EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; glycolate oxidase +, glycolate metabolism in leaf peroxisomes [glyoxysomes], acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], 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; 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, asymmetrical; oogamy; sporophyte +*, multicellular, growth 3-dimensional*, 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 [= MicroTubule Organizing Centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades 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.
Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
II. TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, 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]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); borate cross-linked rhamnogalactan II, xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia in strobili, sporangia adaxial, columella 0; tapetum glandular; sporophyte-gametophyte junction lacking dead gametophytic cells, mucilage, ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; embryo suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], 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; nuclear genome [1C] 7.6-10 pg [mode]; 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 axillary, buds exogenous; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
SEED PLANTS† / SPERMATOPHYTA†
Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; 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, free-nuclear/syncytial to start with, walls then coming to surround the individual nuclei, process proceeding centripetally.
EXTANT SEED PLANTS
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]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated, gravitropism response fast; 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.; branching by 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; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= 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 event], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
IID. ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating 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, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates 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 randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], 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 = T, petal-like, 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 restricted to the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, 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, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (ca 10-)80-20,000 µm h-1, tube 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 gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], 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 [2C] (0.57-)1.45(-3.71) [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 IR expansions, 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 monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (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 [or next node up]; fruit dry [very labile].
EUDICOTS: (Myricetin +), 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], short [<2 x length of ovary]; seed coat?; palaeotetraploidy event.
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ genome duplication [allopolyploidy, 4x x 2x], x = 3 x 7 = 21, 2C genome size (0.79-)1.05(-1.41) pg, PI-dB motif +; small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE / [SANTALALES, CARYOPHYLLALES, SAXIFRAGALES, DILLENIALES, VITALES, ROSIDAE, [BERBERIDOPSIDALES + ASTERIDAE]: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = K + C, K enclosing the flower in bud, with three or more traces, odd K adaxial, C with single trace; A = 2x K/C, in two whorls, alternating, (many, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], when 5 opposite K, whorled, placentation axile, style +, stigma not decurrent, compitum + [one position]; endosperm nuclear/coenocytic; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression, RNase-based gametophytic incompatibility system present.
Phylogeny. Prior to the seventh version of this site asterids were part of a major polytomy that included rosids, Berberidopsidales, Santalales, and Caryophyllales, but then the order of branching below the asterids seemed to be stabilizing, perhaps with a clade [Berberidopsidales [Santalales [Caryophyllales + Asterids]]] while rosid relationships seemed to be [Saxifragales [Vitales + Rosids]]]. However, recent work suggests a polytomy is indeed probably the best way to visualize relationships around here at present. So for further discussion of relationships at the base of asterids and rosids, see the Pentapetalae node.
[SAXIFRAGALES + ROSIDS] / ROSANAE Takhtajan / SUPERROSIDAE: ??
ROSIDS / ROSIDAE: anthers ± dorsifixed, transition to filament narrow, connective thin.
[ROSID I + ROSID II]: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.
ROSID II / MALVIDAE / [[GERANIALES + MYRTALES] [CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]]: ?
[CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]: ?
[PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]: ovules 2/carpel, apical.
[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) Ma (N. Zhang et al. 2012; see also Xue et al. 2012), (102-)96(-90) and (80-)76(-72) Ma (H. Wang et al. 2009), ca 98.25 Ma (Magallón & Castillo 2009), around 93.6-89.9 Ma (Naumann et al. 2013), about 103.5 Ma (Hohmann et al. 2015), ca 111 Ma (Foster et al. 2016a: q.v. for details) or (116.9-)111.5(-106.2) Ma (Muellner-Riehl et al. 2016).
Evolution: Divergence & Distribution. For integument thickness, a possible apomorphy, which, however, reverses, see Endress and Matthew (2006a), moreover, its condition is unclear in Huerteales, etc..
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 109-66Ma 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. A position at this node is one possibility.
There are suggestions that the chloroplast infA gene was lost or became a pseudogene at this node (Logacheva & Shipunov 2017; see also Millen et al. 2001; Su et al. 2014).
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 and 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; inflorescence branches, at least, cymose; A 2 x 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]; exotegmen not fibrous; (embryo chlorophyllous). - 9 families, 479 genera, 6,570 species.
Includes Anacardiaceae, Biebersteiniaceae, Burseraceae, Kirkiaceae, Meliaceae, Nitrariaceae, Rutaceae, Sapindaceae, Simaroubaceae.
Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the precise 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).
Age. The age of crown-group Sapindales has been variously estimated as 117.4, 104.9, and 90.5 Ma (Muellner et al. 2007: c.f. topology) or (110.5-)105(-99) Ma (Muellner-Riehl et al. 2016).
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 Ma 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). Tölke et al. (2018b) discuss the little that is known about osmophores in sapindalean flowers.
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 psyllid 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, and although many Sapindaceae, for example, are more strongly monosymmetric, it is oblique in e.g. Aesculus (Cao et al. 2017). The flowers are often imperfect, but since staminate and carpelate flowers have well-developed pistillodes and staminodes respectively, they can be difficult to distinguish. Floral tubes formed by connate or closely adpressed and flattened filaments occur throughout Meliaceae, in a number of Rutaceae, and in Boswellia dioscorides (Burseraceae); they are uncommon elsewhere. 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. 2006b, 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; H.-T. Li et al. 2019: support very poor), while the relationships [Nitrariaceae [Biebersteiniaceae ...]] in Z.-D. Chen et al. (2016) also had little support; Baker et al. (2021: see Seed Plant Tree) found the relationships [Biebersteiniaceae [Nitrariaceae ...]. However, H.-T. Li et al. (2019) found strong support for a [Meliaceae [Simaroubaceae + Rutaceae]] clade, relationships which have been recovered before (e.g. Magallón et al 2015; Zeng et al. 2017) and this topology is followed below.
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.
Relationships. Bretschneideraceae and Akaniaceae (= Akaniaceae here, see Brassicales here) have been associated with Sapindales, Bretschneidera in particular looking very like a member of Sapindaceae, however, the myrosin cells in the former were not considered to be all that important (Cronquist 1981; Takhtajan 1997).
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 (107.6-)94.5(-79.4) Ma (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 terminal, axis indeterminate; C clawed, (denticulate); nectary glands opposite K; anther thecae opening by single slit; tapetal cells up to 12-nucleate, nuclei fuse; pollen 3-celled, exine striate; gynophore +, short, G , styles separate, impressed, apically connate, stigma capitate; ovule 1/carpel, 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 +/-, pentaploid, embryo somewhat curved, cotyledons foliaceous, incumbent; n = 5, x = ?
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 Ma (Muellner et al. 2007) or (55-)34.7(-16.1) Ma (Muellner-Riehl et al. 2016).
Chemistry, Morphology, etc.. At least some species of Biebersteinia are foul-smelling.
The antipetalous stamens are longest. Takhtajan (1997) and Yamamoto et al. (2014) both described the ovules as being unitegmic; however, Boesewinkel (1988, 1997) thought that the ovules were bitegmic and the micropyle was bistomal. 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).
See also Baillon (1874), Kunth (1912) and Muellner (2011), all general, Hegnauer (1989, as Geraniaceae) and Tzakou et al. (2001: fatty acids), both chemistry, and Kamelina and Konnova (1989: embryology).
Biebersteinia is little known.
Relationships. Biebersteinia has often been more or less closely associated with Geraniaceae (Geraniales) in the past (e.g. Cronquist 1981; Takhtajan 1997). Boesewinkel (1988, 1997), who thought that the ovules were bitegmic (but see above), saw a similarity of the seed coat of Biebersteinia and that of Vivianaceae (= Geraniales-Francoaceae-Vivianeae), especially when young, with both exotesta and endotegmen being tanniniferous.
NITRARIACEAE Lindley - Back to Sapindales
ß-carboline alkaloids +, ethereal oils?, saponins 0; 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 thick/fleshy, ?vernation, simple, ± deeply lobed, stipules +; inflorescence terminal; K (connate); C protects the flower in bud; A 15, filament bases broad, flattened; tapetal cells binucleate; G [3 (4)], stigma as commissural compital lines ± decurrent down style, dry; ovule 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; exotesta cells inflated or not; endotesta short palisade, or not; x = 12 (?11, ?6).
3 [list]/13. 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 Ma (Muellner et al. 2007) or (83.8-)63.1(-41.8) Ma (Muellner-Riehl et al. 2016).
1. Nitraria L.
Plant shrubby, (with thorns); xylem parenchyma aliform-confluent; short shoots +; lamina (toothed or lobed at apex), stipules scarious [?not associated with all leaves], ?intrapetiolar; nectary +; A in triplets, opposite K; G [(6)], style broad at base, tapering; ovules 1/carpel, apotropous; fruit a 1-seeded drupe, mesocarp woody, pock-marked; endosperm slight, embryo chlorophyllous; n = 12 and polyploidy.
1/6. Europe to Asia, the Sahara, Australia.
Age. Crown-group Nitraria is some (51.5-)33.4(-17.6) Ma (Muellner-Riehl et al. 2016).
[Peganum + Tetradiclis]: plant herbaceous; raphides +; stomata in longitudinal bands of small cells; leaves deeply lobed; style impressed; funicle long; testa mucilaginous.
Age. This node is (76.9-)53.4(-33.1) Ma (Muellner-Riehl et al. 2016).
2. Peganum L.
Plant also subshrub; mycorrhizae 0; mucilaginous cells few; two adjacent leaves/node, or one leaf/node, (barely lobed), stipules tiny; flowers single, leaf opposed; K valvate; outer A in pairs opposite C; ovules many/carpel; megaspore mother cells several; fruit a loculicidal capsule or berry; testa weakly multiplicative, exo- and endotesta palisade, endotegmen ± fibrous; endosperm +; n = 12
1/6. Europe to Asia, east Mexico.
Synonymy: Peganaceae Takhtajan
3. Tetradiclis M. Bieberstein
Plant annual; leaves opposite or spiral, very fleshy, (entire), stipules small; inflorescence spike-like, cymose; flowers (3-)4-merous; A = and opposite K, filaments subulate; nectary 0; G , each divided into three parts, placentation basal, placentae long, style ± gynobasic, ± hollow; ovules to ca 6/carpel [4 ovules in central locellus, 1 each in lateral locelli]; fruit a loculicidal capsule [seeds in central locellus only released], endotegmen not fibrous; endosperm slight; 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, salt (NaCl) concentration in Nitraria in particular reaching 14% (Sheahan 2011 for references).
Chemistry, Morphology, etc.. Takhtajan (1997) says that stipules are absent in Tetradiclis; they are present, if small. There may be colleters here and elsewhere in the familu. In general, leaf morphology and nodal anatomy need attention.
Bachelier et al. (2011) discuss floral morphology in detail, discussing features like androecial morphology that have 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).
Most literature has these genera in Zygophyllaceae. 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), Sheahan and Cutler (1993) provide details of anatomy, Bachelier et al. (2011: 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).
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 as circumscribed here are not remotely close to Nitrariaceae, and their similarities may be because both grow in dry and warm habitats; note that no endothelium has been recorded in members of Nitrariaceae (Kapil & Tiwari 1978: c.f. Zygophyllaceae s. str.).
Botanical Trivia. For some reason (?smell) even camels will not eat Peganum (Sheahan 2011).
[[Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Meliaceae [Simaroubaceae + Rutaceae]]]]: wood silicified or with SiO2 grains; tension wood +; resin canals +; persistent floral apex in the center of the gynoecium [?this level]; ovules often 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) Ma and Bell et al. (2010) suggested an age of around (75-)71(-70) My; about 61.75 Ma is the age in Naumann et al. (2013), ca 73.4 Ma in Tank et al. (2015: Table S2), (107.8-)102(-96.1) Ma in Muellner-Riehl et al. (2016), and (83.4-)81.5(-79.9) Ma in Magallón et al. (2018).
Evolution: Divergence & Distribution. Diversification rates may have increased at this node in a nested fashion, (83.4-)81.5(-79.9) Mya and ca 4 Ma before (Magallón et al. 2018).
Ecology & Physiology. All families in this clade (bar Kirkiaceae) include common trees at least 10 cm across in Amazonian forests and 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).
Chemistry, Morphology, etc.. For resin canals in this clade, perhaps only dubiously an apomorphy, see Prado and Demarco (2018).
[Kirkiaceae [Anacardiaceae + Burseraceae]]: cuticle waxes often 0; inflorescence thyrsoid [panicle of cymes]; flowers small [<1 cm across]; K ± connate, C protective in bud; pollen (exine striate); G adnate to central receptacular apex, synascidiate, stigma with uniseriate multicellular papillae, wet; fruit with 1 seed/carpel, endocarp well developed.
Age. The age of this node is somewhere around 93.6, 83.6 or 74.1 Ma (Muellner et al. 2007), (127-)116(-105) Ma (Weeks et al. 2014) or (102.9-)94.6(-85.6) Ma (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?; resin canals?; nodes?; petiole with medullary bundles; glandular hairs with multiseriate stalks; stomata ?anomocytic; leaves ± opposite to spiral, leaflet margins serrate; plants monoecious; inflorescence subdichasial, ultimate branches monochasial; flowers 4-merous; K basally connate, decussate, valvate → open, C with adaxial-basal multicellular glandular hairs; staminate flowers: A = and opposite K; pollen syncolpate; nectary broad, well developed; pistillode +; carpelate flowers: staminodes +; G [4 (8)], ?orientation, extra "loculus" ± developed, receptacle apex convex, swollen, glandular, styluli closely adpressed, erect, finally spreading, apices postgenitally connate, stigmas ± punctiform; ovule usu. 1/carpel, micropyle bistomal, long [to 2 x length of nucellus], outer integument 2-3 cells across, cells much swollen in micropylar region, inner integument 3-4 cells across, parietal tissue ca 14 cells across; fruit a schizocarp, mericarps pendulous from columella; testa "very thin"; endosperm ?type, embryo curved; n = ?, x = ?
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 carpelate 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 i.a. they lack quassinoids and limonoids.
[Anacardiaceae + Burseraceae]: biflavonoids; phloem with vertical intercellular secretory canals, surrounded by a light-coloured, sinuous, sclerenchymatous band [not easy to see]; silicification of wood prominent, (vessel elements with scalariform or reticulate perforations); glandular hairs with uniseriate stalks; (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 2< layers, not oriented, lignified.
Age. Bell et al. (2010) suggested that the two families diverged (73-)64(-56) or (51-)50(-49) Ma, Tank et al. (2015: Table S1, S2) around 0/59.6 Ma, while Wikström et al. (2001) gave ages of (56-)51, 47(-42) Ma, Muellner-Riehl et al. (2016) ages of (97-)87.5(-78.5) Ma, and Weeks et al. (2014) ages of (121-)108(-95) My; a mere 37.7 Ma is the age in Naumann et al. (2013).
Fossils assignable to Burseraceae/Anacardiaceae are known from the early Eocene in England ca 50 Ma (Collinson & Cleal 2001) and from the Deccan Traps of India ce 66 Ma (Wheeler et al. 2017).
Evolution: Divergence & Distribution. Weeks et al. (2014) compared the path of evolution in Burseraceae and Anacardiaceae using clades of the same age and about the same size, and they noted 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 unoriented sclerified and often crystalliferous cells (Wannan & Quinn 1990), as found in Anacardiaceae-Spondiadoideae, and also in Buchanania, Campnosperma and Pentaspadon, included in Anacardioideae (e.g. 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 some Burseraceae and perhaps it, too, is plesiomorphic within the whole clade. Hill (1933, 1937) and others describe germination of such fruits, noting how the operculum gets pushed off by the germinating seed, and also that opercula might have different morphologies, even within the one family.
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; colleters +; leaflets not articulated, margins usu. entire, base of petiole often swollen; breeding system various; flowers (3-)5(-7)-merous, protogynous; (andro/gynophore +), styluli ± separate, terminal to gynobasic, (apex postgenitally connate), stigma capitate (lobed), dry; ovule 1/carpel, apical, apotropous, ± anatropous, micropyle zig-zag (endostomal), funicle long, massive, ponticulus + [?kind of obturator]; fruit a drupe, inner part complex, layered, endocarp crystalliferous; seed often ± pachychalazal, vascular bundle in raphe amphicribral; endosperm oily (and starchy), usu. little-0 at maturity, cotyledons large; x = 15 (?16), nuclear genome [1 C] (0.031-)0.605(-13.019) pg/(440-)1819(-9144) Mb.
80 [list]/873 - five groups below. Tropical, esp. Palaeotropics, 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 Ma (Muellner et al. 2007), (128-)97(-83) Ma (Weeks et al. 2014) and (87-)75(-63.5) Ma (Muellner-Riehl et al. 2016).
Pentaspadon J. D. Hooker
Plant deciduous; dermatitis-inducing metabolites +; flowers perfect; A 5 opposite K/5 + 5 staminodes/10; style short, stigma subcapitate; endocarp with irregularly-oriented sclereids; seeds somewhat flattened; n = ?
1/6. Vietnam to Malesia and the Solomon Islands.
The rest: flowers often imperfect; staminate flowers: A 10; pistilode +; carpelate flowers: staminodes +.
Spondiadoideae de Candolle
(Plant deciduous); (dermatitis-inducing metabolites + - Spondias); pedicels often articulated; G [(3-)4-5], (± free), (style 1), (styluli well separated), stigma little expanded; hypostase +; fruit usually 2< seeded, pericarp with lacuna(e)/not, inner mesocarp of encircling fibres (also/or brachysclereids), operculum +/0; exotestal cells (and hypodermis) sclereidal (not), tegmen ± 0, hypostase persistent, saddle-shaped; embryo straight (curved - Dracontomelon); n = 15, 16, 18.
6/31: Spondias (16). Mexico to southeast Brazil and Bolivia (some Spondias), Old World tropics to the Pacific.
Age. Fruits of Dracontomelon (as Pseudosclerocarya) are known in early Eocene deposits of the London Clay (references in Herrera et al. 2019a).
Synonymy: Spondiadaceae Martynov
Dermatitis-inducing metabolites +; hairs scales/stellate; leaves simple, lamina (auriculate at base); pedicels articulated; G 2, style 0, stigma disciform; fruit 1-seeded, stone lacking germination pores, etc., central lacuna +, fibres 0, inner mesocarp isodiametric sclereids, locular envelope 0; embryo strongly curved [U-shaped]; n = ?
1/16. Tropical, not mainland Africa.
(Plant deciduous); leaves simple; flowers perfect; anthers sagittae; G 4-6, free, 1 fertile, styluli +, stigma obliquely truncate; fruit 1-seeded, lacking germination pores, etc., lacunae 0, inner mesocarp 2-4 layers palisade brachysclereids over irregularly-oriented sclereids, locular envelope +; n = ?
1/22. India, Sri Lanka, south China through Malesia to northeast Australia, west Pacific.
The Sclerocarya Hochst. complex
(Plant deciduous); leaves (unifoliolate), (leaflets serrate); (pedicels articulated); A (-many - Sclerocarya); G (1 [Solenocarpus, Haplospondias]-)4-5(-12)]; hypostase +; fruit usually 2< seeded, pericarp with lacuna(e)/not, inner mesocarp of encircling fibres [locular envelope], operculum +/0; exotestal cells (and hypodermis) sclereidal (not), tegmen ± 0, hypostase persistent, saddle-shaped; (embryo C-shaped - e.g. Lannea), (cotyledons reniform); n = 12(-15, 20).
11/72: Lannea (40). Tropical, inc. Baja California, northeast Australia, west Pacific.
(Vines; perennial herbs), (plant deciduous); exudate gums and resins, 5-deoxyflavonoids, also alkylcathechols and alkylresorcinols [phenols with unsaturated side chains - dermatitis-inducing metabolites] +; (cork cortical); leaves (opposite), frequently simple, (lobed); (flowers monosymmetric), pedicels usu. articulated; (hypanthium +); K and/or C (0), (P /K and C [Toxicodendron] single trace); (nectary + [Mangifera]/glandular hairs on staminal tube [Anacardium]); A (1 [+ staminodes]), 5 [opposite K], 10 (many), (basally connate); (nectary 0); G [3(-6)], (inferior), (highly) asymmetric, one carpel fertile, symplicate zone?, styluli terminal to gynobasic, stigma ± capitate/style, stigma ± lobed, stigma with multicellular papillae, (punctate); ovule apical to basal, (unitegmic, usu. apically bifid, 4-5 cells across), nucellus 5-20 cells across, (apex exposed - Pistacia), ovule (almost circinotropous), (funicle with "knees" and other outgrowths), (ponticulus +); (chalazogamy +); fruit 1-seeded, often asymmetric, ± flattened, (K much accrescent, forming wings), (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); testa collapsed, tegmen undifferentiated/endotegmen lignified; (embryo chlorophyllous), (cotyledons folded - Mangifera); n = (7-12)15(-16), etc..
60/735: Searsia (120), Semecarpus (72), Mangifera (68), Schinus (50), Ozoroa (40[+]). Largely tropical, also temperate.
Age. Woods of Anacardioxylon and Dracontomeloxylon from Cretaceous-Maastrichtian/Palaeocene-Danian deposits in the Deccan Traps ca 66 Ma may belong to Anacardioideae (Wheeler et al. 2017).
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 many ages in the family, see Muellner-Riehl et al. (2016); note the narrow circumscription of the Spondias clade there. For the early Caenozoic fossil history of what are now East Asian endemic Anacardiaceae, see Manchester et al. (2009) - Choerospondias, now growing from N.E. India eastwards, 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; although the African Fegimanra, sister to Anacardium, also has swollen pedicels, they are clearly different (Manchester et al. 2007b; Pell et al. 2011; Collinson et al. 2012 for this and other fossil records). Distinctive fruits that have been identified as the Old World Dracontomelon are known from the Late Eocene of Panama in deposits some 40-37 Ma old and also younger, ca 20 Ma (Herrera et al. 2012, 2019a), while wood identified as that of the Old World Mangifera is reported from Late Middle Eocene deposits ca 39 Ma on the Pacific side of Peru (Woodcock et al. 2017; for Palaeocene leaf fossils from India, see Mehrotra et al. 1998; Q. Li et al. 2019 - ?drift).
Weeks et al. (2014) emphasized the diversity of fruit dispersal types in the family and 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.
Pell (2004) looked at the morphology of the whole family from a phylogenetic point of view. Herrera et al. (2018) catalogued the extensive variation in fruit morphology of Spondiadoideae, in which several different structures are involved in germination, there are often various lacunae, and the woody/stony layer (endocarp s.l.) is nearly always well developed and sometimes remarkably elaborated - details of correlation are to be worked out.
Pollination Biology & Seed Dispersal. Pistacia and Amphipterygium (see Julianaceae below) are both wind pollinated, dioecious, and have reduced flowers (Bachelier & Endress 2007b). Tölke et al. (2018a) summarized the diversity of netar and nectaries in the family, noting the variation in nectar composition, both infraspecific and between closely related taxa, while Tölke et al. (2018b) described the osmophores that produce the very different floral scents of Anacardium and Mangifera. Goldberg et al. (2017) looked at the evolution of breeding systems in Rhus. 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 wings of the fruit may be formed from broad bracts that are adnate to it (Dobinea), the flattened peduncle of the inflorescence (Amphipterygium), much enlarged sepals (Parishia) or petals (Swintonia), or the fruits may be samaras (Loxopterygium), while in Cotinus hairs on the pedicels help in the wind dispersal of the small, nut-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. Germination of the stones of the drupaceous fruits of Spondiadoideae is often faciltated by various opercula, etc., that have developed (see Herrera et al. 2018 for references).
Plant/Animal Interactions. Aphids (Fordinae) that form distinctive galls are closely associated with species of Pistacia and Rhus (H. C. Zhang & Qiao 2007, 2008; Inbar 2009), the sometimes massive, spherical galls produce terpenes that dissuade goats, at least, from eating them (Rostás et al. 2013). Melaphidina aphids have diversified in part by occupying different sites on the one plant species. The primary host of Fordinae-Melaphina is Rhus, the secondary hosts are mosses, and those of Fordina are Pistacia and the roots of Poaceae respectively (Zhang & Qiao 2007). Crown-group Melaphidina have been dated to (79-)73.3(-68.3) Ma (Ren et al. 2017). 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).
Economic Importance. Galls on Rhus produce industrial tannins and and are also used for medicines (Wool 2004).
Chemistry, Morphology, etc.. 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 third or so of the genera may have such compounds, although Mitchell (1990) found that only half of these had been studied in any detail, so it is unclear if Spondias should be included in this list; see also Ding Hou (1978), Aguilar-Ortigosa et al. (2003) and Aguilar-Ortigosa and Sosa (2004).
Schweingruber et al. (2011) emphasize the abundance of tension wood here. Branching in Anacardium may occur on the current flush.
Flowers in Anacardiaceae are small but show a considerable amount of variation. Hardly surprisingly, wind-pollinated taxa often lack a nectariferous 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 (Bachelier & Endress 2009; Sokoloff et al. 2017 for discussion). More generally, the position of the carpel, when single, suggests that the flower is obliquely symmetric (Ronse de Craene 2010). For infraspecific variation in style number - 1, 3 - see Gonzàlez and Vesprini (2010). In Anacardioideae the floral/receptacle apex is sometimes quite short (Bachelier & Endress 2009). In Lithraea, 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). A ponticulus, a protrusion from the funicle, is common, and it appears to be a strongly developed portion of the outer integument that is otherwise adnate to the funicle; it also occurs in taxa with single integuments like Lithraea (Carmello-Guerreiro & Sartori Poli (2005). The fruits are drupes, and the wall, the stone in particular, are layered, some of the layers being produced from division of the endocarpial layer, however, fruits may not be drupes in the strict sense (Wannan & Quinn 1990; Gonzàlez & Vesprini 2010). The fruit often develops well before the seed, and the testa well before the embryo, so for some time the fruit, although quite laege, is almost empty (Copeland 1955, 1962). Ovule and pericarp variation in the family is considerable and needs to be put in a phylogenetic context.
For general information, see Ding Hou (1978), Pell et al. (2011) and Michell et al. (2006). 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 multiseriate ± capitate colleters, see Lacchia et al. (2016), for inflorescences, see Barfod (1988), for floral morphology, Wannan and Quinn (1991), for some embryology, see Grimm (1912), Copeland and Doyel (1940) and Copeland (1955), for fruit anatomy, see Pienaar and von Teichman (1998), for ovules, fruit and seed, see von Teichman and van Wyk (1988) and Carmello-Guerreiro and Sartori Poli (1999), for seed anatomy, see von Teichman (1991, 1994, and references), and for germination of Spondiadoideae, see Hill (1937).
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, included in a study by Chayamarit (1997: sampling limited, relationships different from 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]]]. Fruit anatomy (Herera et al. 2018) suggests that although Buchanania may be in this region, Campnosperma is unlikeley to be.
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). Silva-Luz et al. (2018: much morphology, previous sections, etc., do not hold) examined relationships in Schinus, closely related to Lithraea, Mauria and Euroschinus; [S. terebinthifolia + S. weinmanniifolia] form a clade sister to the rest of the genus.
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 Moffett (2007), Yi et al. (2007) and references, and for a sectional classification of Schinus, see Silva-Luz et al. (2018).
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 carpelate flowers that lack a perianth but are surrounded by an involucre, and finally Podoaceae, with opposite leaves and carpelate 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 serrate, base often ± symmetrical, petiolules and petioles often pulvinate; dioecy common; K induplicate-valvate, ± connate, C valvate; A obdiplostemonous [check]; 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; x = 13 (?14), nuclear genome [1 C] (0.033-)0.701(-16.429) pg.
19[list]/775 (860) - 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) Ma; the estimate in Weeks et al. (2005: n.b. in text as the divergence between Anacardiaceae and Burseraceae) is (61.9-)60(-58.1) Ma, in Muellner-Riehl et al. (2016) it is (85.5-)75.2(-64.5) Ma, and in Weeks et al. (2014) the age is (106-)91(-78) Ma; an age of 120 Ma 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, spinose [spine = petiole apex/rhachis base], axillary bud on base of spine; carpelate inflorescence racemose; G [9-12], symplicate zone short, ovary strongly 9-12-furrowed, style ± 0; ovules superposed; pericarp septifragal, columella massive, strongly ribbed, pyrenes free, apically radially winged, [between the ribs]; germinal epigeal, cotyledons entire.
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 homogeneous); snail glands + [curled ± uniseriate glandular hairs]; (lamina margins entire), ((pseudo-)stipules +); (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, stone 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 is some (60.2-)58(-55.8) Ma (Weeks et al. 2005), (71.7-)62.9(-54.7) Ma (Muellner-Riehl et al. 2016) or (66.5-)63.4, 54.2(-48.8) Ma (Fine et al. 2014), but some estimates, at (116-)98, 92.7(-74.8) Ma, are older (Becerra et al. 2012), and yet older in Becerra (2003, 2005).
2. Garugeae Marchand
(Plant decidous); (cork cambium deeper - Santiria); petiole bundle with medullary strands; (leaflets not pulvinate), ("stipules" +, petiolar or cauline, laciniate to entire); dioecious, or flowers perfect; flowers often 3-merous, (hypanthium +); (C connate); A (connate - Canarium), basifixed [?level], (connective massive), (anthers horizontal); (pollen striate); fruit often not dehiscent, (pyrenes winged); n = (22-24); if germination hypogeal, often phanerocotylar.
11/295: Canarium (120), Dacryodes (90). Tropical, esp. Old World.
Age. Crown-group Garugeae are estimated to be (54.5-)45.6(-36.9) Ma (Federman et al. 2015) or (60.3-)52.5(-47) Ma (Muellner-Riehl et al. 2016).
[Bursereae + Protieae]: petiole bundle with/without medullary strands.
Age. The age of this node can be dated to (66.8-)63.2, 48.6(-46) Ma (Fine et al. 2014) or (67.2-)59.3(-51.8) Ma (Muellner-Riehl et al. 2016).
3. Bursereae de Candolle
Plant usu. decidous; (petiole bundle arcuate - Commiphora); (plant thorny - Commiphora); plant (polygamo-)dioecious; pollen colpi short; (pyrenes tangentially winged), (pseudoaril +); n = (11, 12).
3/286: Commiphora (185), Bursera (110). Tropical America, Africa, 150 species Commiphora from Africa.
Age. Crown-group Bursereae may be around (58.3-)52.5(-47.4) Ma Muellner-Riehl et al. 2016).
Synonymy: Balsameaceae Dumortier
4. Protieae Marchand
C induplicate-valvate, (connate); (stamens = and opposite sepals); (columella ribbed); pyrenes (free); n = (11).
i/140. Mostly neotropical, a few Madagascar and Malesia
Age. Crown-group Protieae can be dated to (43.2-)32.6, 25.7(-18) Ma (Fine et al. 2014) or (40.2-)24.4(-11.7) Ma (Muellner-Riehl et al. 2016).
Evolution: Divergence & Distribution. Dates for the split between Bursera and Commiphora vary from ca 120 to ca 60 Ma - 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 this split to (59.0-)54.7(-50.6) Ma, while it is estimated to be (58.3-)52.5(-47.4)Ma by Muellner-Riehl et al. (2016: q.v. for ages of other clades). Weeks and Simpson (2007) suggested that divergence of Commiphora from the clade now represented by the E. Asian B. tonkinensis occurred some 53-42 Ma in the Eocene; Commiphora itself did not diversify until 32.3-23.2 Ma, 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) Ma (Gostel et al. 2016 and Weeks & Simpson 2007 respectively), but Gostel et al. (2016) suggest that diversification began around 9.5 Ma 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. Ma, although diversification within the genus did not really get going until (23-)20 Mya, 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 Ma. De-Nova et al. (2012) estimated the age of most species of Bursera in these Mexican forests to be ca 7.5 Ma - 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 Ma; diversification in Madagascar, where the genus is now a prominent and speciose component of the rain forest, being dated to a mere 6 Ma 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 (43.2-)32.6, 25.7(-18) Ma, 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), whle within species like P. subserratum there is extensive local-scale parapatric morphological and edaphic variation (Misiewicz & Fine 2014). In groups like Eugenia, Inga, Piper and Psychotria differentiation of secondary metabolites may also be involved (see also below). Indeed, there is substantial variation in monoterpene composition in these taxa and this is largely stable within a plant over time, although within a species there may be some variation, and some monoterpene combinations are found in more than one species (Piva et al 2019).
Bursereae, very largely made up of Bursera and Commiphora (see above for ages), are predominantly denizens of drier forests in the New World and Africa-Madagascar, the grass-poor Succulent Biome (Gagnon et al. 2018 and references). Thus 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 in Mexico. 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. Other major groups in the Succulent Biome include Fabaceae, Cactaceae, including Pereskia, some clades of Euphorbia, etc. (Gagnon et al. 2018 and references).
Pollination Biology & Seed Dispersal. For sexual system evolution in Bursera, dioecy probably being plesiomorphic, see Goldberg et al. (2017).
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). The insect phylogeny matches host plant chemistry rather than its phylogeny (Becerra 1997; Pellmyr 2002). Becerra (2003) suggested that the two had been co-evolving for about 100 Ma, although other estimates for the age of the family (see above) suggest that this figure is very much an over-estimate. In plants that have a squirt defence toxic material in their tissues is under pressure and is ejected up to 2 m when the tissue is perforated by the insect; 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), perhaps promoting niche differentiation and local diversity (see also Endara et al. 2017). Overall chemical diversity in Bursera has increased with time/speciation, if dropping off when considered from a per-speciation-event 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).
Protieae (= Protium s.l.) invest heavily in secondary metabolites, and they are some (22-)40 (average)(-58)% dry weight - although most of the compouinds were not herbivore active metabolites... (Salazar et al. 2018). Protium species with more diverse metabolites that affect herbivores, either positively or negatively, commit less to defence, and herbivore species richness is negatively correlated with metabolite richness (Salazar et al. 2018). Those metabolites that reduced herbivory were more conserved across the plant phylogeny, but there was no particular correlation between the metabolite composition of the plant and herbivore phylogeny, as might be expected for a system such as this where the herbivores are largely generalists, although they by no means feed on all species (Salazar et al. 2018). 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 Ma, before the diversification here (Fine et al. 2014). 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). For similar systems, see Inga, Piper, Eugenia, Passiflora, sundry Solanaceae and Psychotria.
Chemistry, Morphology, etc.. Phytoliths are commonly produced by Burseraceae (Piperno 2006). Some Burseroideae 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; see also Mauritzon 1935; Wiger 1936).
For additional general information, see Lam (1931, 1932), Leenhouts (1956), Forman et al. (1989: Beiselia) 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., i.e. Canarieae) 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. In a comprehensive analysis of Protium and relatives, Fine et al. (2014) found that Tetragastris and Crepidospermum were well embedded in Protium.
Classification. For a classification of the expanded Protium (= Protieae) recognizing nine sections, see Daly and Fine (2018).
[Sapindaceae [Meliaceae [Simaroubaceae + Rutaceae]]]: anthers with a pseudo-pit; nucellar cap +, tapetal cells multinucleate, nuclei fusing to form polyploid mass; outer integument over five cells across, obturator + [?level]; testa multiplicative.
Age. Wikström et al. (2001) dated this node to (61-)57, 55(-51) Ma, Magallón and Castillo (2009) suggested an age of around 70.7 Ma, Tank et al. (2015: Table S1, S2) an age of about 69 Ma, and Bell et al. (2010) an age of (70-)64(-57) or (54-)51(-49) Ma, while (106.5-)100.5(-94.4) Ma is the age in Muellner-Riehl et al. (2016).
Chemistry, Morphology, etc.. For an extensive tabulation of variation in anther, ovule and seed characters of this whole group, see Tobe (2011a).
SAPINDACEAE Jussieu, nom. cons. - Back to Sapindales
Woody; quebrachitol [cyclitol], steroidal saponins, cyclopropane amino acids + [non-protein amino acids], ellagic acid 0 (+); cork also outer cortical; (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, filaments hairy; (tapetal cells 1-3-nucleate); G [(2) 3(-6)], stigma various, dry or wet; ovules variously curved, sessile, campylotropous [?all], micropyle bistomal, outer integument thicker than the inner integument, parietal tissue 4-15 cells across (?0); fruit a loculicidal capsule; seed often pachychalazal; testa vascularized, exotesta palisade (not), unlignified, (mesotestal cell walls thickened and lignified; endotesta crystaliferous), tegmen (multiplicative), limited to radicular pocket, (exotegmen fibrous, lignified or not); endosperm starchy, embryo curved, radicle in pocket formed by seed coat; x = 10 (?8, ?9), nuclear genome [1 C] (0.038-)0.802(-16.721) pg.
144 [list], to subfamilies/1,925 - four subfamilies below, beginning of tribal classification. ± 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) Ma, Bell et al. (2010) suggested an age (53-)42, 41(-30) Ma, and Muellner-Riehl et al. (2016) an age of (96.9-)87.2(-77.4) Ma - alternatively, it is mid Cretaceous and (very approximately) 116-98 Ma (Buerki et al. 2010c). Crown and stem ages of 36 and 55 Ma 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
Plant deciduous; phloem stratified; pericyclic sheath?; stomata anomocytic; buds perulate; flowers large [ca 2.5 cm across], polysymmetric; nectary of golden, horn-like glands alternating with C; pollen spiny; stigma capitate, 3-sulcate; ovules 6-8/carpel, arranged in parallel, outer integument 6-8 cells across, inner integument 3-4 cells across, hypostase +, obturator 0; fruit loculicidal; ?hilum, aril 0; mesotestal cell walls thickened, tegmen multiplicative, with inner layers thick-walled; germination epigeal; n = 15.
1/1: Xanthoceras sorbifolia. N. China.
Synonymy: Xanthocerataceae Buerki, Callmander & Lowry
[Hippocastanoideae [Dodonaeoideae + Sapindoideae]]: pericyclic sheath of phloem fibres and stone cells; laticifers +; flowers often strongly monosymmetric, (4-merous); C with appendages or not; (style hollow), (branched); ovules 2/carpel, apotropous, (obturator -); (megaspore mother cells several); (fruit septicidal), seed usually 1/carpel; cotyledons spiral or not; nuclear genome [1C] (367-)1197(-11149) Mb; germination hypogeal or epigeal.
Age. Wikström et al. (2001) dated this node to (36-)33, 29(-26) Ma, Bell et al. (2010) suggested that it was (46-)37, 35(-26) Ma - alternatively, its age is mid Cretaceous between (very approximately) 116 and 98 Ma (Buerki et al. 2010c), or somewhere in between, variously around 75.5, 65.8, or 58.8 Ma (Muellner et al. 2007) or (91.7-)81.8(-71.8) Ma (Muellner-Riehl et al. 2016).
2. Hippocastanoideae Dumortier
Plant deciduous; ("latex" +), cyanogenic glucosides 0; stomata actinocytic (anomocytic); buds perulate (perulae 0); leaves opposite, palmate or simple, with secondary veins ± palmate, vernation conduplicate-plicate, deciduous; protogynous; A (5-)6-8(-12); stigma dry, papillate; nucellar cap 8-10 cells across; aril 0; (embryo chlorophyllous); x = 20, nuclear genome [1C] 0.6-1.18 pg.
5/144. North temperate, some tropical and then usually montane.
Age. Wikström et al. (2001) dated crown-group Hippocastanoideae to (29-)26, 20(-17) Ma, Bell et al. (2010) to (37-)25(-14) Ma - or they may be (89.8-)88.2(-83.8) Ma (Du et al. 2019), 83±20.5 Ma old (Buerki et al. 2013b) or (75.8-)66.4(-60) Ma (Muellner-Riehl et al. 2016).
2a. Acereae (Durande) Dumortier
(Pericyclic sheath 0); cuticle wax crystalloids quite common [Acer]; leaves simple, (palmate), (odd pinnate); flowers polysymmetric; K with a single trace, C not clawed, (0), appendages 0; nectary annular, also inside A/0; A 5-10; G [2(-5)]; outer integument 3-5 cells across, ?obturator +; style ± 0, branches long; fruit a schizocarp, samaroid.
2/128: Acer (126[-150 - J. Li et al. 2019]). North Temperate, esp. China, Korea and Japan.
Age. The split between Acer and Dipteronia has been dated to (98-)78(-63.5) Ma (Renner et al. 2007b).
The distinctive fruits of Dipteronia are known fossil from North America as long ago as late Palaeocene, 63-60 Ma, and quite commonly from there since, but they are not known fossil from Europe (McClain & Manchester 2001).
Synonymy: Aceraceae Jussieu
2b. Hippocastaneae (de Candolle) Dumortier
(Plant evergreen - Billia); (fructan sugars accumulated as isokestose oligosaccharides [inulins] - Aesculus); (vessel elements with scalariform perforation plates); leaves palmate; flowers monosymmetric, "large"; K connate (free), C with appendages; nectary on one side of flower; outer integument 8-10 cells across, inner integument 3-6 cells across, hypostase 0 [Handeliodendron]; fruit a loculicidal capsule; hilum large, (double arillode + - Handeliodendron); cotyledons incumbent [?level].
3/16: Aesculus (13). North temperate, S. to Ecuador.
Age. Crown-group Hippocastaneae are estimated to be (89.6-)85.9(-80.4) Ma (Du et al. 2020).
Synonymy: Aesculaceae Burnett, Hippocastanaceae A. Richard, Paviaceae Horaninow
[Dodonaeoideae + Sapindoideae]: leaves usu. evergreen, even-pinnate, (bicompound; simple), leaflets opposite or not, (margins entire), (rachis winged); 1 common A-C primordium; seeds often with chalazal/integumentary arils and sarcotesta, (dormancy physical, water gap near hilum); cotyledons unequal [?level].
Age. The age of this node may be mid-Cretaceous very approximately 116-98 Ma (Buerki et al. 2010c) or (88.2-)77.4(-66.5) Ma (Muellner-Riehl et al. 2016).
3. Dodonaeoideae Burnett
Flowers with oblique plant of symmetry [?distribution]; K initiation spiral, C appendages uncommon; tapetal cells uni-/binucleate; nectary (semi)annular; ovule (1/carpel, pendulous), outer integument 8-10 cells across, inner integument 3-4 cells across, parietal tissue 7≤ cells across.
22/140. Pantropical-warm temperate.
Age. Crown-group Dodonaeoideae are 80.5±12.75 Ma (Buerki et al. 2013b) or (71-)53.2(-36) Ma (Muellner-Riehl et al. 2016).
3a. Dodonaeaeae de Candolle
Cork pericyclic [Dodonaea]; stomata cyclocytic [Dodonaea]; flowers obliquely symmetrical, polysymmetric (monosymmetric); C (0 - esp. Dodonaea); A (many - esp. Distichostemon); (pollen in calymmate tetrads - Magonia); ovules (8/carpel, in parallel - Magonia), outer integument (3-4 - Magonia)/8-10 cells across, chalaza pointed [Magonia]; fruit loculicidal, (septicidal-schizocarp); seed (arillate; sarcotestal; winged); n = 10, 12, 14-16.
14/126: Dodonaea (70), Harpullia (26). Pantropical-warm temperate, esp. Australia, to W. Pacific.
Synonymy: Dodonaeaceae Small
3b. Doratoxyleae Radlkofer
Flowers polysymmetric, (K monosymmetric); A 5-8; ovules ± anatropous, epitropous, bistomal, outer integument ca 5 cells across, nucellar beak + [?= nucellar cap], funicular obturator +, of hairs; fruit indehiscent, drupe or berry; aril/sarcotesta 0; outer and inner integuments multiplicative, exotesta lignified; endosperm ruminate, 0 at maturity, chalazal haustorium +, cotyledons large, foliaceous, suspensor 2-3-seriate, ca 5 cells long; n = 16.
8/14. Pantropical, mostly New World and Africa-Madagascar (Ganophyllum to Australia).
4. Sapindoideae Burnett
(Vessel elements with scalariform perforation plates); stomata various; C (0, 5+), ± complex appendages +; A (4[Glenniea]-many); ovules (epitropous), outer integument 4-12 cells across, inner integument 2-7 cells across; fruit also a samara (indehiscent); n = 14-16, chromosomes 0.62-4.36 µm long.
111/1,365: Guioa (65), Cupaniopsis (60), Talisia (42), Cupania (50), Matayba (50). Pantropical.
Age. The crown-group age of this clade is estimated to be (75.6-)63.7(-51) Ma (Muellner-Riehl et al. 2016: Koelreuteria sister).
For Late Cretaceous/Early Palaeocene fossil woods (India, Deccan Traps) and seeds (Europe) that may well be Sapindoideae, see Wheeler et al. (2017).
4a. Koelreuterieae Radlkofer
Flowers with oblique symmetry; K spirally initiated; C 4 (+ 1 reduced, C:A primordia +); 1 A oustide nectary; androgynophore +; micropyle zig-zag, nucellus 10< cells across, nucellar cap +, funicular obturator +.
Synonymy: Koelreuteriaceae J. Agardh
The Rest: ovule 1/carpel.
4b. Paullinieae de Candolle
Shrubs, trees, vines, often lianes climbing by branch tendrils; (secondary thickening anomalous [stem lobed/phloem wedges/etc.]); (stem endodermis +); (latex +, laticifers articulated, non-anastomosing); terminal leaflet well-developed, (stipules or petiolar pseudostipules +, minute to large); inflorescence thyrses with lateral cincinni; C 4; (pollen oblate, triporate - Serjania, etc.); (antipodal cells persistent, multinucleate - Cardiospermum), obturator long; fruit a schizocarp, samaroid, or ± septicidal capsule; (sarcotesta +), (aril +); (amyloid [xyloglucans] in seed - Cardiospermum); n = 10-12.
12/745: Serjania (230), Paullinia (220), Allophylus (1-255). Mostly New World tropics, Allophylus also Old World.
Synonymy: Allophylaceae Martynov
4c. Melicocceae Blume
Flowers polysymmetric; (C appendages 0); fruit indehiscent, ± dry; sarcotesta +; n = 16.
2/62: Talisia (52). New World tropics.
lychee - K. whorled.
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, a floral formula of K 4 C 4 A 10(?+) G [3-4], and placed in Sapindaceae, is known from the middle Eocene of western Canada (Erwin & Stockey 1990), however, Acer and Dipteronia are older (see above). For the early Caenozoic fossil history of what are now East Asian endemics, see Manchester et al. (2009) and for Hippocastanoideae around 50 Ma collected from British Columbia, see references in Greenwood et al. (2016). Muellner-Riehl et al. (2016) suggest dates for more clades and Du et al. (2019) dates for clades in Hippocastaneae.
Buerki et al. (2010c, 2013b) outline the biogeography of the family, in which much dispersal is involved. The subfamilies of Sapindaceae spread in the mid Cretaceous 116-98 Ma, initially from Laurasia, with South East Asia remaining an important area in the evolution of the family (Buerki et al. 2010c, 2013b). Sapindaceae may not be a simple example of a temperate radiation embedded in an otherwise tropical group (c.f. Judd et al. 1994). Xanthoceratoideae and Hippocastanoideae are both predominantly temperate (Du et al. 2019 suggest that Hippocasataneae originated in eastern Asia), although the rest of the family is largely tropical, and the samaras of Acereae (see e.g. Harris et al. 2017b) evolved independantly from those in the rest of the family.
For diversification in Acereae, see Renner et al. (2007b) and Y. Feng et al. (2018), although Dipteronia has only two species, these may have separated around 58.2-46.5 Ma, before diversification in the far larger Acer began. 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 achieved its range within the last two Ma (Harrington & Gadek 2009).
Harris et al. (2009) found that Aesculus parryi, from Baja California, diverged ca 49 Ma and A. californica, rather more widespread, diverged ca 61.2 Ma, in both cases the sister clades being east North American.
Medina et al. (2021) discuss the distribution of laticifers in Sapindaceae, and these are placed as an apomorphy for the family minus Xanthoceratoideae. However, laticifers are not found in all genera, and Medina et al. suggest that they may have originated more than once here. The main constituents in these laticifers are terpenes, found as essential oils and resins, although apparently not as rubber (no not laticifers in the strict sense?), and a variety of less abundant substances; there may be callose or suberin in the walls of these laticifers. The laticifers can be hard to distinguish from idioblasts, which may also be in longitudinal series in the stem like the cells that make up the laticifers and which may be found in the same plant; taxa that lack laticifers have these idioblasts. These idioblasts contain phenolics, uncommon in the laticifers (Medina et al. 2021). Although most Sapindoideae have but a single ovule per carpel, this is not an apomorphy for the subfamily since basal taxa like Ugnandia and Koelreuteria have two ovules per carpel. There are usually 1-3 seeds per fruit, and the size of animal-dispersed fruits depends on the size of the frugivores in the area, as was shown by Brodie (2017) looking at seed and frugivore size across Malesia - Sapindaceae from Sulawesi and Moluccas, with smaller frugivores, had significantly smaller fruits than Sapindaceae from New Guinea or the region of the Sunda shelf, although obviously this is not likely to be unique to Sapindaceae (see also Arecaceae). Paullinia is a valuable resource for frugivorous birds on Barro Colorado Island, Panama, the fruits tending to ripen in the dry season when other trees were not fruiting (Chery et al. 2019a).
Ecology & Physiology. Sapindaceae, along with Bignoniaceae and Fabaceae, are the major components of the liane/vine vegetation of the Neotropics (e.g. Gentry 1991). The largely neotropical Paullinieae (Sapindoideae) include 8 genera of climbers, both vines and lianes, notably Serjania and Paullinia; they contain one third of the species in the family, including around 470 species that are climbers. As might be expected, many of these climbers have stems with anomalous secondary thickening (see below). Lianes in general use water very efficiently and grow remarkably well in the dry season/dry conditions and proportionally much more than trees (van der Sande et al. 2019; Schnitzer et al. 2019; Dias et al. 2019). Lianes are also abundant in forest edges, treefall gaps, and similar habitats where their growth habits will also be advantageous, and they may have negative effects on the growth of co-occurring trees (Schnitzer 2018).
Pollination Biology & Seed Dispersal. Species of Acer like A. rubrum are known for having very labile breeding systems (Blake-Mahmud & Struwe 2019: A. pennsylvanicum); Renner et al. (2007b) suggested that dioecy had evolved several times in the genus and that the sex of the flower might be determined by environmental cues. Interestingly, fully carpellate trees tended to be unhealthy, and although they produced fruits, they might die... (Blake-Mahmud & Struwe 2019: see also Castanea, although monoecy there), furthermore, if the tree was badly damaged (defoliated, severely pruned) trees might well become female, but never male (Blake-Mahmud & Struwe 2020). Goldberg et al. (2017) looked at the evolution of breeding systems in Dodonaea and suggested that dioecy might be plesiomorphic there.
A number of Sapindaceae have winged fruits rather like those of maples (Acer), although constructed in a variety of ways, so, for example, the position of the wing varies. Lentink et al. (2009) studied the aerodynamics of the fruits of three species of maple, and showed that they developed a vortex at the leading edge of the rotating wing that generated lift, so allowing the descending fruit to travel greater distances (Lentink et al. 2009). The wings on the fruits of Paullinia are brightly coloured and may help attract frugivorous birds; the fruits are capsules and contain arillate seeds (Chery et al. 2019a).
Plant-Animal Interactions. Hemipteran rhopalid seed predators have recently switched from native to introduced Sapindaceae in both Australia and Florida (Forbes et al. 2017 and literature). Work by Cenzer (2017) paints a complex picture in Florida, at least, where maladaptive plasticity in hybrid red-shouldered soapberry bugs (Jadera haematoloma) masks differences developed between populations of those bugs feeding on the different sapindaceous species (native Cardiospermum, introduced Koelreuteria). Interestingly, Western boxelder bugs, Boisea trivittata, which fancy the seeds of Acer negundo (and other species of the genus, also Fraxinus) respond to infrared cues in the laboratory (Takács et al. 2017). All these bugs are soapberry bugs, Serinethinae, a group of about 63 rhopalids that specialize on Sapindaceae, especially Sapindoideae but not Dodonaeoideae and Xanthoceratoideae (Carroll & Loye 2012 for insect-host associations).
The cynipoid Pediaspini, found on Acer, are sister to those Diplolepidini, found on Rosa, the two clades separating perhaps 142-133 Ma and together forming a small clade outside Cynipidae (Blaimer et al. 2020).
Vegetative Variation. Stem tendrils of Paullineae grow laterally from the axil of the leaf that subtends them, and there is a basal bud on the side opposite to the direction in which the tendril is growing. Tendrils often develop on inflorescences, and they appear to be modified branches that grow from the axils of prophylls. Cauline secondary thickening in Paulinieae is often anomalous, the liana syndrome. Thus there are unusual patterns of cambial origin, some species developing several independent vascular cylinders whether surrounding each other or not, heteromorphic vessels of two size classes, and parenchyma-like fibre bands alternating in amount of thickening, and cambial activity is also variable, that of some species resulting in xylem outside and cambium inside (Tamaio & Angyalossy 2009; Angyalossy et al. 2015 and other references in Schnitzer et al. 2015; Lopes et al. 2017; da Cunha Neto et al. 2018; Pellissari et al. 2018; Chery et al. 2019b, 2020). The cambial variants, and even some taxa with apparently ordinary vascular tissue, have a 5-lobed star-shaped primary vascular body (Chery et al. 2019b). Interestingly, clade I of Paullinia, sister to the rest of the genus, appears to have ordinary secondary thickening (Chery et al. 2019a). Vessel dimorphism - very wide and very narrow vessels - is common, perhaps ensuring rapid movement of water yet at the same time affording some protection against embolisms (Bastos et al. 2016 and references; Bouda et al. 2019). The root anatomy of these vines/lianas 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).
Genes & Genomes. It has been suggested that the base chromosome number for Sapindaceae is x = 7 (Ferrucci 1989). For chromosome numbers, see also Lombello and Forni-Martens (1998), for chromosome size, see Ferrucci (1989), and for genome size, see Coulleri et al. (2014: not much correlation with anything).
W. Wang et al. (2020) note that size and genome order of plastomes in Acer are similar, but the boundary of the inverted repeat may vary quite considerably.
Chemistry, Morphology, etc.. Gibbs (1958) noted that sections Cissifolia and Negundo of Acer had very low amounts of syringyl lignin, confirming their distinctiveness. A cauline endodermis is reported from some climbing Paullinieae, being recognised as such by its position and large size of its cells and the starch grains they contain rather than by any distinctive pattern of wall thickening (da Cunha Neto et al. 2018). 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. For laticifers in Paullinieae, which can be clustered, see da Cunha Neto et al. (2017); latex is reported to have evolved several times here (Prado & Demarco 2018)..
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. Flowers of Eurycorymbus change from being obliquely symmetric to polysymmetric during the course of development (Cao et al. 2017). 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. The petals of Sapindaceae are often rather complex and have a similarly complex set of terms used to describe them; see "appendages" above.
There is extensive variation in pollen morphology within Sapindaceae, and when the phylogeny settles down some/much of this will probably be found to vary between tribes (see J. Muller & Leenhouts 1976; van den Berg 1978; Acevedo-Rodríguez et al. 2011). Similarly, I have not atempted to integrate variation in stigma/style morphology with the phylogeny. Brizicky (1963) reported that the ovules may be epitropous (see also Gulati & Mathur 1977; 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). Several aspects of the embryology of Filicium are distinctive (Gulati & Mathur 1977), but sampling is too poor to understand the significance of this. 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 also Anacardiaceae) the pericarp grows much faster than the seed, so 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.
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 anatomy of Acer, see Hall (1951), for floral morphology of Litchi and Dimocarpus, see S. X. Xu (1990, 1991), of Koelreuteria, see Ronse Decraene et al. (2000b) and Cao et al. (2018), of Delavaya, Cao & Xia (2009), of Handeliodendron, Cao et al. (2008), of Acer, etc., Gostin and Minea (2007) and Leins and Erbar (2010), and for that of Xanthoceras, Zhou and Liu (2012), for nectaries, which are variously vascularized, see Hall (1951), Solis and Ferucci (2009) and Zini et al. (2014a), for endothecial thickenings, see Manning and Stirton (1994), for style morphology, see Lersten (2004), for embryology, Nair and Joseph (1960), Tobe and Peng (1990), González et al. (2017) and Avalos et al. (2019: Koelreuteria), for fruits of Paullineae, see Weckerle and Rutishauser (2005), and for seeds, see Guérin (1901), van der Pijl (1955), Turner et al. (2009: germination) and Gama-Arachchige et al. (2013: esp. water gap).
Phylogeny. Buerki et al. (2009, 2010b: 81 and 104 genera respectively) carried out extensive phylogenetic studies on the family. Preliminary studies suggested that Xanthoceras 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 it was sister and with 70% bootstrap and ³95% posterior probability support (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, while in an analysis of ca 350 nuclear genes Baker et al. (2021: see Seed Plant Tree) found relationships that were rather different, thus Dodonaeoideae are sister to the rest of the family, while Aesculus hippocastanum was quite far separate from the Hippocastaneae (which include A. pavia).
Hippocastanoideae. For the phylogeny of Acer, see J. Li et al. (2006), Renner et al. (2007b), Li (2011) and Harris et al. (2017b). Evidence that Dipteronia, with pinnate leaves and cyclic samaras, is derived from within Acer, with more regulation-type samaras and usually palmate/ly lobed leaves, is ambiguous. A recent transcriptome analysis (Li et al. 2019: 500 nuclear loci) suggested that the two were sister taxa, and although Harris et al. (2017b) found that A. japonica was sister to [other Acer + Dipteronia], that species was well embedded within Acer both in Renner et al. (2007b: one analysis, ?incomplete sequence) and in Li (2011). For relationships within Acer, where groupings generally agree with sections currently recognized, see Li et al. (2019: ca 2/5 species included). In a plastome analysis representatives of section Negundo was found to be sister to those of the other seven sections included (W. Wang et al. 2020). Harris et al. (2009) examined the phylogeny of Aesculus.
Dodonaeoideae. Relationships within Dodonaea are discussed by Harrington and Gadek (2010). Sapindoideae. 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, and Koelreuteria was in this position in the study by Muellner-Riehl et al. (2016: the two other genera not included). Relationships within Dodonaea are discussed by Harrington and Gadek (2010). For relationships around Cupania, see Buerki et al. (2012a). Acevedo-Rodríguez et al. (2017) looked at relationships around Paulliniodae-Paullinieae. Chery et al. (2019a) clarified relationships within Paullinia itself, which came out as sister to Cardiospermum, in turn sister to [Urvillea + Serjania], although that clade had little support; seven main clades, mostly well supported, were recovered in Paullinia, and Radlkofer's sections held up reasonably well. Cardiospermum itself may be polyphyletic, and this is supported by laticifer distribution - these are not to be found in all the species currently included in the genus (Medina et al. 2021).
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).
For sections in Acer, see de Jong (2004: slightly modified in J. Li et al. 2019).
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.
[Meliaceae [Simaroubaceae + Rutaceae]]: alkaloids, limonoids/protolimonoids +, pentanortriterpenes +; cuticle waxes 0; (leaves trifoliate), (simple); inflorescence branches cymose; x = 9.
Age. Wikström et al. (2001) dated this node to (51-)47, 45(-41) Ma, while an age of ca 53.6 Ma was suggested by Tank et al. (2015: Table S2) - note the topology in these two - and an age of (100.3-)93.5(-86.6)Ma by Muellner-Riehl et al. 2016).
Evolution: Divergence & Distribution. For the base chromosome number of this clade, see Paetzold et al. (2018).
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).
MELIACEAE Jussieu, nom. cons. - Back to Sapindales
Trees; tetranortriterpenes, flavones +, bark often rather bitter; secretory cells with resin, etc. +; nodes 5:5; leaves (even-pinnate), leaflets not articulated (articulated); flowers (3-)5(-8)-merous; K not enclosing C [?level], often connate, (vascular trace single); A connate, 2 x C, connate, tubular, anthers on margin; G (1) [(2-)4-5(-many)], postgenitally united, opposite C, hairy, (placentation parietal), stigma capitate, wet; ovules anatropous/straight/campylotropous, (micropyle exo-/bistomal), outer integument 2-5 cells across, inner integument 2-4(-5) cells across, parietal tissue 3-9(-18) cells across, nucellar cap 3-5(-9) cells across, placental obturator common; seeds often pachychalazal, coat vascularized, testa usu. undistinguished but thick, endotesta crystalliferous, (tegmen multiplicative); embryo white, cotyledons collateral; x = 6, 7?/13 (?14 - Carta et al. 2020), nuclear genome [1C] (0.027-)0.602(-13.394) pg/(269-)541(-856) Mb.
50 [list: subfamilies]/641 - 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) Ma; Muellner et al. (2007, see also 2006) thought that diversification within the family had begun considerably earlier, (98.5-)96, 73.5(-61.5) Ma, Koenen et al. (2015) gave ages of (91.5-)80.5, 59.5(-54) Ma, Muellner-Riehl et al. (2016) ages of (89.8-)79.6(-69.7) Ma, while Wikström et al. (2001) suggested another later date of (40-)36, 30(-26) Ma.
For fossil Meliaceae, see Mabberley (2011).
1. Melioideae Arnott
(Suckering shrublets); (hairs stellate - Aglaia); buds naked; (nodes 3:3); plants dioecious; C (-14), (connate); (style hollow); ovules (1-)2(-many)/carpel, collateral or superposed; archesporium multicellular; (fruit dry, winged [Quivisianthe], inflated); seeds with sarcotesta (0); (exotesta +); 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) Ma (Muellner et al. 2006, 2007 - age in latter a little older), (81.8-)69.9(-57.5) Ma (Muellner-Riehl et al. 2016) or (83-)72.5, 54(-49) Ma (Koenen et al. 2015).
Fossil fruits named as Manchestercarpa vancouverensis found in deposits 79-72 Ma from Vancouver Island, British Columbia, were placed in Melieae, being thought to being very close to Melia itself (Atkinson 2020), although Atkinson does note that the endocarp of the fossil consists of interlocking sclereids, not interwoven bands of fibers, the central hollow is of the same length throughout, rather than being constricted in the middle, etc..
1A. Melieae de Candolle
Plant (deciduous); leaves (to 3-pinnate); polygamous; fruit a drupe; endosperm (slight).
3/10. Tropical to temperate Asia, Iran eastwards, Australia.
[Aglaieae etc., Trichilieae etc.]: C (adnate separately to staminal tube); A (5, opposite K/many, in one whorl); fruit a loculicidal capsule, (berry); seeds (arillate - funicular in Naregamia).
1. Aglaieae Blume, etc.
A (tube cyathiform), anthers on inner side; (gynophore +); (testa multiplicative, all cell walls thick, tegmen cells collapse - Lansium); (cotyledons superposed).
1. Trichilieae de Candolle(inc. Turraeeae, Munronia onwards)
leaves (two-ranked, simple - Turraea); plants hermaphroditic/polygamous; A (± free); (exotegmen fibrous - Trichilia); (embryo chlorophyllous - Trichilia, Nymania).
Synonymy: Aitoniaceae R. A. Dyer, nom. illeg.
2. Cedreloideae Arnott
Buds perulate (naked - Capuronianthus); leaves (opposite), (leaflets ± serrate); plants monoecious; (C connate); (nectary 0); ovules (2 - Capuronianthus) 3-many/carpel, collateral; fruit a septifragal capsule, valves falling off, columella persisting; seeds winged, (fruit ± fleshy, seed single - Walsura), testa (massive, woody or corky - Xylocarpus), (exotegmen fibrous - Swietenia); n = 13, 18, 23, 25, 26, 28; nuclear genome [1C] ca 388 Mb [Xylocarpus].
14/56: Entandrophragma (11), Khaya (9). Pantropical, but largely Old World. [Photo - Flower, Fruit.]
Age. Diversification within Cedreloideae began (86-)75, 67.5(-58) Ma (Muellner et al. 2006, 2007), (75.2-)64.8(-55.6) Ma (Muellner-Riehl et al. 2016), or (59.3-)48.5, 38.6(-33) Ma (Koenen et al. 2015).
2A. Chukrasia A. de Jussieu + Schmardaea H. Karsten
Plant deciduous; C contorted [?S]; (connective forming long apical appendage - Schmardaea); (gynophore + - Chukrasia); columella 0 [Schmardaea]; endosperm +.
2/2. India, Sri Lanka, China to Malaysia, northwest South America.
2B. Cedreleae de Candolle
Plant (deciduous); midrib of C adnate to androgynophore; A =C, free; androgynophore +.
2/14: Cedrela (8). Indo-Malesia, tropical America.
Synonymy: Cedrelaceae R. Brown.
Plant (subdeciduous); leaves ± even pinnate; C contorted; staminal tube globose, anthers on inside [these three in sister taxon Swiet]; ovules 3-4/loculus, superposed; pericarp fleshy, columella 0; sarcotesta +, spongy; cotyledons fused; x = .
2/8: Tropical, inc. the western Pacific, the greater Antilles.
Swieteniaceae E. D. M. Kirchner
Evolution: Divergence & Distribution. For additional divergence dates, see Muellner-Riehl et al. (2016). Atkinson (2020) questioned the identity of a number of fossils previously included in Meliaceae, some near Melia. However, fossils that can be placed in or very close to Melia, now known mainly from the Indo-Malesia-Australian area, have been found in localities scattered throughout the northern hemisphere (Atkinson 2020).
Muellner et al. (2006) discussed the biogeography of Meliaceae, proposing an 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. Atkinson (2020) thought that the Melia-like fossil that he described from Campanian-aged deposits, although to be referred to an important tropical clade, nevertheless did not imply that l.t.r.fs existed then. Indeed, crown-group ages of rainforest clades in the family are a mere 23 Ma (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). Heads (2019a) provides a comprehensive account of the biogeography of the family based on range expansion-vicariance dynamics and also "atypical" habitats in which some Meliaceae are to be found. Monthe et al. (2019) looked at shifts from rain to dry forests in African Cedreloideae, but see differing dates obtained from plastid and ribosomal analyses.
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.
Gama et al. (2020) discussed the evolution of various floral traits in the family, optimising them on the tree in Muellner-Riehl et al. (2016).
Ecology & Physiology. Although only a small family, Meliaceae make up 17% of all trees >10 cm d.b.h. in Sumatra (Mabberley 2011). Carapa procera is one of the four common species mentioned growing in the ca 145,500 km2 of peat in the Cuvette Centrale in the Congo (Dargie et al. 2017). Xylocarpus is a well-known mangrove genus, and for its seeds and germination, see Clarke et al. (2001); there is some information in Ann. Bot. 115(3). 2015 and also the discussion under the mangrove habitat below.
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 carpelate flowers are very similar functionally, although the staminal tube in the former is often somewhat narrower; the staminal tube and the large stigmatic head seem to be integral parts of the pollination mechanism. The whole apex of the style is commonly more or less massively swollen (see also Gama et al. 2020) and is sometimes involved in secondary pollen presentation, as in Vavaea (Ladd 1994). Gama et al. (2020) summarize what little is known about pollinators in the family.
Animal dispersal is common in Melioideae; 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). Some species of Chisocheton are myrmecophytes.
Caterpillars of the pyralid moth Hypsipyla are stem borers, and can cause serious damage; all the host records I have seen are members of Cedreloideae.
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 can 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 epiphyllous inflorescences, flowers appearing between the leaflets, and specimens of this species have been misidentified as Rubiaceae... Capuronianthus (Cedreloideae) has opposite, compound leaves, while the simple-leaved Vavaea and Turraea (both Melioideae) look rather unmeliaceous except when in flower; the leaves of some species in the latter genus can even be two-ranked, borne on short shoots, 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.
Genes & Genomes. For genome sizes, see Lyu et al. (2017).
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).
Resin canals are not reported from Meliaceae by Prado and Demarco (2018). Sieve tube plastids with protein crystalloids and starch occur in Melia and Azederach. Walsura often has leaflets with ± pulvinate petiolules and prominent reticulate venation.
Although the flowers are often apparently perfect, dioecy is widespread; carpelate flowers are the first to be produced in the cymose inflorescences. Gouvêa et al. (2008b) drew the flowers of Swietenia as being inverted. The filaments of Vavaea are largely free, as are those of Cedrela, Toona and Walsura (Cedreloideae-Cedreleae). Indeed, Cedreleae are rather different florally from other Meliaceae, but features found there such as the more or less free stamens may be derived, not plesiomorphous as one might think (c.f. Gouvêa et al. 2008a). A multicellular archesporium is quite common in Melioideae (Prakash et al. 1997). 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 general information, see van Wyk (in Dahlgren & van Wyk 1988: Nymania), T. D. Pennington and Styles (1975: generic monograph), Pennington (1981: Neotropical Meliaceae), Pannell (1992: Aglaia), Mabberley et al. (1995: esp. Malesia), and Mabberley (2011), for chemistry, see Hegnauer (1969, 1990) and Mulholland et al. (2000), for floral anatomy, see Murty and Gupta (1978: both subfamilies), and for embryology, etc., see Wiger (1935; see also Mauritzon 1935; Wiger 1936), Paetow (1931), Nair and Kanta (1961) and N. C. Nair (1962, 1970 and references).
Phylogeny. Cedreloideae and Melioideae are both 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). The clade [Schmardaea + Chukrasia] is sister to the rest of Cedreloideae (Atkinson 2020). Within Melioideae, Melieae (including Owenia) are sister to the rest, but with only moderate support (stronger in Muellner-Riehl et al. 2016; see also Atkinson 2020); 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 sister to other Melioideae in Koenen et al. (2015), who suggested that there may be four more small clades successively sister to other Melioideae. A similar structure was recovered by Atkinson (2020), who also found a larger clade that included Turraea and Trichilia and sometimes (total evidence trees) another that included Guarea and Aphanamixis. Two Malagasy genera previously segregated as separate subfamilies, Quivisianthe and Capuronianthus, have consistently been found to be well 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).
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 the clade [Chukrasia + Schmardaea] is 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); although immediate generic associations are similar to those in Muellner-Riehl et al. (2016), broader relationships within the subfamily differ. In the African Khaya in particular, but also in Entandrophragma, there is conflict between phylogenies obtained from analyses of plastid and ribosomal sequences (Monthe et al. 2019).
Classification. Cedreloideae used to be called Swietenioideae. The classification suggested by Penningron and Stles (1975) will have to be substantially amended, as is evident from the mismatch between their tribes and the phylgeny in Muellner-Riehl et al. (2016; see also Gama et al. 2020). 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 there is somewhat unclear (Grudinski et al. 2014b).
Thanks. I am grateful to David Kenfack for useful information.
[Simaroubaceae + Rutaceae]: ?
Age. The age for this node is estimated at ca 115 Ma (Pfeil & Crisp 2008), about 50 Ma (Tank et al. 2015: Table S1, S2), (101.4-)88.4(-75.9) Ma (Clayton et al. 2009) or (118.1-)104.7, 73.5(-67.8) Ma (Koenen et al. 2015).
Hartl (1958) suggested that there were similarities between Rutaceae and Simaroubaceae in fruit (endocarp) anatomy; he did not include other Sapindales in his comparison. Rutaceae and Simaroubaceae are both reported to have embryo sac haustoria (Mickesell 1990) and carboline alkaloids and canthinones (Waterman & Grundon 1983).
SIMAROUBACEAE Candolle, nom. cons. - Back to Sapindales
Trees; bark very bitter, quassinoids, beta carboline and canthinone alkaloids [with tryptophane nucleus], ellagic acid +; wood often fluorescing; (nodes multilacunar); pith conspicuous, medullary secretory canals +; sclereids common, oil cells uncommon; leaflets not articulated, vernation also supervolute-curved, margins coarsely toothed to entire; breeding system various; plant dioecious; inflorescence thyrsoid, (pedicels articulated), flowers rather small, <1 cm across; K usu. basally connate, C imbricate; A obdiplostemonous; G 1-5(-8), ovaries ± free, style +, often short, stigmas ± recurved, ± pointed, with elongated receptive zone, dry; ovules 1(-2)/carpel, (hemitropous), (micropyle zig-zag), (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; fruit drupelets; 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); x = 8 (?9), nuclear genome [1 C] (0.032-)0.924(-26.595) pg.
19-22 [list]/110 - seven groups below. 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 Ma (Clayton et al. 2009), or somewhat older, (84.5-)74(-63) Ma (Muellner-Riehl et al. 2016).
Woods (Ailanthoxylon, Simarouboxylon) from the Deccan Traps of Late Cretaceous and Early Palaeocene age may be simaroubaceous, and if confirmed would have interesing biogeographic implications (Wheeler et al. 2017).
1. Casteleae Bartling
Thorny shrub to tree; leaves simple, (scale-like); plant mon- or dioecious; inflorescence fasciculate; drupelets ± lenticular and carinate; n = 13.
2/14. Southern U.S.A. to Argentina, the Caribbean and Galápogas Islands.
Age. Crown-group Casteleae are some (40.9-)23.6(-9.3) Ma (Muellner-Riehl et al. 2016).
Synonymy: Castelaceae J. Agardh, Holacanthaceae Jadin, nom. inval.
[Picrasmateae [Ailantheae [Leitnerieae [Nothospondias [Picrolemma + Simaroubeae]]]]]: leaf rhachis collapses at the petiolular nodes.
Age. The age of this clade is around (80.9-)70.3(-60.1) Ma (Muellner-Riehl et al. 2016).
2. Picrasmateae Engler
(Stipules +, cauline); plant mon- or dioecious; C valvate; A 5.
1/8. ± tropical, America and the Caribbean, Asia to Malesia.
Age. Crown-group Picrasma may be (33.6-)16.2(-3.5) Ma (Muellner-Riehl et al. 2016: quass. jav.).
[Ailantheae [Leitnerieae [Nothospondias [Picrolemma + Simaroubeae]]]]: sclereids in leaflet mesophyll; leaves with flat surface glands/(0).
Age. The age of this clade is variously suggested to be around 61.1. 52, or 47.5 Ma (Muellner et al. 2007: inc. Soulamea, check), (66.8-)58.2(-52.2) Ma (Muellner-Riehl et al. 2016) or about 23-21 Ma (Pfeil & Crisp 2008: stem age of Ailanthus).
3. Ailantheae Meisner
(Leaves paripinnate); C induplicate-valvate; tapetal cells binucleate; fruit a samara; n = 32 [= 2 x 16?].
1/5. Turkestan to Indo-Malesia, N. Australia.
Age. Crown-group Ailanthus is (53.6-)35.3(-15.8) Ma (Muellner-Riehl et al. 2016).
Synonymy: Ailanthaceae J. Agardh
[Leitnerieae [Nothospondias [Picrolemma + Simaroubeae]]]]: disc usu. 0; (seeds with starch).
Age. This clade is around (58.9-)49(-38.9) Ma (Muellner-Riehl et al. 2016).
4. Leitnerieae Baillon
(Ellagic acid 0 - Leitneria); oil cells +; stomata paracytic; leaves (simple), (stipules +, cauline - some Soulamea); plant usu. dioecious; (inflorescence ± catkinate - Leitneria; (flowers 3-merous - Soulamea); staminate flowers: (P 0; A (1-)4 - Leitneria); G 1 [Leitneria],  [Soulamea], ca 5; fruit drupelets, ± flattened and carinate, (2-seeded samara - Soulamea); (endosperm +); n = 16.
5/22. S.E. U.S.A. (Leitneria), Africa and tropical and subtropical Asia, Malesia, to N. Australia and Polynesia, inc. New Caledonia.
Age. Crown-group Leitnerieae are (55.8-)45.3(-33.3) Ma (Muellner-Riehl et al. 2016: Leitneria sister).
Synonymy: Ailanthaceae J. Agardh, Leitneriaceae Bentham & J. D. Hooker, Soulameaceae Pfeiffer
[Nothospondias [Picrolemma + Simaroubeae]]: ?
Age. The age of this clade is (54.2-)44(-33.2) Ma (Muellner-Riehl et al. 2016).
5. Nothospondias Baillon
Foliar glands 0; plant dioecious; flowers 4-merous.
1/1: Nothospondias staudtii. Tropical West Africa.
[Picrolemma + Simaroubeae]: gynophore +, nectariferous, stigmatic lobes short, divergent/obscure/(0)/(long).
Age. This clade is some (45.5-)34.7(-24.8) Ma (Muellner-Riehl et al. 2016).
6. Picrolemma Baillon
Mesophyll sclereids 0; plant dioecious; staminate flowers: A 5, opposite K, staminodes +.
1/2. Peru, Brazil.
7. Simaroubeae Dumortier
(Plant geoxylic); leaves (paripinnate), (simple), (lacking glands), (leaflets articulated - Quassia); (flowers perfect); K with a single trace, C (8 - Iridosma), (contorted - e.g. Quassia, Simaba), (valvate), (long, coherent into tube - Quassia); A (5, alternating with staminodes - Eurycoma), filaments with lateral or basal-adaxial scales, (scales 0 - Perriera); G 2, 4-5(-6); (style long, with separate canals or not); (endothelium + - Simaba trichilioides), tissue below embryo sac massive (with central elongated cells - Samadera); fruits (nutlets), drupelets, ± bicarinate; n = 15.
11/52: Homalolepis (28). Pantropical.
Age. Crown-group Simaroubeae are (40.3-)30.1(-21.3) Ma (Muellner-Riehl et al. 2016).
Synonymy: Quassiaceae Bertolini, Simabaceae Horaninow
Evolution: Divergence & Distribution. For more ages in Simaroubaceae, see Muellner-Riehl et al. (2016; also Clayton et al. 2009). In the map above it is obvious that distributions of some genera in the past and the present are very different. Thus Ailanthus, now known only from Asia to Australia, is widespread fossil in the Eocene ca 52 Ma (Corbett & Manchester 2004). Clayton et al. (2009) discussed the fossil history of Leitneria and Chaneya, the latter not certainly Simaroubaceae; fruits identified as Leitneria, a genus now endemic to the southeast U.S.A., are reported from eastern Siberia (Ozerov 2012).
The bulk of the diversification within Simaroubeae has occured within the last (27.4-)19.5(-12.1) Ma (Muellner-Riehl et al. 2016). Despite (or because of?) the fairly good fossil history of the family in the northern hemisphere, the biogeographic history 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).
I have put in some phylogenetic structure above because of its effect on our understanding of character evolution; Simaroubeae are quite well known and have some distinctive features, but they are well embedded in the family, so these features are not family-level apomorphies. See also Devecchi et al. (2017) for the optimization of a number of characters - the focus is on Simaroubeae. J.-X. Ren et al. (2020), looking at the chemistry of Picrasma quassioides, found similarities with Rutaceae - and Asteraceae.
Pollination Biology & Seed Dispersal. There are reports of other than porogamous fertilization in the family (also in Anacardioideae: Wiger 1935; Rao 1970).
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 thorn; the leaves are reduced to scales.
Although the carpels are often more or less free except basally, 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).
For additional information, see Clayton (2011: general), for chemistry, see Hegnauer (1973, 1990, also 1966, 1989, as Leitneriaceae) and Leite and Castilho (2020); see also Jadin (1901) and Boas (1913), both vegetative anatomy, Webster (1936: wood anatomy), Alves et al. (2016: floral morphology of Simaba), Endress et al. (1983: carpel morphology), Wiger (1935; see also Mauritzon 1935; Wiger 1936), all embryology, and Fernando and Quinn (1992: pericarp anatomy), also Abbe (1974) and Tobe (2011a, 2013), inflorescence, floral morphology/anatomy and embryology of Leitneria.
Phylogeny. Relationships in the family are rather pectinate. The topology [Picrasma etc. [Ailanthus [[Soulamea, etc.] [Nothospondias* [Picrolemma [Quassia* [Samadera* + Simarouba etc.]]]]]]] is mostly quite well supported, although support for the first clade is not that strong (it may be two clades - see above: Muellner-Riehl et al. 2016) 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 is embryologically similar to Brucea, in the same clade (= Leitnerieae). Quassia and Samadera are successively sister to the remainder of Simaroubeae; for some relationships in Simaroubeae, see Devecchi et al. (2017); Simaba turns out to be polyphyletic.
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), while part of the polyphyletic Simaba is now to be called Homalolepis (Devecchi et al. 2017).
Previous Relationships. Molecular data have suggested 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; its limits always had been rather problematic.
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 not enclosing C in bud [?level], (2-4), connate or free, C often valvate?, (connate); A filaments ± flattened; (gynophore +); G 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); x = 9, nuclear genome [1 C] (0.115-)1.061(-9.818) pg.
161 [list]/2,085 - four groups below. Largely tropical.
Age. Bell et al. (2010) suggested that this node was (51-)40(-29) My; however, other dates are (87-)82(-74) Ma (Appelhans et al. 2012a), around 93.3, 82.1, or 72.9 Ma (Muellner et al. 2007, see also 2006), (93.4-)84.6(-75.9) (Muellner-Riehl et al. 2016), (72.7-)62.7(-53.3) Ma (Pfeil & Crisp 2008), or (43-)39, 37(-33) Ma (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), 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, not the Indian subcontinent, 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) Ma (Appelhans et al. 2012a) or (84.6-)67.2(-46.9) Ma (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]; (A obdiplostemonous); pollen (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; (endocarp area persisting at adaxial base of seed); (exotesta mucilaginous); nuclear genome [1C] (196-)1278(-8509) Mb. (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) Ma (Pfeil & Crisp 2008), (73.5-)69.5(-62.3) Ma (Appelhans et al. 2012a), (90-)74(-58) Ma (Salvo et al. 2010: q.v. for more dates) or (83.2-)74.5(-66.1) Ma (Muellner-Riehl et al. 2016).
2. Amyridoideae Arnott
Woody; quinolone and acridone [derived from anthranilic acid], (furo-)pyranoquinoline and 1-benzyltetrahydroisoquinoline alkaloids, (limonoids 0); (distinctive tracheal veinlet endings); (foliar sclereids +); oil cells also commonly solitary; (colleters +0); (leaves opposite), (stipules +, intrapetiolar/hooded sheath - Metrodorea); flowers (vertically or obliquely monosymmetric), (4 merous), (T + - Zanthoxylum), C (connate); A (connate), (4), (2, with basal anther appendages, + 3 staminodes - Angostura alliance); ([andro]gynophore +); (G opposite sepals - Zanthoxylum), (styluli terminal), (connate only at apex); (1-2 ovules/carpel, (obturator +); fruit a drupe/follicle/capsule; (seeds winged), (forcibly expelled with endocarp); exotesta often mucilaginous/sarcoexotesta [spongy], irregularly palisade, (variously lignified), (mesotesta sclerotic), lignified endotesta - Melicope, etc.), (mesotesta fibrous - Phellodendron), meso-/endotesta thickened [Zanthoxylum], exotegmen with crossed lignification bars, or not [Skimmia], (meso- and endotegmen tracheidal), (nucellar polyembryony +); (endosperm copious, embryo short to long - Zanthoxylum); n = 18 (7-11...72); 2n genome 0.65-0.87 pg.
113/1755: Melicope (300), Zanthoxylum (225), Agathosma (150 +), Boronia (150), Vepris (80), Zieria (60), Acronychia (48), Conchocarpus (48), Amyris (40). Pantropical, some (warm) Temperate. [Photo - Flower, Flower, Fruit.]
Age. Crown-group Amyridoideae are (79-)70.7(-62.8) Ma (Muellner-Riehl et al. 2016).
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]: (leaves simple, trifoliolate); C imbricate, clawed.
Age. The age for this node is estimated to be some (75.3-)62.9(-50) Ma (Muellner-Riehl et al. 2016).
3. Rutoideae Arnott
Perennial herbs to shrubs; acridone alkaloids reduced at C-1 and C-3, napthalene coumarins +; limonoids 0; C (valvate - Chloroxylum), (fringed - Ruta); (G [2-5]), postgenitally united, (gynophore +); ovules 4-8(-12)/carpel; fruit loculicidal, often ventricidal, capsule, (septicidal, with mericarps); (seeds reniform), (winged); endosperm usu. ± copious, embryo straight to curved; n = (9), 10.
5/20. North (warm) temperate to tropical, some southern Africa, not the Antipodes or South America.
Age. Crown-group Rutoideae are estimated to be some (51.9-)40.4(-29.5) Ma (Muellner-Riehl et al. 2016: Claus. Gly.).
4. Aurantioideae Eaton
Shrubs to trees; methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); leaf (rhachis winged), (leaflets alternate); C (valvate - Micromelum), (A many); G 1, [2-5(-20)], (placentation parietal); ovules 1-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, (ventricidal capsule); (seed pachychalazal - Glycosmis), exotesta in part mucilaginous (not), fibrous, fibres laterally compressed, (with [multicellular] hairs), inner walls lignified, often fibrous, (testa sclereidal-fibrous - Atalanta), (ecto-, meso- and) endotesta with crystal-containing cells, exotegmen fibrous; (multicellular chalazal haustorium/narrowing), (nucellar polyembryony +), (embryo curved), cotyledons thick, not folded (not Micromelum).
28/273: Haplophyllum (66), Glycosmis (50), Citrus (30). Mediterranean to Indo-Malesia and the Pacific, also Africa.
Age. The age of crown-group Aurantioideae is estimated at (28.2-)19.8(-12.1) Ma (Pfeil & Crisp 2008), ca 30 Ma (Muellner et al. 2007) or (52-)40.5(-29.5) Ma (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) and Appelhans et al. (2018a).
Rutaceae are 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). Appelhans et al. (2018a) suggest that the family may be Eurasian in origin. Citrus may have moved from west to east Malesia and Australia some time in the Miocene/Pliocene (Schwartz et al. 2015).
Ca 275 species of Diosmeae are restricted to South Africa, very largely to the Cape Floristic Region (Linder 2003; 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). The crown-group age of Zanthoxylum on Hawai'i (hybridization may have been involved in their origin) is around (17.5-)11.8(-6.9) Ma (Appelhans et al. 2018a). Melicope s.l. has radiated extensively across the Indian and Pacific Oceans, where they are to be found from Madagascar to the Austral islands (Appelhans et al. 2018b). There has been a major radiation of Melicope on Hawai'i of some 55 species, the largest radiation of a woody clade there, the beginning of which predates the ages of the main islands (Paetzold et al. 2018). From Hawai'i there seems to have been dispersal to the Marquesas Islands over 3,500 km away (Paetzold et al. 2018), while the source area for the Hawaiian plants (and for the whole group) is likely to be in the general Australia-New Guinean region, although Vanuatu and New Caledonia also figure prominently as secondary dispersal hubs (Harbaugh et al. 2009b; Appelhans et al. 2014a, 2018b; Hembry 2018). Paetzold et al. (2018) discuss how to reconcile the obvious facility of Melicope when it comes to long distance dispersal with features such as its dioecy on Hawai'i and elsewhere, woodiness and polyploidy (albeit apparently diploidized); a generalist, and/or a specialist, with numerous local island endemics? How Zieria arrived in New Caledonia is unclear, especially if the estimates of the age of Zieria of less than 20 Ma are correct: Z. chevalieri is the only species there, and is sister to the rest of the genus, all Australian (Barrett et al. 2015 and references).
Appelhans et al. (2014b) suggested that the black shiny seeds common in the Acronychia-Melicope clade (probably bird-dispersed - see Appelhans et al. 2018a) were a key innovation, and this clade has 5 (Appelhans et al. 2018b) to 17 times () as many species as Tetracomia and the Euodia clade, successively its sisters. The exotesta of seeds of members of the Acronychia-Melicope clade is edible (birds) and the sclerotesta is thick, while members of the Euodia clade have explosively-dehiscent follicles and seeds with a thin testa (Hartley 2001a; Appelhans et al. 2018b).
Poon et al. (2007) looked at variation in characters of secondary chemistry and morphology in the light of phylogeny. 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.
To Integrate: "Protorutaceae" - Phell./Todd./Tetraidium/Zanth. (70.4-)66.3(-62.6) Ma (Appelhans et al. 2018a).
Ecology & Physiology. Rutaceae have very 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). Robertson et al. (2018) discuss the much greater diversity of alkaloids found in Australian Flindersia growing in drier woodlands/vine thickets over those in more mesic habitats.
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), Boronia and relatives (Australian), and some other Rutaceae have seeds with elaiosomes at the base that are endocarpial in origin and are dispersed by ants (Kubitzki et al. 2011; Bayley et al. 2013).
Plant-Animal Interactions. Caterpillars of Papilionidae-Papilioninae-Papilionini butterflies are notably common on Rutaceae, about ca 1/3 of the records being from here, and 80% of the ca 200 species of Papilio will eat Rutaceae (Aubert et al. 1999; Zakharov et al. 2004). The first time I saw the giant swallowtail, P. cresphontes, I also found its host plant, Ptelea trifoliata, about twenty yards down the path (Shaw Nature Reserve, Missouri). Rutaceae may have been the original food plants for Papilio, since as mentioned even those species whose caterpillars now eat Magnoliales will eat Rutaceae if they have to, and they can detoxify Rutaceae (furanocoumarins are the compounds involved) using cytochrome P450 monooxygenase (Zakharov et al. 2004, but c.f. Fordyce 2010; see also Berenbaum & Feeney 2008; Simonsen et al. 2011; Condamine et al. 2012). As with the magnoliids, e.g. Aristolochiaceae, perhaps the original food plants of Papilionidae-Papilioninae, and Magnoliaceae, it is the alkaloids in part that attract the butterflies, although overall other receptor cues picked up by the ovipositing females are very important in this association (Nishida 1995; Berenbaum et al. 1996). Ehrlich and Raven (1964) noted that P. demodocus was rather anomalous, since it fed on Ptaeroxylon, which then was included in Meliaceae, but since it is now placed in Rutaceae, all is right with the world. Apiaceae (q.v.) are another group with furanocoumarins, and caterpillars of some species of Papilio eat them, too. For more on swallowtails and Rutaceae, see papers in Scriber et al. (1995), and for more on swallowtails in general, see Aristolochiaceae.
Isobutyl glucosinolate has been found in Luvunga scandens, from Thailand (Sirinut et al. 2017).
Genes & Genomes. For the evolution of chromosome numbers in the family, an endeavour that should be reworked, see Stace et al. (1993).
Economic Importance. For relationships in and around Citrus, see Carbonell-Caballero et al. (2015) and for the origin of limes, lemons, etc., see G. A. Wu et al. (2014, 2018) and Curk et al. (2016). The citrus greening disease is, however, a major threat, and in Florida an introduced psyllid, Diaphorina citri, something of a pest in its own right, transmits the gram negative gracilicute Candidatus Liberibacter americanus that lives in the phloem. It is devastating the Citrus industry there, but has spread elsewhere, and other "species" of Liberibacter attack Citrus elsewhere in the world (Gutierrez & Ponti 2013; Wikipedia 19.xii.2020). See also papers in Tropical Plant Pathology 45(3). 2020.
Chemistry, Morphology, etc.. For secondary metabolites, see Hegnauer (1971) and Kubitzki et al. (2011). Da Silva et al. (1988) surveyed the distribution of some 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, see also 2017) describe the development of a hood-shaped leaf base in Metrodorea from initially paired primordia and characterise it as stipular in nature; it is vascularized, and leaflets may arise directly from it (Kaastra 1977). Prickles of Zanthoxylum can be in the stipular position.
Rutaceae are particularly variable in flower and fruit (Boesewinkel 1980b). Erythrochiton hypophyllanthus has epiphyllous inflorescences on the abaxial side of the leaf (c.f. sometimes in Ruscus). 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 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 radially symmetrical to monosymmetric flowers, the later obliquely symmetrical or not, with a lip or not; the corolla postgenitally connate by hairs or papillae, filaments connate and forming a tube, or a tube formed by the serial adnation of filaments and petals; five, three or only two stamens plus three to five staminodes; gynoecium fluted, postgenitally connate apically, style ± impressed, stigma capitate to lobed; ovule variously oriented, outer integument 4-6 cells and inner integument 2-4 cells across (or only one integument), a nucellar beak or not, an obturator or not, the chalazal zone massive, etc. (Pirani & Menezes 2007; Pirani et al. 2010; el Ottra et al. 2011, 2013, esp. 2019; Bruniera et al. 2015). Wei et al. (2011) thought that the plesiomorphic condition for Rutaceae was to have have five stamens.
Triphasia has G , the odd member being adaxial, and the same is true of Cneorum tricoccon, which has 3-merous flowers (see Caris et al. 2006b 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 can be exo-, endo-, or bistomal or the ovule apex may even be naked, and in bitegmic taxa, either integument may be slightly thicker than the other (e.g. Corner 1976), although Mauritzon (1935b) suggested that the outer integument is often thicker - 3-10 cells across (outer) versus 2-4 cells across (inner), and the outer integument is sometimes (Aegle) multiplicative. Nucellar cells above the embryo sac may be in series, and nucellar polyembryony is quite widespread (e.g. Mauritzon 1935b; Mahabalé & Chennaveeraiah 1958). The embryo sac can be relatively quite small relative to a massive nucellus, and in Aegle there is a layer of crystalliferous cells below the exotegmen and 2-3 layers of such cells below the endotegmen (Mahabalé & Chennaveeraiah 1958) - 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), also Straka (1976), Dahlgren and van Wyk (1988), van der Ham et al. (1995) and White and Styles (1966) for Cneoroideae. 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 alkaloids, Fish and Waterman (1973: esp. Zanthoxylum) and Waterman (1975, 1999). For wood anatomy of Cneoroideae, see Appelhans et al. (2012b: phylogenetic signal within the subfamily), for colleters, see Macêdo et al. (2016), for floral development, Zhou et al. (2002) and Wei et al. (2011), for floral orientation, see Eichler (1878), for pollen, see Morton and Kallunki (1993: Cuspariinae), for gynoecium/perianth of Zanthoxylum, see Beurton (1994), for gynoecial morphology, see Gut (1966), Endress et al. (1983), and Lersten (2004), for ovules of Harrisonia, see Wiger (1935; see also Mauritzon 1935; Wiger 1936), 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).
Phylogeny. In a two-gene analysis, the [[Spathelia + Dictyoloma] [[Cneorum + Ptaeroxylum] Harrisonia]] clade (= Cneoroideae) 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). Morton (2015) found Cneoroideae 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; Appelhans et al. 2016).
Within Cneoroideae 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).
Amyridoideae. For relationships around Metrodorea, see Cruz et al. (2017).
Rutoideae. For the circumscription and contents of Rutoideae, now a rather small subfamily, see Appelhans et al. (2016); Chloroxylon, ex Flindersioideae, is sister to the other four genera. Salvo et al. (2011) and Manafzadeh et al. (2011) discussed relationships in the Irano-Turanian Haplophyllum, which has colonized the Mediterranean area more than once.
Aurantioideae. For general relationships, see Pfeil and Crisp (2008) and Bayer et al. (2009). Appelhans et al. (2016) suggest that Haplophyllum and Cneoridium, ex Ruteae, are at the base of Aurantioideae, which rather changes the apomorphies for that group. 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; Shivakumar et al. 2017: ?sampling, rooting), and both have (1-)2 ovules/carpel and similar chromosome numbers (Mou & Zhang 2012). Murraya is very polyphyletic (Z.-D. Chen et al. 2016: Chinese 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, some of which have quite large or fingered fruits, 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; see also G. A. Wu et al. 2018).
Other genera in the family form a single clade within which the classical subfamilies and genera, largely based on variation in fruit morphology (Engler 1931; c.f. Hartley 1981; But et al. 2009) have not held up - Aurantioideae are an exception. 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. Thus neither the large genus Melicope nor Acronychia are monophyletic (Appelhans et al. 2014b); for the latter, see also Appelhans et al. (2018b). 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). 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, that about one quarter of the morphological species appeared to be other than monophyletic, and that relationships suggested by cpDNA were incongruent with those based on morphology. Barrett et al (2018) found major incongruences between relationships based on cpDNA and those based on nrDNA... For relationships in Clauseneae, see Shivakumar et al. (2016), and for those in Protorutaceae, largely composed on Zanthoxylum, see Appelhans et al. (2018a).
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). 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; thus there are ten monotypic genera within the small subtribe Galipeinae (Bruniera et al. 2015). Beyond this, generic limits are difficult, especially around Citrus (Carbonell-Caballero et al. 2015 and references), 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), in Rutaceae, although he gave no reasons for this.
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).