expression (Tsukaya 2005). The leaves of Chisocheton can be rooted (Fisher & Rutishauser 1990), and then they continue to grow for a long time, although I do not know that a tree has ever been produced from a leaf. Species of Chisocheton such as C. pohlianus have an epiphyllous inflorescence, flowers appearing between the leaflets; specimens have been misidentified as Rubiaceae! Capuronianthus (Swietenioideae) has opposite, compound leaves, while the simple-leaved Vavaea and Turraea (both Melioideae) look rather unmeliaceous except when in flower; the leaves of the latter genus can even be two-ranked and lack articulations.

Economic Importance. Azadirachta indica (Melia azadirachta) is the neem tree (for an account, see Singh et al. 2009); the wood of Swietenia spp. is the prized mahogany.

Chemistry, Morphology, etc. Although it was thought that the two subfamilies could be separated by their limonoid types, work on Quivisianthe (Melioideae) suggests that the distinction may not be that simple (Mulholland et al. 2000). Sieve tube plastids with protein crystalloids and starch occur in Melia and Azederach. Walsura often has leaflets with ± pulvinate petiolules and prominent reticulate venation.

Gouvêa et al. (2008b) drew the flowers of Swietenia as being inverted; carpellate flowers are the first to be produced in the cymose inflorescences. The filaments of Vavaea are largely free, as are those of Cedrela and Toona (Cedreloideae-Cedreleae). Indeed, Cedreleae are rather different florally from other Meliaceae, but features found there such as more or less free stamens may be derived, not plesiomorphous as one might think (c.f. Gouvêa et al. 2008a). In Walsura the stamens are also more or less free, and the fruit is often 1-seeded. There is considerable variation in seed morphology and development (e.g. Wiger 1935; Corner 1976), even within the subfamilies, and this will have to be integrated with the phylogeny as it develops.

For chemistry, see Hegnauer (1969, 1990) and Mulholland et al. (2000), for embryology, etc., see Wiger (1935), Paetow (1931), and N. C. Nair (1962, 1970 and references), and for general information, see Mabberley et al. (1995: esp. Malesia), Mabberley (2011) and van Wyk (in Dahlgren & van Wyk 1988: Nymania, distinctive flowers and fruits), T. D. Pennington and Styles (1975: generic monograph), Pennington (1981: monograph of Neotropical Meliaceae), and Pannell (1992: monograph of Aglaia).

Phylogeny. Cedreloideae (Swietenioideae) and Melioideae are clearly monophyletic (Oon et al. 2000: one gene, Cedreloideae not well supported; Muellner et al. 2003: three genes; Muellner et al. 2006: rbcL alone, sampling better; Koenen et al. 2015; Muellner-Riehl et al. 2016). Two Malagasy genera previously segregated as separate subfamilies, Quivisianthe and Capuronianthus, are embedded in Melioideae and Cedreloideae respectively (e.g. Muellner et al. 2003, 2006; Koenen et al. 2015; M. Sun et al. 2016, q.v. for more details).

Within Melioideae, Melieae (including Owenia) are sister to the rest, but with only moderate support (stronger in Muellner-Riehl et al. 2016); relationships along the backbone of the rest of the rather pectinate ITS tree are poorly supported, but rather better resolved by rbcL data (Muellner at al. 2008a). Owenia, paraphyletic and including Melia is also sister to other Melioideae in Koenen et al. (2015), who suggest that there may be four more small clades successively sister to other Melioideae. For relationships in Aglaia, see Muellner et al. (2005) and Grudinski et al. (2014a, b), in Chisocheton, see Fukuda et al. (2003), and in Trichilia, where relationships are [T. havanensis [African species + American species]], see Clarkson et al. (2016: ITS only).

Within Cedreloideae {Chukrasia + Schmardaea] are sister to other members of the subfamily (Koenen et al. 2015; Muellner-Riehl et al. 2016). For relationships in Neotropical Cedreleae, see Muellner et al. (2009).

Classification. Cedreloideae used to be called Swietenioideae. Generic limits in Melioideae in particular are uncertain, genera like Owenia, Lepidotrichilia, Dysoxylum, and Aglaia all being more or less para/polyphyletic (Koenen et al. 2015), and the limits of Trichilia will also bear rexamination (Clarkson et al. 2016).

The connection between species limits in Aglaia and phylogenetic relationships as they are currently understood is somewhat unclear (Grudinski et al. 2014b).

Thanks. I am grateful to David Kenfack for useful information.