Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm2 (to 5 mm/mm2).
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 [so no Maüle reaction]; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; 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 +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening in response to leaf hydration active, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, 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, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, 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, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, 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, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, 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]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], 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]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessels with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: plant woody; (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; palaeohexaploidy [gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: nodes 3:3; stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].
ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); embryo long; genome duplication; 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 scanty.
[HUERTEALES [MALVALES + BRASSICALES]]: ?
[MALVALES + BRASSICALES]: ?
Age. The age of this node was estimated to be (94-)89(-85) or (80-)74(-68) m.y., Bayesian relaxed clock estimates to 96 m.y. (Hengchang Wang et al. 2009), while Argout et al. (2010) give a date for this clade (or perhaps of a bigger clade, one perhaps including the common ancestor of all malvids) of only ca 59 m.y., which has to be a major underestimate. A suggestion by Zhang et al. (2012) is for an age of (82-)73(-60) m.y., while Magallón and Castillo (2009) estimated an age of ca 92 m.y. for this node.
Phylogeny. These two orders were linked in a whole chloroplast genome analysis by S.-B. Lee et al. (2006), although no chloroplast genomes of other rosid II taxa were then available. This grouping/position is supported in the more recent analyses of Worberg et al. (2009).
MALVALES Berchtold & J. Presl Main Tree.
(Cyclopropenoid fatty acids +), flavones, myricetin +; mucilage cells +; C contorted; disc 0; style long; ovules few/carpel; embryo long, radicle short, cotyledons thin. - 10 families, 338 genera, 6005 species.
Age. Wikström et al. (2001) estimate crown Malvales to be (75-)71, 67(-63) m.y.o.; other suggestions are (80-)78(-76) and (76-)74(-72) m.y. (two penalized likelihood dates) (Hengchang Wang et al. 2009).
Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many 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 is the not-so-trivial issue of how ancestral states are reconstructed...
Evolution. Divergence & Distribution. Dating the separation of clades within this group is of considerable interest given the interesting distributions of many of the families.
Malvales contain ca 3.2% eudicot diversity (Magallón 1989) and show moderately high diversification rates (Magallón & Catillo 2009).
Bacterial/Fungal Associations. Taxa with ectomycorrhizal associations are common in this order, e.g. Tilioideae and ex Sterculiaceae, Dipterocarpaceae and Cistaceae (Smith and Read 1997), Sarcolaenaceae (Ducousso et al. 2004); it will be interesting to see just how widely distributed such mycorrhizae are.
Chemistry, Morphology, etc. For the distribution of cyclopropenoid fatty acids, which are also scattered outside Malvales, see Badami and Patil (1981), Gaydou and Ramanoelina (1983) and Bayer et al. (1999). However, as Kubitzki and Chase (2002: Table 1) show, the evolution of this and other features common in the order are difficult to understand. Species with stratified phloem always have wedge-shaped phloem rays, Sarcolaenaceae perhaps excepted (Kubitzki & Chase 2002). The androecium is possibly basically oligomerous, and the earliest initiated or innermost members are oppositisepalous with centrifugal or lateral polyandry. Starchy endosperm may be an apomorphy for the group.
Some general information, esp. carpel orientation, is taken from from Nandi (1998a, b) and Kubitzki and Chase (2002); for wood anatomy, see i.a. den Outer and Vooren (1980) and den Outer and Schütz (1981).
Phylogeny Several clades within Malvales are quite well established, but relationships between them, as well as the position of one or two families, remain unclear. Fay et al. (1998a) and Bayer et al. (1999) discuss general relationships. These may be represented as Muntingiaceae [[[Thymelaeaceae + Sphaerosepalaceae] [Neuradaceae [Sarcolaenaceae [Dipterocarpaceae + Cistaceae]]]] [Bixaceae + Malvaceae]], but few of these relationships have much support, even after successive weighting. Dayanandan et al. (1999) and Morton et al. (1999) relationships within Dipterocarpaceae, and Alverson et al. (1998), Bayer et al. (1999) and especially Alverson et al. (1999) those within Malvaceae s.l. Neuradaceae may be sister to the rest of the order (see also Soltis et al. 2007a). Although Bixaceae are expanded here, it has also been suggested that Cochlospermum and relatives are also close to Diegodendron and Sphaerosepalaceae, less to Bixa (Johnson-Fulton & Watson 2008). The relationships of Sphaerosepalaceae within Malvales are unclear; in Bayer et al. (1999) they are weakly associated with Thymelaeaceae and in Alverson et al. (1998) with Bixaceae and Cochlospermaceae. The relationships between Sarcolaenaceae, Dipterocarpaceae, and Cistaceae are also uncertain (Ducoussu et al. 2004). See also Soltis et al. (2011) for relationships; these are somewhat different from those discussed above, but sampling is poor.
Relationships of Cytinaceae with Malvales have been suggested (Nickrent 2002), and these appeared in all analyses in a more recent study (Nickrent et al. 2004). However, the only Malvales included in Nickrent et al. (2004) were Cistaceae and Malvaceae, and the placement of Cytinaceae remained somewhat provisional. Recently Nickrent (2007), with much better sampling, found that Cytinaceae are sister to the poorly-known Muntingiaceae with moderate (maximum likelihood) to strong (maximum parsimony) support (nuclear small-subunit [SSU] r-DNA was the nuclear gene used in the placement). Both Cytinaceae and other Malvales have exotegmic seeds, and aspects of the perianth of Cytinaceae and Malvaceae can perhaps be compared. The mitochondrial genes cox1 and matR showed considerable divergence, but not the atp1 gene (Barkman et al. 2007). Apodanthaceae are here included in Cucurbitales (see Filipowicz & Renner 2010), with which they show gynoecial similarities in particular, both having a connate androecium and extrose anthers, inferior ovary, parietal placentation, etc., are also somewhat similar morphologically to Malvales (Nickrent et al. 2004).
Previous Relationships. Elaeocarpaceae, previously usually included in (Cronquist 1981) or near Malvales, are here placed unambiguously - if somewhat unexpectedly - in Oxalidales. Most Malvales as delimited here are included in Takhtajan's (1997) Malvanae; the core of Malvales in the past was the families here all included in Malvaceae.
Includes Bixaceae, Cistaceae, Cytinaceae, Dipterocarpaceae, Malvaceae, Muntingiaceae, Neuradaceae, Sarcolaenaceae, Sphaerosepalaceae, Thymelaeaceae.
Synonymy: Aquilariales Link, Bixales Lindley, Bombacales Link, Byttneriales link, Cistales Berchtold & J. Presl, Cytinales Dumortier, Daphnales Lindley, Dipterocarpales Martius, Neuradales Martius, Sterculiales Berchtold & J. Presl, Thymelaeales Berchtold & J. Presl, Tiliales Berchtold & J. Presl
NEURADACEAE Kostelvsky, nom. cons. Back to Malvales
Annual (perennial) ± prostrate herbs/subshrubs; cyclopropenoid fatty acids +, ellagic acid?, tannins?; cork?; cambium storying?; pits not bordered; sieve tube plastids with protein crystalloids and starch; nodes ?; petiole anatomy simple; cuticle waxes 0; hairs unicellular; leaves spiral, lamina margins toothed to pinnatifid, secondary veins subpalmate, stipules ?; inflorescence cymose, ?cincinnus; hypanthium +, short; K valvate, C also imbricate, distinctively coloured when dry; A 10; pollen oblate, with semicolpi merging in threes at each pole, each semicolpus with an os, [tri(tetra)-diporate], trinucleate; G , ± inferior, opposite sepals, ascidiate when young, (2-4 abaxial carpels infertile), styluli +, stigmas capitate; ovule 1/carpel, apotropous, lying horizontally, micropyle bistomal, outer integument ca 4 cells across, inner integument ca 4 cells across, parietal tissue ca 2 cells across; fruit dry, indehiscent, K accrescent, styles persistent, forming spines or not; testa ± crushed, endotestal cells small, tegmen multiplicative, exotegmic cells also tangentially elongated, crystalliferous, other tegmic cells persistent; endosperm ?development, 0, embryo bent; n = 7.
3[list]/10: Grielum (5). Africa to India, dry or desert areas (Map: from Heywood 2007, also floras, esp. Miller & Cope 1996; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006). [Photo - Flower.]
Chemistry, Morphology, etc. The vascular bundles have a mucilaginous sheath. The plant probably lacks stipules, the stipule-like structures that are sometimes seen in fact being a prophyll that develops later than the foliage leaf (Bayer 2002); in addition, the basically cymose inflorescence/plant construction with paired but unequal leaves makes things complicated. The presence/absence of stipules should be confirmed, and this will be of relevance to understanding nodal anatomy.
There appears to be no epicalyx, although the outside of the ovary may have spines which become conspicuous in fruit; these develop centrifugally (Ronse DeCraene & Smets 1995d). The flowers of Grielium are obliquely monosymmetric, some of the carpels on one side of the flower being reduced and non-functional (Murbeck 1916). The corolla of members of Neuradaceae changes colour on drying, as in some Malvaceae (Airy Shaw 1966) - see Huber (1993a). There is sometimes a second, reduced ovule in the carpels (Murbeck 1916). Goldberg (1986) and Takhtajan (1997) describe the carpels as dehiscing ventrally, but this may be confusion with the germinating seed that is still inside the fruit (e.g. Murbeck 1916).
For general information, see Murbeck (1916) and Bayer (2002), and for pollen, see Polevova et al. (2010); the family needs work.
Previous Relationships. Neuradaceae have previously placed been elsewhere, as in Rosales in Cronquist (1981) and Takhtajan (1997), Hutchinson (1973) and Corner (1976) included it in the Rosaceae, and the floral anatomy of the two is similar (Ronse Decraene & Smets 1995), although Corner (1976) noted that the seed coat anatomy appeared to be different.
Thanks. I am grateful to Z. Rogers for comments.
Synonymy: Grielaceae Martynov
[Thymelaeaceae [Sphaerosepalaceae, Bixaceae, [Cistaceae + Sarcolaenaceae + Dipterocarpaceae], [Muntingiaceae + Cytinaceae], Malvaceae]]: pits vestured; phloem stratified, phloem rays wedge-shaped; exotegmen much thickened and lignified, palisade.
Age. The age of this node is around (81-)75, 72(-65) m.y. (Bell et al. 2010: note topolgy).
THYMELAEACEAE Jussieu, nom. cons. Back to Malvales
Cyclopropenoid fatty acids +; wood often fluoresces; vascular tracheids +; secondary phloem fibres unlignified; nodes 1:1; pericyclic fibres 0 [Edgeworthia, Tepuianthus]; crystal sand +; petiole bundle arcuate; epidermal cells (massively) mucilaginous; stomata cyclocytic; hairs simple; leaves spiral, lamina vernation supervolute (conduplicate), stipules 0 or minute; inflorescence cymose; flowers (3-)4-5(-6)-merous; K and C imbricate; tapetal cells uninucleate; pollen trinucleate; ovule 1/carpel, epitropous, micropyle endostomal (zig-zag), outer integument 3-6 cells across, inner integument 3-10 cells across, parietal tissue 3-7 cells across, nucellar cap 2-4 cells across, (± pachychalazal), hypostase + [cone of cells], obturator from near base of stylar canal; (antipodal cells persist, many); (testa fleshy), (tegmen multiplicative), exotegmen with brown contents, endotegmen with brown contents, reticulately thickened and lignified; (suspensor 0), embryo white, cotyledons large.
46-50[list]/891 - 3 groups below. World-wide, esp. trop. Africa and Australia (map: from Domke 1934; Meusel et al. 1978; Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower Flower, Fruit.]
Trees or shrubs, bark bitter; phloem rays narrow; resiniferous cells +; plant androdioecious; flowers small, K and C free, C ± clawed; 5-10 glandular scales; A 5, opposite sepals, or 12-22, in groups opposite petals[?], connective produced or not; pollen colp(or)ate; G [(2)3], styles separate, bifid [parastyles?]; fruit a loculicidal capsule; seeds with an angled raphe; endosperm +; n = ?
1/7. Guayana highlands, northeast South America.
Synonymy: Tepuianthaceae Maguire & Steyermark
[Octolepidoideae + Thymelaeoideae]: C 0; pollen oligo- to polyporate, minutely spinulose; style single, stigma ± capitate, dry; endotegmen with stripes on the inner surface; fruit a loculicidal capsule, berry, or achene.
2. Octolepidoideae Gilg
Trees, shrubs or lianes; secretory cavities + [lamina punctate]; (stomata anomocytic - Octolepis); hypanthium +, at most short, or 0; K (3-)5(6), valvate or imbricate; glandular scales 4-40; A 8-80, not adnate to tube, (connate), anthers usu. recurved and hippocrepiform, connective well developed, (basal layer with pendulous internal processes); G (2-)3-5(-8), (clavate or subglobose parastyles +; stigma punctate); seed with a raphal aril, or angled at the raphe, or funicle swollen; chalazal fold on ventral side only [distribution elsewhere in family?], nucellar tracheids +, (tegmen multiplicative); endosperm copious (or not?); n = ?
8/49: Gonystylus (20). Tropical Africa and Madagascar (Octolepis), Malesia to Australia (Queensland), New Caledonia, Fiji.
Synonymy: Gonystylaceae van Tieghem, nom. cons.
3. Thymelaeoideae Burnett
Trees, shrubs, lianes or herbs; phorbol ester diterpenes [largely orthoesters and 1-alkyldaphnane derivates], cyclopropenoid fatty acids, chelidonic acid +, myricetin, tannins 0; internal phloem +, vascular bundles bicollateral; (stomata anomocytic); leaves often opposite; inflorescence often capitate; flowers 4-5-merous; "hypanthium" long (0), petal-like appendages to 2 x P or 0; A 2-5, opposite (alternate with) P, or 10; pollen crotonoid; nectary disc +, morphology various, (long-tubular), or 0; G 2, one locule often not developed and style then excentric; ovule epitropous; fruit a drupe or achene; (seed with a chalazal fold, and/or caruncle +); (nucellar tracheids +; testal cells enlarged; palisade exotegmen 0; tegmen multiplicative); endosperm 0 (quite copious - e.g. Daphne, Lachnaea); n = (7-)9(10), much polyploidy.
37/690: Gnidia (140), Pimelea (110), Daphnopsis (55), Daphne (ca 100), Lachnaea (40). World-wide, esp. trop. Africa and Australia.
Synonymy: Daphnaceae Ventenat, Gnidiaceae Berchtold & J. Presl, Phaleriaceae Meisner
Economic Importance. A number of taxa scattered through the family produce gaharu or agarwood. This is developed from the heartwood often after wounding and perhaps also after infection by fungi; gaharu is much esteemed as source of incense and medicines, and some species that produce it have been decimated in the wild (Eurlings & Gravendeel 2005).
Chemistry, Morphology, etc. Microsemma (= Lethedon, in Gonystyloideae) has cyclopentenoid cyanogenic glycosides (Spencer & Seigler (1985. Other aspects of the chemistry of Thymelaeaceae, including the presence of phorbol ester diterpenes, are similar to the chemistry of Euphorbiaceae (Seigler 1994).
At least some Thymelaeoideae have a lignified, torus-bearing, pit membrane (Coleman et al. 2004; Dute et al. 2011 and references). The petiole anatomy of Gonystylus needs to be confirmed; the bundle is perhaps unlikely to be arcuate.
Floral morphology in the family is poorly understood. The vasculature of the perianth in Thymelaeaceae was studied by Heinig (1951). The vascular bundles supplying the structures inside the calyx, whether paired and more or less opposite the sepals or single and in the petaline position, came from lateral branches of the sepal vasculature; equating these structures with stipules seems unlikely. Dicranolepis (Octolepidoideae: Africa) has large "petals" that are variable in number but paired and opposite the petals, and they are sometimes serrate or laciniate; the anther connectives are massive. Other taxa have single structures alternating with the lobes of the perianth tube, while in Lachnaea there are paired structures in the perianth tube borne below the instertion of the two whorls of stamens (Herber 2002b). Here I have been conservative, calling the major tubular structure a perianth, I am agnostic about the occurrence of petals and also whether a hypanthium in the strict sense is present or not. Synandrodaphne lacks a floral tube. The pollen of many Thymelaeaceae-Thymelaeoideae is similar to that of Euphorbiaceae-Crotonoideae. The micropyle of Gnidia is zig-zag. Eckardt (1937) discussed gynoecial variation in members of Thymelaeoideae. Spichiger et al. (2004) showed Daphne alpina as having a straight (and sessile) ovule.
The testa of Tepuianthus is about 6 cells thick and unlignified, then there is a layer of lignified palisade cells, the exotegmen, and immediately underneath apparently a layer of low, lignified cells, i.e., the seed coat is similar to that of other members of the family. Reports of a small embryo (Maguire & Steyermark 1981) need to be confirmed. The base of the lamina joins the petiole on the adaxial side, and so the lamina is almost peltate. Illustrations in Maguire and Steyermark (1981) suggest that there are colleters at the base of the calyx. See Roth and Lindorf (1990) for anatomy of the genus.
Some information is taken from Domke (1934), Ding Hou (1960), Herber (2002b), and Horn and Wurdack (ms.) all general, Kubitzki (2002: Tepuianthaceae), Evans and Taylor (1983: phorbol esters), Weberling and Herkommer (1989: inflorescence morphology), Joshi (1936: nectary and gynoecium), Herber (2002a: palynology), and Guérin (1916), Fuchs (1938), Mauritzon (1939a) and Kausik (1940b), ovule and seed.
Phylogeny. For the phylogeny of the family, see van der Bank et al. (2002). They found the following set of relationships [Gilgiodaphne (= Synandrodaphne), Gonystyloideae [Aquilarioideae + Thymelaeoideae]]. These relationships, other than the position of Gilgiodaphne, were well supported: genera like Tepuia and Octolepis were not included, while Gnidia was highly polyphyletic (see also the much more detailed study of Beaumont et al. 2009). Motsi et al. (2010) looked at relationships around Pimelea.
The inclusion of Tepuianthus in this clade makes eminent morphological sense (Wurdack & Horn 2001; Horn & Wurdack, ms.). It has a number of apomorphies of other Thymelaeaceae, while the features in which it differs from them are mostly plesiomorphies, i.e., they are similarities to other Malvales. Tepuianthus has both a well-developed calyx and corolla and also scales outside the androecium, perhaps suggesting that the corolla scales of Gonystylus, and perhaps those of the rest of the family, are homologous with these glandular scales. Furthermore, although it is described as having three separate styles, the stigmas being bilobed or not, these "styles" may be similar to similar processes on top of the ovary in Gonystyloideae, which are called parastyles and are associated with the styles proper. Distinctive epidermal columns in the palisade mesophyll of the leaf of Tepuianthus are found in other Thymelaeaceae such as Solmsia, and its resin cavities may be compared with the secretory cells of Octolepidoideae. The bark of Tepuianthus is described as being bitter, while Thymelaeoideae are well known for often being rather poisonous, unfortunately, the chemistry of Octolepidoideae is poorly known. Finally, the well developed parallel venation of Tepuianthus is very like that of other Thymelaeaceae, and Solmsia (New Caledonia: Octolepidoideae) is vegetatively remarkably similar to Tepuianthus down to details of the base and mucronate apex of the lamina.
Classification. On hold at present. The old Aquilarioideae are monogeneric and where the monogeneric Gilgiodaphnoideae (van der Bank et al. 2002) are to go is unclear. Daphne is probably to include Wikstroemia (Halda 2001); many generic limits will need reconsideration because of the fragmentation of Gnidia, yet Gnidia s.l. is not necessarily "maximally stable" given the poor support for the clade it represents (c.f. Beaumont et al. 2009: 413). For general information, see Zachary Rogers's A World Checklist of Thymelaeaceae (2009 onwards).
Previous Relationships. The pollen of many Thymelaeaceae-Thymelaeoideae is similar to that of Euphorbiaceae-Crotonoideae, and the chemistry is also similar to that of Euphorbiaceae, including the presence of phorbol ester diterpenes (Seigler 1994); Takhtajan (1997) places his Thymelaeales immediately after Euphorbiales. Microsemma (= Lethedon - Gonystyloideae) has cyclopentenoid cyanogenic glycosides; Spencer and Seigler (1985) suggested that because of this, it should be placed in Flacourtiaceae (see Achariaceae here). Thymelaeaceae were included in Myrtales by Cronquist (1981).
Thanks. I am grateful to Z. Rogers for comments.
[Sphaerosepalaceae, Bixaceae, [Cistaceae + Sarcolaenaceae + Dipterocarpaceae], [Muntingiaceae + Cytinaceae], Malvaceae]: hairs often stellate; stipules often well developed; A many, developing centrifugally, from 5 or 10 (15) bundles, when 5 often opposite the petals; ovules several [³6]/carpel, micropyle bistomal.
Age. Magallón and Castillo (2009) estimated an age of a mere 33.9 m.y. for this node.
Morphology, Chemistry, etc. The micropyle is described as being "formed by the outer integument" in Nandi (1998a: 257).
SPHAEROSEPALACEAE van Tieghem Back to Malvales
Deciduous trees; ellagic acid +; cambium storying ?0; pits not vestured; true tracheids +; calcium oxalate crystals +; rays uniseriate; secretory canals +; resin-filled cells outside veins; petiole bundles cylindrical (with adaxial plate; medullary bundles +); (stomata cyclocytic); hairs simple; leaves spiral or two-ranked, lamina vernation conduplicate, (secondary veins palmate), (fine venation closely raised), stipule intrapetiolar, broad [± encircling stem], deciduous, petiole pulvinate; inflorescences with subumbelliform cymules; flowers usu. 4-merous, K usu. 2 + 2, caducous, outer median (persistent), inner larger, C (3-)4(-9), when 4 opposite sepals, clawed, aestivation various, with many short resinous lines, caducous; A with broad connective; pollen usu. ± spinose, pollen with endoapertures larger than ectoapertures; gynophore +, short, nectary on top, G [2(-5)], placentation basal, style continuous to gynobasic, stigma punctate or obscurely lobed; ovules 2-9/carpel, epitropous, micropyle endostomal, fruit ± baccate, muricate to finely verrucose, ± deeply lobed; G separate, or G on one side not developed, 2-9 ovules/carpel, 1 seed/carpel; seeds with funicular aril/0, ruminate or not, testa 6-20 cells across, exotesta mucilaginous, exotegmen conspicuously incurved on either side of hypostase (not), operculum +; endosperm ?development, moderate, ruminate or not, starchy, cotyledons cordate and bilobed apically; n = ?
2[list]/18. Madagascar. [Photos - Collection]
Chemistry, Morphology, etc. Secretory cavities are widespread, and the carpels produce an exudate when cut. The rays are not storied (den Outer & Schütz 1981), and Jansen et al. (2000a) did not find vestured pits (c.f. den Outer & Schütz 1981). Takhtajan (1997) described the stipules as being extrapetiolar and the endosperm as being copious. The lateral sepal bundles are commissural, as in Thymelaeaceae. There are androecial trunk bundles opposite the petals. The apparently terminal style may be modified from the gynobasic condition (Horn 2004).
For more information, see Capuron (1962), Huard (1965), Bayer (2002) and Horn (2004).
Synonymy: Rhopalocarpaceae Takhtajan
Phylogeny. [Bixaceae [Cistaceae + Sarcolaenaceae + Dipterocarpaceae]] form a group morphologically united as follows: plant with secretory canals; K imbricate; seed with bixoid plug, the exotegmen curved inwards in chalazal region, hypostase plug with core and annulus. This bixoid chalazal plug forms a water gap through which water enters the hard seeds with such plaugs, so causing the breaking of the physical dormancy of the such seeds (Baskin et al. 2000). Bixaceae + Cistaceae may form another group: leaf teeth with a single vein proceeding to opaque deciduous apex; embryo long, cotyledons thin, curved or folded, radicle short, stout. Molecular phylogenies are largely silent about the first grouping, but suggest that the second is incorrect.
BIXACEAE Kunth, nom. cons. Back to Malvales
Plant with secretory canals; resin-filled cells outside veins; hairs glandular, not tufted or stellate; lamina margins serrate, a single vein proceeding to opaque deciduous apex of tooth; inflorescence terminal; flowers large; K imbricate; ringwall primordium +, A development centrfugal, 5 or 10 fascicular traces, anthers dehiscing by pores; stigma at most slightly lobed; ovules many/carpel, funicles long, micropyle zig-zag; exotegmen curved inwards in chalazal region, hypostase plug with core and annulus, outer hypostase forming the core; embryo long, cotyledons spatulate, thin, curved or folded, radicle short, stout.
4/21. Pantropical. Three groups below.
1. Cochlospermum et al.
Trees to ± herbs; ellagic acid +; gums +; cork ?; young stem with continuous vascular ring; sieve tube plastids with protein crystalloids and starch; petiole bundles 3, annular; glandular hairs when young; leaves spiral, lamina palmately lobed, vernation conduplicate, margins toothed or entire, stipules narrow; bracteoles 0; flowers ± obscurely monosymmetric; G [3-5], opposite petals or odd member adaxial, (placentation parietal); ovule ± campyltropous, outer integument 3-4 cells across, inner integument 3-7 cells across, parietal tissue ca 6 cells across, nucellar cap 2-4 cells thick; fruit a septicidal capsule, endocarp ± separating from the mesocarp; seeds hairy, gum cavities in inner parenchyma, tegmen with enlarged outer hypodermal cells; endosperm oily, embryo curved, ?color, cotyledons spathulate; n = 6.
2/15: Cochlospermum (12). Pantropical (map: from Poppendieck 1980, 1981; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, Cochlospermum religiosum is widely naturalised from Java to India). [Photo - Habit, Flower.]
Synonymy: Cochlospermaceae Planchon, nom. cons.
[Bixa + Diegodendron]: glandular hairs peltate; petiole bundle cylindrical, with medullary strands; stipules ensheathing bud; G [2-4]; fruit muricate.
2. Bixa L.
Trees or shrubs; flavones, flavonols, ellagic acid, flavonoid sulphates +, non-hydrolysable tannins 0; leaves spiral, often palmate to palmately lobed, lamina vernation conduplicate, margins toothed to entire; (flowers vertically monosymmetric); K with basal abaxial glands, C imbricate; filaments folded horizontally; G [2-4], opposite sepals, individual carpels initially not visible, placentation parietal; ovules with outer integument 3-6 cells across, inner integument 4-5 cells across, parietal tissue ca 2 cells across, nucellar cap ca 4 cells thick postament +; testa pulpy, dye cells in outer parenchyma, endotegmen with ± thickened cells, hypodermal layer of hour-glass cells; endosperm starchy, embryo white; n = 7.
1/5. Tropical America. [Photo - Flower, Fruit, Fruits.]
3. Diegodendron Capuron
Evergreen tree; cork?; nodes ?; mucilage cells?; (stomata cyclocytic); leaves two-ranked, lamina punctate, venation pinnate, stipules intrapetiolar, deciduous; K unequal, C caducous; A ?development, anthers with slits; disc ?inconspicuous; G [2(-4)], orientation?, style gynobasic; ovules 2/carpel, basal, epitropous, ?micropyle, ?funicle; fruit with small glands, indehiscent; seed with a glutinous outer layer, coat thin, so no palisade layer, inwardly-curving exotegmen or hypostase plug, etc.; endosperm 0; n = ?
1/1: Diegodendron humbertii. Madagascar.
Synonymy: Diegodendraceae Capuron
Economic Importance. The orange colouring of Bixa orellana, annatto, is used as a food colouring, e.g. for margarine.
Chemistry, Morphology, etc. In Cochlospermum vitiifolium the median sepal is abaxial, there are no bracteoles, and the sepals are of unequal size (or three "true" sepals + two bracteoles?). Flowers of Cochlospermum are monosymmetric in bud, and the floral vasculature is monosymmetric. The androecium has five or six bundles, and development is centrifugal. Carpel orientation needs to be checked if the flower is inverted. There is no obvious nectary. Amoreuxia has obliquely (?tranversely) monosymmetric flowers, the positionally "upper" stamens being much shorter than the lower ones and differently coloured; the four "upper" petals are bicolored.
The gums of Cochlospermum and those of Sterculia (Malvaceae-Sterculioideae) are similar, both containing acetylated acidic polysaccharides.
See Keating (1970, 1972) and Poppendieck (1980, 2002) for general details and Dathan and Singh (1972) and Ronse Decraene (1989b) for embryology and floral development of Bixa and Cochlospermum.
For general information on Bixa, see Poppendieck (2002). The wood anatomy of Diegodendron is very like that of Sphaerosepalaceae (Dickison 1988), but the genus is otherwise poorly known (see also Bayer 2002).
Classification. From molecular data (Fay et al. 1998a), Diegodendron is very similar to Bixa in particular, and the absence of any distinctive seed coat anatomy in Diegodendron is probably because the fruit is indehiscent. Although Diegodendron does seem morphologically rather different from the other two groups (Kubitzki & Chase 2002, Table 1), nevertheless, all three have much in common. Cochlospermaceae and Diegodendraceae can optionally be placed in Bixaceae s.l. (see A.P.G. II 2003), and this seems reasonable.
Previous Relationships. Diegodendron was included in Ochnaceae by Cronquist (1981), but excluded by Amaral (1991); Diegodendraceae were placed in Malvales by Takhtajan (1997).
[Cistaceae + Sarcolaenaceae + Dipterocarpaceae]: ectomycorrhizae +; tracheids +; ellagic acid +; plant with secretory canals; K with the two outer members often different from the rest, imbricate/quincuncial; filaments not articulated; ovules both anatropous and straight; exotegmen curved inwards in chalazal region, hypostase plug with core and annulus; endosperm starchy.
Age. Ages for this node offered by Wikström et al. (2001) are (41-)39(-37) or (25-)23(-21) m.y., while the ages in Bell et al. (2010) are (56-)46, 42(-28) m.y..
Phylogeny. This grouping is strongly supported in molecular studies, albeit the sampling is poor; indeed, both Sarcolaenaceae and Cistaceae may be embedded within Dipterocarpaceae as currently circumscribed (Kubitzki & Chase 2002; Ducousso et al. 2004). Fancy the nomenclatural brouhaha that will result if this is confirmed! Nandi (1998b) noted several similarities between Cistaceae and Sarcolaenaceae (hollow style, stigma morphology, carpel number and indumentum). In both Fumana (Cistaceae) and Dipterocarpoideae the outer integument is elongated, and ectomycorrhizae are common (Appanah 1998; Ducoussu et al. 2004). Clearly, future morphological studies may well strengthen the characterisation of the whole clade, but equally clearly, clade limits within it are unclear.
CISTACEAE Jussieu, nom. cons. Back to Malvales
Herbs to shrubs; (flavonoid sulphates +); root hairs 0; cambium storying?; phloem not stratified; nodes 1:1; mucilage cells 0?; petiole bundles arcuate; cuticle waxes 0 (platelets, annular rodlets); hairs glandular, or simple, clustered, or stellate, each cell with a basal internal compartment; leaves opposite (spiral), lamina vernation ± conduplicate-curved, margin toothed, secondary veins pinnate or palmate, stipules + or 0; K and C ± opposite, K 5, 2 outer smaller than the others (3), C (3) 5, (imbricate), crumpled in bud; A (3-)many and centrifugal; pollen often starchy, (surface striate-reticulate); G [3, 5(-10)], opposite petals or median member abaxial, placentation parietal (-axile), style hollow, stigmas (sessile), small to capitate and/or lobed, dry, with multicellular multiseriate papillae; ovules (1-)2-many/carpel, straight, (micropyle exostomal), outer integument ca 2 cells across, inner integument 2-4 cells across, parietal tissue ca 2 cells across, nucellar cap ca 2 cells across, hypostase +; (megaspore mother cells several); testa often mucilaginous; embryo ± strongly curved, long, cotyledons thin, curved or folded, radicle short, stout; n = 5, 7, 9-12, 16, etc.
8[list]/175: Helianthemum (80-110), Crocanthemum (24), Cistus (18). Eurasia, North Africa (inc. the Horn of Africa), North America, southern Soth America, esp. Mediterranean region (map: from Meusel et al. 1978; Frankenberg & Klaus 1980; Flora of China 13. 2007). [Photos - Collection]
Outer A staminodial; ovules anatropous; funicles short.
1/9. Europe, Mediterranean.
Ovules straight; funicles long.
Synonymy: Helianthemaceae G. Meyer
Evolution. Ecology & Physiology. Cistus dominates in the shrubby Maquis vegetation in the Medierranean region; Maquis may be transitional to Quercus- and Pinus-dominated vegetation (Comandini et al. 2006).
Pollination Biology. Many Cistaceae have stamens that are sensitive to touch, moving and dusting the insect with pollen when it disturbs them.
Bacterial/Fungal Associations. Endomycorrhizae as well as ectomycorrhizae have been reported from Cistaceae (Comandini 2006; de Vega et al. 2010, 2011), and the latter are also to be found in the tissue of Cytinus (Cytinaceae) a parasite of this family in the Mediterranean region (de Vega et al. 2010, 2011, c.f. Brundrett 2011). Ectomycorrhizal eastern Canadian Hudsonia has lateral roots only ca 59 µm across, rather like the hair roots of Ericaceae (Massicotte et al. 2010.
Chemistry, Morphology, etc. For the absence of root hairs, at least in seedlings, and the fungal associations of the plant, see references in Arrington and Kubitzki (2002); Dickie et al. (2004) also mention ectomycorrhizae in Helianthemum. Kapil and Maheshwari (1965) mention fungal hyphae in the ovules which, however, do not infect the seed. Wood rays are uniseriate and xylem parenchyma is almost absent (Keating 1966).
Corolla initiation in Cistaceae tends to be retarded (Nandi 1998b: it is not retarded in Dipterocarpaceae, Kocyan 2005). The androecium has ten bundles, each member of the oppositisepalous whorl supplies a group of stamens while the traces of the inner whorl usually supply a single stamen only; Saunders (1936) suggested that in Cistus there are five oppositipetalous groups. At least some Cistaceae have starchy pollen grains. The embryo is green (1 record) or white (Nandi 1998a). Fumana has n = 16 (Guzmán & Vargas 2009).
For floral diagrams, see Eichler (1878), for floral development, see Nandi (1998b), for ovule and seed anatomy, Nandi (1998a), for general information, Arrington and Kubitzki (2002, revised in Arrington 2004). For more information on the web, see R. Page's Cistus and Halimium website.
Phylogeny. Fumana and Lechea are successively sister to the remainder of the family with 100% posterior probabilities but mediocre maximum parsimony support (Guzmán & Vargas 2009); the former in particular has a number of features that are plesiomorphic in the family (Arrington 2004). Both have only three petals, the former, alone in the family, has staminodes. Tor the phylogeny of Cistus, see Guzmán and Vargas (2005); the relationships of Halimium and Cistus are intertwined (Civeyrel et al. 2011).
Previous relationships. Takhtajan's Cistales included Cistaceae, Bixaceae and Cochlospermaceae. Corner (1976 1: 97) described Cistaceae as being "little more than variations on a single generic theme", and noted similarities between the three families mentioned.
[Sarcolaenaceae + Dipterocarpaceae]: petiole anatomy complex; stipules usu. well developed.
Age. Ducousso et al. (2004) suggest that Dipterocarpaceae and Sarcolaenaceae had a common ancestor some 88 m.y.a., that is, prior to the split of India and Madagascar; ages suggested by Wikström et al. (2001) are only (30-)28(-26) or (16-)14(-12) m.y.a..
Phylogeny. Perhaps sister taxa (e.g. Alverson et al. 1998), at least if Pakaraimaeoideae are excluded from Dipterocarpaceae (Kubitzki & Chase 2002).
SARCOLAENACEAE Caruel, nom. cons. Back to Malvales
Woody, usu. evergreen; cyclopropenoid fatty acids +; cork?; wood not storied; true tracheids +; sclereids +; secretory canals?; stomata ?; hairs stellate or not; leaves two-ranked, lamina vernation involute [Keller 1996], stipules caducous; inflorescence various, involucre of varying morphology subtending 1 or 2 flowers, (bract [largely two stipules] enclosing flower), K 3(-5), when 5, outer 2 smaller, C 5 (6), disc +; A (10 [Leptolaena]-)many, ± connate into 5-10 bundles or not, of 2 or 3 lengths, anthers basi- or dorsifixed; pollen in tetrads; G (1) [2-4 (5)], densely hairy, placentation basically axile, style hollow, stigma capitate and/or ± lobed, with multicellular papillae; ovules (1-)2-6(-many)/carpel; fruit (indehiscent), with persistent/accrescent bracts or cupule, endocarp hairy; seed hairy or not, often ruminate; endosperm copious (0), cotyledons cordate; n = 11.
8[list]/60. Madagascar, mostly E. and C. [Photos - Collection]
Evolution. Divergence & Distribution. Fossil pollen of Sarcolaenaceae is known from the Tertiary of South Africa (Coetzee & Muller 1984).
Bacterial/Fungal Associations. Sarcolaenaceae are both etomycorrhizal and arbuscular mycorrhizal (Bâ et al. 2011a, b).
Chemistry, Morphology, etc. Sarcolaenaceae are the family with a "fleshy outer tunic". For details of cyclopropenoid fatty acid distribution, see Gaydou and Ramanoelina (1983), for ectomycorrhizae, see Ducousso et al. (2004), and for pollen, see Polevova et al. (2010) and references.
Synonymy: Rhodolaenaceae Bullock, Schizolaenaceae Barnhart
DIPTEROCARPACEAE Blume, nom. cons. Back to Malvales
Trees, (ectomycorrhizal); triterpenoid dipterocarpol, sesquiterpene oleoresins +; cork also outer cortical; cambium storied; (vessel elements with scalariform perforation plates); tyloses +; cortical bundles +; secretory cavities in pith; nodes also 5:5; petiole geniculate; stomata ?; hairs tufted, peltate, etc.; leaves spiral and two-ranked, lamina vernation conduplicate(-plicate); inflorescence axillary, often branched; K (slightly connate); A fasiculate, initiation centrifugal, anthers ± versatile, with conspicuous prolonged connective; median carpel abaxial, stigma slightly lobed or not; ovules apical; K thinnish, enlarging somewhat in fruit; seed usu. 1, testa vascularized; endosperm 0 (+), cotyledons often folded, enclosing radicle.
17[list]/680 - three groups below. Tropical, but overwhelmingly W. Malesian in species diversity (map: from Gottwald & Parameswaran 1966; Ashton 1982).
Age. Moyersoen (2006) suggested that the ectomycorrhizal nature of Pakaraimea, along with that of other members of the family, indicated that ectomycorrhizae inhabited the roots of Diperocarpaceae when they grew on Gondwana some 135 m.y.a..
1. Monotoideae Gilg
Rays usu. uniseriate; adaxial gland at base of lamina; androgynophore +; G [3 (4)]; ovules (1-)2/carpel, (atropous), exostome prolonged; endosperm not starchy; n = ?
3/30: Monotes (26). Africa, Madagascar, South America (Colombian Amazon: Pseudomonotes) (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003 - see above, area in green).
Synonymy: Monotaceae Kostermans
2. Pakaraimaeoideae Maguire, Ashton & de Zeeuw
Included phloem +; rays usu. biseriate; C imbricate, shorter than K; G , orientation?; ovules (2-)4/carpel; n = ?
1/1: Pakaraimaea roraimae. The Guaianan Highlands, South America (map: above, area in blue).
3. Dipterocarpoideae Burnett
Rays usu. multiseriate; resin ducts pervasive in wood; at least lateral bundles leaving central cylinder well before they enter the leaf; K imbricate [Shorea] or valvate; A (= and opposite sepals-)15-many, anthers ± basifixed, (connective not prolonged); pollen tricolpate; G [(2) 3] (inferior); ovules 2(-3)/carpel, micropyle endostomal, outer integument 2-5(-10 - Dipterocarpus) cells across, inner integument 2-9 cells across; fruit usu. 1-seeded, a nut, endocarp hairy, K enlarging unequally and thickish (loculicidal capsule - Upuna); (seed thin-arillate - Upuna), (palisade exotegmen 0); endosperm 0 (+ - Dipterocarpus), not starchy; n = (6-)7, (10-)11(-13).
13/650: Shorea (360), Hopea (105: these two should perhaps be merged), Dipterocarpus (70), Vatica (60). Seychelles, Sri Lanka, India, South East Asia to New Guinea, but mostly W. Malesian, often dominating in mixed-species stands (map: above, area in red). [Photo - Flower, Fruit.]
Age. Substantial resin deposits in Gujarat, western India, are from Dipterocarpoideae and have been dated to the Ypresian (Early Eocene), some 52-50 m.y.a. (Rust et al. 2010), and these have been associated with probable dipterocarp ascomycete ectomycorrhizae (Beimforde et al. 2011). Such deposits contain bicadinanes, the breakdown products of the dammar resin of dipterocarps.
Evolution. Divergence & Distribution. Fossil wood identified as Dipterocarpoideae has been found in east Africa and also in the Horn of Africa (Ashton 1982); there are no extant Dipterocarpoideae on the continent. Resin deposits from Dipterocarpoideae in Gujarat, western India, are from the Eocene 52-50 m.y.a. (Rust et al. 2010), and resin deposits are also found in West Malesia-South East Asia rather later in the Tertiary. This may suggest an origin or early occurrence of the family in India and later dispersal to South East Asia-Malesia after contact of the two was established ca 50 m.y.a. (Dutta et al. 2011). A similar scenario was suggested by Ashton et al. (1988), who also proposed that the distinctive masting behaviour of the family (see below) evolved in Dipterocarpaceae in the seasonal tropics.
Ecology & Physiology. Dipterocarpaceae are large trees that are often dominant in t.l.r.f. from India and Sri Lanka to West Malesia, where they grow both in seasonal and everwet forests (Alexander 1989). In Sri Lanka four species of Stemonopurus are recorded as being individually dominant in montane forest - an unusual habitat for the family - where they represented 33.2-74.5% of the basal area (Greller et al. 1987). Monotes in Africa is also often described as being locally abundant in the woodland to savanna habitats it frequents (White 1983). Dipterocarpaceae are the most diverse family in the West Malesian t.l.r.f. (Gentry 1988), and Shorea is about the most diverse genus there (Davies et al. 2005; see Roubik et al. for general information). In the West Malesian forests Dryobalanops aromatica and Shorea albida in particular may form very extensive and close to monodominant stands (e.g. Connell & Lowman 1989). In Lambir forest, Sarawak, Dipterocarpaceae make up only 7.4% of the species but 41.6% of the basal area (918.4 m2); the figures for Shorea alone are 4.7%, 21%, and 467.8 m2, Dryobalanops aromatica and Dipterocarpus globosus between them accounted for 13.2% of the basal area, and seven dipterocarps (out of the ten most dominant species) accounting for 23.1% (Lee et al. 2002; Davies et al. 2005; also Alexander 1989). Both Dryobalanops aromatica and Dipterocaropus globosus grew on the more humic soils, along with two other dipterocarps of the ten most important species in terms of basal area; the three non-dipterocarps on this list also grew on the same more humic soils (Davies et al. 2005). The trees are larger than the average in the forest, and only 16% of the trees at least 1 cm diameter at breast height are dipterocarps (Lee et al. 2002).
In the lowland wet tropical West Malesian forests there are huge peat lenses on which dipterocarps may dominate (Anderson 1963; Richards 1996; van Schöll et al. 2008). It has been estimated that Southeast Asian tropical peatlands (mostly Malesian, in fact most Indonesian, also largely made up of dipterocarp peats) occupy about 3/5 of the tropical peatland area, close to 250,000 km2, and about 6.2% of the global peatland area (Page et al. 2011). This peat contains some 68.5 Gt carbon, 77% of the tropical and 11-14% of the global totals for peatlands; these figures do not include estimates of the above-ground biomass (Page et al. 2011). Interestingly, in intact forests carbon loss is from recently fixed carbon, while in disturbed forest much older - hundreds to thousands (ca 4,180) of years - carbon is lost (Moore et al. 2013). See also Brown et al. (1993: soil to 1 m only) for biomass estimates, both actual (as impacted by human activities) and potential.
Note that the forests under discussion may be dominated by dipterocarps, but they vary considerably in detail and are often overall highly diverse (e.g. Ashton & Hall 1992; Lee et al. 2002), and in this repect are rather unlike temperate/boreal ectomycorrhizal communities. See also Clade Asymmetries for further discussion.
Shorea robusta (sal) is a gregarious tree that grows in monsoon areas from Pakistan to China, especially in the India-Assam-Myanmar area. Sal forests occupy 115,000 to 120,000 km2 (11.5x106 ha) and make up ca 15% of Indian forests (Tewari 1995). In Africa Monotes is found mostly in areas where ectomycorrhizal Detarieae are common, especially in the Zambezian region and also in Sudanian Brachystegia savanna (White 1983: see map above).
Individual dipterocarp species tend to be mast fruiters, and in the t.l.r.f. of S.W. Sri Lanka and West Malesia all taxa in the family tend to flower and especially fruit at the same time, apparently in response to climatic changes induced by El Niño events; this kind of behaviour is very uncommon in the tropics (Sakai et al. 2005: see Fagaceae for temperate mast fruiters). Pigs, etc., eat practically all the fallen fruits of some populations, but leave others untouched, and this kind of predator satiation - the enhanced recruitment of seedlings of these untouched populations - may be an advantage of masting behaviour (e.g. Janzen 1974a; Curran & Leighton 2000); some of these seed predators are migratory. There are also invertebrate seed predators, many in the small nanophyid weevil genus Damnux, and these can destroy 60-100% of the seed crop (Lyal & Curran 2003). Visser et al. (2011) suggest situations in which masting behaviour could evolve, and the ectomycorrhizal habit of the family has also been implicated in its phenological behaviour and/or predator satiation (Ashton 1982, 2002).
A few Dipterocarpaceae, but especially Eucalyptus and Pinales, are so-called giant trees (70< m tall: Tng et al. 2012).
Pollination Biology & seed Dispersal. Pollination of species of Shorea section Mutica and of other dipterocarps in Sarawak is by chrysomelid beetles and especially curculionids (weevils); in Peninsula Malaysia species of section Mutica are apparently pollinated by thrips (Sakai et al. 1999). Pollination is obviously affected by the generalized flowering common in the family (Sakai et al. 2005: see above).
Fruit dispersal is predominantly by wind; it is the fallen fruits that are eaten by the seed predators.
Bacterial/Fungal Associations. For ectomycorrhizae, see Smits (1994), Appanah (1998), Moyersoen (2006) and M. E. Smith et al. (2013), both Pakaraimoideae, Tedersoo et al. (2007: dipterocarps on the Seychelles), and Brealey (2012: summary); roots may lack root hairs. Vesicular-arbuscular mycorrhizae have also been reported here (Brealey 2012). Dipterocarpaceae apparently lack parasitic rust fungi (Uredinales), unlike many other ectomycorrhizal groups (Malloch et al. 1980); this observation should be confirmed - or not - for other members of this clade.
Plant-Animal Interactions. Hemipteran coccoid Beesonidae form distinctive galls on Dipterocarpoideae, although details of the association are poorly known (Gullan et al. 2005).
Economic Importance. Dipterocarpoideae, with their long, straight and clean boles and gregarious habits, are a major source of commercial hardwood. In the mid 1980s they comprised 25% of the world trade in tropical hardwoods, and 80% of that was made up by timber from Shorea. Furthermore, both oleoresins and hard resins (dammar) are collected from a number of Dipterocarpoideae, and they are also a source of lac (exudate produced by Coccoidea), butter fat from the fruits, etc. (Ashton 1982; Smits 1994 and references; Lambert et al. 2013 for the resins).
Chemistry, Morphology, etc. Bergenin, a derivative of gallic acid, is widespread. Stilbenoids, resveratrol and relatives, are common in Dipterocarpaceae (Wibowo et al. 2011), but I do not know if there is any systematic significance in this.
The stipules of Stemonoporus are extremely caducous. The calyx in many Shoreeae is imbricate in fruit, while the corolla is basally connate in many Dipterocarpeae. Dipterocarpus has vascular bundles in the inner integument.
For additional information on Monotoideae see Catalina Londoño et al. (1995), Morton (1995). For additional information about Pakaraimaea, see Maguire et al. (1977) and Maguire and Ashton (1980). For other information, see Gottwald and Parameswaran (1966: wood anatomy), Ashton (1982: general, 2002: general), Kajita et al. (1998), and Kocyan (2005: floral development).
Phylogeny. See Morton et al. (1999), Dayanandan et al. (1999) and Tsumura et al. (2011) for relationships.
Classification. Ashton (1982) is a convenient account covering most of Dipterocarpodeae. Generic limits within Dipterocarpaceae need attention (Yulita et al. 2005), Neobalanocarpus possibly even being an intergeneric hybrid (Shorea sp. X Hopea sp., see Kamiya et al. 2005).
[Cytinaceae + Muntingiaceae]: ellagitannins +; ovules numerous; fruit a berry; seeds numerous, mucilaginous, mucilage derived from funicle.
Chemistry, Morphology, etc. For general information about this family pair, see Nickrent (2007). Understanding any synapomorphies for the clade depend on more detailed knowledge of all aspects of the poorly-known Muntingiaceae in particular.
CYTINACEAE A. Richard Back to Malvales
Echlorophyllous root parasites, plant endophytic; vessels 0; phloem +; sieve tube plastids without starch or protein inclusions; stomata?; leaves scale-lke, spiral; plant monoecious or dioecious; inflorescence racemose, capitate or spicate; P +, 4-9, basally connate; staminate flowers: A 6-20+, extrorse, connate, monothecal, (P joined by dissepiment to both A and stylodium), nectariferous cavities between stamens, connective massive, with terminal appendage, (branched), (0); pollen 2-4-porate or 3-colpate, (in tetrads); stylodium +; carpellate flowers: staminodes 0; nectariferous cavities near base of style; G [5-14], inferior, placentation intrusive parietal, placentae branched, style +, swollen towards the apex, stigma capitate-radiate, commissural; ovules unvascularized, straight, uni- or bitegmic, micropyle endostomal, outer integument 2-3 cells across, inner integument ca 2 cells across, parietal tissue 0, nucellar epidermis persists; antipodal cells persist; seeds embedded in mucilaginous pulp; exotegmic cells thickened all around [?both genera?]; endosperm +, embryo short, undifferentiated; n = 12, 16.
2/10. Mexico, Mediterranean, South Africa and Madagascar (map: from Jalas & Suominen 1976; Alvarado-Cárdenas et al. 2009). [Photo - Collection of Cytinus, Bdallophytum - Staminate Flower, Carpellate Flower.]
Evolution. Ecology. Cytinus is quite often parasitic on Cistaceae (same order!) in the Mediterranean region, but on a variety of non-Malvalean families, perhaps especially Asteraceae, in Africa (Smythies & Burgoyne 2010). In the Mediterranean, endomycorrhizae from the hosts may also be found in tissues of the parasite, although the physiological significance of this is unclear (de Vega et al. 2010, 2011a, c.f. Brundrett 2011). The American Bdallophytum is most commonly found on species of Bursera (Alvarado-Cárdenas et al. 2009).
Pollination Biology & Seed Dispersal. Pollination of Cytinus hypocistus is by ants, other members of the genus are pollinated by other insects, mammals, and birds (de Vega et al. 2009; Smythies & Burgoyne 2010; Johnson et al. 2011b). De Vega and Herrera (2013) suggested that yeasts transported from flower to flower by ants increased fructose and decreased sucrose concentration of the nectar, but the effect of this on pollination is unclear.
The seeds become embedded in mucilaginous material derived from the placentae and funicles (Nickrent 2007), and seeds of Cytinus hypocistis are ingested and dispersed by the tenebrionid beetle Pimelia costata (de Vega et al. 2011b).
Chemistry, Morphology, etc. The elagitannin recorded for Cytinaceae is isoterchebin (Hegnauer in Meijer 1997). Harms (1935a) reports a nectary at the base of the style and the staminal tube of Cytinus. The outer integument, when present, is much reduced. The seeds of both genera have a blunt projection at both ends (Alvarado-Cárdenas et al. 2009; de Vega et al. 2011).
For general information see the (Nickrent 1998 onwards) and also Heide-Jørgensen (2008), Guzowska (1964) for ovules, embryology, etc., de Vega et al. (2008) for population differentiation in the western Mediterranean, and de Vega et al. (2007) for the anatomy of the endophytic portion of the host.
Classification. For a monograph of Bdallophytum, see Alvarado-Cárdenas et al. (2009).
MUNTINGIACEAE C. Bayer, M. W. Chase & M. F. Fay Back to Malvales
Trees; ellagic acid +; vessels single; pits not vestured; non-septate tracheids +; parenchyma storied; non-dispersive protein bodies?; mucilage canals 0; petiole bundle annular, no pericyclic fibres; stomata ?; hairs stellate or tufted; leaves two-ranked, lamina vernation conduplicate-subplicate [Muntingia], margins toothed, secondary veins pinnate to palmate, stipules 0; prophylls basal, heteromorphic; inflorescence fasciculate, extra-axillary; flowers (4-)5-merous; K valvate, basally connate, C imbricate, shortly clawed, crumpled in bud; tapetal cells binucleate; pollen small, ca 10 µm, triporate; nectary on [inside of] broad disc; G [5(-7)], or inferior, opposite petals, with numerous septae, placentation axile-laminar, or with massive bilobed axile-pendulous placentae, style stout, stigma conical, 5-ridged, or ± capitate; ovules with micropyle exostomal, zig-zag, outer integument ca 2 cells across, inner integument ca 3 cells across, parietal tissue 5-6 cells across, nucellar cap 0, hypostase +, funicle long [Muntingia]; megaspore mother cells several, megaspore micropylar, embryo sac monosporic, tetranucleate [Muntingia]; K persistent or deciduous; tegmen multiplicative, exotesta also mucilaginous, endotesta crystalliferous, cells of exotegmen shortly elongated; endosperm +, slight, ?diploid, starchy [details of seed from Muntingia alone]; n = 15.
3 [list]/3. Tropical America. [Photo - Flower]
Evolution. Pollination Biology. Fertilization occurs 12-15 days after pollination (Corner 1976).
Chemistry, Morphology, etc. Some characters of Muntingiaceae (lack of stipules; pits not vestured) might suggest that the family may be rather basal in Malvales; characters of the young secondary tissue of Muntingia, such as widely flaring rays, stratified phloem, etc., are like those of most other Malvales.
Although Muntingiaceae appear to have stipules, this may not to be the case. Dicraspidia has strikingly asymmetric prophylls; on the adaxial side of the branch they are orbicular, foliaceous and persistent, while on the abaxial side they are linear, thin and caducous. In Muntingia only an adaxial prophyll is present, and it is narrow (Karima Gaafar, pers. comm.: the situation in Neotessmannia is unknown). Sensarma (1957) suggested that the nodes of Muntingia are trilacunar, he interpreted the prophyll as a stipule, nevertheless, nodes indeed appear to be trilacunar. Given that stipules are common in Malvales, their apparent absence in Muntingiaceae needs to be clarified.
Muntingia has a superior, ovary, caducous calyx, and pendulous placentae, the two other genera have inferior ovaries, laminar placentation, and a persistent calyx (?: Neotessmannia). Muntingia has erect uniseriate hairs in addition to its tufted hairs. Stamens, etc., are borne on a massive, almost disc-like structure towards the inside of which are dense hairs; the inner side of this disc as it faces the ovary seems to be nectariferous.
Some information is taken from Benn and Lemke (1991) and Venkata Rao (1952a); the latter suggested that there were glandular, nectar-secreting hairs in Muntingia, but the hairs seem eglandular to me. Bayer (2002) gives a general account of the family. For wood anatomy, see Gasson (1996), for carpel orientation, see Ronse Decraene (1992), and for anatomy, see Carlquist (2005a). I am grateful to Lucia Lohmann for sending me material of Muntingia.
Phylogeny. For relationships, see Bayer et al. (1998c).
Previous relationships. Muntingiaceae were placed in Tiliaceae - Neotessmannioideae by Takhtajan (1997).
MALVACEAE Jussieu, nom. cons. Back to Malvales
Shrubs to trees (herbs); cyclopropenoid fatty acids, terpenoid-based quinones +, gums common; (cork cambium outer cortical); wood commonly fluoresces; pits not vestured; tile cells common; sieve tubes with non-dispersive protein bodies; haits stellate/lepidote; leaves spiral or two-ranked, lamina vernation usu. conduplicate(-plicate), margins entire or toothed, single vein running to the non-glandular apex, secondary venation palmate; inflorescence made up of modified cymose units ["bicolor units"]; (epicalyx +), K valvate, (C imbricate; 0); (androgynophore +); A (5-)many, in five groups opposite the C, but fundamentally obdiplostemonous, basally connate, extrorse; tapetal cells 2(-4)-nucleate; G [(3-)5(-many)], variable in orientation, style usu. 5 branched apically, stigma usu. dry; ovules 1-many carpel; micropyle zig-zag (endo- or exostomal), outer integument develops first, 2-4(-7) cells across, inner integument 2-7(-10) cells across, parietal tissue 3-8 cells, across, nucellar cap 2-5 cells across, hypostase +, obturator +/0 [often of placental hairs]; (megaspore mother cells several), inverse postament +; fruit a capsule (berry, schizocarp, etc.; muricate); (testa mucilaginous), testa multiplicative, vascularized, endotesta crystalliferous, tegmen multiplicative, endotegmic cells ± thickened; endosperm often starchy, embryo often green; sporophytic self-incompatibility system present [in "Sterculiaceae"].
243[list - genera assigned to tribes]/4225+ - 9 groups below. Largely tropical, also temperate. [Photos - Collection]
Age. Estimates of the age of crown Malvaceae are (47-)44, 31(-27) m.y. (Wikström et al. 2001) or (78-)66(-64) and (44-)39(-22) m.y. (Bell et al. 2010).
Fossils placed in the family are considerably older. Wood attributable to Malvaceae is known from the late Maastrichtian (Cretaceous) ca 68 m.y.a.; it has simple perforation plates in radial multiples and storied wood, but tile cells were not reported (Wheeler et al. 1994). Malvaceous wood (Bombacoxylon) has also been found in Campanian sediments in Texas ca 75 m.y. old (Wheeler & Lehman 2000).
[Grewioideae + Byttnerioideae]: ?
Age. An estimate of the age of this node is (37-)33, 37(-23) m.y. (Wikström et al. 2001) or (44-)32, 30(-19) m.y. (Bell et al. (2010).
1. Grewioideae Hochreutiner
(Inflorescence often leaf-opposed); K ± free, no nectary, C usu. clawed, adaxially with various epidermal modifications, nectary basal, hairy (0); A (5-)many, usu. free (connate), (bundles antesepalous), (staminodes +), A development centrifugal; pollen prolate; G [2-10]; fruit fleshy, or capsular (spiny); (seeds winged); n = 7-9(10).
25/770. Pantropical (warm temperate) (map: based on Cheek 2007, modified by Lebrun 1977; Frankenberg & Klaus 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. China 12. 2007; Australia's Virtual Herbarium xii.2012) .
1A. Apeibeae Bentham
K apex with horn-like appendage (0); A in whorls, centrifugal; androgynophore 0 (+, nectariferous); vascular bundles in carpel wall separate; fruit usu. spiny.
11/255: Triumfetta (150), Corchorus (40-100). Tropical, many sp. Australia, to New Zealand.
Synonymy: Sparmanniaceae J. Agardh, nom. cons.
1B. Grewieae Endlicher
C basally laterally constricted, with nectariferous hairs; A primordia complex at first, antesepalaous primordia more pronounced, (fasciculate); androgynophore +; vascular bundles in carpel wall embedded in sclenechymatous sheath.
14/515: Grewia (290), Microcos (60). Pantropical, some warm temperate.
Synonymy: Grewiaceae Doweld & Reveal
2. Byttnerioideae Burnett
Petiole bundle ± incurved-arcuate; leaves (palmate - Herrania), spiral or 2-ranked; K usu. connate, C broad towards the base [hooded; with inrolled margins], limb clawed, spathulate, linear, bifid, etc. (0); A epipetalous, 5(-30), in antepetalous fascicles alone, antesepalous staminodes + (0), petal-like, fascicles + staminodes forming a tube; tapetum false amoeboid [contents of cells resorbed]; nectar exuding through stomata [?level]; style apically ± branched; (fruit septicidal, mericarps), (dehiscence explosive); strophiole common; (testa not multiplicative); n = (5-7) 10(-13).
26/650: Byttneria (135), Hermannia (100), Ayenia (70), Melochia (55: A 5), Theobroma (20). Pantropical, esp. South America, also Australia (map: from Cheek 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; also Australia's Virtual Herbarium i.2013; Google Ayenia...). [Photo - Flower, Flower, Fruit.]
Synonymy: Byttneriaceae R. Brown, nom. cons., Cacaoaceae T. Post & Kuntze, nom. illeg., Hermanniaceae Marquis, Lasiopetalaceae Reichenbach, Melochiaceae J. Agardh, Theobromataceae J. Agardh
[Sterculioideae, Tilioideae, Dombeyoideae, Brownlowioideae, Helicteroideae, [Malvoideae + Bombacoideae]]: 21 bp deletion in ndhF gene.
Age. A possible age for this node is (34-)31, 28(-25) m.y. (Wikström et al. 2001) or (36-)29, 27(-20) m.y. (Bell et al. 2010) - note sampling in both.
3. Sterculioideae Beilschmied
(Polyacetylenes +); petiole bundle annular, with medullary bundle; leaves spiral, often palmately compound [basal?]; plant monoecious; inflorescence axillary, paniculate, obvious bicolor units absent, epicalyx 0; K petal-like, C 0; androgynophore +, (nectariferous hairs at the base); staminate flowers: filaments connate, anthers ± sessile, wall development the basic type? [5-6 cells across]; staminodia 0; pistillate flowers: staminodia?; G largely free, styluli +; integument lobed [Sterculia]; fruit a follicle (indehiscent), (endocarp pubescent); n = (15, 16, 18) 20 (21, etc.). commonly.
12/430: Sterculia (150), Cola (125). Pantropical (Map: from Cheek 2007, see abso Wickens 1976; Arbonnier 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Staminate flowers, Fruit.]
Synonymy: Sterculiaceae R. Salisbury, nom. cons.
4. Tilioideae Arnott
(Plant ectomycorrhizal); stachyose, raffinose + [phloem exudate - Tilia]; some species with siliceous leaves; petiole bundle annular, with medullary phloem strands and inverted bundles; leaves 2-ranked, horizontally conduplicate [?always]; K free, C slightly clawed; (A free), staminodia also antepetalous, antesepalous sector empty; G opposite sepals; (postament +); fruits to 5-seeded; (seeds arillate); cotyledons foliaceous, folded; n = 41.
3/50: Tilia (23). N. temperate, Central America (map: from Meusel et al. 1978; Hultén & Fries 1986; Fl. China 12. 2007; Cheek 2007 [Central America]).
Synonymy: Tiliaceae Jussieu, nom. cons.
5. Dombeyoideae Beilschmied
Leaves spiral; epicalyx +, 3 (spathiform), (0); K connate basally to free, nectary at base, C ± stalked (0); A uniseriate, connate (free), (5-)10-10(-30), elongated antesepalous staminodes + (0), staminodes forming a short tube, (anther wall development the basic type); (tapetum amoeboid); (secondary pollen presentation +); pollen often porate, spinulose; G [(2-)5(-10)], style branched from base, or branches apical; endocarp epidermis often pubescent; (K accrescent), (C persistent, scarious (not); seed with umbonate sarcotestal projections); (seeds winged); cotyledons bifid; n = 19, 20, 30, etc.
21/381: Dombeya (225), Melhania (60). Old World tropics, Australia, St Helena, esp. Madagascar and Mascarenes (Map: partly from Cheek 2007, see also Wood 1997; Arbonnier 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. China 12. 2007; FloraBase i.2013; Australia's Virtual Herbarium 1.2013, etc.).
Synonymy: Dombeyaceae Desfontaines, Pentapetaceae Berchtold & J. Presl
6. Brownlowioideae Burret
Indumentum often lepidote; inflorescences axillary; K connate, campanulate, splitting irregularly into 2-3 lobes; A ca 30, in bundles, anther thecae sagittate, often broadly so, staminodia antesepalous (0), petal-like; style or styles +; ovules 1-2(-6)/carpel; K persistent; (seeds hairy); n = 10.
8/68: Pentace (25). Tropical, esp. Old World (map: from Cheek 2007; Fl. China 12. 2007).
Synonymy: Berryaceae Doweld, Brownlowiaceae Cheek
7. Helicteroideae Meisner
(Indumentum lepidote); (secondary veins pinnate - Durioneae), petiole pulvinate; K connate, C clawed, often with lateral constrictions; androgynophore +; A 10-many, usu. with short tube and/or fascicles, (anthers monothecate), (thecae end-to-end); pollen baculate or microverrucate to suprareticulate; outer and inner integuments 2 cells across; (seeds winged), (arillate); n = 9, 14, 20, 25, etc.
8-10/95: Helicteres (40), Durio (27). Tropical, esp. Southeast Asia and W. Malesia (map: from Cheek 2007). [Photo - Fruit.]
Synonymy: Durionaceae Cheek, Helicteraceae J. Agardh, Triplochitonaceae Schumann, nom. nud.
[Malvoideae + Bombacoideae]: leaves spiral; K connate, adaxially at base with multicellular clavate nectariferous hairs; C adnate to base of A, the two falling off together; fascicles contorted, filaments forming a tube +, anthers monothecal, (locellate [= "polysporangiate": some "basal" members]), anther thecae sessile ["basal" members]; G with unbranched synlateral [± oppositisepalous] vascular bundle +; (inner integument -15 cells across).
Age. A possible age for this node is (24-21, 27(-14) m.y. (Wikström et al. 2001) or (26-)20, 29(-12) m.y. (Bell et al. 2010) - note topology in both.
8. Malvoideae Burnett
Petiole bundle annular; (epicalyx +), median K often abaxial, C basally connate to free; A (dividing into two), centrifugal, tube often with 5 apical teeth, (anthers bisporangiate, monothecal), [staminodes in fascicle; antesepalous member], (synlateral bundle 0); tapetum amoeboid; pollen often spiny, 7+ porate; G (1[2-)3-many], styles often separate, stigmas decurrent [e.g. Malva] to capitate, hairy; ovules 1-many/carpel, campylotropous (anatropous); (fruit schizocarpic); (seeds hairy); embryo curved (straight), cotyledons folded; n = 5-20(+).
78/1670: Hibiscus (580, inc. Pavonia, etc.), Sida (200), Abutilon (100), Nototriche (100), Cristaria (75), Gossypium (40). Temperate to tropical (map: from Hultén & Fries 1986; Meusel et al. 1978; Frankenberg & Klaus 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Australia's Virtual Herbarium xii.2012; New World: Cheek 2007; Skoggan Fl. Canada 3. 1978). [Photo - Flower.]
Age. The age of this clade, or more particularly, a major part of this clade (core Malvoideae, inc. Uladendron), has been estimated at (58-)47, 45(-43) m.y. (Koopman & Baum 2008).
Leaves named as Malvaciphyllum macondicus, found in sediments 60-58 m.y. old from Cérrejon, Colombia, have been placed in Malvoideae (Carvalho et al. 2011). No mention is made of hairs of this fossil, but pollen of Bombacacidites was common in the rocks (Carvalho et al. 2011).
Synonymy: Chiranthodendraceae A. Gray, Hibiscaceae J. Agardh, Sidaceae Berchtold & J. Presl
9. Bombacoideae Burnett
Trunk often stout, with parenchymatous water-storage tissue, so soon becomes punky when cut, bark thin, often green, (with stout prickles); leaves palmate(ly lobed - e.g. Ochroma), petioles pulvinate; flowers axillary, 1-2 together; (K imbricate - Ochroma); K ± connate; filaments usu. fasciculate, (A variously connate; 5), staminodes usu. 0, (anthers bisporangiate, monothecal), wall 5-7 cells across; pollen ± flattened, triangular in polar view; endocarp pubescent; (testa 6-8 cells across - Adansonia); embryo curved, cotyledons folded [latter - general?]; n = 36(-46).
16/120: Pachira (24), Pseudobombax (20). Tropical, esp. America and Africa (map: based on Aubréville 1974; Wickens 1976; Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Australia's Virtual Herbarium i.2013). [Photo - Flower], Seeds.]
Age. Pollen attributed to Bombacoideae (Bombacacidites) has been found in deposits 69-65 m.y. old (Krutzsch 1989; Pfeil et al. 2002 for references).
Synonymy: Bombacaceae Kunth, nom. cons.
Evolution. Divergence & Distribution. For the early Tertiary fossil history of Craigia (Tilioideae), see Manchester et al. (2009); Reevesia (Helicteroideae), now East Asian, is known from throughout the North Hemisphere in the early Tertiary (Ferguson et al. 1997).
Taxa at the nodes at the base of the [Malvoideae + Bombacoideae] clade are likely to have been neotropical (Baum et al. 2004; Nyffeler et al. 2005). Baum et al. (2008: q.v. for dates), discuss the biogeograophy of Malveae. Le Péchon et al. (2010) found that Dombeyoideae had colonized the Mascarenes more than once - and had also acquired dioecy in parallel. Nototriche (Malvoideae) is a remarkable genus of dwarfed plants growing in the high Andes; the flowers are epiphyllous, and there is considerable variation in leaf shape.
Ecology & Physiology. Bombacoideae are an important component of neotropical seasonally dry tropical forest and Amazonian forests in general, being both speciose and having a disproportionally high number of common species (Pennington et al. 2009; ter Steege et al. 2013). Tilia is ectomycorrhizal, and some species are associated with truffels (Tuber).
Plant-Animal Interactions. Caterpillars of the nymphalid Acraea are quite commonly found on members of Malvaceae, as are members of Lycaeninae (Fielder 1995). Acanthoscelides, whose larvae eat seeds, are bruchids (Chrysomeloidea-Bruchidae/Bruchinae) that have diversified on Malvaceae s.l., esp. on Malvoideae, more than on other groups outside their primary hosts, members of Fabaceae (Kergoat et al. 2005). Seed-eating bugs of the Hemiptera-Lygaeidae-Oxycareninae are also concentrated on Malvoideae (Slater 1976).
Pollination Biology. In most Malvaceae studied the nectary is made up of multicellular glandular hairs covering glandular tissue beneath; the same morphology even occurs in the foliar extrafloral nectaries in Triumfetta (Leitão et al. 2005). The nectaries that provide rewards for pollinators are commonly found on the inside of the calyx and the corolla is fused at most basally, the petal lobes soon separating and leaving a space between them through which the pollinator can get at the nectar. These two features are probably connected: Access to the nectar must be permitted to a pollinator probing the center of the flower, and if the corolla were completely connate there would be no easy way for the pollinator to reach the nectar while simultaneously pollinating the flower (for nectary morphology, etc., see Sawidis et al. 1989 and references; Vogel (2000; Leitão et al. 2005). However, overall there is considerable variation in nectary - and staminodium - position and type in the family. Nectaries are borne on the petals in e.g. Grewia and Luehea and on the androgynophore (and leaf!) in e.g. Triumfetta (all Grewioideae: Leitão et al. 2005), while nectar in some Byttnerioideae, at least, is secreted through nectarostomata.
Byttnerioideae often have remarkably complex if sometimes quite tiny "basket" flowers that are pollinated by small flies and the like (see Westerkamp et al. 2006; Whitlock & Hale 2011). The petal often has a concave lower portion more or less enclosing the rest of the flower, the limb of the petal may dangle and twist in the wind, as in Abroma, and the prominent staminodia are opposite the sepals. For pollination in Bombacoideae, see Janka et al. (2008) and references. The flowers of Helicteres isora (Helicteroideae), some species of Pavonia (Malvoideae), and the remarkable Chiranthodendron pentadactylon, the aptly-named devil's hand, refering to the five-branched androecium, are monosymmetric, but I do not know the plane of symmetry.
The pattern of evolution of dioecy in Dombeya, certainly paraphyletic, in the Mascarenes and its dispersal between Madagascar, the Mascarenes, and Africa is complex (Le Péchon et al. 2009); there seem to have been four colonizations of the Mascarenese, with at least three acquisitions of dioecy (Le Péchon et al. 2010; see also Skema 2012).
Genes & Genomes. In addition to genome duplication events, e.g. the genome triplication of the core eudicots (Vekemans et al. 2012), in the lineage leading to Gossypium (Malvoideae) genes duplicated, and then triplicated after its divergence from Cacao (Byttnerioideae) - in total a 30-36-fold duplication within angiosperms (Paterson et al. 2012). Diversification and molecular evolution in Hibisceae pick up almost together (Baum et al. 2002, 2004), while Andreasen and Baldwin (2001) noted that the rate of molecular evolution of 18S–26S nuclear ribosomal DNA in annual Sidalcea was faster than that in the perennials.
Economic Importance. For the domestication of cotton (Gossypium barbadense), see Dillehay et al. (2007); for the evolution of cotton fibres, see Paterson et al. (2012 and references).
Chemistry, Morphology, etc. Tile cells are best observed in radial section; they are of two or three main types (Manchester & Miller 1978; Carlquist 1988b; Tang et al. 2005b). Any correlation of tile cell "type" with phylogeny awaits a more completely resolved tree, thus the Durio type occurs in both Malvoideae and Byttnerioideae. Vestured pitting is reported, but probably incorrectly, from Schoutenia and Ochroma (Jansen et al. 2000a).
Carvalho et al. (2011) discuss leaf venation in the family in considerable detail; additional apomorphies for Malvoideae, at least, may result from such studies. Several taxa have palmate leaves. In Brachychiton and Adansonia there is comparable variation within a flush - the first leaf/leaves have a very short petiole and long, narrow ?phyllode, while later leaves are palmate; any intermediates have winged petioles and a few leaflets.
For a discussion of the various kinds of extrafloral nectaries in Triumfetta, see Letãio et al. (2005).
The inflorescence in most Malvaceae is made up of "bicolor units" - a terminal flower with three bracts, two of which may subtend cymose part inflorescences with normal bracteole number and arrangement and the other subtends nothing. The epicalyx seems to be made up of these three bracts, and so a flower with an epicalyx represents a highly reduced "bicolor unit" (Bayer 1999); it has evolved several times in the family. Although the inflorescence of Sterculioideae seems to be very differently constructed from that of other Malvaceae, it, too, may be made up of much modified bicolor units (Bayer 1999). Nototriche (Malvoideae) has epiphyllous inflorescences.
For androecial development in Malvaceae s.l. compared to that of other Malvales, see Nandi (1998b) and von Balthazar et al. (2006). Von Balthazar et al. (2006) suggest an interpretation of the androecium of [Malvoideae + Bombacoideae] - and extend their findings to determine the basic androecial structure for Malvaceae as a whole. They propose that the basic androecial structure in Malvaceae is obdiplostemonous, with stamens developing in one or both whorls; anther dehiscence is extrorse. In [Malvoideae + Bombacoideae] each androecial unit consists of an antesepalous primordium with its own vascular supply and which remains sterile (usually). It is flanked on either side by a single primordium, each derived from a separate antepetalous primordium and that each give rise to a sessile, elongated theca. Each theca is supplied by a branch from an antepetalous vascular bundle. The androecial unit thus consists of [half anther + sterile primordium + half anther]. Further details are given by Janka et al. (2008), focussing on Adansonia and relatives. Ceiba pentandra has only five alternisepalous stamens, and these are supplied by branches of the oppositipetalous traces, and these and other taxa linke Fremontodendron are described as have bithecal anthers... (Bayer & Kubitzki 2002). For additional details of androecial development in Malvoideae, see Janka (2003) and von Balthazar et al. (2004). For floral morphology and development in Dombeyoideae, see Tang (1998) and Tang et al. (2006). In Grewioideae the stamens may arise from ten or five (then oppositisepalous) primordia, or from ringwall primordia, and the vascular supply to the stamens is variable in origin (Brunken & Bayer 2005); for more, see Brunken (2003; Brunken & Muellner 2012). Van Heel (1966) and Schönenberger and von Balthazar (2006) also discuss androecial development in Malvaceae s.l. The androecia with numerous stalked, unithecate, staminal units so common in this clade are independently derived in Bombacoideae and Malvoideae (von Balthazar et al. 2006). .
Although starchy pollen is common in Malvaceae in the old sense, it is not reported from the old Sterculiaceae; details of variation in the clades recognised here are unclear.
Not only are the carpels of Sterculioideae secondarily free, but in Firmiana they open early in development, exposing the developing seeds on the carpel margins; the ripe carpels with seeds attached are dispersed by wind. However, there is a compitum even in these apocarpous Sterculioideae because of the post-genital connation of the apical parts of the styles (Jenny 1988). The carpels are usually opposite the corolla, although not infrequently (e.g. Hibiscus, Fremontodendron, Sterculia) they are opposite the calyx; when there are three carpels, the median member may be either ad- or abaxial (reports of carpel orientation in individual taxa may conflict - e.g. Eichler 1878; Ronse Decraene 1992).
Although zig-zag micropyles are common here, some taxa have an unitegmic (exostomal) micropyle, but the micropyle is clearly off-centre, while in taxa like Helicteres the micropyle is initially naked but becomes bistomal and zig-zag after fertilization; such variation is connected with the precious development of the outer integument. Ovules of Pterospermum suberifolium are described as lacking parietal tissue but with a nucellar cap up to 16 cells across (Venkata Rao 1952c). For details of embryology, see e.g. Venkata Rao (1950, 1951: exotegmen of Waltheria palisade, 1952b, 1954), Venkata Rao and Sambasiva Rao (1952), and for the embryology of Eriolaena in the context of embryological variation in Dombeyoideae as a whole, see Tang et al. (2009). Leptonychia has parietal placentation, short fibres in the exotegmen, but starchy endosperm, while Helicteres is described as having exotestal fibres (González & Cristóbal 1997); Corner (1976) discussed the seeds of Malvaceae in some detail; see his "durian theory" (e.g. Corner 1953) for the evolution of the tropical rainforest.
For wood anatomy, Chattaway (1933b, 1937), Webber (1934), Manchester and Miller (1978), Carlquist (1988b) and Tang et al. (2005a, b), for gums, see Lambert et al. (2013), for inflorescence structure, Bayer (1994, 1999), for nectaries, Vogel (2000), for petal development in Byttnerioideae, see Leinfellner (1960), for nectary morphology, etc., see Sawidis et al. (1989 and references), for pollen variation in Grewioideae, Tilioideae and Brownlowioideae, see Perveen et al. (2004). For more general information, see the Malvaceae Pages website (Hinsley 2002), Cheek (2007), and especially Bayer and Kubitzki (2002).
Phylogeny. Apart from Malvaceae, here in Malvoideae, all the other families in the old Malvales are highly para- or polyphyletic. For information on relationships in the extended family, see Alverson et al. (1998, 1999) Bayer et al. (1999), and Nyffeler et al. (2005). [Grewioideae + Byttnerioideae] are probably sister to the rest of the family (see also Soltis et al. 2007a), while Sterculioideae are perhaps sister to the well supported [Malvoideae + Bombacoideae]; see the latter for relationships within it. Other relationships between the subfamilies are unclear. However, Dombeyoideae and Tilioideae are sometimes weakly associated (Alverson et al. 1999), but the former may rather be sister to all other taxa in the major polytomy (Nyffeler et al. 2005).
Many taxa in Byttnerioideae have only five stamens, a derived condition, even although developmental work might suggest that the higher numbers may be derived by doubling (Whitlock et al. 2001b; Whitlock & Hale 2011). Whitlock and Hale (2011) found that Byttneria was paraphyletic, with Ayenia embedded in it; growth form was a fairly good indicator of relationships here, while Whitlock et al. (2011) evaluated relationships around Commersonia.
Mortoniodendron is to be included in Tilioideae (Nyffeler et al. 2005).
Wilkie et al. (2006) suggest relationships within Sterculioideae and discuss evolution of fruit types, dispersal mechanisms, etc.; leathery follicles seem to be the basal fruit type of the group.
For relationships within Dombeyoideae, Dombeya certainly being paraphyletic, see Le Péchon et al. (2009, 2010: focus on the Mascarene taxa), Won (2009: to include Corchoropsis) and Skema (2012: focus on the Malagasy taxa).
Within Helicteroideae, Helictereae (ex Sterculiaceae) are sister to Durioneae (ex Bombacaceae), the latter being from Sri Lanka, Burma to West Malesia and having lepidote indumentum and an initially connate epicalyx. The anthers of many Durioneae are polylocular - see also Nyffeler and Baum (2000).
Ochroma may be sister to other members of Bombacoideae; its filaments are connate into a tube. However, it and Patinoa formed a clade with no obvious immediate link with Bombacoideae in some analyses (Alverson et al. 1999; see also Baum et al. 2002, 2004) and are best excluded from it. Sister to the rest - or almost so - in this whole [Malvoideae + Bombacoideae] area may be things like Fremontodendron, which hybridizes with Chiranthodendron, (both ex Sterculiaceae - C 0), etc., and Quararibea, etc. (ex Bombacaceae), but with only weak support (Alverson et al. 1999; c.f. Bayer et al. 1999; Baum et al. 2002). Quararibea, etc., are best placed in Malvoideae, while [Ochroma + Patinoa] and Septotheca are unplaced (Baum et al. 2004). Indeed, Baum et al. (2004) suggest that [Fremontodendron + Chiranthodendron] may be sister to the rest of the [Malvoideae + Bombacoideae] area since they lack a 6 bp deletion in a conserved region of the matK gene found in all other members of this clade, however, there is little other evidence for this position.
For groupings within Malvoideae, see La Duke and Doebley (1995: restriction site analysis) and Judd et al. (2002). Within Malveae, Tate et al. (2005) found that presence or absence of an epicalyx correlated very well with two major clades recognizable on analysis of ITS sequence data, but a subsequent study using this gene and four others found that Malva, at least, was polyphyletic (García et al. 2009). For relationships within Hibisceae, see Pfeil et al. (2002), Pfeil and Crisp (2005) and Koopman and Baum (2008: Malagasy taxa); generic limits around Hibiscus are especially difficult - s. str. or s. lato?, but Hibiscus should probably include Pavonia, etc. Sida is polyphyletic, as is Abutilon (Donnell et al. 2012). For relationships in Gossypieae, complicated by hybridization, see Seelana et al. (1997).
Classification. For a discussion of groupings in the extended family, Robert Brown's comments over 150 years ago (Brown 1814) on family limits in the Malvales (= Malvaceae here) are a good starting point. Malvaceae + Bombacaceae + Sterculiaceae + Tiliaceae make a readily recognized and well circumscribed group, yet the clades within it are mostly difficult to distinguish, even with flowers, so combination seems sensible (Judd & Manchester 1997; Alverson et al. 1999; Bayer et al. 1999); Cheek (2007), however, opted for dismemberment into ten families.
For a tribal classificaton of Grewioideae, see Brunken and Muellner (2012). For generic limits around Commersonia, see Whitlock et al. (2011) and associated papers, for those around Hibisacus, see Pfeil and Crisp (2005) and Koopman and Baum (2008), and for generic changes around Dombeya, see Skema (2012) and Abutilon, see Donnell et al. (2012). Generic limits in Malveae had in the past been based mainly on the number of parts of the epicalyx and their fusion, but fruit characters seem to be more useful features when characterising clades (García et al. 2009).
Additional Synonymy: Plagianthaceae J. Agardh, Philippodendraceae A. Jussieu, Triplobaceae Rafinesque, nom. illeg.