EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open, pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers ± dorsifixed, transition to filament narrow, connective thin.
ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.
ROSID II / MALVIDAE / [[GERANIALES + MYRTALES] [CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]]: ?
[GERANIALES + MYRTALES]: ellagic acid +; K persistent in fruit.
MYRTALES Reichenbach Main Tree.
Bark flaky; flavonols only, myricetin, methylated ellagic acid +; cork cambium deep seated, (polyderm +); vessel elements?; pits vestured; libriform fibres septate; tension wood +; secondary phloem stratified; (interxylary phloem +), internal phloem + [= intraxylary phloem, vascular bundles bicollateral]; nodes 1:1; (spirally-thickened tracheoids +); cuticle waxes often 0; branching from current flush [all?]; leaves opposite, lamina with secondary veins joining an intramarginal vein [brochidodromous venation], margin entire, (stipules +, small; ?= colleters), colleters +; inflorescence racemose; (flowers 4-merous); hypanthium +, nectariferous; K valvate, C clawed; filaments incurved in bud; pollen with pseudocolpi; ovary inferior, (transseptal bundles +), style long, minor stylar bundles +, stigma wet; ovules many/carpel, micropyle bistomal and zig-zag, inner integument ca 2 cells across; antipodal cells ephemeral; (mesotesta sclerotic), exotegmen cells tracheidal, endotesta crystalliferous; endosperm at most slight. - 9 families, 380 genera, 11731 species.
Age. Wikström et al. (2001: note topology) dated crown Myrtales to (83-)79, 75(-71) m. years, Hengchang Wang et al. (2009) to (89-)85, 78(-74) m.y., although a Bayesian relaxed clock estimate for the crown group was as much as 99 m.y., Tank et al. (2015: Table S2) ca 86 m.y., and Bell et al. (2010: note topology) offered dates of (99-)89 m. years. Thornhill et al. (2012a) suggest several dates, but they are all clustered around (98-)93.3-91.7(-85.7) m.y.a.; an age of ca 111 m.y. was suggested by Sytsma et al. (2004), (118.8-)116.4(-113.7) m.y. by Berger et al. (2015), ca 90 m.y. by Sytsma and Berger (2011), and (96.4-)91.6(-86.7) m.y. by Thornhill et al. (2015).
Fossils assignable to Myrtales are some 65 m.y. old (Crepet et al. 2004).
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution: Divergence & Distribution. Myrtales contain ca 6% core eudicot diversity (Magallón et al. 1999).
Berger et al. (2015) discuss the biogeography and diversification of Myrtales in some detail, noting that most families were southern hemisphere, ancestrally being in South America (Lythraceae, Melatomataceae, Onagraceae, Vochysiaceae) or African (the [Crypteroniaceae [Alzateaceae + Penaeaceae]] clade, Myrtaceae).
Ecology & Physiology. Salt tolerance has evolved quite often here, most notably in Combretaceae (12 spp.) Lythraceae (21 spp.) and Myrtaceae (47 spp.: Moray et al. 2015).
Pollination. Energetically costly elements of floral display s(e.g. large flowers) have evolved in parallel in Myrtales, low cost floral elements (e.g. small flowers, shallow flowers) show phylogenetic inertia (i.e. are plesiomorphic?) - see Vasconcelos and Proença (2015).
Plant-Animal Interactions. Lycaenidae caterpillars are quite commonly to be found on members of this order, especially Lythraceae, Myrtaceae, and Combretaceae (Fielder 1991, 1995).
Chemistry, Morphology, etc. Several characters common in Myrtales may be apomorphies there. Raffinose and stachyose are common oligosaccharides in phloem exudate in Myrtaceae, Onagraceae, Lythraceae and Combretaceae, at least (Zimmermann & Ziegler 1975). Polyderm (alternating endodermal and parenchymatous layers laid down by a pericyclic meristem) is known from families like Onagraceae, Lythraceae, Myrtaceae, and probably Penaeaceae, at least (Mylius 1913), while in roots of some aquatic Lythraceae, Melastomataceae, Myrtaceae and Onagraceae (and Euphorbiaceae and Fabaceae) there is a distinctive lacunate cork produced from a pericyclic cork cambium (Little & Stockey 2006); there may also be lacunae in the stem polyderm produced in response to flooding (Lempe et al. 2001). The cork cambium is sometimes initiated in the superficial or mid-cortical position (e.g. Myrtaceae, Melastomataceae. Tracheoidal sclereids with spiral wall thickenings that are associated with the vein endings are known from Vochysiaceae, Lythraceae, Combretaceae, Melastomataceae, Alzateaceae and Penaeaceae (Sajo & Rudall 2002); their more general distribution needs to be checked. Since there is internal phloem, petiole and midrib bundles are often bicollateral; Carlquist (2013) noted the occurrence of interxylary phloem in some Combretaceae, Melastomataceae, Onagraceae and Lythraceae. Weberling (2000) notes that "true rudimentary stipules" occur in Myrtaceae and most myrtalean families; stipules, when they occur, are indeed generally small, often not vascularized, and are likely to be colleters (see also Carr & Carr 1966; LaFrankie 2010; da Silva et al. 2012); colleters may also occur in the flowers (Pimentel et al. 2014).
In Myrtaceae the calyx and corolla originate at about the same time, while in Lythraceae and Onagraceae the calyx is visible considerably before the corolla (Mayr 1969); it will be interesting to know the general distribution of this feature. Many Myrtales, including some Myrtaceae, have notably narrow petal bases, i.e., they are close to being clawed; the definition and distribution of clawed petals in Myrtales may have to be amended, but I have provisionally put "clawed petals" as a feature of the whole clade. Those taxa in which the filaments are straight in bud usually have short filaments, and the length of the style is correlated in part with the length of the hypanthial tube. Distinctive winged fruits are found in Combretaceae and rarely in Oenothera, and even more distinctive fruits that open by the placenta breaking through the ovary wall occur throughout Cuphea (Lythraceae) and in some Sonerila (Melastomataceae). The basic chromosome number for the order may be x = 12 (Graham et al. 1993).
For further information, see Weiss (1890) and van Tieghem (1891b), cork cambium position, Mauritzon (1939a: embryology), Lourteig (1965), Venkateswarlu and Prakash Rao (1971: wood anatomy), Beusekom-Osinga and Beusekom (1975: morphology etc. around Crypteroniaceae), Johnson and Briggs (1985: morphological phylogeny), Van Vliet and Baas (1975, 1985: vegetative anatomy), Rye (1979), Solt and Wurdack (1980: chromosome number), Tobe (1989) and Tobe and Raven (1983a, 1985a, 1985b, 1987a, 1990), all embryology and ovule morphology (ordinal characters are mostly plesiomorphous), Dahlgren and Thorne (1985: general; other papers in Ann. Missouri Bot. Gard. 71(3). 1985), Boesewinkel and Venturelli (1987: ovule and seed), Weberling (1988: inflorescence morphology), Ronse Decraene & Smets (1991b: polyandry), and Almeda (1997: chromosome numbers).
Phylogeny. The position of Myrtales within the rosids was unstable in a rbcL analysis of all angiosperms (Hilu et al. 2003). However, there was some support for a position sister to all other rosids except Geraniales, Vitales and Saxifragales (Zhu et al. 2007), while Wang et al. (2009) suggested that is was sister to Geraniales, the combined group being sister to all other malvids. See also the Pentapetalae and Saxifragales pages for further discussion on the relationships of Myrtales.
Relationships within the order have been extensively studied by Conti et al. (1996, 1998, 1999, 2002), Sytsma et al. (1998, esp. 2004), Clausing and Renner (2001: Melastomataceae), Schönenberger and Conti (2001, 2003: esp. Penaeaceae area, etc.) and Wilson et al. (2005: Myrtaceae s.l.), and the tree is based on these publications. The position of Combretaceae seems still to be unclear (see also Maurin et al. 2010; M. Sun et al. 2016), and Berger and Sytsma (2010), Bell et al. (2010) and Soltis et al. (2011) find at least some support for a position sister to [Onagraceae + Lythraceae]. Anatomy (vestured pits), some morphological features (general leaf type and insertion) and molecular data all strongly suggest that Vochysiaceae are to be included in Myrtales, but at first sight the distinctive monosymmetric spurred flowers of that family are quite unlike those of the rest of the order.
Includes Alzateaceae, Combretaceae, Crypteroniaceae, Lythraceae, Melastomataceae, Myrtaceae, Onagraceae, Penaeaceae, Vochysiaceae.
Synonymy: Melastomatineae J. Presl - Circaeales Martius, Combretales Berchtold & J. Presl, Epilobiales Martius, Henslowiales Martius, Lythrales Link, Melastomatales Berchtold & J. Presl, Memecylales Martius, Myrobalanales link, Oenotherales Bromhead, Onagrales Berchtold & J. Presl, Penaeales Lindley, Trapales J. Presl, Vochysiales Link - Myrtanae Takhtajan - Myrtopsida Bartling, Oenotheropsida Brongniart
COMBRETACEAE R. Brown, nom. cons. Back to Myrtales
Evergreen, trees (or shrubs); 5-desoxyflavonoids, flavonoid sulphates +; (cork epidermal); fibres with at most minutely bordered pits; sclereids +/0; petiole bundle arcuate to annular (wing bundles +); hairs unicellular, pointed, thick-walled, with a basal internal compartment, also lepidote or with stalked glands; lamina vernation conduplicate or supervolute, domatia or other glands common, stipules at most small; (plant monoecious); flowers 4-5(-8)-merous; C often small or 0; A obdiplostemonous, (= and alternate with or opposite sepals; -15), inserted below or at the hypanthial apex; G [2-5(-8)], alternate with K or odd member abaxial, unilocular, placentation apical, (nectary on top of ovary), stigma punctate (capitate); ovules (1-)2-7(-20), outer integument 2-5 cells across, inner integument 2-3 cells across, parietal tissue 5-10 cells across, nucellar cap 3-8 cells across, ± pachychalazal, funicles long, usu. with obturator; fruit indehiscent, dry; seed single, large; (testa multiplicative), endotesta tracheidal or sclerotic, ?not crystalliferous, exotegmen fibrous; embryo often green, cotyledons convolute or plicate; n = (7, 11)12-13.
14[list]/500: 3 groups below. Largely tropical. [Photo - Flower, Flower, Fruit.]
Age. Crown Combretaceae are ca 46 m.y.o. (Sytsma et al. 2004) or (106.5-)102.6(-98.9) m.y. (Berger et al. 2015); Strephonema diverged soon after the origin of stem Combretaceae at ca 90 m.y.a. (Sytsma & Berger 2011).
Fossils of Esgueiria, assigned to Combretaceae, are widespread in the Northern Hemisphere in Late Cretaceous deposits ca 90-70 m.y. old. They seem to have inferior unilocular ovaries with apical placentation and glandular-peltate hairs (Friis et al. 1992, 2011), there is no hypanthium, of the eight stamens, five are in one whorl and three in another, the styles are more or less separate, and the surface of the unicellular hairs of the Japanese, but not the Portugese, material is distinctly rough (Takahashi et al. 1999). The nature of the nectary is unclear; in some specimens there are structures outside the androecium that have been interpreted as possible nectaries (Takahashi et al. 1999), unlike the nectaries in extant Combretaceae. The identity of these fossils should be confirmed - to be compared with Hydrangeaceae? Dilcherocarpus, from the Albian-Cenomanian of the Dakota Group, Kansas, and ca 100 m.y. old, has been assigned to Combretaceae (Manchester & O'Leary 2010).
1. Strephonematoideae Engler & Diels
Imperfect tracheary elements with bordered pits; internal phloem 0; stomata paracytic; hairs appressed, 2-armed; leaves "alternate"; pollen lacking pseudocolpi, only semitectate; G half inferior; fruit largely superior; ovules 2; cotyledons hemispherical, large, conduplicate; germination hypogeal; n = ?
1/3. West Africa (map: from Jongkind 1995; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
2. Combretoideae Beilschmied
(Petiole with glands); flowers often sessile; C not clawed[?]; ovary inferior; (embryo sac tetrasporic, 16-nucleate); cotyledons flattened and variously folded.
13/500. Largely tropical (map: from van Steenis & van Balgooy 1966; Wickens 1976; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase 2006; Stace 2010).
2a. Laguncularieae Engler & Diels
Stomata cyclocytic; lamina (with glands), revolute [Laguncularia]; bracteoles adnate to G; (C clawed); fruits flattened, (winged by the bracteoles); cotyledons spirally folded [convolute]; n = 13.
4/8. Tropical, often mangroves, esp. N. Australia.
Age. Ricklefs et al. (2006) dated crown Laguncularieae to ca 23 m.y.a..
2b. Combreteae Engler
(Plants lianes); included phloem + [= interxylary phloem]; (mucilage ducts - Terminalia); stomata anomocytic; (C small/0); (micropyle endostomal - Guiera), (parietal tissue ca 10 cells across, pachychalazal - Combretum coccineum); fruit ± winged, (drupaceous); (integuments multiplicative); (megaspore mother cells several).
9/490. Largely tropical. Combretum (255), Terminalia (190).
Age. This node is about 33 m.y.o. (Berger et al. 2015).
Synonymy: Bucidaceae Sprengel, Myrobalanaceae Martinov, Sheadendraceae G. Bertolini, nom. invalid., Terminaliaceae Jaume Saint-Hilaire
Evolution: Divergence & Distribution. For the fossil record of winged fruits that can be assigned to Combretaceae, see Manchester and O'Leary (2010).
Diversification of most of the family is a Caenozoic phenomenon (Sytsma & Berger 2011), indeed, there was a significant shift in speciation rates in Combreteae, but when that occured is unclear (Berger et al. 2015).
Ecology & Physiology. Lumnitzera and Laguncularia are mangrove taxa (see articles in Ann. Bot. 115(3). 2015); for more on the mangrove habitat, see Rhizophoraceae.
Seed Dispersal. The flattened and/or winged fruits of Combretaceae are often wind- or water dispersed, and Systma and Berger (2011) note substantial dispersal of the family in the Pacific.
Chemistry, Morphology, etc. Wood fibres are usually non-septate, but those of Lythraceae, at least, are septate. The islands of included phloem in Combretum are connected in a reticulating fashion (Robert et al. 2011); den Outer and van Veenendaal (1995) noted that this system was more important in the transport of assimilates that the phloem outside the xylem - and that it was interesting that these plants were shrubs or trees, not lianas where odd vascular construction is almost the norm. Keating (1985) describes the stomata as being paracytic while Dahgren and Thorne (1985) call them anomocytic; in any event, variation in stomatal morphology is extensive (Tilney 2002).
There are hairs lining the ovary loculus walls in Combretum.
Some information is taken from Stace (2006: general; 2010: New World taxa), Graham (1964: general), Verhoeven and van der Schijff (1974: anatomy, inc. root cork cambium), Mauritzon (1939a), Fagerlind (1941a) and Venkateswarlu (1952b), all embryology, Venkateswarlu and Prakash Rao (1971) and Jongkind (1995), both Strephonema, El Ghazali et al. (1998: pollen). For obdiplostemony, see Eckert (1966, also Tomlinson 1986).
Phylogeny. Strephonema may be sister to the rest of the family. Lumnitzera and Laguncularia, both mangrove plants, are sister taxa, but Conocarpus, also found in similar habitats, is not immediately related (Tan et al. 2002; Maurin et al. 2010). Indeed, M. Sun et al. (2016) found that Conocarpus was sister to the rest of the family, although otherwise relationships are as noted above. Maurin et al. (2010) in particular discuss details of relationships within the family, especially in the large genera Terminalia and Combretum.
Classification. For generic limits, especially around Combretum, see Stace (2007), while Maurin et al. (2010) suggest that the limits of Terminalia, currently paraphyletic, be expanded; support values underpinning change in neither case are very high.
[[Onagraceae + Lythraceae] [[Vochysiaceae + Myrtaceae] [Melastomataceae [Crypteroniaceae [Alzataeaceae + Penaeaceae]]]]: ?
Age. This node has been dated to end-Albian at ca 100 m.y. (Sytsma et al. 2004), around 62 m.y. (Naumann et al. (2013), or a mere ca 47.4-43 m.y. (Xue et al. 2012).
Evolution. Ecology & Physiology. This clade has distinctively small seeds (Cornwell et al. 2014).
[Onagraceae + Lythraceae]: tannins often not abundant, soluble oxalate accumulating; vessels grouped; fibres with at most minutely bordered pits; petiole bundle arcuate; (flowers vertically monosymmetric); tapetal cells binucleate; (pollen at anthesis with starch); nucellus with starch grains, hypostase +; megaspore mother cells several; K persistent; exotegmen fibrous; starch grains in nucellus; x = 8.
Age. The two families are estimated to have separated at the end-Cenomanian ca 93 m.y. (Sytsma et al. 2004) or earlier, around (109.1-)104.6(-100.2) m.y.a. (Berger et al. 2015), or somewhat later, about 72.2/68.2 m.y.a. (Tank et al. 2015: Table S2), or (80-)67, 63(-49) (Bell et al. 2010), or (71-)67, 57(-53) m.y. (Wikström et al. (2001).
Evolution: Divergence & Distribution. For attempts to relate the development of the female gametophyte of Onagraceae to that of Lythraceae, see e.g. Mauritzon (1934e).
Chemistry, Morphology, etc. Both Trapa and some species of Ludwigia are aquatics with distinctive floating rosettes of expanded leaves. Decodon is the only typically pentamerous genus in Lythraceae (Graham 2006), as is Ludwigia (Onagraceae). Since both may be sister to the rest of their respective families, working out where floral merism changes on the tree becomes difficult. A number of Lythraceae, including Trapa, have capitate stigmas, and this could be another feature uniting the two families.
ONAGRACEAE Jussieu, nom. cons. Back to Myrtales
Plants herbaceous; flavonoid sulphates +; phloem loading via intermediary cells [specialized companion cells with numerous plasmodesmata, raffinose etc. involved]; raphides +; (leaves spiral), lamina vernation ± flat to involute, margins toothed, stipules 0); inflorescence raceme or spike, (flowers axillary), bracteoles often 0; protogyny common [ca 55%]; C deciduous, (not clawed); anthers polythecate, filaments straight in bud; pollen with viscin threads [attached proximally], starchy, (colpate), apertures protruding, ektexine paracrystalline, beaded; ovary alternating with K, (placentation parietal), stigma capitate; ovules with outer integument 2-5 cells across, inner integument 2(-3) cells across, (epistase +), parietal tissue ca 2(?-13 - Vesque) cells across, nucellar cap ca 2 cells across, hypostase +/0; micropylar megaspore functional, embryo sac 4-nucleate [Oenothera type]; fruit opening loculicidally down the sides; exotesta often hairy or papillate, inner walls thickened and lignified (mesotestal cells thickened, ± sclerotic; endotegmic cells longitudinally elongated, "tanniniferous", inner walls thickened); endosperm nuclear, diploid.
22[list]/656 - two subfamilies below. World-wide (map: based on Raven 1963, 1967; Meusel et al. 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; P. Hoch & W. Wagner, pers. comm.).
Age. Onagraceae are ca 82 m.y.o. (Sytsma et al. 2004) or (96.2-)85.4(-73.3) m.y. (Berger et al. 2015).
1. Jussiaeoideae Beilschmied
Flowers 4-5-merous; hypanthium 0; (A 10); pollen in tetrads (monads; large irregular clumps); G with central vascular bundles, style short; nectary on top of ovary; ovules with parietal tissue 3-6 cells across, hypostase +; megasporocyte 1.
1/82: World-wide, esp. America. [Photo - Flower.]
2. Onagroideae Beilschmied
(Plant woody - esp. Fuchsia], included phloem +; (stipuliform structures + - Fuchsia); flowers 4-merous, (monosymmetric - Lopezia), hypanthium long, deciduous, (0); (petals lobed); (A 1 [abaxial] + 1 staminode, vertical), (2, lateral - Circaea); pollen oblate, transseptal vascular bundles + (0), (style short), minor stylar bundles 0, (stylar bundles 0), (stigma 4-lobed; dry); (ovules wth parietal tissue 10-25 cells across); (fruit baccate), K not persistent; (seeds with chalazal hairs - Epilobium); n = 5+.
21/574: Epilobium (165), Oenothera (145: inc. Gaura, etc.), Fuchsia (105), Clarkia (42), Lopezia (22). World-wide, but esp. western North America. [Photo - Flower, Flower.]
Synonymy: Circaeaceae Berchtold & J. Presl, Epilobiaceae Ventenat, Fuchsiaceae Lilja, Isnardiaceae Martinov, Jussiaeaceae Martinov, Lopeziaceae Lilja, Oenotheraceae C. C. Robin
Evolution: Divergence & Distribution. For the fossil history of the family, see Grímsson et al. (2011a) and Lee et al. (2013) and references; the fossil pollen is very distinctive and is known from the Maastrichtian, at least 66 m.y.a..
Plant-Animal Interactions. Some caterpillars are found both on Vitaceae and Onagraceae (Forbes 1956) - and both contain raphides. Different rusts occur on Onagroideae and Jussiaeaoideae (Savile 1979b).
Pollination Biology. For details of floral morphology in Onagraceae and its relation to pollination, see Wagner et al. (2007). Pollination in North American members of the family has been studied in great detail (e.g. references in Linsley et al. 1973; Clinebell et al. 2004). Interestingly, 12 species of oligolectic Andrena bees are major visitors to Camissonia campestris alone (Linsley et al. 1973), while Clinebell et al. (2004) documented a wide variety of potenital pollinators visiting the four species of Onagraceae and three other species that they studied. How petal spots develop in Clarkia gracilis has recently been worked out in some detail (Martins et al. 2012).
Protogyny is common here; the non-protogynous taxa are either protandrous or undecided in equal numbers (Newman 1993). For a general survey of reproductive biology in Onagraceae, see Raven (1979).
Genes & Genomes. All the chromosomes in some species of Oenothera form a ring, joined by a series of permanent translocations; the whole genome forms a single linkage unit (Cleland 1972). There is paternal transmission of chloroplasts. Particular combinations of genome and plastome may be incompatible, and the resultant inviability of some genome/plastome combinations may provide genetic barriers between taxa (Stubbe & Steiner 1999). Although these permanent translocation hybrids self, they show an increased diversification rate over sexual species, interestingly, there are frequent reversals from the hybrid state to sexuality (Johnson et al. 2011). The whole system sometimes breaks down (see Harte 1993: the contributions of Oenothera to biology; Stubbe & Steiner 1999 and references: translocation, etc; Wagner et al. 2007). Golczyk et al. (2014) found that breaks occurred subterminally between between two distinct chromatin regions, and there were no normal telomeres; translocation did not involve whole arms.
Chemistry, Morphology, etc. The stipules of Ludwigia can be quite prominent.
There are some very distinctive floral morphologies in Onagroideae. Thus Circaea has only two deeply-lobed petals (adaxial-abaxial) and two lateral stamens, the latter being opposite the sepals. The strongly monosymmetric flowers of Lopezia have only a single abaxial stamen that becomes extrorse and a petal-like adaxial staminode; the two adaxial petals may be recurved and have pseudonectaries on their claws (Eyde & Morgan 1973). Gongylocarpus has sessile flowers, as is quite common in Onagraceae, but after pollination the ovary becomes completely enveloped by stem tissue. The viscin threads that characterize the family vary considerably in morphology, often being annular-vermiform, but they are also smooth or irregularly beaded (Skvarla et al. 1976). The style of Ludwigia has minor bundles, but these are absent in other members of the family. In Oenothera, more than one spore from the same megaspore mother cell may germinate and - presumably - compete (Noher de Halac & Harte 1977). x = 10, 11, 15 in the basal clades of Onagroideae, ?18 in Epilobeae, and 7 in Onagreae (Wagner et al. 2007).
For other information, see Johansen (1928: hypostase and its correlation with the environment), Eyde (1982: floral anatomy), Maheshwari (1947), Tobe and Raven (1986a, b, 1987d, 1996) and Hoch et al. (1993: variation in anther septum development, embryology), Praglowski et al. (1983, 1994: pollen), Skvarla et al. (1978: viscin threads), Tobe et al. (1987d: seed coat anatomy), the Onagraceae website (general) and Wagner et al. (2007: superb summary).
Phylogeny. Ludwigia is sister to the rest of the family, and within Ludwigia, taxa with five and those with ten stamens form separate clades (Barber et al. 2008). Knowledge of relationships along the backbone of the tree seems to be stabilising [Hauya [[Fuchsia + Circaea] [Lopezia [Gongylocarpus [Epilobeae + Onagreae]]]]] may be the structure (Levin et al. 2003, 2004), however, Ford and Gottlieb (2007) found a clade [Hauya [Fuchsia + Circaea]] that was sister to other Onagroideae (see also M. Sun et al. 2016).
Classification. Wagner et al. (2007) enumerate all supraspecific taxa. Reflecting the new, but for the most part well supported phylogeny of the family, generic limits have been adjusted, so Oenothera has been expanded and Camissonia very much cut up (e.g. Levin et al. 2004); for appropriate nomenclatural changes, see Hoch and Wagner (2007). The Onagraceae website contains a largely up-to-date summary of classification, etc.
Botanical Trivia. In 1827 Robert Brown recorded the phenomenon that is now called Brownian motion when observing the pollen grains of Clarkia pulchella.
Hugo de Vries thought that the abrupt appearance of O. lamarckiana was an example of normal evolution, which for him was a process in which mutation = major change/speciation, natural selection not being involved. However, O. lamarckiana is a morphological variant caused by the breakdown of the permanent translocation system mentioned above (c.f. Linnaeus and Peloria [= Linaria, Plantaginaceae]).
LYTHRACEAE Jaume Saint-Hilaire, nom. cons. Back to Myrtales
Herbs to trees; quinolizidine alkaloids +; mucilage cells common; hairs uni- or bi(multi)cellular; leaves (spiral), lamina vernation flat to conduplicate, (margins dentate - Trapa), stipules +/0; (inflorescence determinate); pedicel articulated [?always]; flowers (3) 4 (5) 6(-16)-merous, heterostyly common; hypanthium/K often strongly ribbed, appendages [= epicalyx] alternating with sepals, (hypanthium spurred), (0, but with K + C tube), C crumpled in bud, (0); A basically obdiplostemonous, (1 - = and opposite sepals - many, centrifugal or centripetal), inserted just below C to near ovary, filaments of unequal length; (tapetal cells multinucleate); (pollen porate), (pseudocolpi 0, 6), (surface striate); (nectary at base of G); G superior, [2-6(-many)], (inferior), orientation variable, (placentation parietal), stigma capitate to punctate, also dry; ovules (1[Trapa]-few/carpel), outer integument 2-7(-9) cells across, inner integument 2(-3) cells across, parietal tissue 2-9(-15 - Cuphea) cells across, "chalazal strand" +, (postament +); (embryo sac much elongated); fruit a capsule, dehiscence often irregular, also circumscissile, loculicidal (indehiscent; berry), K often ± enclosing fruit; seeds usu. flattened; testa multiplicative, many-layered (not - Duabanga), exotesta various, invaginated mucilage hairs + (0), (sarcotesta - Punica), endotestal cells often elongated and tracheidal/sclerotic, (crystalliferous), (endotegmen of crossing fibres); (cotyledons folded); n = (5-)8(-11, + polyploids), chromosomes 1-4 µm long; chloroplast rpl2 intron 0.
31[list]/620: Cuphea (250), Diplusodon (75), Lagerstroemia (55 - A centrifugal), Nesaea (55 - probably to include Ammannia - then = 80), Rotala (45), Lythrum (36). Tropical, but some temperate (map: from van Balgooy 1975; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Graham et al. 2005). [Photo - Flower]
Age. Estimates of the age of the family are (65-)50, 46(-29) m.y. (Bell et al. 2010: minus Deocodon), ca 60 m.y.o. (Sytsma et al. 2004) or rather older, (99.7-)95.5(-91.7) m.y. (Berger et al. 2015).
However, fossil evidence suggests that a crown group age for the whole family is likely to be at least 85 m.y.. Pollen from Montana dated to the Lower Campanian 82-81 m.y.a. has reliably been identified as Lythrum or its segregate, Peplis; there is somewhat younger (72-78 m.y.) pollen from Siberia (Grímsson et al. 2011b: exquisite micrographs; S. Graham 2013 for a summary). The fossil Trapago is found in deposits 73-65 m.y. old, and other fossils assignable to Myrtales in general are perhaps slightly older (Crepet et al. 2004 and references).
Evolution: Divergence & Distribution. Sonneratia, a mangrove genus, has a long fossil record, its pollen, Florschuetzia, being distinctive (Müller 1978, 1984), and it may be Oligocene in age; for the evolution of the mangrove habitat, see Rhizophoraceae. Decodon, now restricted to eastern North American, was widely distributed in the North Hemisphere from the Eocene onwards and was more divese than it is now (Ferguson et al. 1997 and references; Little et al. 2004); it is also known from the late Cretaceous of Mexico (Grímsson et al. 2012). See Graham (2013) for a summary and evaluation of the fossil record of the family.
Ecology & Physiology. Sonneratia, with ca 7 species, is a notable element of mangrove vegetation from Southeast Asia to the Pacific; see also articles in Ann. Bot. 115(3). 2015.
Seed Dispersal. Taxa whose seeds have mucilaginous hairs are more or less myxospermous; the hairs evert when the seed is wetted (Western 2011 for references). The fruits of Cuphea open by the placenta expanding and moving laterally, breaking through both the thin ovary wall and the hypanthium; the seeds are exposed on the placenta.
Genes & Genomes. S. Graham and Cavalcanti (2001) suggest that x = 8 is the basic chromosome number for the family.
Chemistry, Morphology, etc. The stamens may be held on one side of the flower (also in some Onagraceae) and so causing rather weak monosymmetry; this is much more marked in Melastomataceae. Some species of Cuphea, e.g. C. glutinosa, have quite strongly monosymmetric flowers. Androecial development is both centrifugal and centripetal (Weberling 1989 and references; Ronse Decraene & Smets 1991). Pollen is notably variable (Graham 2006). Species of the large genus Cuphea consistently have eleven stamens. When G = K, the carpels may alternate with or be opposite to them, when G = 2, the carpels may be transverse or median, when G = 3, the odd carpel is adaxial (Eichler 1878; Baillon 1877; Spichiger et al. 2002). Ovule morphology varies considerably. In taxa like Trapa, Sonneratia and Cuphea the embryo sac is much elongated, the nucellus sometimes being massive. There is usually a postament, and the base of the endosperm may be abruptly narrowed and protrudes into the hypostase (see e.g. Täckholm 1915; Tischler 1917; Mauritzon 1934e; Joshi and Venkateswarlu 1936; Venkateswarlu 1937; Ram 1956: Trapa, and references). Taxa with everting testa hairs, which vary in their morphologies, are unique to the family but are scattered through it (S. A. Graham & Graham 2014).
The inferior ovary of Punica granatum is unique in flowering plants, appearing to have two (or three) superposed layers of carpels, the basal with axile and the others with intrusive parietal placentation; the placentation is fundamentally axile, the appearance of parietal placentation being the result of growth at the base of the ovary (Sinha & Joshi 1959 for vasculature; Leins 1988 for androecial development). In the other species of the genus, P. proto-punica, there is a more ordinary semi-inferior ovary. The seeds of Punica have a sarcotesta, although this is often described as being an aril, not least by Wikipedia.
For general information, see Tobe et al. (1998: morphological matrix) and S. Graham (1964, 2006); for some vegetative anatomy, see Little et al. (2004), for pollen, see Muller (1981b) and A. Graham et al. (1990, for ovules, see Mauritzon (1939a), and for seed anatomy and morphology, see Grütter (1893) and S. Graham and Graham (2014).
Phylogeny. S. Graham et al. (2005) found maximum parsimony support for the topology [Decodon [[Lythrum + Peplis] [remainder of the family]]]; the remainder of the family formed two large clades. However, support along the back-bone was weak, and in maximum likelihood analyses there was weak support for the three genera just mentioned being sister to one of these two clades. Z.-D. Chen et al. (2016) found that Rotala was sister to the rest of the family, but support for this position was weak. If Decodon is sister to the rest of the family, then seeds with mucilage hairs and 6-merous flowers are probably synapomorphies for the rest of the family. The old Sonneratiaceae (Sonneratia and Duabanga), plants of mangroves, are not monophyletic (Shi et al. 2000; Huang & Shi 2002; S. Graham et al. 2005; Narzary et al. 2016); Sonneratia itself may be sister to Trapa (e.g. Z.-D. Chen et al. 2016). The distinctive Punica was found to be sister to Woodfordia (Narzary et al. 2016).
Rotala and Ammannia, previously thought to be close, are well separated, and relationships within the former genus have been clarified (S. Graham et al. 2011). For a phylogeny of Cuphea, see S. Graham et al. (2006).
Some taxa with particularly distinctive morphologies:
Classification. For likely changes in generic limits around Ammannia, see S. Graham et al. (2010, esp. 2011).
Some morphologically distinctive taxa until recently separated as their own families - Trapaceae (water chestnut), Sonneratiaceae, Punicaceae (pomegranate) - nestle firmly within Lythraceae.
Synonymy: Ammanniaceae Horaninow, Blattiaceae Engler, Duabangaceae Takhtajan, Lagerstroemiaceae J. Agardh, Lawsoniaceae J. Agardh, Punicaceae Berchtold & J. Presl, nom. cons., Sonneratiaceae Engler, nom. cons., Trapaceae Dumortier
[[Vochysiaceae + Myrtaceae] [Melastomataceae [Crypteroniaceae [Alzataeaceae + Penaeaceae]]]]: inflorescences with at least the branches cymose.
Age. This node has been dated to around 88.2 m.y. (Tank et al. 2015: Table S1), (84-)79, 74(-69) m.y. (Wikström et al. 2001: internal relationships ± scrambled), or (90-)75, 73(-59) m.y. (Bell et al. 2010).
Chemistry, Morphology, etc. Oil glands are found in the anthers of many Myrtaceae, and a number of other taxa in the Melastomataceae-Crypteroniaceae clade also have a very much expanded connective. Whether some staminal features - perhaps linked with pollination - are a higher-level apomorphy in this clade awaits further study.
[Vochysiaceae + Myrtaceae]: hairs simple, 1-2-celled; K and C imbricate; style depressed in apex of gynoecium; fruit a capsule.
Age. The two families diverged 100-93 m.y.a. (Sytsma et al. 2004), (107-)101(-95) m.y.a. (Berger et al. 2015), or 72.3/61.9 m.y. (Tank et al. 2015: Table S2).
Evolution: Divergence & Distribution. Sytsma et al. (2004) discussed the age and biogeographic history of the whole group in some detail.
Phylogeny. Conti et al. (1996) found a well supported [Heteropyxidaceae + Psiloxylaceae] sister to [Myrtaceae + Vochysiaceae]; note, however, that the pollen grains of the first two are similar to those of Myrtaceae (Dahlgren & Thorne 1985). Monophyly of Myrtaceae s. str. (= Myrtoideae) was not strong (Conti et al. 1996, 1998). However, Wilson et al. (2005: matK only) found Myrtaceae s. str. to have 80% jacknife support, while Myrtaceae s. str. + [Heteropyxidaceae + Psiloxylaceae] (all together = Myrtaceae here) had ³95% support; a similar set of relationships were found by Sytsma et al. (2004; matK and ndhF).
VOCHYSIACEAE A. Saint-Hilaire, nom. cons. Back to Myrtales
Trees (lianes); 5-deoxyflavonoids +; plants Al-accumulators; axial parenchyma banded; pericyclic fibres at most few; (secretory canals in pith); sclereids, mucilage cells +; (nodes 3:3 - Ruizterania), leaf traces run along stem before entering petiole; cuticle waxes as ± grouped parallel platelets; stomata also paracytic; indumentum often brown, hairs unicellular, (T-shaped or stellate); leaves leathery, lamina vernation conduplicate, (venation eucamptodromous - Callisthene), stipules cauline, (with associated large glands), sometimes colleter-like; inflorescence terminal (axillary), with lateral cincinni; flowers strongly mono- or asymmetric, plane oblique; hypanthium 0, K basally connate, one adaxial-lateral sepal larger and with nectariferous spur from floral axis, (three K petal-like - Korupodendron), C 1, 5 (3), unequal; A 1, more or less opposite abaxial lateral petal, (staminodes 2), filaments straight in bud; G [3 (4)], odd member adaxial, stigma punctate to subcapitate; ovules with outer integument 2-3 cells across, inner integument ca 2 cells across; fruit samaroid [by 4 or 5 accrescent K lobes], or loculicidal capsules; seeds variously winged, testa thin, mesotesta ?not sclerotic, endotestal cells ± thickened, pectic, mesotegmic cells fibrous, thick-walled or not, or testa multiplicative, exotesta with thickened hairs, a few other layers persisting, but rest and tegmen disorganised; cotyledons folded; n = 11, 12.
7[list]/190: Vochysia (100), Qualea (60). Lowland tropical America, apart from Erismadelphus and Korupodendron from W. Africa (map: from Stafleu 1954; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]
Age. The age of crown-group Vochysiaceae is some 36-33 m.y. (Sytsma et al. 2004) or (52-)39(-28) m.y. (Berger et al. 2015).
Evolution: Divergence & Distribution. The phylogenetic "stem" of Vochysiaceae is around 60 m.y. (Berger et al. 2105). The present distribution of Vochysiaceae on either side of the Atlantic is likely to be the result of dispersal (Sytsma et al. 2004; Berger et al. 2015: differences in detail).
Chemistry, Morphology, etc. Leaves of small saplings may have short petioles and swollen leaf bases. At least in Vochysia guatemalensis there are conspicuous, symmetrically-arranged mucilage canals in the pith; Ruizterania has trilacunar nodes (pers. obs.).
The single stamen may be opposite either the abaxial-lateral C or the adjacent K; in the latter case, it is off the plane of symmetry (Kawasaki 1998; also Litt & Stevenson 2003b). The ovary is initiated in an inferior position, the superior position in the mature flower being secondary (Litt 1999; Litt & Stevenson 2003a). Baillon (1874) drew the flower as being inverted and with the odd carpel adaxial, while Corner (1976) described the ovules of Qualea sp. as being long-exostomal.
For a general account, see Kawasaki (2006), for anatomy, see Quirk (1980) and Sajo and Rudall (2002), and for floral development and morphology, see Litt and Stevenson (2003a, b).
Phylogeny. relationships are unclear. Erismieae, containing the tropical American Erisma and the West African Erismadelphus and Korupodendron, are monophyletic. They have cortical/subepidermal phellogen; G 1, ± inferior (perhaps plesiomorphic), 1-2 lateral to apical ovules/carpel; fruit samaroid, with persistent enlarged K; testa undifferentiated, with vascular bundles. Vochysieae are probably not monophyletic (Litt 1999).
Previous Relationships. Because of their monosymmetric, spurred flowers Vochysiaceae were often associated with families that are no longer thought to be at all closely related. They often included Euphronia (e.g. Mabberley 1997; Takhtajan 1997: see Malpighiales-Euphroniaceae), and Takhtajan's (1997) Vochysiales included families like Malpighiaceae (Malpighiales), Tremandraceae (= Oxalidales-Elaeocarpaceae) and Krameriaceae (Zygophyllales); Cronquists' (1981) Polygalales was even more heterogeneous
MYRTACEAE Jussieu, nom. cons. Back to Myrtales
Ethereal oils [usu. terpenes] +; wood fibres with distinctly bordered pits; leaves with gland dots; apex of anther connective glandular [terpene-producing]; pollen parasyncolpate, the colpi margins spreading and forming a triangular apocolpial polar area.
131[list]/4,620, three groups below. Worldwide, mostly tropical-warm temperate.
Age. Crown Myrtaceae may date to 87-85 m.y. (Biffin et al. 2010a), 95-84 m.y. (Sytsma et al. 2004), or (88-)85(-84) m.y. (Berger et al. 2015); ages in Wilson (2011) are largely similar. In a comprehensive analysis also using fossil pollen, Thornhill et al. (2012a: dates for root-only calibrated tree much younger) suggest ages for crown group Myrtaceae of (97-)91, 85(-74) m.y.a., while (93-)85(-75) m.y. is the age spread in Thornhill et al. (2015: calibrated node).
For a summary of fossils attributed to Myrtaceae see Biffin et al. (2010a; also Crepet 2008); Thornhill and Macphail (2012) evaluate the fossil pollen record. For interesting Eocene fossils from Australia, see Basinger et al. (2007) and from Colorado, see Manchester et al. (1998); for fossil Eucalyptus, see below. Pigg et al. (1992) described a fossil from the Palaeocene that they thought was close to Myrtaceae-Myrteae-Psidium, although Cretaceous pollen can be assigned to the family (Wilson 2011; see also Thornhill & Macphail 2012).
1. Psiloxyloideae Schmid
Plant "tanniniferous"; leaves spiral; plant dioecious; A erect in bud, each stamen with separate traces; staminate flowers: anther sacs each opening separately, pollen with closely-fitting island in polar apocolpial area; pistillode +; carpellate flowers: staminodia +; G superior, , base narrow; embryo sac bisporic, 8-nucleate [Allium type]; endotesta crystalliferous, cells periclinally elongated; x = 12.
2/4. S.E. Africa, Mascarenes.
Age. Thornhill et al. (2012a) suggested that the age of crown-group Psiloxyloideae (77.5-)44.4, 41.4(-21.4) m.y.; (45-)40(-38) m.y. is the suggestion in Sytsma et al. (2004) and (60.6-)39.7(-20.2) m.y. in Thornhill et al. (2015).
1A. Heteropyxideae Harvey
Trees; axial xylem parenchyma 0 [?Psil]; epidermal wax crystalloids as small platelets; leaves with domatia, stipules minute; (plant monoecious); staminate flowers: stamens = and opposite petals (+ 1-3 opposite sepals); carpellate flowers: (G ), style impressed, stigma capitate; style green, persistent; ovules hemitropous; seeds with wings at either end, exotesta with tangentially elongated cells, walls scalariform-reticulately thickened, exotegmic cells elongated.
1/3. South eastern Africa (Map: from MO herbarium records, green).
Synonymy: Heteropyxidaceae Engler & Gilg, nom. cons.
1B. Psiloxyleae (Croizat) A. J. Scott Back to Myrtales
Trees; secretory canals in the young stem; vestured pits?; fibres septate, crystalliferous; nodes ?; glands not producing ethereal oils; plant glabrous; stipules colleter-like; (plant polygamodioecious), pedicels articulated; flowers 4-5(-6)-merous; C coriaceous, caducous, punctate, staminate flowers: A 2x C, anthers versatile; carpellate flowers: (G also ), style 0, stigma large, lobed; ovules hemicampylotropous; fruit baccate, punctate; exotesta cells large, exotegmen crushed.
1/1: Psiloxylum mauritianum. Mascarenes (Map: red, see above).
Synonymy: Psiloxylaceae Croizat
2. Myrtoideae Sweet
(Ectomycorrhizal) trees and shrubs; terpenes diverse and abundant, exudates kinos; (plants Al accumulators); (cork cambium superficial); axial parenchyma +; sieve tubes with non-dispersive protein bodies; (stomata paracytic); (hairs multicellular); leaves opposite or spiral, lamina vernation variable, (secondary veins palmate), stipules 2, or several, colleter-like, or 0; flowers (3-)4-5(-8)-merous; (K or P calyptrate, circumscissile), C (0-)4-5(-12), often deciduous; A many, conspicuous, (5, opposite C, 10), in fascicles opposite C (K), in ring, development centripetal to centrifugal, (filaments straight in bud); (pollen syncolpate; brevicolpate - Myrteae); G [2(-18], at least partly inferior, alternate or opposite petals or odd member abaxial, placentae well-developed, (1-locular, placentation basal), transseptal bundles +, minor stylar bundles 0, stigma punctate to capitate (peltate), also dry; ovules (1-15/carpel), micropyle zig-zag [?always], outer integument 2-6(-12) cells across, inner integument 2(-4) cells across, (unitegmic, integument 6-8 cells across, vascularized), parietal tissue 2-12 cells across, nucellar cap 0 (2 - v. rare), hypostase 0/+, (postament +), (obturator +); (fruit baccate); (seed pachychalazal), exotesta variously thickened, endotesta thickened or not, (sclerotic palisade cells at the micropyle), (testa multiplicative, ± sclerotic [e.g. Psidium, Myrtus]), (exotegmen 0); embryo (± undifferentiated, hypocotylar - Eugenia), green or white, straight or curved, cotyledons often connate, accumbent or incumbent, intricately folded, etc.; n = (5-)11(12).
129/5330: Eugenia (1115), Syzygium (1045), Eucalyptus (800), Myrcia (780), Melaleuca (220), Corymbia (115), Verticordia (100), Psidium (100), Campomanesia (80), Leptospermum (80), Calytrix (75), Kunzea (60), Metrosideros (60), Myrcianthes (50), Darwinia (45), Xanthostemon (45), Tristania (40). Tropical, also temperate, esp in Australia (map: from Meusel et al. 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Lucas 2007). [Photo - Bark, Flower, Flower, Fruit.]
Age. Thornhill et al. (2012a) gave ages for crown-group Myrtoideae of (90.3-)83, 71.3(-64.9) m.y., the lower date, some (78.3-)71.5(-65.4) m.y. was preferred by Thornhill et al. (2015); (86-)80(-70) m.y. are the ages suggested by Sytsma et al. (2004) and around 62 m.y. by Berger et al. (2015).
Synonymy: Baeckeaaceae Berchtold & J. Presl, Chamelauciaceae Rudophi, Eugeniaceae Berchtold & J. Presl, Kaniaceae Nakai, Leptospermaceae Berchtold & J. Presl, Melaleucaceae Vest, Myrrhiniaceae Arnott
Evolution: Divergence & Distribution. Eucalyptus is known fossil from Patagonia, and Hermsen et al. (2012), in evaluating this and other fossil evidence, inclined to dating crown-group Eucalypteae to early Eoceae. Ladiges et al. (2011, see also 2012) suggested that within two clades of Eucalyptus s.l. there was independent adaptation to arid/semi-arid conditions, and they suggested that the age of Eucalyptus s.l. was Late Cretaceous-Palaeocene. There are fossils of Eucalyptus, possibly of the relatively widespread subgenus Symphyomyrtus, in early Eocene deposits of Argentinian Patagonia ca 51.9 m.y. old (Wilf et al. 2010; esp. Gandolfo et al. 2011; Hermsen et al. 2012), while Thornhill et al. (2015) date crown-group Eucalyptus to (35-)34.4(-33.9) m.y. ago. There are also fossils of Eucalyptus from Early Miocene New Zealand (Rozefelds 1996; Pole 2003). Eucalypteae are no longer found in either South America or New Zealand.
Fossils of Metrosideros, perhaps subgenus Metrosideros, have recently been discovered in Oligocene deposits ca 30 m.y.o. in Tasmania. The genus, growing in eastern Malesia, the Bonin Islands, and throughout Melanesia and Polynesia, including Hawaii, is unknown from Australia. Metrosideros polymorpha from Hawai'1 is a very important nectar source for birds, and the genus may have radiated from New Zealand, its seeds being dispersed by wind (Wright et al. 2000, 2001; see also Pillon et al. 2015). Its arrival in Hawai'i is estimated to be a mere (6-)3.9 m.y.a., probably on Kaua'i (Percy et al. 2008). However, understanding the biogeography of the genus is difficult, partly because relationships within it are unclear, and partly because it also includes the South African M. angustifolia and the Chilean M. stipularis, perhaps sister species but of unknown more general relationships (Pillon et al. 2015).
For ages of various clades in the family, see Biffin et al. (2010a); Thornhill et al. (2012a, 2015) also give dates for a number of clades. The pollen record suggests the existence of at least some tribes in the late Cretaceous (Wilson 2011), but this is inconsistent with many molecular divergence dates. Thornhill et al. (2015) suggested that although Myrtaceae may have been Gondwanan in origin, none of the 22 disjunctions they examined could unambiguously be linked to geological vicariance events. Sytsma et al. (2004) suggested that Psiloxylon might have been hopping about on islands in the Indian Ocean for almost 40 m.y. (see also Berger et al. 2015: ca 10 m.y.; Thornhill et al. 2015).
Psiloxyloideae join other examples in the family of species-poor geographically restricted taxa that are sister to much more diverse clades (Thornhill et al. 2015). A shift in speciation rates in Myrtaceae has been provisionally placed around the K/P boundary in stem Myrtoideae (Berger et al. 2015), although its exact position and cause(s) remained somewhat unclear. The increasing aridity of the Oligocene-Miocene led to the rapid divergence of major clades within the family (Wilson 2011).
The shift to fleshy fruits in Syzygieae and Myrteae seems to have been accompanied by increased diversification rates (Biffin et al. 2010a). The Malesian Syzygium is notably diverse on New Caledonia (ca 70 species: see Biffin et al. 2006 for a phylogeny) while in the New World Eugenia is the most species-rich tree genus in the Mata Altantica forest of Brazil (Mazine et al. 2014). Eugenia arrived in Africa from the New World twice (Bernardini et al. 2014).
Ecology & Physiology. There are around 1,600 Australian species of Myrtaceae, including ca 800 species of Eucalyptus and friends (Crisp et al. 2011); Eucalyptus s.l. in particular dominates over 90% of the fire-dependent savannas, woodlands and forests there (Lawler & Foley 2002). About 90% of Eucalyptus s.l. species have epicormic strands in their bark, and/or lignotubers, and these epicormic strands are associated with the development of additional axillary buds in the young stems (Burrows 2013, and references). Epicormic strands are initially meristematic strands up to several centimetres long, and although they do not often have organised buds, resprouting occurs from them after even quite severe fires. This happens both in many species of Eucalyptus s.l. (but not in e.g. E. regnans) and also in some other Australian Myrtaceae (Burrows 2002; Burrows et al. 2010). Hence Eucalyptus-dominated savanna responds differently to fire than do other savannas, since in the latter woody species with epicormic buds are vanishingly uncommon (Moncrieff et al. 2016). Australian Eucalyptus-dominated savanna is also distinctive becase eucalypts tend to be notably tall and narrow compared with other savanna trees (Moncrieff et al. 2014). Crisp et al. (2011: 95% HPD) link the evolution of these epicormic strands/buds with biome evolution in Australia some (62-)62, 60(-58) m.y.a.; dates for crown-group Eucalypteae in Thornhill et al. (2012) are a little younger - (66.2-)60, 55.3(-50.9) m.y. ago. Interestingly, crown-group diversification of the Australian Banksia (Proteaceae), many of which are also fire-associated, is also quite early (He et al. 2011). However, there is little evidence of fire in Australia until the mid-Miocene (e.g. Bond & Scott 2010). Eucalypt woodland was once more widespread, occuring in New Zealand at the end of the Early Miocene (along with palms) (Pole 2003) and in Patagonian South America in the early Eocene ca 52 m.y.a. (Hermsen et al. 2012), and its subsequent disappearance may be because climates became wetter (Crisp et al. 2011).
Biomass accumulation in eucalypt woodlands can be great; average figures of 1,867 tonnes C ha-1 living and dead biomass have been recorded for Eucalyptus regnans-dominated forests (Keith et al. 2009: the highest values are ca 1,000 tons more); E. regnans is one of these giant tress, and the way in which it griws means that much light penetrates the canopy and there is a well-developed understory. However, little seems to be known about the role ectomycorrhizal associations might play in the ecological dominance of the family in Australia; Sebacinaceae (also in Ericaceae and Orchidaceae) have been recorded (Glen et al. 2002).
Eucalypts growing in arid environments have thick leaf blades with apparently overly-closely spaced veins ca 24 mm mm-2, i.e., the distance between veins is less that the distance between veins and stomata Zwieniecki & Boyce 2014; c.f. Zwieniecki & Boyce 2014). This may enable such leaves to achieve maximum photosynthatic rate very soon after rain falls; these leaves are also amphistomatous (Zwieniecki & Boyce 2014).
Nine species of Eucalyptus, along with Pinales and a few Dipterocarpaceae, include the majority of giant trees (70< m tall) known (Tng et al. 2012). These giant eucalypts, not immediately related to one another, may be an odd sort of rain forest pioneer. They usually depend on fire for their regeneration, and several of them are seeders rather than resprouters; rain-forest trees later move in under the eucalypt canopy, which is not very dense (Tng et al. 2012).
Although Myrtaceae are notably common in terms of numbers of species with stems at least 10 cm across in the Amazonian tree flora, individual speciesa seem never to be locally common (ter Steege et al. 2013).
Pollination Biology & Seed Dispersal. The floral diversity of Myrtaceae in Australia is striking, and all told ca 300 species there may be bird-pollinated, especially by lorikeets (Ford et al. 1979); these may eat pollen (Stiles 1981 and references). In many Myrtaceae the numerous stamens with their brightly coloured filaments are the visual attractant for the pollinator, and in taxa such as Callistemon, the bottle-brush, the flowers are aggregated into inflorescences all the flowers of which open simultaneously. Calothamnus has similarly aggregated flowers in which the stamen fascicles form flattened structures, the individual flowers being more or less monosymmetric (Westerkamp & Claßen-Bockhoff 2007), while Verticordia has elaborately-fringed sepals - and sometimes also petals and staminodes. The anther glands (see e.g. Landrum & Bonilla 1996) produce oils, sometimes to attract pollinators, but they also help in the attachment of pollen to stylar hairs, as in the secondary pollen presentation devices of Verticordia and a number of other Australian taxa (Howell et al. 1993; Ladd et al. 1999). Most Syzygium and Myrteae are bee-pollinated (Biffin et al. 2010a). See Keighery (1982) for pollination of Western Australian species of Myrtaceae.
Fleshy-fruited Myrtaceae are commonly dispersed by bats (Muscarella & Fleming 2008).
Staggemeier et al (2015b and references) looked at phenological patterns in Myrtaceae from the Atlantic forest of Brazil.
Plant-Animal Interactions. Myrtoideae are noted for the amount and diversity of the terpenes that they produce (Keszei et al. 2010), and these compounds were thought to be involved in defence against herbivores (Lawler & Foley 2002). However, they seem rather to be signalling compounds, and a variety of formylated phloroglucinol compounds, for the most part biosynthetically unrelated to terpenes, are actually involved in herbivore deterrence (Moore et al. 2004).
About half the galls on Australian plants have been recorded from Myrtaceae (Mani 1964). Thus Eriococcidae (scale insects) are widely distributed on Eucalyptus and other members of the family (Gullan et al. 2005). Another set of galls are found on species of Eucalyptus as well as other unrelated Australian Myrtaceae such as Syzygium, Melaleuca and the like. These genera are part of a three-way mutualistic association that also involves the actual gall-former, a nematode, Fergusobia, as well as a dipteran, Fergusonina, which the nematode parasitises for part of its life cycle and the larvae of which determine the internal structure of the gall (Taylor et al. 2005; Ye et al. 2007; Nelson et al. 2014). Although the relationship is often 1:1:1, deep cospeciation appears not to be involved, the stem age of Fergusoninidae being around 42 m.y.a., much younger than those of its hosts, however, lower-level cospeciation is possible (Nelson et al. 2014). This is a very interesting tritrophic association, however, little more than its outline is currently understood, and there may be several hundred different fly-nematode associations (Nelson et al. 2014).
Larvae of 90 or more species of pergid sawflies are found on Eucalyptus, far more species than are found on non-myrtaceous/rainforest plants (Schmidt & Walter 2014). Tortricine moths (Epitymbiini) larvae feed on Myrtaceae leaf litter in Australia, and some other moth groups are also foliovores on this family there (Powell et al. 1999). For the insects that eat Metrosideros, which has quite recently moved to Hawai'i, see Gruner (2004).
Bacterial/Fungal Associations. Dry-fruited Myrtoideae, including Melaleuca and Eucalyptus, are often ectomycorrhizal (e.g. Chilvers & Pryor 1965: many species of Eucalyptus; Smith & Read 1997; Tedersoo et al. 2008; Bâ et al. 2011a; see also Moyersoen et al. 2001). They are especially abundant in Australia, but although Brundrett (2009) estimated 1,800 species may be involved, little is known about the eco-physiological dimensions of these associations. ECM fungi found on Nothofagaceae and Myrtaceae, both southern groups, are similar, perhaps because ECM fungi moved from Nothofagaceae on to Myrtaceae as the climate became drier in the Tertiary (Tedersoo et al. 2008, 2014a). At least some species of Eucalyptus form both ecto- and endomycorrhizal associations (Adjoud-Sadadou & Halli-Hargas 2000; Kariman et al. 2012). Bacterial mycorrhization helpers are known for both ecto- and endomycorrhizal Eucalyptus ((Duponnois & Plenchette 2003).
Economic Importance. For Eucalyptus s.l., now widely grown for its timber and essential oils, see Coppen (2002).
Chemistry, Morphology, etc. For polyhydroxyalkaloid distribution (pyrrolizidine, pyrrolidine, and piperidine alkaloids), see Porter et al. (2000); they occur both in Psiloxylon and in some Myrtoideae. A number of Myrtoideae produce gums s.l. (these have been called kinos - Lambert et al. 2007b, 2013) and especially terpenes (Keszei et al. 2010), while some have high silica content in their leaves (Westbrook et al. 2009). Da Silva et al. (2012) noted that a diversity of colleter morphologies occurred in the family, although they did not record any colleters from Eucalypteae; see Pimentel et al. (2014) for colleters in the flowers.
Perianth parts of some Eucalyptus relatives may be undifferentiated and/or variously fused (e.g. Drinnan & Ladiges 1989a, b; Bohte & Drinnan 2005); circumscissile abscission of the hypanthium occurs in various ways. Androecial variation is extreme, even in quite closely-related taxa. Flowers with apparently oppositisepalous stamens are developmentally derived from an oppositipetalous androecium (see e.g. Carrucan & Drinnan 2000; Drinnan & Carrucan 2005; see also Orlovich et al. 1999 and references for floral development). Thornhill and Crisp (2012) discuss pollen evolution in the family. Johnson and Briggs (1984) emphasized the fully superior nature of the ovary in Psiloxyloideae (= their Psiloxylaceae), with its relatively narrow base, comparing it with the more or less inferior ovary of Myrtoideae (Myrtaceae), which always had a broad base. Pimentel et al. (2014) suggest that the inferior ovary in Myrteae may be either appendicular or receptacular (also placentae may be cauline or carpellary). There is considerable variation in ovule morphology (Bohte & Drinnan 2005), and the parietal tissue varies greatly in thickness (very thick in Eugenia - see van Wyk & Botha 1984); Corner (1976) described the micropyle as being exostomal; it is variable, but perhaps most commonly bistomal.
Seed coat (see also ovule) and embryo vary greatly, e.g. van Wyk and Botha (1984) and Biffin et al. (2006). Testa anatomy correlates with fruit type: capsular fruits have exotestal seeds; baccate fruits have seeds with a generally sclerotic testa. There is commonly a more or less elaborated basal portion of the hypocotyl that bears root hairs, however, in Angophora a broad, disc-like structure there is apparently devoid of such hairs (Baranov 1957).
For the phytochemistry of Heteropyxis, see Mohammed et al. (2009); the plant apparently lacks terpenes. Heteropyxideae are perhaps most similar to Myrtoideae-Leptospermeae; both wood anatomy (e.g. bordered pits) and pollen are like those of Myrtoideae (Stern & Brizicky 1958). The stamens have separate traces and the androecium shows no signs of being fasciated.
For general information, see Schmid (1980) and especially Wilson (2011), for inflorescence structure of Myrtoideae, see Briggs and Johnson (1979), for information on the very large genus Syzygium s.l., see Parnell et al. (2007) and Soh and Parnell (2011: leaf anatomy), for Heteropyxis, see Van Wyk (in Dahlgren & Van Wyk 1988), for Eucalyptus and immediate relatives, see McKinnon et al. (2008) and Brooker and Nicolle (2013: venation and oil glands), for Eugenia, see van Wyk and Botha (1984: seed coat, etc.) and van Wyk et al. (1980: cork cambium initiation) and other papers by van Wyk and collaborators, for terpenes in Australian Myrtaceae, see Keszei et al. (2008), for lamina anatomy of Brazilian Myrtoideae, see Cardoso et al. (2009), for filament curvature in Myrteae, see Vasconcelos et al. (2015: correlates with major clades), for a comprehensive pollen survey, see Thornhill et al. (2012b and references), and for embryology, in which there is considerable variation, see Mauritzon (1939a: integuments in bitegmic ovules consistently 2 cells across) and Narayanaswami and Roy (1960 and references).
Phylogeny. The limits of major clades (tribes) are similar in Wilson et al. (2005: matK) and Biffin et al. (2007: ITS), but the relationships between the clades are less so, although they are poorly supported. The capsular-fruited Myrtoideae are paraphyletic (Sytsma et al. 1998; Wilson et al. 2001; Salywon et al. 2002), while fleshy-fruited taxa (Myrteae, = the old Myrtoideae s. str.) are largely derived and monophyletic, although the large genus Syzygium s.l. represents an independant acquisition of fleshy fruits (see also Johnson & Briggs 1984); for relationships in these plants, see also Biffin et al. (2010a).
Within Myrteae, for relationships in Myrceugenia and its immediate relatives like Blepharocalyx, etc., see Murillo-A. et al. (2012, 2013). Mazine et al. (2014, see also Mazine Capelo et al. 2011) begin the task of disentangling relationships in the largely New World Eugenia; there are two major clades in the genus (see also Bernardini et al. 2014). The fleshy-fruited Myrcia is strongly paraphyletic and forms a large clade with i.a. Calyptranthes (Lucas et al. 2011, also Wilson et al. 2016; Santos et al. 2016), and Marlierea, which it also includes, is notably polyphyletic (Staggemeier et al. 2015a).
Eugenia (connate cotyledons, especially New World) and Syzygium (free cotyledons, Old World) were confused in the past; the two are not immediately related (see Schmid 1972 for a pre-molecular resolution of the problem). After disentangling the two, the relationships of Syzygium to genera like Acmena had to be worked out (Harrington & Gadek 2004: ?rooting). As Biffin et al. (2006, see also Biffin & Craven 2011) found, Acmena and Waterhousea are in a well supported clade along with Syzygium s. str., while admittedly poorly supported sister clades to this group are also largely made up of Syzygium.
Phylogenetic relationships around the Australian Eucalyptus s.l. are discussed by Parra-O. et al. (2009), Steane et al. (2011), Bayly et al. (2013a: chloroplast genomes), Rutherford et al. (2016), Jones et al. (2016: much low-level hybridization, species polyphyly, etc.), and references. Although Melaleuceae, another predominantly Australian group, are strongly supported as being monophyletic, the three main clades that make it up have high posterior probabilities but only moderate to low bootstrap support; most of the small genera previously recognised in this tribe fall into a single one of these clades, along with a group of species of Melaleuca s. str. (Edwards et al. 2010; see also Brown et al. 2001). See van der Merwe (2005) for relationships in Eugenia, mostly African, de Lange et al. (2010) for a phylogeny of the Antipodean Kunzea, and Pillon et al. (2015) for relationships in the largely East Malesian-Pacific Metrosideros, still poorly understood.
Classification. Myrtaceae s. str. (excluding Psiloxyloideae) were traditionally divided into Leptospermoideae - leaves spiral to opposite; fruit dry, dehiscent - and Myrtoideae - polyhydroxyalkaloids common; leaves opposite; terpenoid-containing glands in the apex of the connective, stigma dry; fruit fleshy, indehiscent. This distinction is untenable (see above). For a classification of Myrtoideae in which 15 tribes are recognized, see Wilson et al. (2005) and Wilson (2011)
Generic limits in Myrteae are problematic (Lucas et al. 2005, 2007; Wilson 2011). Thus the limits of and infrageneric groupings within Myrcia/Calyptranthes need attention (Lucas et al. 2011; Wilson et al. 2016), Myrcia is to be expanded and to include Marlierea as well (Staggemeier et al. 2015a). Biffin et al. (2006; see also Craven 2001; Biffin et al. 2007; Biffin & Craven 2011) suggest that Syzygium should be delimited broadly, at least pending a better understanding of the morphological variation of this clade; an infrageneric classification needed to be put in place, and if some of the groups were difficult to recognise, that of course would be true if Syzygium were split up and they were recognised as genera; Craven and Biffin (2010) provide an infrageneric classification, although since 80-90% of the species belong to subg. Syzygium, within which relationships are poorly understood, there is still plenty to do! Eucalyptus may be in the process of being dismembered (Parra-O. et al. 2009 and references). On the other hand, the limits of Melalauca are being expanded; if genera were segregated they would both be small and undiagnosable, distinctive characters being highly homoplastic in the group (Edwards et al. 2010). Generic limits in Chamelaucieae are in a state of flux (Rye 2015 and references). The limits of Neotropical Eugenia are best expanded (Mazune Capelo et al. 2011 for a summary). For a classification of the eucalypts, see Nicolle (2015).
Govaerts et al. (2008) provide a world checklist of Myrtaceae.
Botanical Trivia. Eucalyptus regnans, the snow gum, is the tallest known angiosperm, although in mass much less than Sequoia or Sequoiadendron (Cupressaceae). It may grow up to 101 m (ca 330 feet) tall, however, before the logging of the last century and a half there may have been individuals substantially over 400 feet tall (Carder 1995).
Thanks. I am grateful to Z. Rogers for discussion about Heteropyxis.
[Melastomataceae [Crypteroniaceae [Alzataeaceae + Penaeaceae]]]: (plants Al accumulators); (nodes swollen); branched or unbranched sclereids +/0 within same family; C clawed?; connective abaxially much expanded; endothecial thickening absent/atypical; nectary 0; exotestal cells ± longitudinally elongated.
Evolution: Divergence & Distribution. Estimates of the age of this node are (99-)91(-82) m.y. (Berger et al. 2015), ca 84 m.y. (Morley & Dick 2003), ca 82 m.y.a. (Sytsma et al. 2004), about 80 m.y.a. (Renner et al. 2001) or about 68.1/65.4 m.y. (Tank et al. 2015: Table S1, S2).
Chemistry, Morphology, etc. A number of taxa, but apparently not Melastomataceae, have more than a single branch from the leaf axil. Nodes other than simple unilacunar are quite widespread, however, a survey of nodal anatomy, particularly that of Melastomataceae, is much needed. The connective is least expanded in Penaeaceae - Rhynchocalyx. Endothecium evolution may be more complex than denotion of its absence as an apomorphy for the clade implies (Cortez et al. 2014; see esp. Melastomataceae).
Phylogeny. For relationships in this area, see Conti et al. (2002).
MELASTOMATACEAE Jussieu, nom. cons. Back to Myrtales
Trees or shrubs; (plants Al-accumulators); included phloem +; veins with terminal sclereids; (crystals/styloids +); leaves with 2 or 4 strong secondary veins, from (near) the base; K quincuncial, C contorted; anthers with branched vascular trace; carpels opposite petals, stigma punctate; outer and inner integuments ca 2 cells across; radicle bent.
170 [list]/5,105. Very largely tropical, also subtropical. Two main groups below, tribal characterizations in Melastomatoideae and generic synonymy under development!.
Age. Renner et al. (2001, also Renner & Meyer 2001) suggested that crown group diversification began about 53 m.y.a. and Wikström et al. (2001) offered the somewhat younger age of (51-)47, 41(-37) m.y., Morley and Dick (2003) suggested the substantially older date of ca 82 m.y.; dates suggested by Bell et al. (2010) are (65-)48, 41(-28) m.y., while Systma et al. (2004) suggested an age of ca 56 m.y. and Berger et al. (2015) an age (75-)64.5(-56) m. years.
1. Olisbeoideae Burnett
Libriform septate fibres 0; vessel ray pits half bordered; (nodes 1:3); sclereids, inc. terminal foliar sclereids + (0); crystal styloids + (0); petiole bundle(s) arcuate, annular; (leaf veins lacking fibrous sheath); stomata paracytic; plant usu. glabrous, (hairs uniseriate); stem apex frequently aborting, branching (complex) from previous flush; lamina vernation flat [Memecylon] or revolute [Mouriri], (secondary veins pinnate), stipules + [seedlings]; inflorescence often fasciculate, pedicels articulated; flowers small, 4(-5)-merous: (K imbricate), (truncate, C protective in bud - most Memecylon); A 2x K, dehiscing by pores to slits, anther endothecium + [cells thickened all around], connective with depressed elliptic oil-producing gland (0), (filaments straight in bud - Votomita); ovary inferior, placentation basal or parietal (axile, 2-, 4-locular), stigma wet; ovules 1-18(-many)/carpel, apotropous, (outer integument 4-5 cells across - Mouriri), parietal tissue ca 3 cells across; fruit a berry; seeds large, 1-5(-12), (some sclerotic hypodermal exotestal cells: Memecylon), exotegmen fibrous, massively sclerotic subhilum; embryo large (small), green, cotyledons thick, (large, ± crumpled - Memecylon); n = 7; hypocotyl elongated or not in germination, cotyledons lobed.
6/485: Memecylon (405), Mouriri (85). Tropical (map: from Morley 1976; Schatz 2001; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower, Fruit.]
Synonymy: Memecylaceae Candolle, Mouririaceae Gardner
2. Melastomatoideae Seringe
Acylated anthocyanins +; anthocyanins in the root tip; vessel-ray pit simple; (nodes 1:3; split laterals); cortical (and medullary) bundles +; lamina vernation conduplicate or supervolute, tertiary veins at right angles to the midrib, stipules 0; flowers ± monosymmetric by the androecium; heteranthy common; pollen 3-colporoidate; ovary superior to inferior, opposite sepals, often spaces between ovary wall and tube, placentation basal, axile, or parietal; ovule with nucellar cap; fruit dehiscing down its inferior part (capsule); seeds small, many, with hilar operculum, radicle in testal pocket, exotesta palisade to cuboid and lignified, (sclerotic mesotesta +), tegmen crushed; cotyledons often unequal.
182[list]/4570. Largely tropical and subtropical, esp. South America, although ca 400 spp. endemic to the Caribbean. [Photo - Flower, Fruit, Fruit.]
2A. Kibessieae Krasse
Small tree; cork cambium superficial; petiole bundle arcuate; stomata anomo-cyclocytic; hairs uniseriate; flowers 4-merous; endothecium restricted to inner wall of inner sporangium only; carpel orientation?, placentation parietal [ovary divided by septae]; capsule fleshy; n = ?
1/20: Pternandra (20). South Thailand, Malesia (map: based on Maxwell 1981).
[Astronieae + The Rest]: included phloem 0; petiole bundles variable; leaf veins lacking fibrous sheath; inflorescence often terminal; G developing before A; (K connate, calyptrate); anthers dehiscing by pores, endothecium 0; carpels opposite K.
2. Astronieae Triana
Shrubs to trees; petiole bundle complex, open; stomata mostly anomocytic; indumentum as peltate scales; (anthers opening by slits); carpels opposite petals; placentation basal to basal-axile.
4/150: Astronidium (70), Astronia (60). Indomalesia and Pacific.
The Rest: (cork cambium superficial); petiole bundle(s) arcuate or complex; stomata variable, poly- and cyclocytic, etc.; hair types very diverse, including short-stalked glands; lamina vernation (± curved), (margins serrulate), (stipuliform structures + - Tibouchina); (plant dioecious); flowers (3-)4-5(-10)-merous; K open [?level], (with alternating lobes); A (= and opposite sepals; = and opposite petals; many), (heteranthous), with pores, 3 middle layers of wall with thickened cells, connective with a basal appendage or not, (staminodes +); (nectar produced from stamens); tapetal cells uninucleate; G 2-many, placentation axile, (style hollow), (stigma capitate); ovule (1-few/carpel), micropyle zig-zag, outer integument 2-4 cells across, inner integument 2-3 cells across, parietal tissue 2-6 cells across, ?endothelium +, hypostase +: embryo sac long and thin, curved or not; fruit (baccate), (dehiscence irregular); cotyledons incumbent; n = (8-)9(-)12(-)17 (23, 31).
177/4,305: Medinilla (400), Tibouchina (245), Leandra (215), Sonerila (?180), Clidemia (120), Gravesia (105). Largely tropical and subtropical, esp. South America, and there esp. Colombia (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Quian & Ricklefs 2004; FloraBase 2007; Woodgyer 2007).
2. Henrietteeae Penneys, Michelangeli, Judd & Almeda
Medullary and cortical bundles 0; styloids +; (lamina margin serrate); inflorescence various, fasciculate, flowers axillary; K calyptrate to valvate; fruit a berry; n = 15, 20, 28.
3/77: Henriettea (67). S. Mexico to Bolivia and Brazil, the Caribbean.
2. Merianieae Triana
(Lianes; roots from internodal areas); (hairs with subulate cells, ± mesifixed).
Meriana (75), Graffenrieda (44).
2. Miconieae de Candolle
Miconia (1000 - Conostegia (75), Tococa (50)).
Synonymy: Miconiaceae Martius
2. Rupestrea Goldenberg et al.
K conspicuous; G semi-inferior; ovules 1/carpel; fruit indehiscent; seed cochleate, "orthocampylotropous"; n = ?
1/2. Atlantic Forest, Bahia, Brazil.
2. Microlicieae Naudin
K not conspicuous; seeds oblong-reniform, surface foveolate.
2. Rhexieae de Candolle
seeds cochleate, surgace complexly costate-tuberculate.
Synonymy: Rhexiaceae Dumortier
2. Melastomateae Bartling
(interxylary phloem + - Dissotis); seeds cochleate, surface tuberculate, hilar operculum round.
2. Blakeeae Bentham & J. D. Hooker
(Lianas); flowers usu. 6-merous; K usu with external projections, calyptrate, valvate (imbricate); n = ?
2/190: Blakea (180). Mexico (Chiapas to Bolivia and Brazil, Lesser Antilles, Jamaica.
Synonymy: Blakeaceae Barnhart
2. Cyphostyleae Gleason
(Herbs); (lamina venation pinnate); K calyptrate (not - Quipuanthus); A 5, opposite K; G inferior; fruit dry, breaking apart when seeds are released, (capsular); n = ?
4/21. Inter-Andean valleys from Colombia to Peru.
Age. Ages for taxa in this clade ([Medinilla [Rhexia + Tibouchina]]) in Rutschmann et al. (2004) were around 111.7-25.3 m.y., depending on fossil calibration and analytic techniques used.
Evolution: Divergence & Distribution. Renner et al. (2001, also Renner & Meyer 2001) thought that there was little substantial diversification within Melastomataceae until ca 30 m.y.a., and movement into Africa occurred still more recently some ca (18-)14(-10) m.y.a. Morley and Dick (2003), on the other hand, were inclined to think that the broad outlines of diversification in the family could be linked with major tectonic (drift) events, and there was much diversification within the family, including the separation of the African/Malagasy clades, before ca 68 m.y., roughly when Madagascar and India separated. Clearly, these are incompatible scenarios. Renner (2004a, b) again suggested that dispersal, not drift, was more likely, with separate Miocene dispersal events resulting in the species found on Madagascar, for example. Berger et al. (2015) date a shift in speciation rates in the family to after the divergence of Kibessieae, which they date to around 64 m.y.a., and place this in South America.
The North American Rhexia - well, North American now - occurs fossil (as the distinctive seeds) throughout Eurasia in the Caenozoic (Michelangeli et al. 2012 and references), which has important implications both for dating and biogeographical scenarios.
Melastomataceae s.l. are centered in the New World tropics where some 70% of the family is to be found, and there is a fair bit of geographical structuring of the major clades (see Reginato & Michelangeli 2015). Columbia alone has one third of the species and Brazil one half (Almeda et al. 2009). In Brazil, some 580 species (14% of the whole family), largely in nine major clades, are to be found in the Atlantic Forest (Michelangeli et al. 2015). 200 species of Microlicieae alone have radiated into the fire-prone Cerrado, crown group diversification being dated to ca 10 m.y.a. (Fritsch et al. 2004); other melastomes are also common there, and much diversification in this species-rich habitat began rather later, within the last 5 m.y. (Simon et al. 2009). Nearly all of the ca 215 species of Leandra are from eastern Brazil (Reginato & Michelangeli 2015). Bécquer-Granados et al. (2008) and Michelangeli et al. (2008b) discuss the complex biogeography of the speciose Antillean melastomes, while Goldenberg et al. (2008) find substantial geographical signal correlating with major clades in Miconia and its relatives - common in the family (e.g. Penneys & Judd 2005; Michelangeli et al. 2008b, 2012, 2013). Memecylon is particularly diverse in Madagascar, where there are large numbers of very localized species and about 140 species overall (Stone 2012).
For floral evolution in Leandra, see Reginato and Michelangeli (2016).
Ecology & Physiology. Melastomatoideae are an important component of the understory vegetation of tropical forests, especially in the New World; in Amazonian forests they are represented by a large number of species with stems at least 10 cm across, but none is common (ter Steege et al. 2013); species are also quite often early successional. Woody epiphytes are quite common in Melastomatoideae, for example in the palaeotropical Medinilla (e.g. Benzing 1990), and in the New World are particularly common in montane habitats. New World epiphytic melastomes may have distinctive anatomical traits that can be connected with water stress, but they do not have CAM photosynthesis (Ocampo & Almeida 2013b). Some species are scramblers, whether with hook-shaped roots, or climbing by roots that attach directly to the support; some of the latter taxa have pseudo-2-ranked leaves, one leaf of the pair being much reduced (see Zeigler 1925; Clausing & Renner 2001a; Gamba-Moreno & Almeida 2014 for anisophylly).
The family is overwhelmingly mesophytic, but most Microlicieae, along with a few other species, are adapted to the seasonally dry and fire-prone Cerrado vegatation of Brazil (Fritsch et al. 2004; Simon et al. 2009).
In Brazil, at least, apomictic species are disproportionally likely to be pioneers or invasives (dos Santos et al. 2012).
Pollination Biology & Seed Dispersal. Monosymmetry of the flower is most evident in the androecium, and the stamens, often distinctively different in colour from the petals, may form a serried rank on one side of the flower. The petals of Melastomatoideae are usually more or less widely spreading, and buzz pollination is common, flowers being visited by females of many species of bees in search of pollen (Renner 1989; Harter et al. 2002). Different species of bees tend to visit different species of Melastomataceae, although the bees involved are not oligolectic; thus mass-flowering Miconia cinerascens in Brazil is visited by the stingless Melipona (Harter et al. 2002) which also visits other plants. In Brazil, widespread and sometimes very extensive damage to the anthers was caused by pollen-robbing Trigona bees (Renner 1983). Goldenberg et al. (2008) suggest quite complex relationships between anther morphology and pollinator in Miconia and relatives, and in Andean Miconia, not only has there been independent evolution of broader anther pores, but also white anthers (from variously coloured), dioecy, and polysymmetric flowers (Burke et al. 2012). It has been suggested that buzz-pollinated Melastomataceae and their pollinators are trapped on an adaptive peak (Berger et al 2015) - see also Solanaceae, Malpighiaceae - but certainly in terms of overall diversification the trap would seem to be quite pleasant.
Some Melastomataceae have nectariferous anther connectives, the nectar exuding through cracks in the tissue or through stomata (Blakaea, Penneys & Judd 2013b), or nectar is produced on the corolla (Medinilla), hypanthium, or even on the stigma or on top of the ovary (some Miconia), and in these cases the contorted petals form a tube and anthers often open by longitudinal slits (although lacking an endothecium?). Here pollination is likely to be by birds and perhaps rodents (Renner 1989; Stein & Tobe 1989; Vogel 1997; Varassin et al. 2007, esp. 2008; Penneys & Judd 2013b). Pollination by tanagers has recently been demonstrated in Axinaea where the birds eat a sucrose-rich appendage on the anthers which also acts as bellows, pollen being puffed out the anther pores and dusting the the bird's head at the same time (Dellinger et al. 2014). Axinaea grows at 1000-3600 m in the Andes, and some other Melastomataceae from higher altitudes have also adopted vertebrate pollination and produce nectar as a reward (Varassin et al. 2008; Dellinger et al. 2014 and references; Brito et al. 2016).
In many Olisbeoideae oil is the reward for the pollinator. There genera of Centridini, Exomalopsini, Euglossini and Tetrapedini collect exudate from the oil-producing anther glands, also collecting pollen by buzz pollination. Flowers with these glands (the great majority of species) are blue, rarely yellow, flowers without them are white (Buchmann & Buchmann 1981; Buchmann 1987), however, there is much infraspecific variability in flower colour (Morley 1976).
Apomixis/polyembryony is common in Melastomataceae from Cerrado and Campo Rupestre vegetation types in Brazil, where it has been found in about one third of the species; apomixis was more common in the widely-distributed species (dos Santos et al. 2012; Rodrigues & Oliveira 2012). In Miconieae, apomictic species were little visited by pollinators (Brito et al. 2016). For apomixis - and also hybridization - in Leandra, see Reginato and Michelangeli (2015).
Within Melastomatoideae, capsular fruits are linked with superior ovaries and fleshy fruits with inferior ovaries, although this is not an absolute correlation. Fleshy fruits have arisen more than once, and in both the Old and New Worlds. Throughout the Neotropics fruits of Melastomatoideae are a major resource for frugivorous birds, smaller species in particular (Stone 1981). Thus fleshy fruits of Miconieae in the Colombian Andes comprise about 11.5% by weight of fleshy fruits but ca 32% of all fruit eaten by birds (Kessler-Rios & Kattan 2012). Taxa with fleshy fruits and small seeds are much eaten by tanagers, which, being "mashers", tend to remove seeds more than 2 mm long before swallowing the fruit, while manakins, "gulpers", eat fruits with larger seeds and gulp the fruit whole; both groups of birds are restricted to the New World (Stiles & Rosselli 1993; see also Renner 1986)). The sugar-rich fruits of the largely aseasonally-fruiting Melastomatoideae in the understory of Malesian forests are an important food source for the birds there (Leighton & Leighton 1983), and the Old-World Melastoma has fruits which dehisce to expose mounds of small seeds with fleshy testas that are eaten by birds. Olisbeoideae have fleshy fruits, but with few and larger seeds.
In the New World, taxa with dry fruit tend be commoner at higher altitudes and in savannas and more seasonal forests (Stiles & Rosselli 1993). A few taxa with dry, dehiscent fruits do have inferior ovaries, and there the outer fruit wall may fall away, the fruit proper then functioning as an ordinary capsule (Michelangeli et al. 2008a); a group of these genera form a clade (Michelangeli et al. 2011: they also have stamens opposite the sepals).
Flowers of Miconia sect. Cremanium, whose stomatiferous anthers have broad pores, are visited by a variety of pollinators, and here generalist pollination is derived from more specialized buzz pollination (Kriebel & Zumbado 2014). Indeed, in Miconieae as a whole generalist pollination, in which flies are involved, has evolved several times from specialist pollination, in which wasps and/or bees alone are involved. In turn generalist pollination is linked with short anthers, large anther aperture, nectar as a reward, altitude, and also with seed size, flowers pollinated by generalists tending to have fruits with fewer, larger seeds (Brito et al. 2016).
Plant-Animal Interactions. Clidemia heterophylla and species of Tococa like T. guianensis in western Amazonia live in close association with the ant Myrmelachista which creates mono- or oligospecific "devil's gardens" by injecting formic acid into the leaves of the surrounding vegetation, which is thus suppressed (Morawetz et al. 1992; Frederickson et al. 2005; Salas-Lopez et al. 2014). Bacteria livING off colony debris in Tococa may be eaten by rhabditid nematodes that are possibly in turn eaten by the ants (Maschwitz et al. 2016). Petiolar or laminar ant domatia are quite common in Blakeeae and Miconieae; in Maieta guianensis ca 80% of the host plant's nitrogen is derived from the waste deposited by the ant Pheidole minutula that lives in the domatia (Solano & Dejean 2004). Chomicki and Renner (2015: fig. S10) estimate that there may have been eight gains of myrmecophily in Miconieae alone, and almost as many losses.
Chemistry, Morphology, etc. The roots have anthocyanins. Poay et al. (2011) described galloylated cyanogenic glucosides from Phyllogathis. For wood anatomy, see van Vliet et al. (1981); vessel:ray pits are simple. Within Olisbeoideae, vessel:ray pits are half bordered, and the rays are 2-5 cells wide and heterocellular, compared to 1(-4) cells wide and homocellular elsewhere in this clade. For foliar sclereids, see Rao (1957, 1983). A survey of nodal anatomy is needed; split laterals are probably quite common (pers. obs., see also R. A. Howard in van Vliet & Baas 1975), and cortical bundles running along the raised angles of the stem are also to be found. In Dissochaeta and Pternandra there is a prominent interpetiolar flange below the leaves. Vernation may seem to be plicate because the secondary veins are so prominent; the leaves of Mouriri remain folded as they elongate.
Little is known about floral development, although Wanntorp et al. (2011b) studied that of Conostegia, in which there has been increase in floral meristicy, and some other genera; stamen primordia opposite the petals may split. The floral vasculature of Mouriri is distinctive (Morley 1976). Venkatesh (1955) found that the anthers of Memecylon had a normal endothecium, while in those of Mouriri the walls of the cells of the hypodermal layer were thickened all around. In Miconia, at least, the anther epidermis has a thick cuticle, except that in the pore area, which lacks a cuticle (Cortez et al. 2014). Anthers and anther wall development in Miconia are very diverse, some species having bisporangiate anthers, monocot wall development, crystals in the tapetal cells, etc. (Cortez et al. 2015). For the development and anatomy of the fleshy fruit of Miconia, see Cortez and Carmello-Guerreiro (2008). The seed coat may vary considerably, but with little phylogenetic signal (Ocampo & Almeda 2013a).
Much other information is taken from Morley (1976: Olisbeoideae), Renner (1993) and Jaques-Félix (1995: African Melastomataceae). For anatomical studies, see van Tieghem (1891a, b); for floral morphology, embryology and much else, see Zeigler (1925), for ovules and embryology, see Subramanyam (1942, 1949), for seed morphology, see Groenendijk et al. (1996: Miconia) and Martin and Michelangeli (2009: Leandra), and for ovules and stamens, see Zeigler (1925). For general information, see Penneys (2004 onwards) Melastomataceae of the World.
Phylogeny. Mouriri + Memecylon are sister to Pternandra, in turn sister to the rest of the family in ndhF trees (Renner 1993); Morley (1953, 1976) had early suggested this general relationship. For a molecular phylogeny, see Clausing and Renner (2001: also morphology; Renner et al. 2001; Renner 2004b). Pternandra is sister to all other Melastomatoideae, Astronieae perhaps next (Clausing & Renner 2001: moderately good support in a 3-gene analysis; Renner 2004b). However, in a recent chloroplast genome analysis Henriettea (Henriettieae) was sister to the 15 other Melastomatoideae included, which represented most major clades (Reginato et al. 2016). A clade that included Merianieae and Miconieae was stable, and was sister to clade in which Bertolonieae were sister to a group that included Melastomeae but in which relationships were not entirely stable (Reginato et al. 2016). These relationships are quite similar to those in Michelangeli et al. (2014) and Oldenberg et al. (2015). However, in the latter in particular Henriettieae associated with Astronieae while the odd genus Rupestrea, there newly described, was strongly supported as being sister to a clade that included Microlicieae, Rhexieae, and Melastomeae, although more detailed relationships in that clade were not well supported (Oldenberg et al. 2015).
Within Olisbeoideae, Spathandra is probably sister to the large, paleotropical Memecylon, although support is weak and it sometimes links with the [Votomita + Mouriri] clade, Lijnedia and Warneckia are successively sister to the whole group, although sometimes the two form a single clade (Stone 2006; Stone & Andreasen 2010). All six morphologically-based genera of Olisbeoideae have molecular support (Stone 2006). Within Memecylon, the small African subgenus Mouriroidea is sister to the rest (Stone 2014), although branch lengths along the spine of the phylogeny tend to be short.
For a phylogeny of the fleshy-fruited, speciose, and paraphyletic Miconieae (Melastomatoideae), see Michelangeli et al. (2004), Martin et al. (2008) and Majure et al. (2015); genera and sections are not monophyletic, in part because of over-reliance on anther morphology for providing characters to delimit taxa (Goldenberg et al. 2008; Burke et al. 2012). Gamba-Moreno and Almeida (2014) look at relationships in the Octopleura clade here. Judd (1989) and Judd and Skean (1991) provide morphology-based phylogenetic analyses of axillary- and terminal-flowered Miconieae respectively. For relationships in a somewhat expanded Conostegia, see Kriebel et al. (2014: variation in position of major clades, nice morphology) and for those in the speciose Leandra, see Reginato and Michelangeli (2015). Generic limits in Merianeae are difficult (Schulman & Hyvönen 2003); Michelangeli et al. (2012) looked ar relationships within the New World Melastomateae and Penneys and Judd (2013b) analyzed both molecular and morphological characters in Blakeeae. For the polyphyletic Leandra, see Martin et al. (2008), and for the African-Madagascan Warneckea, see Stone and Andreasen (2010). Recent broad studies in neotropical melastomes provide an inkling of the new relationships (Guimaraes et al. 2010; Penneys & Judd 2010, esp. 2011: 111 morphological characters; Judd et al. 2010).
Classification. The inclusion of Memecylaceae in Melastomataceae was an option in A.P.G. II, and this was formalized in A.P.G. III (2009). Sampling of New World taxa of Melastomatoideae in particular is rapidly being extended and so needed generic and tribal changes are beginning - e.g. Penneys et al. (2010: Henrietteeae), Michelangeli et al. (2011: Cyphostyleae), Penneys and Judd 2013a (Blakeeae), and Schulman and Hyvönen (2003: Merianeae). For genera in Miconieae, see Goldenberg et al. (2008 and references); Majure et al. (2013) discuss the homoplasy of previously-used "generic" characters and argue for a broadly delimited Miconia (see also Majure et al. 2015).
For names in the family, see MEL names (Renner et al. 2007c).
Thanks. I am grateful to S. Renner for comments.
[Crypteroniaceae [Alzateaceae + Penaeaceae]]: vessel-ray and vessel-parenchyma pits half bordered; foliar sclereids +; stipules minute; stamens = and opposite petals; endothecium ephemeral; fruit a loculicidal capsule; endotegmen not fibrous.
Age. Renner et al. (2001) thought that the age of this node was only ca 21 m.y. and Tank et al. (2015: Table S2) about 39.8 m.y., while Conti et al. (2002: calibration in part circular, based on drift events) estimated it at 141-106 m.y. ago. The crown group estimate in Moyle (2004) was (78.6-)68(-57.4) m.y., and that in Morley and Dick (2003) was ca 68 m.y.; ca 52 m.y. was the estimate in Sytsma et al. (2004) and (66-)53(-40) m.y. that in Berger et al. (2015). Rutschmann et al. (2004) used a variety of analytic methods, and the ages they obtained spanned almost all others, around (152.6-)109-58.9(-35.9) m. years.
Evolution: Divergence & Distribution. Renner et al. (2001) thought that the dispersal was responsible for the distributions of taxa in this clade, while Conti et al. (2002) thought that many of the distribution patterns reflected vicariance events, specifically continental drift (see also Morley & Dick 2003).
Chemistry, Morphology, etc. Details of internal exine structure of Alzatea are similar to those of some Crypteroniaceae. Laterocytic stomata are known i.a. from Alzatea, Dactylocladus, and Rhynchocalyx (Baranova 1983). For pollen of much of this group, see Muller (1975), for anatomy - very variable - see van Vliet and Baas (1975: detailed comparison within Myrtales), for gross morphology, see van Beusekom-Osinga and van Beusekom (1975), and for perianth morphology, see Schönenberger and von Balthazar (2006).
Phylogeny. Some of the relationships within this clade are only weakly supported (see Schönenberger & Conti 2003 for phylogeny and floral evolution of the whole group).
Classification. Van Beusekom-Osinga and van Beusekom (1975) included Alzateaceae and Rhynchocalycaceae in their expanded Crypteroniaceae. However, great expansion was deemed too radical, but Penaeaceae has been moderately broadened to include Oliniaceae and Rhynchocalycaceae (A.P.G. III 2009).
CRYPTERONIACEAE A.-L. de Candolle, nom. cons. Back to Myrtales
Trees; plants Al-accumulators; cork also subepidermal; septate fibres 0, fiber tracheids +, pits bordered; nodes 3:3 [by split laterals], 1:3 with girdling bundles, cortical bundles ± developed or 0; sclereids +/0; petiole bundles annular (with medullary trace) or arcuate, wing bundles +; stomata paracytic (anomocytic - Dactylandra); plant glabrous (hairs unicellular); lamina with secondary veins pinnate to palmate; plant polygamodioecious, or flowers bisexual; inflorescence racemose (spicate), with long branches; flowers 4-5-merous; C 0, 4-5; (A 2x K), connective thickened apically or not; (pollen bisyncolporate); G [2-6], ± inferior, placentation parietal or basal, (transseptal bundles +), style usu. slender, stigma capitate; ovules 1-3 or many [Cryteronia]/carpel, parietal tissue 2 cells across, nucellar tissue disintegrates early, (endothelium + - Axinandra); fruit a capsule, flattened or not, K deciduous; seeds winged, exotestal cells elongated, endotesta crystalliferous, endotegmen tanniniferous, other layers ± degenerate; n = 8.
3 [list]/10. South East Asia, Malesia, Sri Lanka (map: from van Beusekom-Osinga 1977).
Age. Conti et al. (2002, see also Conti et al. 2004; Rutschmann et al. 2004, esp. 2007) suggested an origin any time from the Early to Late Cretaceous, a later date being favoured (60-45 m.y. in Conti et al. 2002). Again, crown-group estimates in Moyle (2004) are much younger (48.6-)39(-29.4) m.y., while those in Rutschmann et al. (2004, see also 2007) were 82.6-17.9 m.y..
Evolution: Divergence & Distribution. Conti et al. (2002, see also Conti et al. 2004; Rutschmann et al. 2004, esp. 2007) suggest that Crypteronia and relatives rafted from Gondwana (Africa) to Asia via India. For Moyle (2004), drift would not be involved
Chemistry, Morphology, etc. Some information on Crypteronia and relatives is taken from Tobe and Raven (1983b, 1987b, c) and Renner (2006b: general).
Phylogeny. Dactylocladus is sister to the other two genera, but with only weak support (Conti et al. 2002).
Synonymy: Henslowiaceae Lindley
[Alzateaceae + Penaeaceae]: style stout.
Age. Ages for this node in Rutschmann et al. (2004) were around (135.6-)92.4-53(-26) m.y..
ALZATEACEAE S. Graham Back to Myrtales
Trees or shrubs; plants not Al accumulators, myricetin 0; vessel-ray and vessel-parenchyma pits simple; septate fibres +, fibre pits barely bordered; branches tending to be several together; nodes 3:3, cortical bundles +; sclereids +; petiole bundle annular and with wing bundles; stipules 0; flowers small, 5(-6)-merous; K pointed in bud, C rudimentary even in bud; anther thecae along apical margin of connective, connective wide, with backwards-directed appendage, filaments short; pollen pseudocolpi 0 [faint]; G , placentation intrusive parietal and with an incomplete septum, transseptal bundles +, stigma capitate; ovule many/carpel, micropyle endostomal; megaspore mother cells several, embryo sac bisporic [chalazal dyad], eight-celled [Allium-type]; capsule flattened, K persistent; seeds several, winged all around, with hair-pin bundle; exotestal cells low, with irregularly sinuous anticlinal walls, everything else collapsed; suspensor small; n = 14.
1 [list]/?2. Costa Rica to Peru (map: see Silverstone-Sopkin & Graham 1986). [Photo - Flowers.]
Evolution. Bacterial/Fungal Associations. Alzatea is reported to have ectendomycorrhizae - i.e. there is both a Hartig net and arbuscules formed by a glomeromycete (Peterson 2012 and references).
Chemistry, Morphology, etc. See Graham (1985, 2006) for general information on Alzatea.
PENAEACEAE Guillemin Back to Myrtales
Trees or shrubs; lamina with "glandular" tip; parietal tissue 3-4 cells across; x = 10.
9 [list]/29. E. and S. Africa, overwhelmingly South African, and St Helena. 3 groups below.
1. Rhynchocalyceae Beusekom
Myricetin 0; septate fibres +, fibre pits barely bordered; branches tending to be several together; plants Al accumulators; cork cortical; petiole bundle arcuate, sclereids + [not in stem?]; stipules colleter-like; flowers 6-merous; K pointed, C lobed; A loculi all opening separately, epidermis only persisting; G [2 (3)], placentation parietal, transseptal bundles +, stigma ± punctate; ovules many/carpel, micropyle endostomal, nucellar cap ca 3 cells across; megaspore mother cells several; capsule flattened; seeds several, winged, embryo basal; exotesta tanniniferous, outer wall lignified, all coat cells persist.
1/1: Rhynchocalyx lawsonioides. South Africa, coastal Natal and Transkei.
Synonymy: Rhynchocalycaceae L. A. S. Johnson & B. G. Briggs
[Penaeeae + Olinieae]: plants not Al accumulators; non-hydrolysable tannins +; hypanthium well developed, pollen grains psilate, foot layer and tectum thick; exotegmen fibrous; embryo suspensor 0.
2. Penaeeae A. de Candolle
Small ericoid shrubs; libriform septate fibres 0; mesophyll with (spirally thickened) fibres; leaves often sessile, (lamina lacking "glandular" tip), stipules ± colleter-like; flowers axillary, 4-merous; K petal-like, C 0; (connective with branched vascular bundle), (filaments straight in bud); G 4, opposite petals, style also filiform, stigma capitate or lobed; ovules 2-4/carpel, parietal tissue ca 3 calls across, chalazal nucellar region massive; embryo sac tetrasporic, 16-celled [Penaea type]; seeds with funicular elaiosome; exotestal cells much developed or endotestal cells much elongated, other layer crushed, endotegmen fibrous[?]; endosperm pentaploid, chalazal ["basal"] endosperm haustorium +, suspensor 0, embryo with large hypocotyl, cotyledons tiny.
7/23: Stylapterus (8). South Africa, S. and S.W. parts of the Cape. [Photo - Habit.]
Synonymy: Plectroniaceae Hiern
3. Olinieae Horaninow
Cork subepidermal; cyanogenic compounds +; veins with terminal sclereids; stomata variable; stipules cauline-on leaf base; flowers (4-)5-merous; ?epicalyx +, small, K ± spatulate, C concave, thick ["scale-like"], hairy; filaments very short; pollen heteropolar; G [(2-)4-5], inferior, opposite sepals, transseptal bundles +, stigma ± clavate, (commissural); ovules 2-10/carpel, apo-/orthotropous, campylotropous, outer integument 3-5 cells across, chalaza strongly vascularized, hypostase +; fruit drupaceous, 1-seeded, K not persisting; exotegmic cells fibrous; cotyledons spirally twisted or irregularly folded; n = 12, ?15, ?20.
1/5. Africa, St. Helena (map: from Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Fruit, Flowers.]
Synonymy: Oliniaceae Harvey & Sonder
Evolution. Pollination Biology & Seed Dispersal. Penaeeae often have ant-dsipersed seeds (Lengyel et al. 2010).
Chemistry, Morphology, etc. The vegetative anatomy of Penaeeae is undistinguished, but their embryo sac is unique. Nectar is secreted from the base of the hypanthium. Crushed or broken plant parts of Olinieae smell of almonds; they contain the cyanogenic glucoside, prunasin. The ovules have been reported as being apotropous and ascending (Baillon 1877). The interpretation of the perianth of Olinia is a matter of some dispute; here I follow Schönenberger and Conti (2003) although the exact nature of the outer whorl of very small appendages is still unclear (described as "?epicalyx" above). The haploid chromosome number of Olinia is 12, according to Takhtajan (1997), but c.f. Goldblatt (1976).
See Van Wyk (in Dahlgren & Van Wyk 1988) for general information, Schönenberger (2006: Rhynchocalyx), Schönenberger et al. (2006: Penaea), etc., and von Balthazar and Schönenberger (2006: Olinia); for embryology, see Tobe and Raven (1984b, c, 1985b) and Stephens (1909b), and for the embryo suspensor of Penaea and relatives, see Ross and Sumner (2005) and Stephens (1909b).
Phylogeny. M. Sun et al. (2016) found that a clade [Olinia + Rhynchocalyx] was weakly supported as sister to the rest of the family.