LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, 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 cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

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

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

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

Chemistry, Morphology, etc. for integument thickness (which, however, reverses, and its condition is unclear in Huerteales, etc.), see Endress and Matthew (2006a).

Phylogeny. The only recently established clade Huerteales is strongly supported as being monophyletic (Peng et al 2003: three gene analysis, sampling sketchy; Worberg et al. 2009: all genera included). However, relationships within other malvids are somewhat uncertain, and it remains unclear just what group is sister to Brassicales. The clade [Malvales + Sapindales] is a possible candidate (Soltis et al. 2000; Peng et al 2003: both weak support), and Endress and Matthews (2006) note that there are some features perhaps more common in these first two families than elsewhere. [Malvales + Sapindales] may also be sister to [Brassicales + Tapisciales] (Soltis et al. 2007a: support weak for the latter pair). However, Bausher et al. (2006) in an analysis of whole chloroplast genomes found strong support for the clade [Brassicales + Malvales], but only one species from the three orders, and no Huerteales, were included (see also Jansen et al. 2007; Moore et al. 2007). There was also some support for this topology in analyses by Savolainen et al. (2000) and Hilu et al. (2003); Alford (2006) suggested that [Huerteales (Perrottetia not included) + Brassicales + Malvales] might be sister to Sapindales. Worberg et al. (2007b, 2009) recovered the relationships [Sapindales [Huerteales [Brassicales + Malvales]]], with strong support, and also for the monophyly of each of the four orders. In studies including the mitochondrial matR gene, although the malvid clade was recovered, relationships within it were unclear (Zhu et al. 2007), however, I follow Worberg et al. (2009) here.

SAPINDALES Berchtold & J. Presl  Main Tree, Synapomorphies.

Interesting secondary compounds, ethereal oils, myricetin +; (secretory cells/tissue +); silicified wood or wood with SiO₂ grains in all major families [esp. Anacardiaceae and Burseraceae]; tension wood +; mucilage cells with swollen layered inner periclinal walls [position varies]; branching from previous innovation, petioles leaving a prominent scar; leaves spiral, odd-pinnately compound, leaflets opposite, vernation conduplicate; A 2x K; (exine distinctly striate); nectary well developed; G opposite petals [therefore flowers obdiplostemonous...] or odd member adaxial; ovules few/carpel, epitropous; seed coat?; (embryo green). - 9 families, 471 genera, 6070 species.

Evolution. Divergence & Distribution. Wikström et al. (2001: relationships are [Brassicales [Malvales + Sapindales]]]) date the origin of stem Sapindales to (84-)80(-76) million years before present, the crown group age being (71-)67(-63) million years before present. The age of crown group Sapindales was estimated as (66-)63(-60) and (73-)71(-69) million years (two penalized likelihood dates), the stem group age being (102-)96(-90) and (80-)76(-72) million years; Bayesian relaxed clock estimates were only slightly different, to 76 million years for the first analysis and in the upper range of the second analysis (Wang et al. 2009), while Magallón and Castillo (2009) suggested ages of ca 98.1 and 98.4 million years for relaxed and constrained penalized likelihood datings for stem Sapindales, and ages of 70.6 and 70.7 million years (again relaxed and constrained ages) for the crown group.

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

Plant-Animal Interactions. Associated with the accumulation of noxious secondary metabolites in this group, specialised herbivores are found on many of them. Thus the hemipteran Calophya eats largely Anacardiaceae, Burseraceae, Simaroubaceae and Rutaceae (Burckhardt & Basset 2000) - plus a couple of records from entirely unrelated families. Galls are quite common, perhaps especially on Sapindaceae and Anacardiaceae (Mani 1964).

Chemistry, Morphology, etc. Biebersteiniaceae and Nitrariaceae are particularly poorly known morphologically, 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). The stipules are sometimes clearly modified leaflets and 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).

The flowers are often imperfect, but since staminate and carpellate flowers have well-developed pistillodes and staminodes respectively, they can be difficult to distinguish. Bachelier and Endress (2009) suggest some floral developmental features found widely in this clade. Pollen with striate exine is scattered through the order. Septal cavities have been noticed in Cneorum (Rutaceae) and Koelreuteria (Sapindaceae), but they do not secrete nectar (Caris et al. 2006, cf. septal nectaries in monocots). For some details of embryology, see Mauritzon (1936).

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 suggest the poorly supported basal relationships in the tree here (also poorly supported in Soltis et al. 2011), a fair bit of resolution elsewhere, excepting only a moderately-supported sister group relationship between Meliaceae and Simaroubaceae (cf. Gadek et al. 1996; Soltis et al. 29011: sampling), so a trichotomy including Rutaceae is shown on the tree. Relationships are somewhat different in Wang et al. (2009), but support was weak and sampling poor. Molecular data place Biebersteinia in Sapindales, albeit with a long branch (Bakker et al. 1998).

Previous Relationships. In the past Bretschneideraceae and Akaniaceae (= Akaniaceae here) have been associated with Sapindales, Bretschneidera in particular looking very like a member of Sapindaceae; the presence of myrosin cells in the former was not considered to be all that important (Cronquist 1981; Takhtajan 1997). Morphological phylogenetic analyses may continue to suggest this position, however, Akaniaceae s.l. are to be included in Brassicales (e.g. Ronse de Craene & Haston 2006).

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

Synonymy: 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

BIEBERSTEINIACEAE Schnitzlein   Back to Sapindales

Rhizomatous perennial herbs; vessels?; nodes?; hairs glandular; leaves (2-3 compound), leaflets lobed, margins toothed, stipules petiolar, lobed or not; inflorescence racemose; C clawed, (denticulate); nectary glands opposite K; pollen 3-celled, exine striate; gynophore +, short, G [5], styles separate, impressed, apically connate, stigma capitate; ovule 1/carpel, micropyle endostomal; embryo sac tetrasporic, 16-nucleate, 13-celled [Penaea type]; fruit a schizocarp, columella persisting, K ± accrescent; testa ± collapsed, exotegmen thick-walled, lignified, anticlinal walls sinuous, endotegmen lignified, cells polygonal; endosperm development?, embryo somewhat curved, cotyledons foliaceous; n = 5.

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

• Biebersteiniaceae are perennial, glandular-hairy herbs that have odd-pinnate leaves with lobed to compound leaflets and petiolar stipules. Ihe inflorescence is erect and racemose and the flowers are large. The fruit has a single seed per carpel and a persistent columella.

Chemistry, Morphology, etc. Biebersteinia is little known. At least some species are foul-smelling. The ante-petalous stamens are longest. Takhtajan (1997) described the ovules as being unitegmic.

The herbaceous habit of Biebersteinia is rather unusual in the order, but ethereal oils (no oxygenated sequiterpenes, high proportion of aliphatic hydrocarbons), single ovule/carpel, etc., are all congruent with a position here.

Additional information is taken from Baillon (1874), Kunth (1912: general), Hegnauer (1989, as Geraniaceae: chemistry), Boesewinkel (1997: seeds), Tzakou et al. (2001: fatty acids) and Muellner (2011: general).

Previous relationships. Previously Biebersteinia has been more or less closely associated with Geraniaceae (Geraniales) (e.g. Cronquist 1981; Takhtajan 1997). The exotegmen of Biebersteinia is rather like that of Ledocarpaceae and Vivianaceae (both Geraniales), especially when young, since both exotesta and endotegmen are tanniniferous (Boesewinkel 1988), but it has distinctive flavones and methyl ethers quite like Rutaceae in part, but unlike Geraniaceae (Bate Smith 1973; Greenham et al. 2001).

[Nitrariaceae [[Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Simaroubaceae [Rutaceae + Meliaceae]]]]]: stigmatic head from postgenitally united free carpel tips, papillate.

NITRARIACEAE Lindley   Back to Sapindales

Annual to perennial herbs to shrubs; mycorrhizae absent [Peganum]; ß-carbalin alkaloids +, ethereal oils?; cork in inner cortex; wood storied; nodes?; petiole bundle arcuate, with wing bundles; astomata in longitudinal bands of small cells [not Nitraria]; mucilage cells +, throughout plant or not; cuticle waxes 0 (platelets, rodlets); leaves two per node, adjacent, (spiral), entire or pinnatifid, ?vernation, stipules minute or foliaceous, ± cauline; inflorescence terminal, cymose, or flower single; K (connate), (valvate - Peganum]; C protects the flower in bud; A (5-)15, in triplets opposite K, filament bases broad, flattened, [Nitraria, Peganum), or flower (3-)4-merous; A basically[?] haplostemonous, 4, opposite K [Tetradiclis]); nectaries antepetalous [Nitraria, Peganum], or 0 [Tetradiclis; G [2-4(-6)], (opposite C - Nitraria), style long to rather short, basal and ± impressed [Nitraria, ± hollow, Tetradiclis], stigma as commissural compital lines down part of its length, dry; ovules 1 apotropous or 6-many ?epitropous/carpel, micropyle zig-zag or bistomal, outer integument 2-4 cells across, inner integument 2-3 or 4-7 cells across, parietal tissue ca 3 cells across, funicle long [not Nitatria]; megaspore mother cells several [Peganum]; fruit a capsule, drupe, 1-seeded. mesocarp woody [Nitraria], or berry [Malacocarpus]; (testa weakly multiplicative - Peganum), exotesta cells inflated or not, often mucilaginous; endotesta short palisade, or not, endotegmen ± fibrous [Peganum] or not [Tetradiclis]; endosperm copious (not Nitraria), (embryo green); n = 7, 12.

3[list]/16. Usu. ± arid regions from North Africa to East Asia, also S.W. Australia and E. Mexico (map: Pan et al. 1999; Brummitt 2007; FloraBase 2007). [Photo - Flowers.]

Chemistry, Morphology, etc. Some of the variation in this group is rather puzzling...

Nitraria often has two or three leaves at a node (= ?short shoot), although not only some have scarious stipules; the leaves are occasionally toothed or lobed. It also has apotropous ovules (Takhtajan 1997) and aliform-confluent xylem parenchyma.

Peganum also may have two much-divided leaves at a node, in this case also with more or less foliaceous and divided stipules - see also Malacocarpus; it has foliar raphides, but there are only a few mucilaginous cells. The androecium 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). There are many ovules per carpel and the fruit a loculicidal capsule or berry.

The flowers of Tetradiclis are (3-)4-merous, the stamens equal in number to and opposite the sepals, and there is no nectary. There are usually four carpels, each divided into three parts; of the 6 ovules in each carpel, all borne on end of long placenta arising at base of ovary, four ovules are in a central locellus, and one each in lateral locelli; the style is more or less basal, stigmatic ridges extending down the expanded apical portion; n = 7. The distinctive fruit is a loculicidal capsule, but only the seeds in the central locelli are released when the capsule opens, the other two being retained. Takhtajan (1997) says that stipules there are absent; they are present, if small.

No endothelium has been recorded in members of Nitrariaceae (Kapil & Tiwari 1978), cf. Zygophyllaceae s. str.

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

Phylogeny. Molecular data suggest the relationships [[[Peganum + Malacocarpus] Tetradiclis] Nitraria] (Sheahan & Chase 1996), and place the group in Sapindales.

Previous Relationships. There are similarities betweeen Nitrariaceae and Zygophyllaceae in general appearance, and also in features like wood anatomy, and perhaps also chemistry (Nag et al. 1995); since both grow in dry and warm habitats, this may account for some of these similarities. Indeed, the two families used to be together in Zygophyllaceae (Cronquist 1981), although Takhtajan (1997) placed the genera here included in Nitrariaceae as three separate families in his Zygophyllales. Zygophyllales in A.P.G. III (2009) include Zygophyllaceae s. str. and the monogeneric Krameriaceae and are not remotely close to Nitrariaceae.

Synonymy: Peganaceae Takhtajan, Tetradiclidaceae Takhtajan

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

[Kirkiaceae [Anacardiaceae + Burseraceae]]: inflorescence thyrsoid [panicle of cymes]; (pollen exine striate); G adnate to central receptacular apex, synascidiate, stigma with uniseriate multicellular papillae, wet; fruits with 1 seed/carpel, endocarp well developed.

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

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

• Kirkiaceae are woody plants that have often rather closely-set odd-pinnate leaves with toothed leaflets. Ihe inflorescence is dichasial, although the ultimate branches may be monochasial, and the flowers are small and 4-merous. The fruit is a ridged or angled schizocarp with persistent if slender columella strands.

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 branches have female flowers, while flowers on higher order branches are male (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 Simaroubaceae (Cronquist 1983, but with some doubt) or near that family (Takhtajan 1997), but they lack quassinoids and limonoids.

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

Evolution. Divergence & Distribution. Fossils assignable to Burseraceae/Anacardiaceae are known from the early Eocene in England ca 50 milliion years ago (Collinson & Cleal 2001).

Chemistry, Morphology, etc. Note that Anacardiaceae like Pachycormus have thin, brown, flaking bark and vegetatively look quite like Burseraceae; the wood anatomy of the two is very similar (Daly et al. 2011). Bachelier and Endress (2009) discuss the floral morphology and anatomy of this clade in detail. The basic endocarp condition for [Anacardiaceae + Burseraceae] seems to be that of an unoriented mass of sclerified and often crystalliferous cells (Wannan & Quinn 1990). Such an endocarp characterises Spondiadoideae, and it is also found in Buchanania, Campnosperma and Pentaspadon, included in Anarcardioideae, as by Pell (2004: unfortunately, Campnosperma was not sequenced), as well as in Burseraceae. It has been suggested that an operculum may be derived twice in Anacardiaceae (Pell & Urbatsch 2001), but it is also found in fruits of Burseraceae and perhaps it, too, is plesiomorphic within the whole clade.

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

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

Trees or shrubs (climbers); resinous exudate black or becoming blackish; (cork cortical); pith loose, shining; wood often fluorescing; nodes usu. 3:3; petiole with annular wing bundles; leaflets not articulated, margins toothed or not, base of petiole often swollen; breeding system various; flowers (3-)5(-7)-merous; (K, C 0); A (1-10<), when 5, opposite sepals; (stamens on nectary; nectary 0); (andro/gynophore +), styles separate (single), terminal to gynobasic, connate apically, stigma capitate (lobed), dry; ovule 1/carpel, usu. apotropous, ± anatropous, (perichalazal), uni- or bitegmic, micropyle zig-zag (endostomal), funicle often long, ponticulus +; seed often ± pachychalazal, vascular bundles in this area, endotegmen usu. ± thickened, lignified; endosperm oily (and starchy), embryo often curved (cotyledons folded - Mangifera); n = 7-12, 14-16, 21.

81[list]/873. Tropical, also temperate (map: from Barkley 1937; Heywood 1976; George 1985; Meusel et al. 1978; Nie et al. 2009). Two groups below. [Photo - Flower, Fleshy fruit, Dry fruits.]

1. Spondioideae Arnott

A obdiplostemonous; G (1-[pseudomonomerous? - Solenocarpus])[2-)4-5(-12)] and as many locules; ovule ± apical, (2/ovules carpel, one epitropous), hypostase +, funicle massive; exocarp thick, operculum +/0; exotestal cells (and hypodermis) thickened or not, ± persistent, tegmen ± 0, hypostase persistent, saddle-shaped.

10/115. Tropical [or 21/138: Lannea (40)].

Synonymy: Spondiadaceae Martynov

2. Anacardioideae Link

5-deoxyflavonoids, also alkylcathechols and alkylresorcinols [phenols with unsaturated side chains - allergenic] +; leaves (opposite), simple to compound; (flowers monosymmetric); (K and/or C 0); A (1 [+ staminodes]), 5, 10 (many), (basally connate); G 1 [pseudomonomerous?], [3(-6)], (highly) asymmetrical, antesepalous carpel alone fertile, symplicate zone?, (stigma punctate); ovule apical to basal, (unitegmic, funicle massive, with outgrowths - Pistacia, etc.); (chalazogamy +); drupe often asymmetrical, ± flattened, (K much accrescent); exocarp thin, epidermis lignified, endocarp with up to three layers of palisade lignified sclereids, internal to these a crystalliferous layer [= stratified], (operculum 0); seed coat undifferentiated; (embryo green).

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

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

• Anacardiaceae may be fairly readily recognised because of their often black and/or rather resinous-smelling exudate; the leaves often have black discolorations and the blade may dry a distinctive grey colour. In herbarium specimens, the dry, black exudate may entirely cover the cut surface of the twig, or it may form a distinctive black ring around the periphery. The leaves are often odd-pinnate and the leaflets are opposite to alternate. The flowers are small, and the fruits are often flattened drupes with excentric style or styles.

Evolution. Divergence & Distribution. For the early Tertiary fossil history of what are now East Asian endemic Anacardiaceae, see Manchester et al. (2009) - Choerospondias has been found in Lower Eocene deposits of the London Clay. Middle Eocene deposits from Germany include fossils of the distinctive fruits of the New World Anacardium, with their much-swollen pedicels; the African Fegimanra, sister to Anacardium, also has swollen pedicels, although they are clearly different (Manchester et al. 2007b - see also Pell et al. 2011 for other fossil records).

Plant-Animal Interactions. Anacardiaceae are noted for the sometimes extremely violent allergenic reactions their exudates cause; catechols, resorcinols and other types of phenolic compounds - often in a mixture, as in urushiol - are involved. About a quarter of the genera - all Anacardioideae - have such compounds.

Aphids (Fordinae) that form distinctive galls are closely associated with species of Pistacia (Inbar 2009), while a gall-forming jumping plant louse, the hemipteran Calophya, is notably common on Schinus, and other psyllids occur on Anacardiaceae (Burckhardt & Basset 2000; Burckhardt 2005).

Pollination Biology & Seed Dispersal. In Pistacia, and perhaps other genera, chalazogamy occurs, the pollen tube moving from the funicle via the ponticulus, an outgrowth of the funicle that bridges the gap between it and the chalaza (Martínez-Pallé & Herrero 1995; Bachelier & Endress 2009).

Anacardioideae have a number of different kinds of disseminules that have modifications for wind dispersal. These include fruits adnate to broad bracts (Dobinea), samaras (Loxopterygium), fruits with a wing formed by the flattened peduncle of the inflorescence (Amphipterygium), much enlarged sepals (Parishia), or even much enlarged petals (Swintonia). The evolution of these fruit types seems to be correlated with the adoption of a drier habitat (Pell & Mitchell 2007). Other structures may be part of the dispersal unit, including a fleshy swollen pedicel, as in Anacardium, while in Cotinus hairs on the pedicels are involved in the wind dispersal of the fruits.

Chemistry, Morphology, etc. Branching in Anacardium may occur on the current flush. Wind-pollinated taxa often lack a disc, also petals. Mangifera has one or two stamens borne inside the disc. In Anacardium the single stamen is on an oblique plane of symmetry; more generally, the position of the carpel, when single, suggests that the flower has oblique symmetry. In Anacardioideae the floral/receptacle apex is sometimes quite short (Bachelier & Endress 2009). Pistacia and Amphipterygium (see Julianaceae below) both are wind pollinated, dioecious, and with reduced flowers. Their ovules are distinctive, being unitegmic and with a massive funicle, etc. (Bachelier & Endress 2007b). For infraspecific variation in style number - 1, 3! - see Gonzàlez and Vesprini (2010). Although the fruits are commonly described as drupes, the origins of the various layers of the fruit wall do not correspond to those of a drupe in the strict sense (Gonzàlez & Vesprini 2010).

For general information, see Ding Hou (1978), for fruit anatomy, Wannan and Quinn (1990) and González and Vesprini (2010), for ovules, fruit and seed, see von Teichman and van Wyk (1988 and references), for floral morphology, Wannan and Quinn (1991), for general chemistry, Young (1976), for chemistry of Julianaceae, see Hegnauer (1966, 1989), for seed anatomy, see von Teichman (1991, 1994, and references), and for wood anatomy, see Gupta and Agarwal (2008). Pell (2004) covers the morphology of the whole family in a phylogenetic context, which she provides; Mitchell et al. (2006) focus more on Spondiadoideae, while Pell et al. (2011) provide a general account of the family.

Phylogeny. Spondiadeae and some Rhoeeae - the clade includes Pegia, Tapirira and Cyrtocarpa = Spondiadoideae (see Aguilar-Ortigosa & Sosa 2004 and Pell 2004, the latter with a list of included genera) - are sister to the rest of the family, Anacardioideae (Pell & Urbatsch 2000, 2001; Pell 2004 and Mitchell et al. 2006 for a list of genera, but see below); wind-dispersed taxa in this latter subfamily do not form a single group (Pell & Mitchell 2007, c.f. Pell & Urbatsch 2001). However, Pell et al. (2011) suggest that Spondioideae may be polyphyletic. Buchanania in some analyses is quite well supported as sister to Anacardioideae (Aguilar-Ortigosa & Sosa 2004; Wannan 2006), consistent both with its chemistry, endocarp anatomy (see above), carpel number of 4-6, and different position of the fertile carpel, but its position is not fixed in other analyses (Pell & Mitchell 2007, cf. abstract). Note that Campnosperma, so far included in only one study (Chayamarit 1997, sampling limited, relationships suggested are unlike those in other studies, no support values), has an endocarp similar to that of Buchanania and the fruit is sometimes two-locular. The morphology of neither of these genera is accounted for in the Anacardioideae as characterized here; if they are, the subfamily will probably lack much in the way of apomorphies.

For the limits of Rhus, which seem best narrowly drawn (i.e., restricted to ca 35 species in the genus), see Yi et al. (2006, and references).

Classification. Note that Pell et al. (2011) include 21 genera in their Spondioideae, which they consider to be polyphyletic...

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

BURSERACEAE Kunth, nom. cons.   Back to Sapindales

Trees or shrubs; oleoresins with mono- and bicyclic monoterpenes, triterpenes with ursane and oleanane components; bark often flaky, light grey; colorless to white resinous exudate common; 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 often toothed, petiolules and petioles often pulvinate; dioecy common; K induplicate-valvate, ± connate, C valvate; ventral carpel bundles fused bundles of adjacent placentae, style usu. short; ovules 2/carpel, campylotropous, outer and inner integuments ca 4 cells across, nucellar cap quite massive, nucellus 6-12 cells across; fruit septifragal, drupe often angled, stone with valves, K deciduous; (exotesta with shortly radially elongate but unthickened cells), endotesta lignified, ± tracheidal; embryo reserves hemicellulosic.

19[list]/755. Tropical. Two groups below.[Photo - Leaf, Flower, Fruit.]

1. Beiselieae Thulin, Beier & Razafimandimbison

(Vessel elements with scalariform perforation plates); leaf ?bases persistent, with a spine; G [9-12], symplicate zone short, ovary strongly furrowed; ovules superposed; pericarp splitting septifragally separately from the endocarp, mericarps apically winged, columella with deep flanges; n = ?

1/1: Beiselia mexicana. Mexico.

2. Bursereae DC, Garugeae Marchand, Protieae Marchand

(Cork cambium deeper - Santiria); petiole bundle often with medullary strands, (arcuate - Commiphora); snail glands [curled ± uniseriate glandular hairs] common; stipules petiolar or cauline, laciniate to entire, or 0; C also induplicate-valvate, etc., (connate); A (apparently in a single whorl), (connate - canarium), (stamens = and opposite sepals; (pollen psilate or striate); G [(2-)3-5], (one carpel developing), symplicate zone well developed, receptacle enclosed by the gynoecium; ovules collateral, (integument 1); pyrenes (winged), usu. with pericarpial pseudoaril, or fruit indehiscent, seeds embedded in ± fleshy pericarp; mesocarp quite frequently splits down loculicidal radius; fruit with columella (pyrenes winged; often only one loculus developing); vascular bundle in outer integument; cotyledons straight to variously folded, entire to palmately lobed; n = 11-13, 22-24.

Synonymy: Balsameaceae Dumortier

18/754: Commiphora (185, 150 from Africa), Protium (180), Canarium (120), Bursera (100), Dacryodes (70). Tropical, but esp. America and N.E. Africa (map: from Rzedowski 1978; D. C. Daly, pers. comm.).

• Burseraceae are recognisable by their often scented resinous exudate and smooth, flaking bark; compound, odd-pinnate leaves with opposite, often long-petiolulate and more or less pulvinate leaflets that have prominent fine venation especially when dry; and petioles, petiolules and rachis that tend to be brownish and more or less scurfy. The swollen leaf base is often concave adaxially. The calyx is often connate and 3- or 4-lobed, and the angled drupes have a wrinkled surface when dry. The resinous exudate often smells of almonds (myrrh, frankincense), and in some genera the leaflets are strikingly symmetrical.

Evolution. Divergence & Distribution. Daly et al. (2011) discuss the fossil record of the family. The split between Bursera and Commiphora has been dated to some 120 million years before present, with diversification within the former genus starting some 70 million years before present (Becerra 2005); these dates seem something of an overestimate. Weeks and Simpson (2007) suggest that divergence of Commiphora from the clade now represented by the E. Asian B. tonkinensis occurred some 53-41.6 million years before present (Eocene). Commiphora itself did not diversify until 32.3-23.2 million years before present, Neogene aridification of Africa occurring more or less at that time (Weeks & Simpson 2007), while Bursera, of which some 85% of the species - often quite narrowly distributed - are found in dry, tropical, Mexican forests - diversified within about the last 25 million years (Becerra et al 2009). Weeks et al. (2005) and Weeks and Simpson (2007) provide further details on the complex biogeographic relationships within Burseraceae.

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). Species with a squirt defence - toxic material is under pressure and when tissues are perforated it is ejected to a diastance of up to 2 m - have rather a rather simple terpenoid defence (Becerra et al. 2009). Locally, species of Bursera tend to be chemically more dissimilar than would be expected at random (Becerra 2007). Overall chemical diversity in Bursera has increased with time/speciation, if dropping off when considered from a per speciation point of view as variation seems to become permutational, terpene diversification occurring in the local ecological context (Becerra et al. 2009).

Chemistry, Morphology, etc. For chemistry, see Khalid (1983).

Some Burseraceae have foliaceous stipules; these are usually interpreted as being the reduced basal pair of leaflets of the 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).

For general information, see Lam (1931, 1932), Leenhouts (1956), Forman et al. (1989: esp. Beiselia), and in particular, Daly et al. (2011). For pollen morphology, see Harley and Daly (1995: Protieae) and Harley et al. (2005: considerable variation).

Phylogeny. Beiselia (B. mexicana is the only species) has simple cotyledons; molecular studies suggest that it is sister to the rest of the family (e.g. Clarkson 2002). This has considerable implications for character evolution, including cotyledon morphology; Beiselia also has several probably autapomorphic features like its gynoecium with its 9-12 carpels. Commiphora may be embedded in Bursera, but the support is weak (Weeks et al. 2005). A recent study suggested that the clades, Protieae, Bursereae, and Garugeae (the latter including Canarium, etc.) had strong support individually and also as sister to Beiselia, but relationships between the first three tribes were unclear (Thulin et al. 2008).

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

Chemistry, Morphology, etc. The style in at least some Rutaceae and Sapindaceae is hollow (Lersten 2004). Tobe (2011a) provides an extensive tabulation of variation in anther, ovule and seed characters of this clade.

SAPINDACEAE Jussieu, nom. cons.   Back to Sapindales

Woody; quebrachitol [cyclitol], toxic saponins, cyclopropane [non-protein] amino acids +, ellagic acid 0 (+); cork also outer cortex (pericyclic - Dodonaea); latex of sorts not uncommon; (vessel elements with scalariform perforation plates; petiole bundle with cortical or adaxial bundles); (epidermal cells mucilaginous), cuticle waxes 0 (platelets, rodlets); leaves spiral, leaflets articulated [check basal pectinations], vernation also conduplicate-plicate, margins serrate, colleters common; inflorescence paniculate, the flowers often in clusters, imperfect; pedicels articulated; flowers 4-5-merous, [K5 C4; K4 C4; etc], C clawed; nectary +, (lobed); A (4-[Glenniea])8, hairy; tapetal cells 1-3-nucleate; G [(2) 3(-6)], (style hollow; style branches +), stigma strongly 3-lobed or not, dry or wet; ovules variously curved, sessile, often apotropous, (micropyle bistomal), outer integument thicker than the inner integument, parietal tissue 4-15 cells across (?0), funicular obturator +; fruit a capsule, or a schizocarp with 1-seeded samaras; seed often pachychalazal, chalazal/integumentary arils and sarcotesta common; testa (and tegmen) multiplicative, testa vascularized, exotesta palisade (not), unlignified, tegmen limited to radicular pocket, (mesotestal cell walls thickened and lignified; endotesta crystaliferous, exotegmen fibrous, lignified or not); endosperm 0, starchy, embryo curved, the radicle in a pocket of the testa, cotyledons spiral or not; germination hypogeal or epigeal.

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

1. Xanthoceroideae Thorne & Reveal

Phloem stratified; stomata anomocytic; bud scales +; leaves deciduous; flowers large; nectary with golden, horn-like glands; pollen spiny; ovules 6-8/carpel, campylotropous, outer integument 7-8 cells across, inner integument 4-5 cells across; aril 0; mesotestal cell walls thickened, tegmen multiplicative, with inner layers thick-walled.

1/1: Xanthoceras sorbifolia. N. China.

Synonymy: Xanthoceraceae Buerki, Callmander & Lowry

[Hippocastanoideae [Dodonaeoideae + Sapindoideae]]: pericyclic sheath of phloem fibres and stone cells; flowers often strongly obliquely or vertically [Aesculus] monosymmetric; ovules apotropous; (megaspore mother cells several).

2. Hippocastanoideae Dumortier

Cyanogenic glucosides 0; (pericyclic sheath 0); cuticle wax crystalloids quite common [Acer]; stomata actinocytic (anomocytic); bud scales + (0); leaves opposite, palmate (odd pinnate; simple), deciduous; (flowers large - Aesculus; polysymmetric); C (not clawed - Acer), (with appendages); A (50)6-8(-12); (nectary - Acer); (style long-branched), stigma dry; outer integument 3-5 [Acer] or 8-10 cells across, inner integument 3-6 cells across - Handeliodendron), nucellar cap 8-10 cells layers across, (hypostase 0 - Handeliodendron); (fruit schizocarp, a samara); (aril + - Handeliodendron); n = 20.

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

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

[Dodonaeoideae + Sapindoideae]: leaves even-pinnate, (bicompound; simple), leaflets opposite or not, (margins entire), (rachis winged); (seeds with physical dormancy, water gap near hilum).

3. Dodonaeoideae Burnett

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

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

Synonymy: Dodonaeaceae Small

4. Sapindoideae Burnett

(Lianes with branch tendrils); (secondary thickening anomalous); stomata various; (stipules or petiolar pseudostipules +); C (0, 5+), with various ± complex appendages; A (4-many); (pollen oblate, triporate - Serjania, etc.); ovule often 1/carpel, outer integument 4-12 cells across, inner integument 2-6 cells across; (antipodal cells persistent - Cardiospermum); fruit also indehiscent, schizocarp with samaras, or septicidal; seeds usu. arillate or with arillode or sarcotesta; (amyloid [xyloglucans] in seed - Cardiospermum); n = esp. 10-12 [climbers] and 14-16 [non-climbers]; chromosomes 0.62-4.36 µm long.

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

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

• Sapindaceae are recognisable by their often spiral, pinnately-compound leaves that often have subopposite leaflets and a terminal rhachis tip, although many taxa have ternately/palmately-compound leaves. The base of the petiole is quite strongly swollen and the stem is ridged. The leaflets may be coarsely serrate and the fine venation is often prominent when dry. The inflorescences are paniculate, and the flowers are often borne in congested groups along the axis. The flowers are often rather small and are conspicuously hairy inside; there are often eight stamens and complex folds or scales on the petals. The fruits have only one or two seeds per carpel and are often deeply lobed, or a single carpel only may develop, the other one or two carpels persisting at the base; samaras of various types are common. The radicular pocket in the testa is distinctive.

Evolution. Divergence & Distribution. It has been suggested that all subfamilies of Sapindaceae diverged in the mid Cretaceous between (very approximately) 116-98 million years ago, spreading initially from Laurasia, with South East Asia remaining an important area in the evolution of the family (Buerki et al. 2010c). Fossils ascribable to Sapindaceae are known from the later Cretaceous, while Cupaniopsis-type pollen is widespread in the fossil record, including from several sites in Africa, although Sapindaceae with this pollen are no longer found there (Coetzee & Muller 1984). Wehrwolfea, with striate pollen and a floral formula of K 4 C 4 A 10(?+) G 3-4, is known from the middle Eocene of western Canada (Erwin & Stockey 1990).

For the biogeography of the family, in which much dispersal is involved, see Buerki et al. (2010c: methodological comparisons). The split between Acer and Dipteronia has been dated to (98-)78(-63.5) million years ago (Renner et al. 2007b). For the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. (2009). The very widespread Dodonaea viscosa has spread and diversified within the last two million years (Harrington & Gadek 2009).

Ecology. The largely neotropical Paullineae (Sapindoideae), with 8 genera including Serjania and Paullinia, contain one third of the species in the family. Many are vines and have trunks with several vascular cylinders that soon become independent of one another (Tamaio & Angyalossy 2009). Sapindaceae, along with Bignoniaceae and Fabaceae, are the major components of the viny vegetation of the Neotropics (e.g. Gentry 1991).

Floral Biology. Species of Acer like A. rubrum are known for having very labile breeding systems; see Renner et al. (2007b) for a study of breeding systems in the genus, with dioecy evolving several times.

Chemistry, Morphology, etc. Aesculus has bud scales, Billia has naked buds, but both branch from previous flush. "Ordinary-looking" stipules are known only from climbing species, but leaflets looking like stipules (pseudostipules) occur elsewhere in the family; there may not be any real distinction between the two.

Radlkofer (1892-1900) shows Serjania as having strongly obliquely symmetrical flowers, with the odd gynoecial member abaxial on the plane of symmetry. The abaxial corolla member is absent, but the stamens are abaxial, the two adaxial(?)-lateral members being missing. The petals of Sapindaceae are often rather complex, and have a similarly complex set of terms used to describe them. In Acer, the samaras are oblique (Schnizlein 1843-1870); Ronse de Craene (2010) depicts gynoecial orientation as varying within an inflorescence in Acer. Brizicky (1963) reports that the ovules may be epitropous, while those of Koelreuteria and other taxa are both epitropous (the lower ovule) and apotropous (the upper ovule) in the same loculus (Mauritzon 1936; Danilova 1996). Corner (1976) noted that the outer integument of Nephelium lappaceum was slightly thinner than the inner integument, amd he recorded a definite funicle from Aesculus, at least after fertilization. The fruit looks like a follicle when only one carpel develops; dehiscence is, however, down the abaxial side. In many Sapindaceae (and some 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. It has been suggested that the base chromosome number for Sapindaceae is x = 7 (Ferrucci 1989).

For an early tribal classification, see Radlkofer (1890), for a still useful account of the family, see Radlkofer (1933 to 1934), for seeds, see Guérin (1901), van der Pijl (1955) and Turner et al. (2009: germination), for chemistry, see Hegnauer (1964, 1966, 1973, 1989, 1990, also under Aceraceae and Hippocastanaceae), for pollen, see Muller and Leenhouts (1976), for wood anatomy, see Klaassen (1999) and Agarwal et al. (2005), for embryology, Tobe and Peng (1990), for chromosome numbers, Lombello and Forni-Martens (1998), for chromosome size, see Ferrucci (1989), for floral morphology of Koelreuteria, see Ronse Decraene et al. (2000b), of Handeliodendron, see Cao et al. (2008), and of Acer, etc., see Leins and Erbar (2010), for fruits of Paullineae, see Weckerle and Rutishauser (2005), for epidermal features, see Cao and Xia (2008) and Pole (2010), and for nectaries, which may have three vascular traces, see Solis and Ferucci (2009). Acevedo-Rodríguez et al. (2011).

Phylogeny. Preliminary studies suggested that Xanthoceras, with simply 5-merous, polysymmetric flowers, ovules arrranged in parallel (see also Magonia), and complex, golden nectaries borne outside the eight stamens, might be sister to all other Sapindaceae, and that the genera included in the erstwhile Aceraceae and Hippocastanaceae formed monophyletic sister taxa, the combined clade being sister to the remainder of the family (see Klaassen 1999; Savolainen et al. 2000a; Soltis et al. 2007a). Recent two-gene studies (Harrington et al. 2005, 2009 - the latter incorporating information about secondary structure of the ribosomal DNA examined, extensive sampling in Dodonaeoideae but not including any Sapindoideae) have largely confirmed these results. Harrington et al. (2005) found that Xanthoceras was not sister to the rest of the family in single gene analyses, being somewhat embedded, but without strong support; it was only in the joint analysis that is was sister to all other Sapindaceae (70% bootstrap, ³95% posterior probability: see also Buerki et al. 2010a, 2010b, support for the position still very low). Early morphological analyses (Judd et al. 1994) suggested a rather different set of relationships. For extensive phylogenetic studies of the family - 81 and 104 genera respectively - see Buerki et al. (2009, 2010b); the limits of some tribes need re-evaluating. For the phylogeny of Acer, see Li et al. (2006) and Renner et al. (2007b), and for the phylogeny of Dodonaea, see Harrington and Gadek (2010).

Classification. The phenetically distinctive Aceraceae and Hippocastanaceae are here included in Sapindaceae, with which they have much in common; Buerki et al. (2010b) prefer to recognize them (and Xanthoceras, as Xanthoceraceae) as families. For subfamilies, see Buerki et al. (2009). There is extensive polyphyly of the classically-recognized tribes (Buerki et al. 2010b).

Previous Relationships. Sapindaceae are chemically similar in some respects to Fabaceae (e.g. both have non-protein amino acids: for a summary of these, see Fowden et al. 1979), and both have compound leaves, but they are unlikely to be immediately related.

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

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).

Hartl (1958b) sugested that there were similarities betwreen Rutaceae and Simaroubaceae in fruit (endocarp) anatomy; he did not include other members of Sapindales in his comparison. Rutaceae and Simaroubaceae are reported to have embryo sac haustoria (Mickesell 1990). For some information on carpel development, see van Heel (1983).

SIMAROUBACEAE Candolle, nom. cons.   Back to Sapindales

Trees or shrubs; bark very bitter by simaroubilide quassinoids, carboline alkaloids and canthinones [with trptophane nucleus), ellagic acid +; wood often fluorescing; (nodes multilacunar); pith conspicuous, medullary secretory canals common; sclereids common, oil cells uncommon; (stomata paracytic); leaflet not articulated, vernation also supervolute-curved, (flat surface glands +), margins coarsely toothed to entire, (stipules +, cauline [Picrasma, some Soulamea] or petiolar); breeding system various; (pedicel articulated), flowers rather small, (3-)4-6(-8)-merous; K connate or free (0), (C 0); A (4, 5, opposite sepals, [with 4-5 staminodes]; 10<), with lateral or basal-adaxial scales or 0; tapetal cells 3-12-nucleate; gynophore short and stout/0, G 1-5(-8), ± free to connate, style +/0, or styluli +, often ± basal, stigmas ± recurved, ± pointed, with elongated receptive zone, dry; ovule 1(-2)/carpel, (hemitropous), micropyle (bistomal? - Samadera) zig-zag, (inner integument very long, folded), outer integument 3-10 cells across, inner integument 2-8 cells across, parietal tissue 6-20 cells across, (ovule close to epidermis - Samadera), nucellar cap ca 2 cells across; fruit commonly a schizocarp, a 1-seeded drupelet or samara; seed (pachychalazal), with undistinguished testa (mesotegmen with reticulate thickenings) or scattered lignified cells, endotesta often slightly lignified, tegmen crushed; (endosperm with starch [Leitneria] or hemicellulose reserve), (perisperm +, thin); n = 8-13.

19-22[list]/110: Simaba (25). Largely tropical; a few (e.g. Ailanthus) temperate (map: from Nooteboom 1962; Heywood 1978; Thomas 1990; 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] [Photo - Fruit]

• Simaroubaceae can be recognised because the twigs have conspicuous pith - herbarium specimens are often notably light - and the bark is bitter, even when dry; the leaflets of the odd-compound leaves often have rather coarse, blunt, teeth and flat glands on the lower surface, sometimes close to the margin, and the leaf rhachis collapses at the nodes. The flowers are rather small, the petals usually barely exceeding the sepals. The fruits are often separate drupelets or samaras.

Evolution. Divergence & Distribution. Ailanthus is known as widespread fossils from the Eocene ca 52 million years before present; it has not been recorded from the Palaeocene (Corbett & Manchester 2004; see also Clayton et al. 2009 for the fossil history of this genus, Leitneria, and Chaneya, the latter not certainly to be included in Simaroubaceae). The age of crown group Simaroubaceae has been estimated as some 52 million years (Muellner et al. 2007), although better sampling in the family suggested a rather older date in the Cretaceous-Maastrichtian a little more than 65 million years ago. However, most diversification within the family has been in the Caenozoic (Clayton et al. 2009).

Despite (or because of?) the fairly good fossil history of the family in the northern hemisphere, the biogeographic hisory of Simaroubaceae is of considerable complexity with much dispersal (and some extinction) needed to explain the current distribution of taxa (Clayton et al. 2009).

Chemistry, Morphology, etc. The quassinoids charactistic of Simaroubaceae replace other limonoids (Waterman 1993). The adult plant of Holacantha is basically a giant branched thorn system; the leaves are reduced to scales. Although the carpels may be ± free, there is often only a single style. The gynoecium of Leitneria is described as having a single carpel with two ovules, of which only one is fertile (Tobe 2011a). Even in taxa with unitegmic ovules, the axis of the embryo and that of the micropyle are offset at a sharp angle, hence the latter is zig-zag. There are reports of other than porogamous fertilisation in the family (cf. Anacardioideae: Rao 1970).

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

Phylogeny. [Picrasma [Holacantha + Castela]] form a clade with rather weak support that is sister to the rest of the family, Ailanthus and [Leitneria, Soulamea, Brucea, etc.] are successively sister to the remainder; much of the phylogenetic structure along the backbone of the family is well supported (Clayton et al. 2007a, esp. b; 2009). There are five major clades, and only Quassia and Nothospondias are of uncertain position, bracketing Picrolemma (Clayton et al. 2007b). Leitneria is well embedded in Simaroubaceae so it cannot be kept separate (Clayton et al. 2007b) - it is wind pollinated, the plant is more or less dioecious, and hardly surprisingly the flowers are much reduced and in short catkins: C 0?, pollen reticulate; G 1, stigma decurrent; inner integument long, folded; testa multiplicative, mesotegmen with reticulate thickenings, only entotegmen persists; endosperm starchy (see Tobe 2011a in part, some confusion as to whether the testa is multiplicative; note that Leitneria has embryological similarities with Bruca). Its bark does not taste bitter.

The very poorly-known Gumillea (ex Cunoniaceae) should perhaps be included in Simaroubaceae, although the stamens do not appear to have scales and there are many ovules per carpel - the latter feature in particular would be rather odd for any member of Sapindales. Its stamens alternate with its petals, so making membership in Picramniales unlikely (and ovule number also militates against this).

Previous Relationships. Simaroubaceae have been very difficult to delimit, and molecular data suggest the excision of Suriana and its relatives (here in Surianaceae - Fabales), Harrisonia (Rutaceae), and Picramnia and Alvaradoa (Picramniaceae - Picramniales, sister to [Sapindales [Huerteales etc.]]) (e.g. Fernando et al. 1995).

Synonymy: Ailanthaceae J. Agardh, Castelaceae J. Agardh, Holacanthaceae Jadin, nom. inval., Leitneriaceae Bentham & J. D. Hooker, Quassiaceae Bertolini, Simabaceae Horaninow, Soulameaceae Pfeiffer

[Rutaceae + Meliaceae]: tetranortriterpenes, flavones +; stigma capitate.

RUTACEAE Jussieu, nom. cons.   Back to Sapindales

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

161[list]/2070 - three groups below. Largely tropical (map: from Meusel et al. 1978; Brummitt 2007).

1. Cneoroideae Webb

Pyranochromones, (diterpenoid cneorubin X; quassinoids) +; oil cavities 0 (+, e.g. Spathelia), oil cells commonly solitary; petiole bundle more or less cylindrical, of two opposed plates (arcuate - Bottegoa); stomata anomocytic to cyclocytic; solitary oil cells + (0), (schizogenous cavities 0); (leaves bicompound), (stipules and stipular thorns +); C valvate; A 4-5 [haplostemonous], (8-10), filaments with appendages; pollen reticulate; ovules 1-2(-5)/carpel, apotropous or epitropous, campylotropous, micropyle endostomal, outer integument ca 2 cells across, inner integument ca 3 cells across, parietal tissue ca 5 cells across; fruit a loculicidal capsule, the carpels opening adaxially and separating laterally and from columella, a winged drupe, or follicle; (testa multiplicative, exotestal cells large, outer walls thickened - Harrisonia); n + ?

7/35: Spathelia (20). Throughout the tropics, also N. Australia and the Mediterranean.

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

Aurantioideae + Rutoideae: (exine striate); outer integument 3-6 cells across, inner integument 2-5(-6) cells across, parietal tissue 5-12 cells across, nucellar cap several layered; (exotesta mucilaginous).

2. Aurantioideae Eaton

Methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); (leaf rhachis winged), (leaflets alternate); C imbricate; (A many); G postgenitally united; (ovule unitegmic - Glycosmia); fruit a ± dry berry with mucilaginous pulp directly from endocarp or multicellular hairs; exotesta mucilaginous, inner walls lignified, often fibrous, exo- and endotesta with crystal-containing cells; n = 9.

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

Synonymy: Amyridaceae Kunth, Aurantiaceae Jussieu, Citraceae Roussel

3. Rutoideae Arnott

(Herbs); alkaloids as quinolones and acridones derived from anthranilic acid, or from furo-pyranoquinolines and -pyranoquinolines; (distinctive tracheal veinlet endings); oil cells also commonly solitary; (leaves opposite), (stipules intrapetiolar/petiolar sheath - Metrodorea); flowers (vertically or obliquely monosymmetric); C fringed - Ruta); A (connate), (2, with basal anther appendages, + 3 staminodes - Angostura alliance), (obdiplostemonous); ([andro]gynophore +); (G 2+), (opposite sepals - Zanthoxylum), (styluli [marginal] +), (connate only at apex); carpels separating in fruit; also seeds winged, or forcibly expelled with endocarp; exotesta often mucilaginous, irregularly palisade, lignified or not, or fibrous and lignified, (mesotesta sclerotic), (sarcotesta +, lignified endotesta), meso-/endotesta thickened [Zanthoxylum], exotegmen with crossed lignification bars, or not [Skimmia), (meso- and endo- tegmen tracheidal); n = (7-)8-9(-11).

120/1827: Melicope (235), Zanthoxylum (225), Agathosma (150 +), Boronia (150), Vepris (80), Haplophyllum (70), Zieria (60), Acronychia (48), Conchocarpus (45), Amyris (40). Pantropical, some (warm) Temperate. [Photo - Flower, Flower, Fruit.]

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

• Rutaceae are recognisable because of their often opposite, compound and punctate leaves; their cymose inflorescences; their flowers, with the stamens often arranged in a ring, thick filaments, conspicuous disc at the base of the ovary, and expanded stigma, are quite distinctive. Although the fruits are variable, many have a glandular-punctate pericarp, while others are dry, deeply lobed, and dehisce to reveal the black and shiny seeds.

Evolution. Divergence & Distribution. Salvo et al. (2010, which see for more dates) suggest that [Rutoideae + Aurantioideae] diverged from other core Rutaceae in the late Cretaceous ca (90-)74(-58) milion years ago. For dates of diversification within Rutaceae, especially Aurantioideae, see Pfeil and Crisp (2008; cf. in part Muellner et al. 2007); the family is relatively young, and distributions are unlikely to be much affected by continental drift events (but cf. Kubitzki et al. 2011; Hartley 2001a, 2001b; Ladiges & Cantrill 2007).

Melicope had undergone a major radiation on Hawaii of 50+ species; the source area is likely to be in the general Australia-New Guinean region, and from Hawaii there seems to have been dispersal to the Marquesas Islands (Harbaugh et al. 2009b). For the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. (2009); Gregor (1989) discussed fossils of seeds from the Tertiary.

Plant-Animal Interactions. Rutaceae have exceptionally diverse secondary metabolites, some of which (essential oils, coumarins, etc.) are similar to those in Apiaceae, Asteraceae, Papaveraceae, etc. (Hegnauer 1971; Kubitzki et al. 2011), while their alkaloids are like those found in some magnoliids - and are produced via nine or more different biosynthetic pathways. 1-benzyltetrahydroisoquinoline alkaloids are found in a small group of related Rutoideae, and also in Papaveraceae (and a couple of other families), which exercised phytochemists' imaginations in the past (Kubitzki et al. 2011). Caterpillars of Papilionidae-Papilionini butterflies are notably common on Rutaceae, indeed, ca 1/3 of the records are from this family, and 80% of the ca 550 species of Papilio will eat this family (Zakharov et al. 2004). Like the magnoliids, e.g. Aristolochiaceae, on which closely related Papilioninae are also found, it is the alkaloids that attract the butterflies. It is possible that Rutaceae were the original food plants for Papilio, since even those caterpillars which now eat Magnoliales will eat Rutaceae if they have to (Zakharov et al. 2004, but cf. Fordyce 2010; see also Berenbaum & Feeny 2008).

Seed Dispersal. Ca 250 species of Diosmeae are restricted to South Africa, largely to the Cape Floristic Region (Trinder-Smith et al. 2007). This group, as well as Boronia are relatives, (Australian), have seeds with elaiosomes that are endocarpial in origin and are dispersed by ants (Kubitzki et al. 2011).

Chemistry, Morphology, etc. Rutaceae as circumscribed here are a variable group. For their diverse secondary metabolites, see Hegnauer (1971) and Kubitzki et al. (2011). Rutaceae and associated "families" once segregated from them all have pyranochromones. Da Silva et al. (1988) surveyed these 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.).

Prickles of Zanthoxylum can be in the stipular position.

Rutaceae are variable in flower and fruit, if less so vegetatively. Monosymmetry is scattered in the family, occurring in Dictamnus (relationships uncertain) and Erythrochiton, for example. Kallunki (1992) illustrates the flowers of Erythrochiton fallax as having the median sepal adaxial, but their exact orientation and how they are actually 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 belongs, may have only two stamens plus staminodes, a connate corolla, filaments connate and forming a tube, or a corolla that forms a tube only because of the serial adnation of filaments and petals; variation in gynoecial development is also considerable (Pirani & Menezes 2007; el Ottra et al. 2011 for a summary). 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. Wei et al. (2011) sugest that Rutaceae may plesiomorphically have five stamens.

Triphasia has G [3], the odd member being adaxial, and the same is true of Cneorum tricoccon, which has 3-merous flowers (see Caris et al. 2006 for floral development). Carpel (stylar) fusion may be postgenital (Gut 1966). Ovules of Glycosmis are unitegmic, and both apotropous and epitropous ovules are recorded from the family. In bitegmic taxa, either integument may be slightly thicker than the other (Corner 1976). Nucellar polyembryony is widespread. The endocarp divides periclinally during development (Hartl 1958), resulting in a pronounced layering of the mature capsule, especially in Rutoideae. 

For gynoecial morphology in particular, see Gut (1966), for general information, see van der Ham et al. (1995) and White and Styles (1966), for general chemistry, see Hegnauer (1973, 1990, also 1964, 1989 as Cneoraceae), Waterman and Grundon (1983), Mulholland et al. (2000, esp. "Ptaeroxylaceae"), and Yan et al. (2011 and references, Harrisonia in particular), for alkaloid chemistry, see Waterman (1975, 1999), for floral development of Cneorum, Caris et al. (2006b), for floral morphology, see Zhou et al. (2002) and Wei et al. (2011), for floral orientation, see Eichler (1878), for ovules of Harrisonia, see Wiger (1935), and for fruit anatomy, see Brückner (1991). For the chalazal opening (?vascular bundle) in the seed, see Wilson (1998) and Hartley (2003). See also Dahlgren and van Wyk (1988), van der Ham et al. (1995) and White and Styles (1966) for information about some Cneoroideae. Kubitzki et al. (2011) provide a detailed overview of the family.

Phylogeny. Relationships are discussed in considerable detail by Kubitzki et al. (2011). General relationships in a two-gene analysis were found to be that most of Rutaceae were sister to the [[Spathelia + Dictyoloma] [[Cneorum + Ptaeroxylum] Harrisonia]] clade, both genus pairs with good support, but the position of Harrisonia, with sequences from only a single gene, was less clear (Chase et al. 1999; see also Groppo et al. 2008). 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 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 and Fernando et al. (1995) suggested that its removal from Simaroubaceae was justified on both molecular and morphological grounds. Although these few genera form a fairly distinct group, inclusion within Rutaceae seems reasonable (Groppo et al. 2008). Razafimandimbison et al. (2010) again found a small group of genera including those mentioned above that formed a weakly/moderately supported clade in which [Spathelia + Dictyoloma] are sister to the rest that included the old Ptaeroxylaceae, and this basic topology was found again in a study using denser sampling and five chloroplast genes; support for the groups was strong, and a number of morphological characters (many original observations!) - were plotted on the tree (Appelhans et al. 2011). Appelhans et al. 2011) also provide a tribal classification for the whole clade, which is morphologically quite heterogeneous - like the rest of the family; it is recognised as Cneoroideae above.

Hartley (e.g. 1981, 1997, 2001a, b) suggested some generic realignments in Malesian-Pacific Rutaceae that largely ignored then then-conventional subfamilies; this work has since been confirmed by molecular data. Within core Rutaceae, [Aurantioideae (distinctive fruit with fleshy hairs in the loculi; fibrous exotegmen; endosperm 0; x = 9) [Chloroxylon, Boenninghausenia, Ruta, etc.]] do form a poorly to well-supported clade (e.g. Groppo et al. 2008; Salvo et al. 2010; e.g. see also Morton et al. 2003). For relationships within the group, see Pfeil and Crisp (2008) and Bayer et al. (2009); Clauseneae may not be monophyletic (Morton 2009). For subtribal relationships, see Morton (2009), and for relationships around Citrus, see Scott et al. (2000), Samuel et al. (2001), Araújo et al. (2003), and Bayer et al. (2009).

Salvo et al. (2008, also 2010) found that Dictamnus is widely separate from the other members of Ruteae, linking with Casimoroa and Skimmia (Groppo et al. 2008). Most other Rutaceae form a clade sister to Dictamnus et al. (see Poon et al. 2007; Groppo et al. 2008; Salvo et al. 2010), and subfamilies other than Aurantioideae are interspersed in this group, within which relationships are uncertain. Zanthoxylum may be sister to the rest (see also Muellner et al. 2007); it is certainly part of a well-supported clade with distinctive isoquinoline alkaloids that may be sister to Ptelea. Flindersia and relatives, in another part of this major clade, have secretory cells in the stem only and their capsule is septifragal, perhaps reminiscent of Meliaceae, but their furoquinoline alkaloids, schizogenous cavities, and subterete filaments are consistent with a position in Rutaceae. Euodia and relatives form a moderately supported clade perhaps forming a clade with the Flindersia group (Salvo et al. 2010), but other than that, relationships are unclear (Poon et al. 2007). For relationships in Galipeinae see Kallunki and Groppo (2007), in the largely South African Diosmeae, see Trinder-Smith et al. (2007), and the Irano-Turanian Haplophyllum which subsequently colonized the Mediterranean area more than once, see Salvo et al. (2011) and Manafzadeh et al. (2011).

Classification. Some of the fruit characters used to distinguish the classic subfamilies in the rest of Rutaceae are proving unreliable in delimiting major clades (e.g. see Hartley 1981; But et al. 2009), and tribal limits for the most part also need overhauling (e.g. Salvo et al. 2008; Poon et al. 2008). The same is true of generic limits, especially around Citrus (Scott et al. 2000; Samuel et al. 2001; Bayer et al. 2009), as also in Galipeinae (Kallunki & Groppo 2007) and Diosmeae (Trinder-Smith et al. 2007), and changes are gradually taking place. Here I follow Kubitzki et al. (2011) for subfamilial limits; they note that 1/4 of the genera in the family are monotypic.

Previous Relationships. Cronquist (1981) included Cneorum in Sapindaceae; 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. Harrisonia has also been included in Rutaceae, as by Thorne (1992), although no reasons were given, Waterman (1993) noted that the genus contained no quassinoids.

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

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

MELIACEAE Jussieu, nom. cons.   Back to Sapindales

Trees; bark often rather bitter; secretory cells with resin, etc. +; nodes 5:5; (hairs stellate); (leaves even-pinnate), leaflets not articulated (articulated), (margins toothed); plants often dioecious, but flowers apparently perfect, (3-)5(-8)-merous; K often connate, A 2x C, connate (5-30 in a single whorl); tapetal cells 2-4(-10)-nucleate; G (1) [2-6(-many)], postgenitally united, opposite C, style-head discoid or capitate (± lobed), stigma wet; ovules ?anatropous, (micropyle exo/bistomal), outer integument 2-5 cells across, inner integument 2-4 cells across, parietal tissue 3-9(-18) cells across, placental obturator common; megaspore mother cells often many; seeds often pachychalazal, coat vascularized, testa and tegmen multiplicative (not), testa undistinguished but thick, endotesta crystalliferous, exotegmen fibrous [Trichilia, Swietenia] (not); embryo white [green - Trichilia]; x ?= 6, 7.

50[list]/615 - 2 groups below. Pantropical, but largely Old World; plants of the lowlands (map: see Wickens 1976; Pennington 1981; FloraBase 2006; GBIF x.2009).

1. Melioideae Arnott

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

36/558. Aglaia (120), Dysoxylum (80), Trichilia (70), Turraea (60), Chisocheton (50), Guarea (50). Pantropical, but largely Old World.

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

2. Cedreloideae Arnott

Buds perulate (naked - Capuronianthus); (leaves opposite); (C connate); (A at least partly free); (nectary 0); ovules (2 [Capuronianthus]) 3-many/carpel, collateral; fruit a septifragal capsule, valves falling off, columella persisting and seeds winged, or slight columella and seeds with massive woody or corky testa; n = 13, 18, 23, 25, 26, 28.

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

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

• Meliaceae are recognisable by their usually spiral and odd-compound leaves with well-developed leaf buttresses, i.e. the leaf bases are swollen and more or less elongated vertically. The leaflets are often opposite and dry thin and brittle, with little in the way of tertiary venation evident. The bark may smell - sweet, like garlic, etc. - and milky exudates occur sporadically. The flower buds are often longer than broad, with petals much longer than the sepals, and most members have a staminal tube and a large stigma. The fruits and seeds are usually quite large. [Photo - Flower, Fruit.]

Evolution. Divergence & Distribution. Muellner et al. (2006) discuss the biogeography of the family, suggesting its origin in Africa and subsequent dispersal; the family is ca 85-76 million years old, diversification within it beginning ca 75-67.5 million years before present. For fossil Meliaceae, see Mabberley (2011). For the biogeography of Aglaia, see Muellner et al. (2008b).

Although only a small family, Meliaceae make up 17% of all trees >10 cm bole diameter in Sumatra (Mabberley 2011).

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

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

Vegetative Variation. Most species of Guarea (tropical America) and Chisocheton (Malesia), both Melioideae, have indefinitely growing leaves. In Guarea the apical part of the leaf is shoot-like in its gene expression (Tsukaya 2005), while in species of Chisocheton such as C. pohlianus the inflorescence may be epiphyllous (Fisher & Rutishauser 1990), flowers appearing between the leaflets (specimens have been misidentified as Rubiaceae!). In the latter genus the leaves can be rooted, and then they continue to grow for a long time, although I do not know of any case where a tree has been produced from a leaf. Capuronianthus (Swietenioideae) has opposite, compound leaves, while the simple-leaved Vavaea and Turraea (both Melioideae) look rather unlike other Meliaceae, except when in flower; the leaves of the latter genus may even be two-ranked and lack articulations.

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

Chemistry, Morphology, etc. Munronia is ± herbaceous. Sieve tube plastids with protein crystalloids and starch occur in Melia and Azederach. Gouvêa et al. (2008b) draw the flowers of Swietenia as being inverted; as might be expected, carpellate flowers are the first to be produced in the cymose inflorescences. The filaments of Vavaea are largely free, as are those of Cedrela and Toona (Swietenioideae-Cedreleae). Indeed, Cedreleae are rather different florally from other Meliaceae, but features found there such as more or less free stamens may be derived, not plesiomorphous as one might think a priori (cf. Gouvêa et al. 2008a). Walsura often has leaflets with ± pulvinate petiolules and prominent reticulate venation, the stamens are also more or less free, and the fruit is often 1-seeded. Turner et al. (2009) document a water gap near the hilum in the hard seeds of Dodonaea.

For chemistry, see Hegnauer (1969, 1990) and Mulholland et al. (2000), for embryology, etc., see Wiger (1935), Paetow (1931), and Nair (1970), and for general information, see Mabberley et al. (1995: esp. Malesia) and Mabberley (2011).

Phylogeny. Cedreloideae (Swietenioideae) and Melioideae are clearly monophyletic clades (Oon et al. 2000: one gene, Cedreloideae not well supported; Muellner et al. 2003: three genes; Muellner et al. 2006: rbcL alone, sampling better). Although the two subfamilies can be separated chemically based on limonoid types, recent work on Quivisianthe suggests that the distinction may not be that simple (Mulholland et al. 2000). Two Malagasy genera previously segregated as separate subfamilies, Quivisianthe and in particular Capuronianthus, are embedded in Melioideae and Cedreloideae respectively (e.g. Muellner et al. 2003, 2006). Within Melioideae, Melieae (probably including Owenia) are sister to the rest, but with only moderate support; 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). For relationships in Aglaia, see Muellner et al. (2005); see Fukuda et al. (2003) for a phylogeny of Chisocheton; for Neotropical Cedreleae, see Muellner et al. (2009).

Classification. For a generic monograph, see Pennington and Styles (1975), for a monograph of Neotropical Meliaceae, see Pennington (1981), and for a monograph of Aglaia, see Pannell (1992).

Cedreloideae used to be called Swietenioideae.

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