EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; 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; mblepharoplast +, 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, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [= MicroTubule Organizing Centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; 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 dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening]; stomata numerous, involved in gas exchange.
II. TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia 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; archegonia embedded/sunken [only neck protruding]; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome size [1C] = 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
SEED PLANTS† / SPERMATOPHYTA†
Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; 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], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ - zeta - duplication], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating from inner layer of root cap, trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P = T, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (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 gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [2C] (0.57-)1.45(-3.71) [1 pg = 109 base pairs], ??whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast 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]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0 [or next node up]; fruit dry [very labile].
EUDICOTS: (Myricetin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; 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], x = 21, 2C genome size (0.79-)1.05(-1.41) pg, PI-dB motif +; small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = K + C, K enclosing the flower in bud, with three or more traces, C with single trace; A = 2x K/C, in two whorls, internal/adaxial to C, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], whorled, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression.
[BERBERIDOPSIDALES [SANTALALES [CARYOPHYLLALES + ASTERIDAE]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[SANTALALES [CARYOPHYLLALES + ASTERIDAE]]: ?
[CARYOPHYLLALES + ASTERIDAE]: seed exotestal; embryo long.
ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; if nectary +, gynoecial; G , style single, long; ovules unitegmic, integument thick [5< cells across], endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
Age. This node can be dated to around 127 Ma (K. Bremer et al. 2004a). Janssens et al. (2009) gave a date of 123±10.5 Ma, Lemaire et al. (2011b) one of (132-)128(-124) Ma, Tank and Olmstead (pers. comm.) one of (136.9-)121.8(-107) Ma and Foster et al. (2016a: q.v. for details) an age of (124-)116(-108) Ma, while Moore et al. (2010: 95% highest posterior density) suggest substantially younger ages of (85-)81(-76) Ma, Bell et al. (2010) ages of (116-)108, 99(-93) Ma, Tank et al. (2015: Table S1) an age of ca 98.8 Ma, Magallón and Castillo (2009) and Magallón et al. (2013) an age of around 105.3 Ma, Hoshino et al. (2016) an age of ca 105.8 Ma, and Magallón et al. (2015) an age of 112.3 My; 132.6-122.1 Ma is the age in Nylinder et al. (2012: suppl.), ca 137 Ma in Z. Wu et al. (2014) and (126-)123(-113) Ma in Wikström et al. (2015).
Evolution: Divergence & Distribution. Endress (2011a) suggested that a key innovation at this level was sympetaly, although it is placed at the asterid node for the time being. There is extensive variation in corolla development in Ericales and Cornales in particular, but perhaps also in the (ex-)Icacinalean woody clades at the base of the lamiids and campanulids (see elsewhere). Zhong and Preston (2015) discussed the development of sympetaly, distinguishing between the lower corolla tube, which comes from the elongation of common petal/stamen bases, and the upper corolla tube, often with postgenital fusion.
Sympetalae of older studies were defined largely by their sympetalous corolla, but some families here included in the asterids, perhaps particularly in some of the basal clades, seem to be polypetalous. However, developmental studies like those of Erbar (1991) suggest that at least some apparently polypetalous taxa have a ring primordium very early on (see, for example, Reidt & Leins 1994), i.e., they show early sympetaly. (It is somewhat paradoxical that early corolla tube formation should quite often be linked with a corolla that appears to have separate petals at maturity!) However, the position of early initiation of the corolla tube on the tree is quite uncertain. Apiales, Asterales, and Dipsacales have many members with such initiation, as do both Oleaceae and Rubiaceae, "basal" or almost so in their orders in the lamiids, and also some Cornales (see Erbar & Leins 2011 for a recent survey). Sampling still leaves much to be desired, but the condition of early initiation could conceivably be a synapomorphy for the asterids (see Erbar & Leins 1996b; Leins & Erbar 2003b for more details), even if the basic condition could be flowers in which the petals were functionally ± free, at least at anthesis. There may be an association between early corolla tube formation and flowers with an inferior ovary (Ronse Decraene and Smets 2000) and families like Oleaceae with superior ovaries and apparently early corolla tube formation need more study from this point of view, and the character needs re-evaluation. Only in many Ericales and other asterids does the mature flower have a decided corolla tube, hence the tentative assignment of posession of a corolla tube as an apomorphy for [Ericales + other asterids] - but see Stull et al. (2018); taxa with a pronounced corolla tube quite often have late corolla tube initiation, the petal primordia initially being free.
ERICALES Dumortier - Main Tree.
Woody; nonhydrolysable tannins, triterpenoids incl. saponins +; vessel elements with simple perforation plates; nodes 1:1; leaves spiral, teeth with single vein and opaque deciduous cap; sepals persistent in fruit; duplication of the PI gene. - 22 families, 346 genera, 11,705 species.
Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the 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).
Age. Sytsma et al. (2006) proposed that diversification of Ericales began 109-103 Ma, Rose et al. (2018) put the time at ca 110 Ma, Wikström et al. (2001: note topology) offered an age of (97-)92, 85(-80) Ma, Anderson et al. (2005) an age of 103-99 Ma, while Janssens et al. (2009) dated the crown group to 117±9.2 Ma and K. Bremer et al. (2004a) to 114 Ma. Soltis et al. (2008: a variety of estimates) suggested an age of (126-)113(-85) Ma, Magallón and Castillo (2009) one of ca 98.85 Ma, Bell et al. (2010) an age of (102-)92 Ma, Shenk and Hufford (2010) an age of 100.7-87 Ma, Tank and Olmstead (pers. comm.) an age of (101.4-)96.2(-92.4) Ma, and Lemaire et al. (2011b) an age of (125-)118(-110) My; around 103.6 Ma is the age in Magallón et al. (2015) and (117-)109(-100) Ma in Wikström et al. (2015).
The fossil Archaeamphora was assigned to Sarraceniaceae and was described from rocks about the same age as those in which Archaefructus was found, i.e. ca 124 Ma (Li 2005), although it is probably a conifer gall (Herendeen et al. 2017 for literature). Otherwise the oldest fossils assignable to Ericales are in rocks ca 90 Ma old (Crepet et al. 2004; see also Martínez-Millán 2010). Indeed, in the late Cretaceous of E. North America there is a great diversity of fossil flowers that may belong to Ericales (Crepet et al. 2001, 2004; see also Herendeen et al. 1999; Friis et al. 2011). Some of these fossil flowers are quite unlike extant members of the clade, e.g. some have sepals with numerous huge abaxial and/or marginal glands (Crepet 2008), or are covered with scales on the outside, scales which also cover the gynoecium, the tiny flowers having the rather odd floral formula ↑ K  valvate; C 5; A 8 + 8 nectariferous staminodes; G  (Crepet et al. 2018: Teuschestanthes). This plant, from rocks some 90 Ma, comes out around Cyrilla and Clethra in morphological analyses, although with little support; note that its flowers are drawn inverted (Crepet et al. 2018). Schönenberger and Friis (2001) described Paradinandra from the Late Cretaceous of Sweden, and this has a number of Ericalean features, some suggesting relationships with Pentaphylacaceae in particular (perhaps the relationships could more accurately be described as being with Ericales minus the Balsaminaceae and Polemoniaceae clades). Its placentation was intrusive parietal, the pollen was tricolpate, and there was a nectary disc around the base of the ovary; there were paired stamens opposite the petals and single stamens opposite the petals, as in some Sapotaceae, Ebenaceae, Styracaceae, Pentaphylacaceae and perhaps even Actinidiaceae (see also Friis 1985: ?Diapensiaceae; Keller et al. 1996: ?Actinidiaceae; Martínez-Millán et al. 2009: ?Pentaphylacaceae). Tricolpate pollen is uncommon in extant Ericales, being known only from Lecythidaceae and Balsaminaceae.
Evolution: Divergence & Distribution. For a good summary of the diverse Late Cretaceous fossils assigned to the order, see Friis et al. (2011).
Magallón et al. (2018) suggested that there was an increase in diversification at this node and dated it to (112.3-)107.8(-103.6) Ma.
Sytsma et al. 2006 (see also Magallón et al. 2015; Wikström et al. 2015) thought that almost all families in Ericales had diverged by the early Eocene 50 Ma. However, Rose et al. (2018) found that all families had separated by ca 79 Ma in the Late Cretaceous. Interestingly, stems of the 22 families of the order were ca 20 Ma or more, and over 50 Ma for Symplocaceae, with the exception of Ericaceae, with a stem of less than 2 Ma, and Clethraceae, Balsaminaceae and Sladeniaceae, all with stems of ca 10 Ma. Small, species-poor clades with long stem branches are commonly sister to more speciose clades (Rose et al. 2018). Rose et al. (2018) discuss many other aspects of diversification - clade ages (some have been added below), diversification rate changes (many) and biogeography - and their paper should be consulted for details.
Chartier et al. (2017) looked at how clades (families, groups of families) occupied the total floral morphospace of the order, a morphospace (≡ morphological diversity, disparity) defined by variation in 37 floral characters. They found that, somewhat to their surprise, androecial characters contributed most to this disparity, androecial variation being particularly extensive in Lecythidaceae (see also below). The seven family groups (e.g. Ericaceae + Clethraceae + Cyrillaceae) plus three isolated families (e.g. Theaceae) tended to be in different areas of this morphospace, although overall it was more or less continuous, the ten clades just mentioned occupying adjacent areas (Chartier et al. 2017). Four families, Lecythidaceae, Ericaceae, Sapotaceae and Primulaceae together contributed ca 50% to the total disparity in the order (Chartier et al. 2017) - but those families include ca 2/3 of all ericalean species.
Ericales are an important component of the diversity of the understory in tropical rainforests and contain ca 5.9% of eudicot diversity (Magallón et al. 1999), however, one third of the order is made up of Ericaceae alone, not a noteworthy component of such rainforests (see below).
Schönenberger et al. (2005) examined character evolution in Ericales, which perhaps is beginning to make some sense, although there is extensive homoplasy and relationships still need to be clarified (see below). For pollen evolution, see Y. Yu et al. (2018).
Ecology. Ericales are important in the understory in tropical rainforests, including ca 10% of the species and some 22% of the total stems (Davis et al. 2005a); families like Sapotaceae, Lecythidaceae and Ebenaceae are involved. This forest may have developed only early in the Caenozoic (Burnham & Johnson 2004), when the clades now making it up initially diverged; members of Malpighiales are the other main component of this vegetation. Lens et al. (2007b: characters of wood anatomy optimized on a tree with rather different topology than that below), suggested that the ancestors of Ericales-Cornales grew under more temperate conditions in the present boreal-arctic area and later moved into tropical lowland rainforest.
Genes & Genomes. Viaene et al. (2009) discuss the complex history of PI gene duplication, sub- and neofunctionalisation, and loss in the clade. All taxa in which they found two copies of the PI gene have connate filaments; they thought that the PI gene may have facilitated floral diversification (Viaene et al. 2009). However, close attention should be paid to the nature of staminal connation and corolla tube formation which vary considerably in the order, and, as they noted, Primulaceae-Theophrastoideae have connate filaments but only a single copy of the PI gene.
Studies on the duplication of the RPB2 gene show that the I copy persists here almost alone in the eudicots + Trochodendrales + Gunnerales (and also in the lamiids: Oxelman et al. 2004). Many taxa lack the mitochondrial coxII.i3 intron, but it is known from the Ericaceae-Maesoideae (and Balsaminaceae - plesiomorphic presence?) clades and also from Ebenaceae and Styracaceae (Joly et al. 2001).
Chemistry, Morphology, etc. For leaf teeth that have a "?", their morphology is unknown. Schneider and Carlquist (2003) suggest that pit membrane remnants occur in some of this clade - perhaps mostly in some members of the terminal polytomy.
For details of ovary placentation, see Ng (1991). Truly parietal placentation does occur (e.g. Ericaceae-Pyroloideae), and although most other reports are incorrect, placentation at the apex of the ovary may be parietal (Löfstrand & Schönenberger 2015). A stylar canal in the symplicate zone is common in the order (Löfstrand & Schönenberger 2015).
For a summary of some chemical features of Ericales, see Grayer et al. (1999) and do Nascimento Rocha (2015: not easy to follow), for aluminium accumulation, see S. Jansen et al. (2004a, c), and for wood anatomy, see Lens (2005) and Lens et al. (2007b).
Phylogeny. Relationships within the order have for some time been poorly understood (e.g. R. J. Bayer et al. 1996; Morton et al. 1997a: both largely molecular data; Anderberg 1992: morphological data). However, Polemoniaceae + Fouquieraceae, Myrsinaceae and relatives, Ericaceae and relatives, and Balsaminaceae and relatives formed distinct clades, and Styracaceae + Diapensiaceae were moderately (D. Soltis et al. 2000, 2007) or poorly (Albach et al. 2001b) supported. A study by Anderberg et al. (2002: five genes, both plastid and mitochondrial) suggested a beginning of resolution of basal relationships within the order; this forms the backbone of the tree here. B. Bremer et al. (2002) suggested a similar set of relationships, although the resolution (and sampling) is less extensive. Lecythidaceae, linked loosely with Sapotaceae in some earlier analyses (and versions 7 and earlier of this page) remain without a clear position (see also Wikström et al. 2015), indeed, Rose et al. (2018) found some support for a clade [Mitrastemonaceae + Lecythidaceae] that is sister to all other Ericales except the Balsaminaceae and relatives clade; the latter are strongly supported as sister to all other Ericales although support for other relationships along most of the backbone of the order is weak - the position of Lecythidaceae in Rose et al. (2018) relative to that of [Polemoniaceae + Fouquieraceae] in the tree above is reversed. Details of the tree have been adapted to follow the relationships suggested by Schönenberger et al. (2005), however, caution is still in order when interpreting this (and other) phylogenies (the tree in Duangjai et al. 2006b also shows support for Lecythidaceae sister to most other Ericales, if rather weak [73% bootstrap] - relationships in the order are not the focus of that study). The relationships just mentioned were largely recovered by Sytsma et al. (2006), and with strong support, but c.f. in part Soltis et al. (2011: sampling). Hardy and Cook (2012) recovered rather different relationships: Fouquieraceae were not sister to Polemoniaceae, Symplocaceae were sister to the Cyrillaceae-Clethraceae-Ericaceae clade. Relationships suggested by Z.-D. Chen et al. (2016: Chinese taxa) differ considerably from those here, but support is poor. Yu et al. (2017) found that Primulaceae were sister to Pentaphylacaceae and other Ericaceae that they examined, but this may be a sampling artefact; Theaceae were the focus of their study. In a study of plastid genomes, Yan et al. (2018) found that Polemoniaceae were embedded in the Sapotaceae-Primulaceae clade, although support was weak and this, too, may be a sampling problem.
Geuten et al. (2004) in a Bayesian analysis of some 13 kb of nucleotide sequences suggest a further clarification of relationships within the terminal polytomy. Within this polytomy, the inverted anther clade (Actinidiaceae, Ericaceae, etc.) may be sister to [[Theaceae s. str. + Symplocacaeae] [Styracaceae + Diapensiaceae]], all relationships with strong support in some analyses; Pentaphylacaceae and Primulaceae s.l. were sister taxa (Geuten et al. 2004). However, they included only 16 terminals, for instance, the whole of the [[Sarraceniaceae [Actinidiaceae + Roridulaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]] clade was represented by just two taxa. In a rather more extensive study employing some 59 terminals, nearly 20 kb of sequences, and a variety of analyses, Schönenberger et al. (2005) recovered a group differing only in some details from the Theaceae-Ericaceae-Sarraceniaceae clade just mentioned; they did not recover the [Pentaphylacaceae + Primulaceae] clade, rather, Primulaceae s.l. linked with Sapotaceae and Ebenaceae. However, Hao et al. (2010) note that the chimaeric nature of the mitochondrial atp1 gene in species of Ternstroemia (see Pentaphylacaceae) caused some of the odd findings in the Schönenberger et al. (2005) study. The relationships [Clethraceae [Actinidiaceae + Ericaceae]] were recovered in ML analyses of chloroplast genomes, but the positions of the first two reversed in Bayesian trees.
The peregrinations of taxa that used to be included in or near Theaceae are interesting. There were suggestions that Pentaphylacaceae, placed close to Theaceae by both Cronquist and Takhtajan, linked with Balsaminaceae, etc., in Ericales (Nandi et al. 1998). Prince (1998), although focussing on Theoideae, found that a) Theaceae were not monophyletic, and b) the two parts into which it split were associated with other Ericales included in the study. Thus Sladenia tended to associate with Theaceae s. str. in matK analyses, and although it was unplaced in morphological analyses, in these Ficalhoa was included in Theaceae s. str. (Pentaphylax was not included). Wei et al. (1999) compared the pollen of Pentaphylax with that of Clematoclethra (Actinidiaceae), another member of Ericales, and found the two to be similar. Although Pentaphylacaceae were associated with Gonocaryum (Aquifoliales-Cardiopteridaceae) in the early study by Savolainen et al. (2000a), this position has not been recovered in other studies and the latter are usually strongly associated with Aquifoliales (e.g. D. Soltis et al. 2000; Kårehed 2001; Lens et al. 2008b). Tsou et al. (2016: Ficalhoa not included) found that Sladenia was sister to Freziereae in ITS analyses, yet sister to Pentaphylacaceae in trnL-F analyses, but support for the latter position in particular was very weak. Pentaphylax was placed sister to Ternstroemiaceae s. str. (Anderberg et al. 2001), and this is its resting place for now, but the limits of the family need confirmation. Rose et al. (2018) found a well supported clade of [Pentaphylacaceae + Sladeniaceae], but its position relative to the Sapotaceae-Primulaceae clade (poorly supported) was reversed when compared with that in the tree here, although support there, too, was low.
Both Pellicieraceae and Tetrameristaceae were in the Theales of Cronquist (1981). Pelliciera had been compared with Marcgraviaceae by Beauvisage (1920); details of wood anatomy suggest relationships with Tetrameristaceae (Baretta-Kuipers 1976; see also above). Pellicieraceae and Tetrameristaceae formed a well-supported clade in the morphological analysis of Luna and Ochoterena (2004), but Marcgraviaceae did not join them, nor were other Ericales part of the clade. However, monophyly of balsaminoid clade is well supported, and it is probably sister to rest of Ericales (e.g. Källersjo et al. 1998; Nandi et al. 1998; Soltis et al. 2000, 2011; Savolainen et al. 2000a; Geuten et al. 2004). For relationships within the balsaminoids, see e.g. K. Bremer et al. (2004a) and Morton (2011: nuclear Xdh gene). If Balsaminaceae and Marcgraviaceae are sister taxa (Geuten et al. 2004; Janssens et al. 2009: ML bootstrap support 98%), there are no obvious synapomorphies for the family pair. Rose et al. (2018) also recovered the relationships [Marcgraviaceae [Balsaminaceae + Tetrameristaceae]].
The position of the holoparasitic Mitrastemonaceae has been difficult to establish. Along with Cytinaceae and Rafflesiaceae, relationships of Mitrastemonaceae to Malvales have been suggested (Nickrent 2002). Barkman et al. (2004, also 2007: poor sampling) used mitochondrial sequences to place Mitrastemonaceae in Ericales, a position that also appeared in most analyses in Nickrent et al. (2004), and Hardy and Cook (2012) thought that Mitrastemonaceae were sister to most of Ericales except the Marcgraviaceae-Tetrameristaceae-Balsaminaceae clade. The cellular endosperm of Mitrastemon is certainly compatible with a position in Asterids, and its extrorse anthers are perhaps comparable with those of Ericaceae and their relatives, however, its parietal placentation and inferior ovary in particular are features found in many other parasitic angiosperms so they are not taxonomically particularly informative. Placing Mitrastemonaceae next to Ericaceae and their immediate relatives in the tree is partly for convenience; as mentioned above, Rose et al. (2018) found that it was sister to Lecythidaceae, albeit its position there was weakly supported.
Previous Relationships. Theales of Cronquist (1981) included mostly families now in Malvales, Ericales, and Malpighiales. Takhtajan's Theanae were largely equivalent (Takhtajan 1997). Ericales as here delimited are made up largely of Sarracenianae, Ericanae, Primulanae, and some families in Theanae, all adjacent groups in the Dilleniidae of Takhtajan (1997); its members are more widely scattered in Cronquist (1981). It is the asterid III group of some early phylogenetic studies.
Includes Actinidiaceae, Balsaminaceae, Cyrillaceae, Clethraceae, Diapensiaceae, Ebenaceae, Ericaceae, Fouquieriaceae, Lecythidaceae, Marcgraviaceae, Mitrastemonaceae, Pentaphylacaceae, Polemoniaceae, Primulaceae, Roridulaceae, Sapotaceae, Sarraceniaceae, Sladeniaceae, Styracaceae, Symplocaceae, Tetrameristaceae, Theaceae.
Synonymy: Ericopsida Bartling - Ericidae C. Y. Wu et al. - Lecythidaneae Reveal - Barringtoniineae J. Presl, Empetrineae Link, Epacridineae Link, Ericineae Link, Primulineae Burnett, Pyrolineae J. Presl, Rhododendrineae J. Presl, Sarraceniineae Reveal, Scytopetalineae Engler, - Actinidiales Reveal, Aegiceratales Martius, Ardisiales J. Presl, Balsaminales Link, Barringtoniales Martius, Camelliales Link, Cyrillales Doweld, Diapensiales Engler & Gilg, Diospyrales Prantl, Ebenales Engler, Empetrales Martius, Epacridales Berchtold & J. Presl, Fouquieriales Martius, Gordoniales J. Presl, Halesiales Link, Lecythidales Martius, Lysimachiales Döll, Marcgraviales Martius, Mitrastemonales Makino, Monotropales Berchtold & J. Presl, Myrsinales Berchtold & J. Presl, Polemoniales Berchtold & J. Presl, Primulales Berchtold & J. Presl, Rhodorales Horaninow, Roridulales Nakai, Samolales Dumortier, Sapotales Berchtold & J. Presl, Sarraceniales Martius, Styracales Martius, Ternstroemiales Martius, Theales Berchtold & J. Presl, Vacciniales Dumortier
[Marcgraviaceae [Balsaminaceae + Tetrameristaceae]] / balsaminoid clade: non hydrolysable tannins [myricetin] +, ellagic acid 0; raphide sacs +, druses 0; vessels in radial multiples; paratracheal parenchyma +; ± branched sclereids +; lamina supervolute, elongating in bud, with obscure abaxial lines, toothed; inflorescence racemose; bracteoles immediately below the flower; cells with mucilage, tannins +; K and C rather similar in size and colour, K with a single trace at base; abaxial surface of C with stomata; nectary outside A; stamens = and opposite sepals, free from C, anthers (near) basifixed, thread-like structures along the stomium, filaments broad; mucilaginous secretion in the ovary, style short, stigma little expanded; ovules bitegmic; style persistent in fruit; endosperm at most slight.
Age. This node was dated to just under 65Ma by K. Bremer et al. (2004a), to (66-)52, 49(-34)Ma by Bell et al. (2010), ca 55.4Ma by Magallón et al. (2015) and ca 43.6 or 45.2Ma by Tank et al. (2015: Table S1, S2); the estimate was ca 81.7 Ma in Rose et al. (2018). With different topologies, the common ancestor of this clade was estimated at (52-)48, 44(-40) Ma (Wikström et al. 2001: Balsaminaceae sister to the rest) or (85-)59(-38) Ma (Wikström et al. 2015) and that of the [Balsaminaceae + Marcgraviaceae] clade was dated to the middle Palaeocene ca 58.9 Ma (Janssens et al. 2009).
Evolution: Divergence & Distribution. Looking at the floral morphospace of Ericales, Chartier et al. (2017) thought that this clade was morphologically rather homogeneous, although they noted that they did not include features like the colour and shape of perianth members in their analysis.
If Balsaminaceae and Marcgraviaceae are sister taxa (Geuten et al. 2004; Janssens et al. 2009: ML bootstrap support 98%), there are no obvious synapomorphies for the family pair, even when one examines floral development closely (see Schönenberger et al. 2010; Schönenberger & von Balthazar 2010; von Balthazar & Schönenberger 2013). Some of the similarities between Pellicieraceae and Marcgraviaceae may be because they are both woody, but, depending on the topology, they could be synapomorphies/plesiomorphies for the whole clade, the corresponding features of Balsaminaceae being apomorphies for that family.
Geuten et al. (2006) suggest that heterotopic SEP3-like gene expression in bracteoles and calyx in members of this clade was present in its common ancestor; the gene is normally expressed in the corolla and other inner whorls. Indeed, most taxa in this clade have more or less petal-like sepals, bracts or bracteoles, although Tetramerista and Pentamerista, derived members, lack such expression patterns. Schönenberger et al. (2010: see also Schönenberger & von Balthazar 2010) suggest that thread-like structures bordering the stomium - they vary in their morphological nature - are an apomorphy for the whole clade. Schönenberger et al. (2010) emphasized that the nectary was situated in the periphery of the flower, that there are mucilage cells in the flower, etc., while von Balthazar and Schönenberger (2013) discussed these and other possible apomorphies of the clade.
Chemistry, Morphology, etc. Beauvisage (1920) noted that both Pelliciera and Marcgraviaceae have large air spaces in the cortex. The raphide sacs are white pockets in the stem; they are visible under the dissecting microscope.
For the wood anatomy of this group, see Lens et al. (2005b), that of Balsaminaceae is paedomorphic, for palynology, see Lens et al. (2005: Marcgraviaceae) and Janssens et al. (2005: the rest), and for general floral morphology, see Schönenberger et al. (2010) and in particular von Balthazar and Schönenberger (2013).
MARCGRAVIACEAE Berchtold & J. Presl, nom. cons. - Back to Ericales
Lianes, climbing by weakly twining and/or roots, and/or hemiepiphytes; (vessel elements with scalariform perforation plates); rays broad [Marcgravia]; petiole bundle deeply arcuate, or annular with inverted adaxial plate; cells with essential oils; stomata staurocytic; lamina margin entire, with marginal to abaxial cavities (black dots); inflorescence often umbellate; bracts abaxially ascidiate, nectariferous, recaulescent on pedicel; K quincuncial; A many; G [2-20], opposite ?, placentation very intrusive parietal, stigma?, dry; ovules many/carpel; fruit with more or less irregular dehiscence, placentae fleshy; seeds many, small; exotestal cells ± enlarged, inner walls much thickened; endosperm with micropylar haustorium, cotyledons large to small; x = 18.
7 [list]/130 - two subfamilies below. New World tropics (map: from Heywood 1978). [Photo - Flowers, Fruits.]
Age. Diversification in Marcgraviaceae is estimated to have begun ca 23.9 Ma by Rose et al. (2018).
1. Marcgravioideae Choisy
Leaves strongly heterophyllous, 2-ranked; apical flowers sterile, nectariferous; flowers 4-merous; C connate, calyptrate [calyptra thrown off at anthesis]; G ?; inner integument ca 3 cells across; embryo sac long; n = (?16, 19), Cx [diploid spp.] = 2.55-4.04 pg.
1/60. New World Tropics.
2. Noranteoideae Choisy
Also shrubs; leaves spiral; inflorescence also spike; nectaries associated with each flower, (bracts with paired, petal-like appendages); flowers 5-merous; C basally connate, reflexed, deciduoud; (A 4-15), (style +), stigma wet [Souroubea]; (ovules 5<); n = (?16, ?17, 19), Cx [diploid spp.] = 5.55-6.2 pg.
6/70: Souroubea (19). New World tropics.
Evolution: Pollination Biology & Seed Dispersal. The distinctive inflorescences with nectar secreted in the cup-shaped (ascidiate) bracts attract a variety of large pollinators including hummingbirds and bats (e.g. Dressler 1999; Tschapka et al. 2006; Fleming et al. 2009). Although individual flowers of Marcgraviaceae are polysymmetric, the inflorescences of Margravia and the flowers of taxa like Souroubea are monosymmetric from the point of view of their pollinators, which get pollen dusted on their heads (usually) as they take nectar from the modified bracts (see also Westerkamp & Claßen-Bockhoff 2007). Marcgravia evenia is a bat pollinated plant that has a concave bract above the inflorescence which reflects the signals of echo-locating nectarivorous bats, so helping them find the flowers more readily (Simon et al. 2011). Pollen of S. guianensis is associated with oil produced by the tapetum (Machado & Lopes 2000).
Seeds of Marcgraviaceae may quite often be dispersed by fruit-eating bats (Lobova 2009).
Genes & Genomes. Some polyploid species in The Rest have massive genomes of 2C = 14-21.5 pg or so (Schneider et al. 2014b).
Chemistry, Morphology, etc. For the epiphytic habit in the family, see Zotz (2013). The black dots on the margin of the leaf blade make the leaf appear "serrate", but here that character is not so much about serrations per se, as the marginal glands, etc., that terminate any serrations that are present.
I do not know if the pollen grains are starchy (c.f. Balsaminaceae). Juel (1887) shows both integuments as being two cells across. Johri et al. (1992) described the seeds as being arillate.
For general information, see Dressler (2004) and Schneider et al. (2014b), for vegetative anatomy, see Beauvisage (1920), and for information on embryology in Marcgravia, see Mauritzon (1939c).
Phylogeny. Ward and Price (2002) suggest phylogenetic relationships within the family. Marcgravia, with its reversible heterophylly, two-ranked leaves, 4-merous flowers, calyptrate corolla, and nectaries adnate to abortive flowers, is distinct, but in the rest of the family both synapomorphies and generic limits are unclear.
Synonymy: Noranteaceae Martius
[Balsaminaceae + Tetrameristaceae]: K ± petal-like, with adaxial nectar glands; A latrorse; filaments postgenitally adnate to ovary; G , stylar canal +, 5-radiate, stigma with often inconspicuous commissural lobes; ovule 1/carpel, ?orientation, with chalazal constriction, funicle stout; K not persistent in fruit; endosperm with micropylar haustorium.
Age. K. Bremer et al. (2004a) dated this node to around 56 Ma, while around 50.5 Ma was the age in Magallón et al. (2015), (77-)51(-30) Ma in Wikström et al. (2015), ca 42.7 Ma in Tank et al. (2015: Table S2), and as much as ca 81 Ma in Rose et al. (2018).
Evolution: Divergence & Distribution. For possible apomorphies of this clade, see Schönenberger et al. (2010), Schönenberger and von Balthazar (2010), and von Balthazar and Schönenberger (2013).
BALSAMINACEAE A. Richard, nom. cons. - Back to Ericales
Fleshy herbs; non-hydrolysable tannins, naphthoquinones +; cork?; vessels single; sclereids 0; petiole bundle arcuate; mucilage sacs +; plant glabrous; nodes swollen; lamina lacking obscure abaxial lines, vernation involute, (extrafloral nectaries +, sometimes as paired glands or foliaceous lateral flaps on leaf base/stem); inflorescence axillary; flowers vertically monosymmetric, resupinate [median sepal abaxial]; functionally abaxial sepal with prominent nectariferous spur, K 3, C 5; anthers postgenitally ± connate and forming cap over stigma, (with tapetal trabeculae in loculi [= locellate]), filaments stout; tapetal cells 2(-4)-nucleate; cellulose threads from cell walls holding pollen grains to anther, with raphides, starchy, pollen often rectangular in polar view, endexine lamellate; G [5 (4)], opposite petals, stigma fairly broad, wet; ovules (hemitropous), apotropous, suprachalazal zone long, with elongated cells; embryo sac bisporic, 8-nucleate [Allium type], becoming very long; seed pachychalazal; endosperm also with chalazal haustorium, (xyloglucans +), cotyledons large; germination epigeal, radicle soon dies [?all].
2[list]/1001: Impatiens (1000) - two genera below. Cool temperate to tropical, not Central and South America, the Antipodes, or Oceania (map: from Hultén 1971; Meusel et al. 1978; Grey-Wilson 1980a; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011).
Age. Diversification in Balsaminaceae began (39.3-)30.7(-22.1) Ma (Janssens et al. 2009) or ca 69.8 Ma by Rose et al. (2018).
1. Hydrocera Blume
Plant semi-aquatic; K 5, C 5; tapetum amoeboid; G loculi divided longitudinally into three parts; ovules apically bitegmic, micropyle endostomal, outer integument 8-9 clles across, inner integument 6-7 clles across; fruit a drupe, stones 5, separating, each with two longitudinal air sacs; testa sclerotic, 6-8 layers thickened cells, ca 5 layers unthickened; endosperm with micropylar haustorium several nucleate, protruding through the mictopyle, chalazal haustorium uniseriate, embryo suspensor short [2-3-celled]; n = 8.
1/1: Hydrocera triflora. South India, Sri Lanka, Hainan to Peninsula Malaysia, Java, the Celebes.
Synonymy: Hydroceraceae Wilbred
2. Impatiens L.
Plant (annual), (woody), (tuberous), (epiphytic); (indumentum +); leaves (opposite); lateral petals connate in pairs, (all four connate); (inflorescence cymose), (bracteoles 0); K (1), (spur 0), when K 1, adaxial C often with a sepal-like keel; pollen (porate), 4-aperturate; ovules (-several/carpel, uni- to biseriate), bitegmic, cuter integument 2-10 cells across, inner integument 2-6 cells across/unitegmic 9-15 cells across; (embryo sac unisporic, 8 nucleate); fruit an explosive capsule, septifragal, walls inrolling from base; only exotestal cells thickened, ("hairs" with spiral thickenings), (mucilaginous); n = (3-)7-10(-12<); nuclear genome [1C] (1125-)1922(-3182) Mb.
1/1000. The range of the family, most Old World, Africa (esp. Madagascar) to mountains of S.E. Asia. [Photo - Flower.]
Synonymy: Impatientaceae Barnhart
Evolution: Divergence & Distribution. Impatiens is most diverse in tropical and subtropical montane forests, and the imbalance in species numbers between it and the monotypic Hydrocera is striking. Within Impatiens diversification began only in the Early Miocene (28.1-)22.5(-16.9) Ma, but the speciation rate much increased in the early Pliocene within the last 5 Ma, climate change causing much population fragmentation, isolation, and migration (Janssens et al. 2009), however, diversification may have begun 59.3 Ma ( Rose et al. 2018)... The S.E. Asian/China region may be the centres of origin for the genus.
The combination of non-hydrolysable tannins and raphides, both of which are found in Balsaminaceae, is rarely found in herbs (Fischer 2004a). However, the family is indeed likely to be primitively herbaceous. Increase in width of the stem is by expansion of pith cells (Troll & Rauh 1950), and although some species of Impatiens do produce a small amount of wood, it is derived and paedomorphic (Smets et al. 2011; Lens et al. 2012). For apomorphies of the two genera and of major clades within Impatiens, see Yu et al. (2015).
Balsaminaceae are vegetatively relatively uniform, if florally very diverse; there has been duplication and probable subfunctionalisation of the class B DEF gene in this clade (Janssens et al. 2006b; Geuten et al. 2006).
Pollination Biology & Seed Dispersal. The flowers are protandrous. As the anther walls break down and then retract, the cellulose threads produced hold the exposed pollen as if in a lattice (Vogel & Cocucci 1988); the pollinator picks up the pollen from there.
The common name for some Impatiens spp., Busy Lizzie or Touch-Me-Not, refers to the explosive dehiscence of the fruits which can be triggered by gently squeezing a ripe fruit; the valves separate and incurve (rather unusual), flinging out the seeds as they do so. In I. glandulifera ca 80% of the septal area cracks before the explosive event itself, and stored elastic energy efficiently used results in the seeds being dispersed with an initial velocity of up to 4 m/s, although not all species have exactly the same mechanism/energy efficiency (Deegan 2012). Indeed, in I. capensis, only ca 0.5% of the stored energy is transmitted to the seed, the great majority of which are predicted to be thrown around 0.5 m or less (Hayashi et al. 2009). The seeds are not very dense, being rich in lipids, which also makes this initial dispersal less efficient, but they may also be secondarily dispersed by water (Hayashi et al. 2009), indeed, the plant, native in North America, is an effective competitor.
Genes & Genomes. Cytological variation in Impatiens is considerable; species with n = 9 often have a bimodal karyotype (Song et al. 2003).
Chemistry, Morphology, etc. The paired glands or foliaceous lateral flaps on the leaf base or stem near the leaf base are at least sometimes vascularized (Colomb 1887).
For an interpretation of floral morphology in which two of the sepals - the adaxial-lateral pair (non-inverted orientation) - are perhaps better interpreted as prophylls/bracteoles borne immediately below the flower, as in other members of the balsaminoid clade, see von Balthazar and Schönenberger (2013); given the evidence presented, this seems reasonable, and is followed here. The abaxial-lateral sepal pair is often reduced, perhaps becoming fused with the abaxial petal, or it is entirely absent (Caris et al. 2006a; see also Grey-Wilson 1980c). Interestingly, in Impatiens with three sepals there are four carpels, the adaxial carpel being larger than the other three (Yu et al. 2010).
Janssens et al. (2012b) notes the variety of stamen form that is obscured by the bland statement "anthers connate and forming cap over stigma" (see above). The integuments are quite thick and are free only at the micropyle (e.g. van Tieghem 1898); L. L. Narayana (1970) also illustrates more conventional ovules. A study by McAbee et al. (2007) shows considerable variability in integument development in the family, although many species have more or less well developed congenital fusion of the integuments (and bitegmy may be derived). There is variation in the embryo sac, Hydrocera and at least some species of Impatiens having a bisporic, 8-celled embryo sac (Venkateswarlu & Lakshminarayana 1958); this may be an apomorphy for the family. The fruit type of Hydrocera is unclear (see Wood 1975), Venkateswarlu and Lakshminarayana (1958) describing a testa with the outermost ca 6 layers consisting of thickened cells, which one normally would not expect to find in a drupe (they have reduced testas), while Grey-Wilson (1980a) described the fruit as being a drupe with separate stones. The micropylar endosperm haustorium is massive and may invade the funicle and even the placenta.
For general information, see Sandt (1921), Grey-Wilson (1980c: African taxa), Fischer (2004a) and Leins and Erbar (2010), for chemistry, see Szewczyk 2018), for lamina epidermis, see X.-X. Zhang et al. (2013), for information on floral anatomy, development, etc., see also Grey-Wilson (1980b) and on the gynoecium, see Shimizu and Takao (1982, 1985), for pollen morphology and evolution, see Janssens et al. (2012: African species more often porate, Asian species 4-aperturate), for ovule variation and seed anatomy and development, see Guignard (1893), Chandresekhara Naidu (1985) and Boesewinkel and Bouman (1991), for some embryology, see Dahlgren (1934a) and Narayana (1963), for seed morphology, Utami and Shmizu (2005: variation considerable) and for germination, see Hofmann and Ludewig (1985).
Phylogeny. Hydrocera and Impatiens are sister taxa (Yuan et al. 2004; esp. Janssens et al. 2006a). Taxa of Impatiens with three sepals are scattered through the genus, so that condition is apparently at least sometimes derived (Janssens et al. 2006a); see also Janssens et al. (2012a) and Yu et al. (2015) for relationships, while Ruchisansakun et al. (2015) explore the limits of section Semeiocardium.
Classification. The current infrageneric classification of Impatiens needs complete overhaul (Janssens et al. 2006a); Yu et al. (2015: two subgenera, etc.) suggested a new classification, but it clearly has its limits (see Ruchisansakun et al. 2015).
Previous Relationships. Balsaminaceae were included in Geraniales-Rosidae by Cronquist (1981; see also Takhtajan 1997).
TETRAMERISTACEAE Hutchinson - Back to Ericales
Evergreen trees; chemistry?; intervessel pitting opposite-alternate; petioles short [<1 cm]; bracteoles rather large, ± caducous; fruit indehiscent; ?endosperm development.
3 [list]/5 - two groups below. W. Malesia, Central and N. South America.
Age. K. Bremer et al. (2004a) estimated the age of crown-group Tetrameristaceae to be 41 My; (31-)28, 25(-22) Ma was the age suggested by Wikström et al. (2001) and (53-)31(-13)Ma by Wikström et al. (2015) - other estimates, (42-)30, 28(-15) Ma (Bell et al. 2010) and ca 44.6 Ma (Rose et al. 2018).
Chemistry, Morphology, etc. The lamina narrows gradually towards the base, and any petiole can be difficult to make out - it is at best short.
1. Pelliciereae Trianon & Planchon
Fluted buttresses made up of "adventitious" roots; vessels in multiples; petiole bundle more or less flat where it joins the stem, becoming annular; stomata cyclocytic; lamina vernation involute, base asymmetric, colleters?; flowers terminal, single, ca 10 cm across ["very large"]; bracteoles petal-like; K with two traces at base, quincuncial; A extrorse, anthers very long [>4.5 cm long], connective prolonged into a point; pollen strongly verrucate; G apparently 2-carpellate at maturity, style long, stigma bifid, punctate; ovule apical, pendulous, campylotropous; fruit ± dry, K and C caducous; seeds large, coat?; cotyledons large; n = 17, nuclear genome size [2Cx] 2.52-2.56 pg; ; seeds ± viviparous [embryo breaking the seed coat while still on the plant], germination phanerocotylar, hypogeal.
1/1: Pelliciera rhizophorae. Central and N. South America, on both the Caribbean and Pacific shores (map: from A. Graham 1977). [Photo - Flower, Fruit.]
Evolution: Divergence & Distribution. Records of fossil pollen suggest that Pelliciera was once much more widespread (A. Graham 1977), even being found in the Old World. However, the fossil history of the genus is uncertain. Martínez-Millán (2010) did not accept New World records of the genus, which are based on pollen; Old World records are also based on pollen (see also Ellison et al. 1999; Plaziat et al. 2001). Manchester et al. (2015) note that pollen of Alangium (Cornales-Cornaceae) can be confused with that of Pelliciera.
Ecology & Physiology. For the evolution of the mangrove habitat, to which Pelliciera is restricted, see Rhizophoraceae. The fruits of Pelliciera lose their pericarps as they are floating, and germination begins (Rabinowitz 1978).
Genes & Genomes. For the cytology, etc., of Pelliciera, see Garzón-Bautista et al. (2018).
Chemistry, Morphology, etc. Although the gynoecium apears to be bicarpellate at maturity, the stylar canal is five-radiate and the gynoecium may be basically 5-carpellate (Schönenberger et al. 2010).
For some vegetative anatomy, see Beauvisage (1920). General information is taken in part from Kobuski (1951), Tomlinson (1986), Maas and Westra (1993) and Kubitzki (2004b).
Synonymy: Pellicieraceae Bullock
2. Tetrameristeae Hallier
Cork inner cortical; (vessel elements with scalariform perforation plates); wood fluorescing [1 sp. tested]; nodes 3:3; stone cells [in stem] +, branched sclereids ?0; lamina with marginal "glands"; (bracteoles persistent); flowers 4- or 5-merous, rather small; filaments slightly connate at the base; G [(4)]; ovule basal, ?epitropous; fruit a berry; testa several layers thick, walls thickened; endosperm copious, cotyledons small; n = ?
2/4. Malesia (Tetramerista), Venezuelan Guyana (Pentamerista).
Chemistry, Morphology, etc. There are no reports that Pelliciera accumulates aluminium, again unlike Theaceae s.l., in which it has often been included. Nodal anatomy of [Tetramerista + Pentamerista] is extrapolated from petiole scars. The products of different marginal glands of the one leaf may not be the same (Collins et al. 1977).
The floral diagram of Pelliciera in Tomlinson (1986) suggests that either the two carpels are oblique, or the bracteoles are not in the lateral position and the carpels are transverse. In Tetramerista there are glistening dots on the adaxial surface of both calyx and corolla.
For general information, see Kubitzki (2004b).
The embryology, morphology and anatomy of Pellicieraceae s.l. are poorly known.
Previous Relationships. Pellicieraceae s. str. and Tetrameristaceae s. str. were included in Theales by Cronquist (1981) and Takhtajan (1997).
[[Polemoniaceae + Fouquieriaceae], Lecythidaceae, [[Sladeniaceae + Pentaphylacaceae], [Sapotaceae [Ebenaceae + Primulaceae]], [Mitrastemonaceae, Theaceae, [Symplocaceae [Styracaceae + Diapensiaceae]], [[Sarraceniaceae [Roridulaceae + Actinidiaceae] [Clethraceae [Cyrillaceae + Ericaceae]]]]]: corolla connate, tube well developed; style long.
Age. This node may be (95-)85, 82(-72) Ma in age (Bell et al. 2010), around 99.7 Ma (Magallón et al. 2015), (106-)99(-94) Ma (Wikström et al. 2015) - note topologies in all.
Genes & Genomes. The ACCHβ genome duplication event, dated at ca 85.6 Ma, may be placed at this node (Landis et al. 2018: ?Lecythidaceae).
[Polemoniaceae + Fouquieriaceae]: kaempferol, quercetin +; cork cambium outer cortical; inflorescences terminal, determinate; K with scarious margins; A adnate to the corolla, thecal septum at most short and indistinct [septum 0]; gynoecial nectary +, with stomata; G , style hollow, style 3-branched; ovules in two ranks, apotropous, micropyle zig-zag [abruptly turned towards central axis]; fruit a loculicidal capsule, seeds on central columella; seeds winged; exotesta with circular/annular thickenings; endosperm scanty; mitochondrial coxII.i3 intron 0.
Age. The age of this node is estimated at (98-)51(-50)Ma by Wikström et al. (2015), (77-)65, 61(-48)Ma by Bell et al. (2010), ca 79.6Ma by Tank et al. (2015: Table S2), around 83Ma by Magallón et al. (2015), ca 99.4Ma by Rose et al. (2018) and (95.8-)75.5(-60.3) Ma (De-Nova et al. 2018).
Evolution: Divergence & Distribution. Schönenberger (2006a, especially 2009) lists many other features occurring in this family pair, including free sepals, stomata on the abaxial surface of the calyx (also e.g. Ericaceae - ?general distribution of this feature?), anastomosing vascular bundles in sepals and petals, and details of gynoecial development. Chartier et al. (2017) commented that these two families were rather different, at least based on the 37 floral features that they examined.
Chemistry, Morphology, etc. Both families have late corolla tube formation (Schönenberger 2009); for general floral morphology, see Schönenberger et al. (2010).
POLEMONIACEAE Jussieu, nom. cons. - Back to Ericales
Fructan sugars accumulated as kestose and isokestose oligosaccharides [levans and inulins], cucurbitacins +, ellagic acid 0; cork cambium also pericyclic; (vessel elements with scalariform perforation plates); (wood rayless); stomata paracytic); leaves opposite to spiral, lamina conduplicate, margins entire to deeply lobed; bracteoles 0; (flowers monosymmetric); K connate, aestivation open, lobes with green midrib and colorless intermediate portion, tips terete/spine-like, C lobes usu. right-contortuplicate; K/C tube well developed, stamens = and opposite sepals, inserted at different levels or filaments of different lengths, anthers ventrifixed (basifixed); pollen pantoporate; nectary usu. not vascularized, prominent; G [(2-4)], median member adaxial, placentae protruding, stigma dry, decurrent the length of the arms; ovules 1-many/carpel, vascular bundle not reaching chalaza; seeds often mucilaginous when wetted, exotesta variously thickened, endotesta a pigment layer, radial walls ± thickened; endosperm nuclear, haustoria 0, embryo green or white.
Ca 18 [list]/385 - three subfamilies below. N. temperate, W. North America, South America (map: from Hultén 1971; Meusel et al. 1978).
Age. Crown-group Polemoniaceae are estimated to be (40-)36, 33(-29) Ma (Wikström et al. 2001), (47-)36, 31(-20) Ma (Bell et al. 2010) or ca 53.9 Ma (Rose et al. 2018: Acanth sister).
Gilisenium hueberi, perhaps close to Gilia, is known from the middle Eocene of Utah ca 40.4 Ma (Lott et al. 1998; Martínez-Millán 2010).
1. Polemonioideae Arnott
Mostly ± desert-dwelling herbs (subshrubs), (short shoots +); leaves compound to simple; (flowers monosymmetric, median petal ab- or adaxial); C veins usu. free or connected well above the base; filaments usu. merged with corolla; (pollen 6-9 colporate); integument (3)7-20 cells across, hypostase +; seeds not winged (narrowly winged - Loeselia), (testa ± multiplicative); n = (6) 7 (8) 9, chromosomes "larger" [not Loeselia]; also sporophytic incompatibility system present.
13-22/350 [list]: Phlox (70), Linanthus (35), Navarretia (30), Polemonium (27), Gilia (25). Especially western North America, also a few N. temperate, southern South America. Several predominantly western North American genera have a few species in southern South America (see below). [Photos - Collection (all except Cobaea).]
2. Cobaeoideae Arnott
Mostly mesic vines with leaf tendrils to small trees (herbs); (short shoots +): leaves usu. unequal-pinnate (palmate, simple); flowers large, (mostly positionally monosymmetric - Cobaea); K (basally connate), usu. herbaceous throughout, C veins connected at the base of lobe (and in upper lobe); A traces in two whorls, filaments often superficially adnate to C; pollen (exine verrucate), (100-220 µm long); ovules with nucellar cap; fruit septicidal and/or loculicidal; seed wing broad (narrow - Bonplandia); mesotestal cell walls thinly lignified; n = 15, 26, 27, [x = 7-9?] chromosomes "small".
4/34 [list]. Baja California, tropical America. [Photo - Flower & Fruits.]
Synonymy: Cobaeaceae D. Don
3. Acanthogilioideae J. M. Porter & L. A. Johnson
Shrubby; short shoots +, leaves very dimorphic, as persistent branched spines on long shoots, unbranched on short shoots; pollen 4< equatorially colporate, exine coarsely verrucate; seeds few; n = 9, chromosomes 2-4 µm long.
1/1 [list]: Acanthogilia gloriosa. Baja California.
Evolution: Divergence & Distribution. There are some 15 species of Polemoniaceae-Polemonioideae in western South America that have their closest relatives in North America; these disjunctions are up to 19.5 Ma and may well be the result of the mucilaginous seeds sticking to migratory birds (Johnson & Porter 2017). Details of speciation patterns vary, but in no cases have there been extensive radiations in South America, in a few cases the South American representatives do not even represent distinct species, or they may be allopolyploids, hybridisation happening in South America, but with one or both parents extinct, and so on - very complex scenarios are possible in the examples discussed (Johnson & Porter 2017). There are also clusters of similar events in Poaceae (Peterson et al. 2010b) and Boraginaceae (Guilliams et al. 2017).
Schönenberger (2009) lists additional features that may be apomorphies for Polemoniaceae.
Pollination Biology & Seed Dispersal. For floral variation in the context of different pollinators, see the classic work of Grant and Grant (1965). De Groot (2011) found remarkable infraspecific variation in floral orientation in Eriastrum eremicum (Polemoniaceae), and the flowers in this species also show considerable variation in their lobing (5:0, 3:2, 2:3, etc.); in both Eriastrum and Ipomopsis the median petal may be ad- or abaxial, the variation even being infraspecific in Eriastrum.
A number of Polemonioideae have myxospermous seeds (Winter 2012).
Chemistry, Morphology, etc. The cambium is sometimes storied; raylessness is frequent. In Cobaea the leaves are tendrillar and the basal pair of leaflets is foliaceous-stipuliform.
Pollen morphology is variable.
For inflorescence morphology, see Weberling (1989), for floral development, see Schönenberger (2009), for pollen, see Monfils and Prather (2004, and references), for some embryology, see Kapil et al. (1969), for seed morphology, see Johnson et al. (2004), for general information, see Day and Moran (1986: esp. Acanthogilia), Grant (1998), Johnson et al. (1996, 1999), Porter (1997), Porter and Johnson (1998) and Wilken (2004).
Phylogeny. Acanthogilia has been placed in its own subfamily (Porter et al. 2000), and it may be sister to the Cobaea et al. clade (Prather et al. 2000) or even sister to the whole of the rest of the family (Schönenberger et al. 2005, only four taxa included) - its position is unclear (Johnson et al. 2008 and references), although Rose et al. (2018) also found it to be sister to the rest of the family. It has very dimorphic leaves and short shoots are in this is like Fouquieraceae, its branched spines are reduced leaves like those found scattered in Polemonioideae, and its sepals have a green midrib, as in Cobaeoideae.
Johnson et al. (2008) suggest the following relationships within Polemonioideae - [[Polemonieae (one genus) + Phlocidae] [Gilieae + Loselieae]]. For the phylogeny of Phlox, see Ferguson et al. (2008).
Classification. For a phylogenetic classification of the family, see Porter and Johnson (2000). The limits of the genera Ipomopsis (Porter et al. 2010) and Gilia (Prather et al. 2000; Johnson et al. 2008) need to be redrawn.
Previous Relationships. Polemoniaceae were included as Polemoniales in Solananae by Takhtajan (1997).
FOUQUIERIACEAE Candolle, nom. cons. - Back to Ericales
Woody, xeromorphic, with long and short shoots; flavonols only, ellagic acid, route I secoiridoids +, myricetin 0; root cork cambium outer cortical; stem cortex often with fibrous ridges, etc; cork cambium underneath; cuticle wax crystalloids 0; leaves heteromorphic, lamina (isobilateral), margins entire, petiolar spines on long shoots; K separate, ± scarious, imbricate; A 10(-23), long-exserted, only very shortly adnate to corolla; pollen with oil bodies; nectary tissue in base of ovary, vascularized; placentation intrusive parietal most of the length of the ovary, style with long branches, stigmas punctate (subcapitate); ovules 3-20/carpel, apotropous, bitegmic, micropyle endostomal, outer integument 3-4 cells across, inner integument (3-)7-8 cells across, suprachalazal zone massive; embryo sac tetrasporic, with lateral haustorium; (suspensor long, thin); testa and tegmen multiplicative, becoming crushed, testa hypodermis with banded thickenings; endosperm with micropylar and chalazal haustorium; n = 8, 12.
1 [list]/11. S.W. North America (map: from Henrickson 1972b). [Photos - Habit, Branch, Flowers.]
Age. Diversification began here (20.9-)12.7(-7.8) Ma (De-Nova et al. 2018).
Evolution: Divergence & Distribution. Diversification began at the Miocene-Pliocene boundary; there is a ca 60 Ma stem, and molecular evolution in Fouquieraceae has been around twice that in Polemoniaceae (De-Nova et al. 2018). Schönenberger (2009) lists other features that may be apomorphies for Fouquieriaceae, including sepals and corolla lobes being similar in size and histology - but they are not notably similar in size...
Chemistry, Morphology, etc. Layers of fibrous cells alternate with layers of cork cells in the stem cork, while the cork cambium in the root is described as being superficial (Henrickson 1969), the unusual position for angiosperms, although perhaps commoner in desert plants.
For an asymmetric phase in early floral development, see Schönenberger (2009); this may be connected with the fact that the perianth parts are borne in a distinct spiral. Members of the androecium have been described as being borne in a single whorl, but they are diplostemonous, and the antepetalous stamens are doubled in some species (Schönenberger 2009; Schönenberger & Grenhagen 2005). There is quite a lot of variation in the development of the embryo sac, but it always seems to be tetrasporic (Johansen 1936).
See Henrickson (1972b) and Kubitzki (2004b) for general information, for some root and stem anatomy, see Henrickson (1936a), for pollen, see Henrickson (1973), for ovule morphology and embryology, see Mauritzon (1936b), and for seeds, see Corner (1976).
Phylogeny. For relationships within the family, see Schultheis and Baldwin (1999) and De-Nova et al. (2018).
Previous Relationships. Fouquieriaceae were placed in Violales by Cronquist (1981).
LECYTHIDACEAE A. Richard, nom. cons. - Back to Ericales
Trees (lianes); flavonols, ellagic acid +, kaempferol 0; (vessel elements with scalariform perforation plates); cortical vascular bundles +; (wood siliceous and/or with SiO2 grains); phloem stratified (with wedge-shaped rays); nodes 3 or more:3 or more; petiole with numerous arcuate or annular bundles in arcs, etc.; stomata usu. anisocytic; lamina margins toothed or entire, (tertiary veins subparallel, ± at right angles to midrib), stipules cauline, small or 0, colleters +; pedicels articulated; flowers large; K (2-)4-6(-12), variously arranged, connate or not, valvate; A latrorse, filaments not articulated, outer A staminodial; tapetum amoeboid, cells binucleate; pollen grains tricolpate, tricellular; nectary +; ovary inferior, [2-8], style short/0, stigma ± capitate (punctate, divided), wet or dry; ovules 1-many/carpel, bitegmic, micropyle endostomal, micropyle long [longer than embryo sac + chalaza]; antipodals ephemeral; K persistent in fruit; seeds often arillate, testa ?multiplicative, vascularized, exotestal cells variously thickened, palisade, or low with sinuous anticlinal walls, mesotesta sclerotic or not; endosperm nuclear, 0; mitochondrial coxII.i3 intron 0 [but sampling].
Ca 25 [list: to subfamilies]/353 - five groups below. Tropical, especially America and W. Africa.
Age. Crown-group diversification in Lecythidaceae may have begun (65-)84, 46(-30) Ma (Bell et al. 2010), ca 82.9 Ma Rose et al. (2018), or (71-)65, 61(-55) Ma (Wikström et al. 2001).
1. Napoleonaeoideae (A. Richard) Bentham
Secondary xylem with crystal chains; ?stomata; leaves 2-ranked, lamina supervolute, often with glands abaxially at the base, margin serrate, stipules +/0; flowers ± sessile, axillary, or plant cauliflorous; G initiated before A; K with nectariferous glands or not, C valvate, connate, plicate, margin serrate; A adnate to C, 10, paired, opposite C, extrorse, ± connate, monothecal, alternating with pairs of staminodia, stamens + staminodes incurved, 2 additional whorls of staminodia, outer subulate, free, inner connate, nectary at base; tapetal cells binucleate; G opposite petals, style 0, stigma broad, pentagonal, flat; ovules 4/carpel, apical, collateral in pairs, outer integument 5-7 cells across, inner integument 9-11 cells across, integuments basally connate, ?micropyle length, endothelium 0; fruit a 1-several seeded drupe; testal bundle single; endosperm 0; embryo curved; n = 16.
1/16. W. tropical Africa (map: from Liben 1971b; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]
Synonymy: Belvisiaceae R. Br., Napoleonaeaceae A. Richard
[Scytopetaloideae [Lecythidoideae [Barringtonioideae + Foetidioideae]]]: A many [15-1200], initiated as ring primordium, development centrifugal (centripetal), in concentric series or not, basally connate; G opposite sepals.
Age. The age of this clade is ca 64.8 Ma (Rose et al. 2018).
2. Scytopetaloideae (Engler) O. Appel
Growth ?sympodial; plants Al-accumulators; nodes?, bundles leave stele two internodes before entering leaves; (cristarque cells +), sclereids +; ?crystal chains, crystals octahedral; leaves amphistomatous); leaves 2-ranked, stipules +, minute; inflorescence axillary, branched to 1-flowered, axis terminated by a flower; (pedicels not articulated); K connate, ([2-)3-lobed, imbricate), C [?= staminodes] thick, connate, (splitting into 6-16 segments), (thin, plicate, margins serrate - Asteranthos, Crateranthus); A many, basally adnate to C, (anthers longer than filaments), (dehiscing by apical slit), (connective produced), (endothecium encircling whole anther - Crateranthus); tapetum glandular; (pollen tricolporoidate); (nectary 0); G superior (half superior), style relatively long, slender, stigma punctate to lobed; ovules 2-many carpel, (apical, campylotropous - Crateranthus), outer integument 5-8 (16-18 - Crateranthus) cells across, inner integument 5-9 cells across, endothelium +, (supra-chalazal zone long, narrow); fruit indehiscent (loculicidal capsule - Oubanguia); seeds often 1, with unicellular hairs or not, ruminate or not; testa cells often with crystals, testal bundle single or branched; endosperm +, ruminate (not Oubanguia), walls irregularly thickened, hemicellulosic, (embryo J-shaped), cotyledons accumbent, at least half the length of the embryo (ca 1/4 - Asteranthos); n = 11, 18, 21.
7/24. West tropical Africa, Asteranthos upper Rio Negro and Orinoco in Venezuela, Brazil, Colombia (map: See Prance & Mori 1979; Heywood 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Fruit.]
Synonymy: Asteranthaceae R. Knuth, nom. cons., Rhaptopetalaceae van Tieghem, Scytopetalaceae Engler, nom. cons.
[Lecythidoideae [Barringtonioideae + Foetidioideae]]: endosperm 0, embryo usually starchy.
Age. The age of this clade is ca 59.9 Ma (Rose et al. 2018).
3. Lecythidoideae Beilschmied
Secondary xylem with crystal chains; (colleters +); leaves two-ranked or spiral, lamina involute; (inflorescence cauliflorous); (flowers monosymmetric via connate androecium); C (4-5) 6; A incurved, filaments contracted at the apex; pollen tricolp/oroidate, (fodder pollen +); nectary 0/+; G [2-8] carpellate, style (long), stigma (lobed - Grias); ovules 3-many/carpel, (pendulous/erect), outer integument 5-25 cells across, inner integument 3-8 cells across, (outer integument with micropylar arilloid), (integuments basally connate), (micropyle short), outer epidermis 9-16 cells across, inner epidermis 5-9 cells across, endothelium +/0; fruit operculate (indehiscent); seed with swollen funicle, or aril (= wing), or neither, testal bundles (1-)2<; (endosperm sparse - Grias), embryo curved or not, hypocotylar or with long radicle and leaf-like (folded) or fat cotyledons; n = 17 (18); germination epigeal or hypogeal.
10/215: Eschweilera (ca 100), Gustavia (40). Neotropical (map, blue: from Prance & Mori 1979; Mori & Prance 1990). [Photos - Flower, Fruit, Flower, Fruits.]
Synonymy: Gustaviaceae Burnett
[Barringtonioideae + Foetidioideae]: cortical vascular bundles inverted; nodes 1:1; leaves supervolute; style long; fruit indehiscent; seeds 1/fruit.
Age. This clade is ca 29.5 Ma (Rose et al. 2018).
4. Barringtonioideae Beilschmied
Secondary xylem without crystal chains, axial parenchyma diffuse-in-aggregates; leaves spiral, vernation?, glands in the stipular position; K imbricate; (adaxial whorl(s) of A staminodial; pollen syntricolpate, strong colpus margin ridge; nectary annular; stigma punctate; ovules 1-many/carpel, (pendulous), endothelium 0 (+); (fruit many-seeded - Careya); testal bundles 2<; (endosperm sparse), embryo hypocotylar, (radicle long, coiled), (cotyledons plicate - Planchonia), (0 - Barringtonia); n = 13; nuclear genome [1C] ca 1319 Mb; germination epigeal/hypogeal/hypogeal, with first leaves reduced.
6/91: Barringtonia (73). Paleotropical (map above, Old World only, red: from van Steenis & van Balgooy 1966; Payens 1967; Liben 1971b; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower]
Age. Wood referrable to Barringtonia or Petersianthus is reported from the Late Cretaceous/Early Palaeocene Deccan Traps (Manchester et al. 2015 and references; Wheeler et al. 2017).
Synonymy: Barringtoniaceae F. Rudolphi, nom. cons.
5. Foetidioideae Niedenzu
Secondary xylem with crystal chains; leaves elongating in bud, petiole inconspicuous; K woody, C 0; A free, introrse; nectary indistinct; style 3- or 4-fid; ovules in two rows, ± campylotropous, integument largely connate, endothelium +; testal bundles 4-5; ?cotyledons; n = ?
1/18. E. Africa (Tanzania, Pemba), Madagascar, Comores, Mauritius and Reunion.
Synonymy: Foetidiaceae Airy Shaw
Evolution: Divergence & Distribution. For additional ages, see Rose et al. (2018).
Mori rt al. (2017) discussed the biogeography of Lecythidaceae in some detail.
Chartier et al. (2017) commented on the extent of androecial variation in the family compared to that in other ericalean families.
Ecology & Physiology. 19 of the 107 species of Lecythidaceae-Lecythidoideae from Amazonian forests are in the 227 species that make up half the stems of trees >10 cm across, so are disproportionally well represented (almost 8.4% of the total). They are second in terms of numbers of these species, although they are quite a small group, and they are third in terms of numbers of individuals (ter Steege et al. 2013: Fabaceae #1, Sapotaceae #2; c.f. in part Levis et al. 2017; Maezumi et al. 2018). 3 species are in the top 20 in terms of above-ground woody biomass, where they make up 3.96% of the total (Fauset et al. 2015: Fabaceae are #1).
Pollination Biology & Seed Dispersal. Monosymmetric Lecythidoideae are pollinated largely by euglossine bees. Several taxa have fodder pollen produced by the anthers in the hood (sometimes by some of those in the ring), and and as a result the pollen is heteromorphic; fodder pollen may even be in tetrads, unlike the pollen of the ring stamens (Ormond et al. 1981); nectar is also found in some of these taxa (Prance & Mori 1979; Mori & Prance 1990). These monosymmetric flowers are unlike those of any other angiosperm, with the monosymmetry primarily being evident in the massive development of the abaxial part of the staminal ring that leads to the production of the sometimes complexly coiled staminal hood into which the bees force their way. A rather close evolutionary association between euglossine bees and monosymmetric Lectythidoideae has been suggested (e.g. Mori & Boeke 1987); divergence of crown-group euglossines occurred some 42-27 Ma (Ramírez et al. 2010), that of the relevant Lecythidoideae...? Polysymmetric Lecythidoideae are pollinated by a variety of bees other than euglossines. Details of floral development, incuding the origin of monosymmetry, are to be found placed in a phylogenetic context in Tsou and Mori (2007). Interestingly, the polysymmetric Allantoma is embedded in the monosymmetric clade (e.g. Y.-Y. Huang et al. 2015).
Napoleonaea vogelii pollination and floral morphology has been described in detail (Frame & Durou 2001). Despite the size of the flower, pollination by thrips is suggested; there are also nectaries inside the flowers at the bases of some of the staminodes and also on the outside of the calyx.
The seeds of Lecythidoideae are large and are probably mostly dispersed by mammals, especially primates.
Chemistry, Morphology, etc. Lecythidoideae have characteristically fibrous bark. Gustavia has inverted cortical bundles in the stem (Metcalfe & Chalk 1950). There is banded apotracheal parenchyma (c.f. Sapotaceae!) and crystals in the axial parenchyma, the latter common in several other Ericales, but wood anatomy suggests little about groupings within Lecythidaceae (but see Mori & Prance 1990) and relationships of the family (c.f. Lens et al. 2007b). In both Barringtonioideae and Foetidioideae the nodal anatomy appears to be 3:3 if one looks only at the base of the petiole, but the nodes are 1:1 in a t.s. of the stem. Ditsch and Barthlott (1994) suggested that the rather dimorphic wax platelets of Asteranthos differ from those of Scytopetalaceae, but such platelets also occur in some species of Barringtonia (c.f. their figs 26, 27, 29), so are not out of place in Lecythidaceae. In at least some species of Barringtonia there are little glands in the stipular position; these are perhaps to be compared with the minute "stipules" of Scytopetaloideae (for which, see Breteler 2002). Cariniana is reported to have colleters on the leaf margin whose exudate provides lubricarion for the expansion of the young leaves (Paiva 2012; see also Fernandes et al. 2016); are these glands of Barringtonia, the teeth of other Lecythidaceae, and the stipules, also colleters...?
The Cariniana ianeirensis clade is described as having obliquely monosymmetric flowers (Mori et al. 2007, 2017; Huang et al. 2008), but this refers to the apex of the staminal tube, not the orientation of the whole flower with respect to the vertical axis. Androecial variation in Lecythidoideae is extreme - note that the erect and reflexed stamens mentioned by Mori et al. (2017: esp. Fig. 5) are here described as being incurved - and there is both centripetal and centrifugal androecial development (Tsou 1994). The carpels are shown as being opposite the petals (Ronse de Craene 2010, 2011) or opposite the sepals (Frame & Durou 2001). Although Tobe and Raven (1983a) suggested that Lecythidaceae have a multicellular archesporium, this would seem to be a mistake (see the observations of Tsou 1994). Are the ovules apotropous (Baillon 1877)?
The exact nature of the petal-like structures in the flower, especially in those of Napoleonoideae and some Scytopetaloideae, has been a matter of much discussion. Ronse de Craene (2010, esp. 2011) considers the former subfamily, at least, to have five petals that become fused and plicate, and there are more or less thread-like staminodes developing from all three androecial whorls. Prance and Jongkind (2015) suggest that the innermost incurved whorl of staminodes and stamens of Napoleonaea may represent two whorls, one staminal, the other staminodial; this would imply that there are four androecial whorls. The single "perianth" whorl of Asteranthos could be equated with either of the petaloid whorls in Napoleonaea (one the corolla, the other staminodial). More developmental studies on Napoleonoideae and Scytopetaloideae in particular are needed. (If Napoleonaea is considered to lack petals, the basic condition of the corolla for the family is ambiguous - c.f. Ronse de Craene 2011.) The diversity of embryo morphology, and hence details of germination, in Lecythidaceae is considerable (e.g. Payens 1967 and references).
For general information, see van Tieghem (1905b, as Rhaptopetalaceae), Prance and Mori (1979: monograph, 2004), Mori and Prance (1990: monograph), Prance (2008: Foetidia), Prance and Jongkind (2015: African taxa), Mori et al. (2017), and Mori's The Lecythidaceae Pages, Appel (1996, 2004), Letousey (1961), all Scytopetalaceae, Liben (1971a) and Prance (2004), both Napoleonaceae, also Endress (1994b: floral morphology), Mori et al. (2015a: placentation, Lecythidoideae), Mauritzon (1939a), Venkateswarlu (1952a), Vijayaraghavan and Dhar (1976: Scytopetaloideae) and Tsou (1994: not Scytopetaloideae), all embryology, Tsou and Mori (2002: seed coat anatomy in Lecythidoideae), and Takhtajan (1992: endothelium and testal vasculature.
Phylogeny. The set of relationships [Napoleonaeoideae [Scytopetaloideae [Lecythidoideae [Planchonoideae + Foetidioideae]]]] were recovered by Morton et al. (1998), Mori et al. (2007) and Rose et al. (2018). Initially there were no rbcL sequences for Crateranthus, but it was placed with Napoleonaea in joint analyses (see also this site prior to x.2014); matK analyses place it with Scytopetaloideae (D. Kenfack, pers. comm.). The relationships of Asteranthos were uncertain (e.g. Prance & Mori 1979; Mori & Prance 1990). In chemistry, morphology, etc., including its connate, serrate-margined "petals", Asteranthos is similar to Napoleonaeoideae (but c.f. style, endosperm), yet sequence data align it with Scytopetaloideae, and it is florally quite similar to Crateranthus, also in Scytopetaloideae. For phylogeny, see also Morton et al. (1997c, esp. 1998).
Within Lecythidoideae, there is a terminal polytomy made up of four genera (with a total of 115+ species), that is itself only weakly supported, and so it may collapse into a larger polytomy that also includes the [Allantoma + Cariniana decandra] clade (= Allantoma s.l., see Y.-Y. Huang et al. 2008; Mori et al. 2007). This latter may be an example of the derivation of polysymmetric flowers from a monosymmetric ancestor (there are many similar examples in the euasterids), but the current phylogeny does not yet provide strong support for this hypothesis. However, there is strong support for the hypothesis that the flowers of Lecythidoideae were initially polysymmetric, even if most species are monosymmetric (Mori et al. 2007). A morphological analysis of some 86 Lecythidoideae provided little phylogenetic structure, the biggest of the clades with over 50% bootstrap support (52%) containing only six species (Huang et al. 2011). Huang et al. (2015) found that Lecythis and Eschweilera were in eight clades among which Corythophora and Bertholettia were interspersed. Confirmation of relationships would be comforting...
Classification. Scytopetaloideae plus plus Asteranthos are placed as a subfamily in an extended Lecythidaceae, which can more or less be characterised, however, Lecythidaceae, as restricted to the last three subfamilies in the summary phylogeny above, cannot. Appel (1996) morphologically characterized two major groupings in Scytopelaloideae. For the beginnings of a phylogeny-based classification of Lecythidoideae, see Y.-Y. Huang et al. (2015) and Mori et al. (2015b).
Previous Relationships. Scytopetalaceae were considered quite distinct until recently, e.g. Cronquist (1981: in Theales) and Takhtajan (1997: in Ochnales) - both Dilleniidae.
[[Sladeniaceae + Pentaphylacaceae], [Sapotaceae [Ebenaceae + Primulaceae]], [Mitrastemonaceae, Theaceae, [Symplocaceae [Styracaceae + Diapensiaceae]], [[Sarraceniaceae [Roridulaceae + Actinidiaceae] [Clethraceae [Cyrillaceae + Ericaceae]]]]]: endothelium?
Age. K. Bremer et al. (2004a: but note topology) estimated the age of this node at around 107 My; ca 69.1 Ma is the estimate in Tank et al. (2015: Table S1), but stem Pentaphylacaceae, which are included here, are 83.4 Ma (Table S2), so something has gone wrong.
Chemistry, Morphology, etc. Vessel elements with vestured pits or walls are scattered, if uncommon, in this group - e.g. in some Symplocaceae, Theaceae, Ericaceae, Clethraceae, and Pentaphylacaceae (Ohtani 1983; S. Jansen et al. 1998 for general summary).
[Sladeniaceae + Pentaphylacaceae]: evergreen, woody; vessel elements with scalariform perforation plates; vessel-fibre pits bordered; nodes 1:1; petiole bundle arcuate; mucilage cells +; hairs unicellular; inflorescences/flowers axillary; C ± campanulate, only basally connate, white/whitish; A basifixed; pollen 14-30 µm long, surface usu. little ornamented; nectary 0; placentae becoming ± swollen; ovules bitegmic, micropyle endostomal, inner integument 3-4 cells across; fruit a loculicidal capsule, columella persistent, K persisting; endosperm +, embryo long.
Age. K. Bremer et al. (2004a) estimated this node to be ca 102 Ma, while Rose et al. (2018) estimated an age of ca 95 Ma, (97-)92(-90) Ma is the estimate in Wikström et al. (2015) and (100-)87.5(-73.5) Ma in Yu et al. (2017: note overall topology).
Pentapetalum trifasciculandricus is a fossil ca 91 Ma old from New Jersey that is placed either with Theaceae or in the Pentaphylacaceae area depending on the analysis (Martínez-Millán et al. 2009); the latter position was preferred by Martínez-Millán (2010).
Chemistry, Morphology, etc. The placenta is very well developed in Ficalhoa and many Ternstroemieae and Frezierieae.
Beauvisage (1920) remains a useful account of the vegetative anatomy - and general morphology - of the old Ternstroemiaceae. See Luna and Ochoterena (2004) and Martínez-Millán et al. (2009) for morphology.
Phylogeny. Luna and Ochoterena (2004) and Martínez-Millán et al. (2009) were unable to recover much in the way of strongly supported relationships in this area in morphological phylogenetic analyses. In some analyses in the latter paper Calophyllaceae (see Malpighiales) were included in Theales, and adding morphology in joint analyses tended to reduce support measures, perhaps especially bootstrap support.
A position of Pentaphylacaceae in Ericales seems reasonable from the gross morphological point of view. The anthers are superficially like those of Diapensiaceae, while Pentaphylax and Theaceae s.l. are generally similar. The seed is Ericalean (Huber 1991). For further discussion on the relationships of this clade, see the introduction to Ericales above.
Classification. Pentaphylacaceae have been recognised as a monotypic family (see e.g. A.P.G. 1998; first versions here), and A.P.G. II (2003) suggested as an option recognising three families, i.e. Pentaphylacaceae, Ternstroemiaceae, and Sladeniaceae. However, the first two are quite similar phenetically, far more so than they are to Sladeniaceae, and so two families are recognised in A.P.G. III (2009), Pentaphylacaceae being expanded to include Ternstroemiaceae.
Previous Relationships. See Theaceae for a family that largely included this whole group in the past.
SLADENIACEAE Airy Shaw - Back to Ericales
Chemistry?; cork cambium pericyclic; intervessel pitting opposite-alternate; lamina margins toothed; inflorescences cymose; flowers small [5³ mm long]; A (8-)10(-13), 15, anthers opening apically; style at most short, with relatively long pointed lobes.
2 [list]/3. S.E. Asia, tropical E. Africa.
Age. Rose et al. (2018) thought that the two genera included here diverged ca 88 Ma.
1. Ficalhoa Hiern
Exudate +; vessels not grouped; perulae 0; leaves 2-ranked, lamina vernation involute; C connate; A 15, in groups of 3 alternating with C, anther thecae dehiscing as slits across the apex; G , opposite K, placentation axile, placentae large, style short, slightly impressed; ovules many/carpel; fruit loculicidal capsule, smooth, K deciduous, style persistent; testa crustose, exotesta cells ± polygonal, little thickened; endosperm slight; n = ?
1/1: Ficalhoa laurifolia. Tropical E. Africa (map: see Verdcourt 1962; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
2. Sladenia Kurz
Vessels in radial groups; petiole also with wing bundles; perulae +; leaves spiral, lamina (margins entire); C basally connate; A (8-)10(-13), anthers sagittate, dehiscing by pores, monocot anther wall development; microsporogenesis successive [tetrads tetragonal]; G , placentation apical, gradually narrowed to indistinct/short style; ovules 2/carpel, apical, outer integument ca 3 cells across; embryo sac tetrasporic, 8-nucleate [Adoxa type]; fruit a ?schizocarp, longitudinally ridged, K persistent, endocarp crustaceous; seeds irregulary winged, testa thin, transparent; endosperm 0; n = 24.
1/2. S.W. China, adjacent Myanmar, Thailand and Vietnam (map: see above, from Flora of China 12, for fossil Sladenia [blue], see Giraud et al. 1992).
Age. The wood of extant Sladenia is distinctive, and matches fossil wood initially thought to be ca 100 Ma from the ?Cretaceous-Albian/Cenomanian of northern Sudan remarkably closely (Giraud et al. 1992), although redating has suggested that the wood is only around 72 Ma (references in Atkinson et al. 2017).
Chemistry, Morphology, etc. The pollen morphology and wood anatomy of Sladenia are very much those of Pentaphylacaceae, but there are no sclereids. Ficalhoa is very poorly known; it, too, lacks sclereids, but it was not associated with Sladenia in anatomical studies (especially Deng & Baas 1991). Li et al. (2003) have recently described a number of very distinctive embryological, etc., features for Sladenia, including monocot anther wall development; it will be interesting to see if Ficalhoa is similar in these respects..
For general information, see Stevens and Weitzman (2004).
Phylogeny. Sladenia was sister to Pentaphylacaceae (Ternstroemiaceae) in rbcL studies (Savolainen et al. 2000b), albeit the DNA was rather degraded. Sladenia and Ficalhoa come out as sister taxa in some recent molecular analyses (Anderberg et al. 2002); note, however, that Schönenberger et al. (2005) did not find support for this clade.
Previous Relationships. Sladenia has often been included in Theaceae, e.g. as Sladenioideae (see Takhtajan 1997).
PENTAPHYLACACEAE Engler, nom. cons. - Back to Ericales
Plants Al-accumulators; parenchyma apotracheal, diffuse or in short tangential lines; intervessel pitting opposite-scalariform; lamina supervolute; flowers single, from axils of reduced leaves; first A whorl opposite K, anthers with crystals in the connective [?Pentaphlylax]; style hollow; ovules campylotropous to hemitropous, apotropous when few [?Symplococarpon]; testa multiplicative, mesotesta well developed; embryo U-shaped.
12 [list - as tribes]/345 - three tribes below. Tropical and subtropical, but few in Africa.
Age. Rose et al. (2018) estimated the age of this clade to be ca 78.1 m years.
Pentaphylax and Visnea are reported fossil from late Cretaceous (Maastrichtian, ca 69 My) and Eurya from Santonian (ca 85 My) deposits in Europe (Knobloch & Mai 1986). If the latter date is confirmed, it would suggest an age for this node of at least 90 Ma.
1. Pentaphylaceae P. F. Stevens & A. L. Weitzman
Chemistry?; druses 0; buds perulate; stomata mostly paracytic; lamina margins entire; A 5, thecae valvate, filaments very broad, narrowed and incurved apically; pollen smooth, tectum thin, columellae poorly developed, endexine thick; G , opposite ?sepals, stigmas shortly radiate; ovules 2/carpel, apical, apotropous, outer integument ca 2 cells across, inner integument ca 2 cells across, ?parietal tissue; fruit with midrib separating from rest of valve [= teeth], endocarp cells transversely elongated; seeds flattened; exotestal cells slightly thickened, elongated, mesotestal cells large, ± thin-walled; endosperm development?, slight, cotyledons longer than the radicle; n = ?
1/1: Pentaphylax euryoides. Kwangtung and Hainan to Sumatra, scattered.
[Ternstroemieae + Frezierieae]: ellagic acid +, iridoids 0; (pits vestured); pith often with diaphragms; sclereids +; stomata anomocytic; perulae 0; C (whitish to yellowish to greenish); androecium initially with ± indistinct ring primordium, stamen formation centripetal; filaments to 2x longer than anthers, latter variable in length, connective usu. prolonged; fruit ± fleshy; mesotestal cells lignified, ± crystalliferous; endosperm +, ?nuclear, cotyledons incumbent, shorter than radicle.
Age. This node was dated to around 66.7 (Rose et al. 2018), (61-)55, 54(-48) (Wikström et al. 2001) or (69-)54, 51(-35) Ma (Bell et al. 2010).
2. Ternstroemieae de Candolle
Sclereids much branched; leaves pseudoverticillate, lamina often with black spots, margins entire to crenulate; K opposite C, C to 2/3 connate, (with narrowed then broadened apical portion - Anneslea); A in oppositipetalous fascicles, development centripetal, filaments shorter than anthers; G [2-3], (inferior - Anneslea); ovules 4-12/carpel, apical, outer integument 6-9 cells across; fruit dehiscing irregularly; seeds few, ± dangling, >3 mm long, brown, sarcotestal [either exotesta or pockets of fleshy cells on either side of seed], unlignified exo-/mesotesta to 10 cells across, lignified mesotesta 7-15 cells across; n = 20, 25.
2/103: Ternstroemia (100). Tropics, esp. Malesia and Central to South America (map: from Camp 1947; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Australia's Virtual Herbarium viii.2013; M. Sosef, pers. comm.). [Photo - Flowers & Fruits © Nick Turland.]
Synonymy: Ternstroemiaceae de Candolle
3. Freziereae de Candolle
(Nodes 1:3, 3:3 [some Freziera]); sclereids usu. little branched; leaves scattered along shoot, two-ranked (spiral), lamina margins entire to serrate; plant dioecious or flowers perfect; inflorescence also fasciculate, (flowers from axils of expanded leaves); (K connate); C (urceolate), (orange-red - Balthasaria, purplish); A 5-30(-60), from ring primordium, in a single whorl, (filaments to 5x longer than anthers - Cleyera), (connective not prolonged); G [(1-)3(-10)] (inferior - Symplococarpon), (placentation parietal), (styluli +); ovules 4-many/carpel, outer integument 3-4 cells across; fruit indehiscent, fleshy, a berry (drupe); seeds (1-)many, <4(-6) mm long, brown or black, inner walls of exotesta thickened and lignified or not, lignified mesotesta 1-5 cells across; (embryo curved); n = (12, 13(?), 15, 18) 21 (-23), etc.
9/240: Adinandra (80), Eurya (75), Freziera (63). Southeast Asia to Malesia, Hawaii, Central to South America, E. (Balthasaria) and W. (Adinandra) Africa, and Canaries (Visnea) (map: from Camp 1947; Verdcourt 1962; van Balgooy 1975; Weitzman 1987). [Photo - Eurya Flower, Flowers & Fruits, Flower, Fruit.]
Age. The crown group age of Freziereae is ca 51.9 Ma (Rose et al. 2018: Visnea sister).
Fossils of Eurya are reported from Europe from the late Cretaceous ca 70 Ma onwards (H. Zhu et al. 2016) - which disagrees with the ages above, and oc course Eurya is now no longer known from Europe.
Evolution: Divergence & Distribution. Visnea mocanera (Frezierieae), from the Canary Islands/Madeira, is very isolated (see map) from the rest of the family, whether as the result of vicariance as the North Atlantic opened 120-100 Ma (Grehan 2017: less likely), or dispersal from the East, Palaeo-Macaronesia being 60 Ma or more old (the oldest currently emergent Canary Island is ca 21 My: see Gelmacher et al. 2005; Fernández-Palacios et al. 2011).
Pollination Biology. Buzz pollination has been described in Ternstroemia. Thus the partly connate petals of T. laevigata form a tube with a narrow, fluted apical opening and the spreading sepals with their red margins perhaps function as petals (Bittrich et al. 1993). Anneslea has remarkable petals that become narrowed, but a broadened apical portion surrounds the protruding style - buzz pollination here, too?
Genes & Genomes. Hao et al. (2010) note that the atp1 mitochondrial gene in species of Ternstroemia is highly chimaeric, and transfer (?how), probably from Vaccinium, may have occurred ca 15-50 Ma; some "host" genes have been converted by Vaccinium mitochondrial genes...
Chemistry, Morphology, etc. Freziera shows considerable variation in nodal anatomy and stomatal morphology (Weitzman 1987). Although the leaves of Pentaphylax are entire, they, the bracts, and some sepals, are terminated by blackish, deciduous and probably glandular points, rather similar to those found in the rest of the Pentaphylacaceae. Its pericylic sheath consists of fibres alternating with lignified parenchymatous cells (Beauvisage 1920). Cleyera (Freziereae) lacks pericyclic fibres in the petiole.
The flowers are very often single in the axils of reduced leaves; if the shoot of Pentaphylax does not develop expanded leaves after the flowers appear, the inflorescence appears to be racemose. If the flower-bearing shoot is very much reduced, then the inflorescence is fasciculate. For variation in seed type and pollen surface of Freziera, see Weitzman (1987). Cleyera, and also Eurya (for which see W. H. Brown 1938), secrete nectary from the basal part of the ovary wall. Taxa such as Cleyera have quite long filaments. The reports of an aril in Ternstroemieae (e.g. Keng 1962) are incorrect; there is a sarcotesta which may, by its expansion, aid in the irregular rupture of the fruit.
For general information, see Weitzman et al. (2004, as Ternstroemiaceae), for some embryology, see Mauritzon (1936a), for floral development, see Tsou (1995), Zhang et al. (2007), and Zhang and Schönenberger, and for pollen, see Lobreau-Callen (1977) and Wei (1997).
Pentaphylax is particularly poorly known.
Phylogeny. For a phylogeny that includes Theaceae s. str. and a few other Ericales, see Yang et al. (2006: relationships unclear) and Su et al. (2011: mostly Theaceae included); the latter found that Euryodendron was well supported as sister to Eurya. The tribes above were recovered by Tsou et al. (2016), although relationships within Freziereae in part depended on the marker used, and also by Rose et al. (2018).
Pentaphylacaceae-Frezierieae and -Ternstroemieae are morphologically amply distinct from Theaceae. The former have pollen 14-28.5 µm long (versus 36.5-54.5 µm), vessel-fiber pits bordered (versus unbordered), etc.. However, differences in the relative length of the radicle in the embryo (long radicle in Pentaphylacaceae, short in Theaceae) are not so clear-cut given the inclusion of Pentaphylax itself and Sladeniaceae in the mix.
Previous Relationships. Theaceae often included Ternstroemia and relatives; thus Ternstroemioideae were a subfamily of Theaceae in Takhtajan (1997). On the other hand, Beauvisage's (1920) Ternstroemiaceae included Theaceae, even if he also removed some seventeen separate elements from the family (including Pentaphylax), most of which he thought were unrelated to each other. They included genera now placed in Marcgraviaceae, Ochnaceae-Medusagynoideae, Calophyllaceae, Bonnetiaceae, Actindiaceae, Stachyuraceae, Strasburgeriaceae, and so on. Cronquist (1981) circumscribed Theaceae quite broadly, but the families he did remove he thought were close to them. Theaceae were a major linking family in evolutionary classifications - "It is generally agreed that the Theaceae are closely related to the Dilleniaceae..." (Cronquist 1981: p. 323).
[Sapotaceae [Ebenaceae + Primulaceae]]: ellagic acid 0; C connate; ovules apotropous.
Age. The age of this node is around 84.3 or 82.3 Ma (Tank et al. 2015: Table S1 and S2), 94.4 Ma (Magallón et al. 2015), (101-)92(-79) Ma (Wikström et al. 2015) or ca 102.3 Ma (Rose et al. 2018).
Chemistry, Morphology, etc. For ovules, see Warming (1913).
Phylogeny. Sapotaceae and Primulaceae s.l. were sister taxa (89% bootstrap) in a six-gene study focusing on Ebenaceae (Duangjai et al. 2006b); the latter was part of a polytomy including many other Ericales.
SAPOTACEAE Jussieu, nom. cons. - Back to Ericales
Trees and shrubs; saponins, C-30 oxidised triterpenes, pyrrolizidine alkaloids, flavonols, leucodelphinidin, gutta, myricetin +; (vessel elements with scalariform perforation plates); wood siliceous and/or with SiO2 grains; nodes (1:1) 3:3; (medullary bundles +); petiole bundle arcuate, horizontal D-shaped or annular (wing bundles +); latex sacs +; sclereids +; hairs T-shaped, arms unequal or not, unicellular (not in Delpyodon), brownish; leaves (two-ranked, opposite), lamina vernation conduplicate, margins entire (toothed), secondary veins often rather close, stipules +, cauline; inflorescences cymose, fasciculate, pedicels not articulated; flowers (anisomerous); K ± connate at base, C 4-18, A = C, opposite C, introrse to extrorse, staminodes +, opposite K; tapetal cells multinucleate; pollen 3-6-colporate, infratectum ± granular; disc + (0); G with hairs on the inside of the ovary, placentation axile to axile-basal, (style short), stigma punctate or minutely lobed, dry; ovules 1(-5)/carpel, ascending, integument single, "thick", (vascularized), hypostase 0; fruit a berry (drupe), K persistent; seeds large, hard, shiny, hilar scar large, white; testa multiplicative, outer part with isodiametric heavily lignified cells; endosperm nuclear, + or 0; n = (10-)13(-14).
53 [list]/1,100 (1,275) - four clades below. Pantropical.
Age. Crown-group Sapotaceae have been dated to (105-)84.5(-67.1) Ma (Richardson et al. 2014), ca 107 Ma is the age used in Armstrong et al. (2014), while Rose et al (2018) estimate an age of only 58.3 Ma.
1. Sarcospermatoideae Swenson & Anderberg
Leaves ± opposite, (stipels +); inflorescence axis apparently well developed [actually a reduced branch]; A basifixed, staminodes short, broad, scale-like; disc 0; G 1[-2], style stout; seeds not laterally compressed; endosperm 0, cotyledons ± connate; n = ?
1/6. Indo-Malesia (map: from Aubréville 1964).
Synonymy: Sarcospermataceae H. J. Lam
[Eberhardtia [Sapotoideae + Chrysophylloideae]]: ?
Age. Rose et al. (2018) suggest that this node is ca 41 Ma old.
C with three segments, centre segment narrow; A 5, staminodes with versatile inverted V-shaped staminode; endosperm copious; n = ?
1/3. South China, Vietnam, Laos, Sabah.
[Sapotoideae + Chrysophylloideae]: (stipules 0); (plants di- or monoecious); C variously lobed or not; stamens = and opposite to 2x (-6x) C lobes, staminodes often ± petal-like (0); G 1-[2-14(-30)]; endosperm +/0, (cell walls with xyloglucans [thick, pitted - amyloid]); nuclear genome [1C] (274-)1979(-2513) Mb. [Photos - Collection, Fruit].
Throughout the tropics (map: from Aubréville 1964).
Age. This node, containing the bulk of diversity in the family, is estimated to be a mere 30.4.Ma by Rose et al (2018).
Hofmann (2018) records a diversity of sapotaceous pollen from western Europe; by around 56 Ma there was pollen she placed in Sarcospermoideae and at least two clades in Chrysophylloideae, one now largely South American and another Australasian, and by that time or soon after there was also pollen identifiable as Sapotoideae.
2. Sapotoideae Eaton
Stipules cauline/0; (K in two whorls of 2-4 valvate members in each), (petals with three segments); (A = 2 X C - Isonandreae); seed with lateral? hilum; endosperm ?.
27/543: Palaquium (120), Madhuca (110), Manilkara (80), Sideroxylum (75), Mimusops (50). Pantropical.
Synonymy: Achradaceae Vest, Boerlagellaceae H. J. Lam, Bumeliaceae Barnhart
3. Chrysophylloideae Luersson
A high in the tube, (several stamens opposite each C), (staminodes outside/above the staminal whorl); (style with separate stigmatic areas); endosperm copious or 0, cotyledons foliaceous, radicle exserted or not.
25/550: Pouteria (235 - number very uncertain), Planchonella (110), Chrysophyllum (80), Pycnandra (66), Pleioluma (ca 40), Micropholis (38). Pantropical.
Age. Crown Chrysophylloideae are some (105-)91.7(-79) Ma (Bartisch et al. 2010).
Evolution: Divergence & Distribution. Bartish et al. (2010) discuss the historical biogeography of Chrysophylloideae, and find long distance dispersal to dominate when explaining the current distributions of members of the group. The southeast Asian Xantolis is sister to the rest, and early diversification of other Chrysophlloideae perhaps occurred in Africa in the Campanian 83-73 Ma, although much diversification in the subfamily is Caenozoic in age. It is possible that Australian elements arrived from America via an Antarctic land bridge (Bartish et al. 2010, q.v. for further discussion, dates, etc.). The largely New Caledonian Niemeyera clade (= Pycnandra, the largest endemic clade on the island) reached there in the latter part of the Oligocene (Swenson et al. 2008c; c.f. Ladiges & Cantrill 2007), overall, it is estimated that Chrysophylloideae have moved to New Caledonia around nine times since the emergence of the island around 37 Ma (Grandcolas et al. 2008; Swenson et al. 2014; see also Nattier et al. 2017). For diversification within Pycnandra, which seems to include cryptic species separated by geography, soil and/or altitude, see Swenson et al. (2015).
The descendents of a possible ancient hybridisation 43-36.6. Ma between a basically African clade and a basically American clade in Sideroxylon (Sapotoideae) were previously segregated as Nesoluma; they are now to be found on very young islands in the Pacific and may have been hopping from island to island for the last 40 Ma or so (Smedmark & Anderberg 2007; for other taxa behaving similarly, see Hillebrandia [Begoniaceae], Psiloxylum [Myrtaceae], various Rutaceae, etc.). Isonandreae also show much dispersal both across water and over land, especially from the Sundaland area (Richardson et al. 2014, q.v. for dates). Sapotoideae in general are quite old, but drift cannot be implicated in causing their disjunct distributions, migration via the boreotropical route stopped around 33 Ma, and so long distance dispersal may well be responsible for disjunct distributions like those in Manilkara (Armstrong et al. 2014).
Morphological characters are highly homoplasious and characters for the subfamilies are hard to come by; see Smedmark et al. (2006) for character evolution in Sapotoideae.
Ecology & Physiology. Sapotaceae are notably common in terms of both numbers of species and individuals in the Amazonian tree flora, ranking second in the latter category (Fabaceae are #1) althouth they are not notably well represented in the 227 species that make up half the stems 10 cm. or more d.b.h. in Amazonian forests (ter Steege et al. 2008, 2013, but c.f. in part Levis et al. 2017; Maezumi et al. 2018). 22 species of Pouteria have been found in a single hectare there, and Sedio et al. (2017) suggest that such aggregations are allowed by extensive interspecific variation in secondary metabolites affecting herbivory.
The New Caledonian Sebertia acuminata (sève bleue) is a nickel hyperaccumulator, and its sap contains some 11% wet weight, 25.7% dry weight of the metal (Jaffré et al. 1976).
Seed Dispersal. For the cautionary tale of the dodo and the tambalacoque, see Herhey (2004). Seeds of the argan tree, Argania spinosa, are dispersed when the goats that eat the fruit as they graze the canopy of the tree (they are arboreal) spit the seeds out while chewing their cud (Delibes et al. 2017).
Genes & Genomes. The mitochondrial coxII.i3 intron is absent in Chrysophyllum, at least (Joly et al. 2001).
Economic Uses. Chicle, a complex rubber once used in chewing gum, is the exudate of Manilkara zapota.
Chemistry, Morphology, etc. There is banded apotracheal parenchyma in Sapotaceae (c.f. Lecythidaceae). Some species of Sarcosperma have paired stipels at the apex of the petiole, a rather unexpected character for a member of Ericales. Anderberg and Ståhl (1995) suggest that bracteoles are absent, Wood and Channell (1960) that they are present.
Floral variation is considerable and most characters are very homoplasious (e.g. Swenson et al. 2008a, b, c). The flowers are sometimes described as being up to 6-merous, i.e. following the number of sepals in a single whorl, however, petals, androecium and gynoecium must then be considered to have doubled in number (see Pennington 2004: a good summary of floral variation). Swenson and Anderberg (2005) suggest that the basic floral morphology of the family is K5, C5, A 5 + 5 staminodes, however, anisomery is scattered in Sapotaceae, with different numbers of parts in different whorls (Swenson et al. 2008c; see also Wanntorp et al. 2011). Kümpers et al. (2016) looked at floral variation, particularly merosity, in Sapotaceae in considerable detail, and noted a variety of ways in which it could change, which led to increases in numbers of all or most parts of the flower, however, carpel and stamen number sometimes increased independently of any general changes in merosity. Swenson and Anderberg (2005) suggested that the staminodes common in Chrysophylloideae were perhaps derived within the clade, and were mot immediately comparable with those of other members of the family; the former are outside the staminal whorl while the latter are in the same whorl as the stamens. Penningon (2004) described the fruit of Eberhardtia as being a loculicidal capsule, but it appears to be a berry (e.g. S.-g. Li & Pennington 1996). Three genera do have capsular fruits, but there is only one seed, little or no endosperm, and they are African (Penningon 2004).
Amyloid is also known from the seeds of Omphalocarpum, a clade that is close to sister to the rest of Chrysophylloideae (see Kooiman 1960).
For general information see Franceschi (1993), and Ng (1991), and especially Pennington (1991, 2004). For pollen, see Harley (1991), for the androecium, see Ronse De Craene and Bull-Hereñu (2016).
Phylogeny. Sarcosperma is sister to the rest of the family. Its seed has a shiny testa, albeit not as thick as that of most other Sapotaceae; the genus was placed in Sideroxyleae by Pennington (1991). Recent work suggests that Eberhardtia may be sister to the remainder (Z.-D. Chen et al. 2016; Rose et al. 2018).
Within the rest of the family there are two major clades, the (Isonandreae + Mimusopeae + Sideroxyleae) (= Sapotoideae) and (Chrysophylleae + Omphalocarpeae) (= Chrysophylloideae) (e.g. Swenson & Anderberg 2005). These clades also appeared in a combined molecular + morphological analysis and after successive weighting, the latter still with only moderate support (79% jacknife) because of the inclusion of Xantolis, the rest of that clade minus Xantolis having 97% support (Swenson & Anderberg 2005; see also Anderberg & Swenson 2003; Bartisch et al. 2010). However, in a study that focussed on Isonandreae (Sapotoideae), relationships are messier, and Eberhardtia was well separated from other Isonandreae and sister to a clade that includes Chrysophylloideae that is embedded in Sapotoideae (Richardson et al. 2014).
See Smedmark et al. (2006) for a general discussion of relationships in Sapotoideae. For relationships in Sideroxylon, see Stride et al. (2014).
Swenson et al. (2007a, 2008a, 2013) discuss generic limits in Australasian members of Chrysophylloideae; the whole lot are monophyletic, and Beccariella is sister to the rest. For relationships among the monophyletic group of the ca 80 species of the Pouteria complex on New Caledonia, see Bartish et al. (2005); Pouteria sensu Pennington is polyphyletic (Triono et al. 2007), as is Chrysophyllum (Terra-Araujo et al. 2015), the former appearing in eight places in a tree of neotropical Chrysophylloideae and the latter three times (De Faria et al. 2017). See Swenson et al. (2007b) for Planchonella and Swenson et al. (2008c) for its sister group, the largely New Caledonian Niemeyera complex. Spiniluma is to be included in this subfamily (Stride et al. 2014).
Classification. For a classification of Chrysophylloideae in Southeast Asia/Oceania, see Swenson et al. (2013).
Generic limits have been notoriously fickle in Sapotaceae: "it is difficult to understand how two authors working on the same family could have come to such widely different conclusions" (Pennington 1990, p. 29). Pennington himself (1991) helped clarify things somewhat and molecular data are providing much further information. Thus clade limits in e.g. New Caledonian Sapotaceae-Chrysophylloideae are clear enough so that species can be described in their proper genera (e.g. Swenson et al. 2008b, esp. c), however, sampling in neotropical Chrysophylloideae has to be improved before generic limits can be addressed (De Faria et al. 2017). For a checklist and bibliography, see Govaerts et al. (2001), but generic limits are dated.
[Ebenaceae + Primulaceae]: ovules bitegmic, inner integument thicker than the outer.
Age. This node is ca 81.1 Ma (Tank et al. 2015: Table S2), around 87 Ma (Magallón et al. 2015), (99-)88(-74) Ma (Wikström et al. 2015), (105.5-)96.5(-84) Ma (Yu et al. 2017: note overall topology) or ca 100.9 Ma (Rose et al. 2018).
EBENACEAE Gücke, nom. cons. - Back to Ericales
Trees, bark and roots black; petiole bundle arcuate; sclereids +; leaves two-ranked, lamina margins entire, lower surface with flat glands; pedicels articulated; flowers imperfect, ?4-merous; K connate, C contorted; staminate flowers: stamens adnate to corolla, in two series, basifixed, anthers long, connective prolonged, pistillode +; carpellate flowers: staminodes +, style ± divided; ovules 2/carpel, pendulous, apotropous; fruit a berry, K persistent; testa vascularized; endosperm copious, hard, mannose-rich polysaccharides +, radicle long.
4 [list]/553 (800) - two subfamilies below. Tropical (to temperate).
Age. Crown-group Ebenaceae are estimated to be some (65-)54(-42) Ma (Turner et al. 2013a) or ca 57.1 Ma (Rose et al. 2018).
1. Lissocarpoideae Wallnöfer
Chemistry?; cork?; (vessel elements with scalariform perforation plates); (petiole bundle arcuate but with recurved edges and wing bundles); stomata anomocytic and cyclocytic; plant glabrous; dioecious; flowers axillary, or inflorescences subfasciculate; bracteoles large, apical; flowers 4(-5)-merous; C often with an 8-lobed corona; nectary?; staminate flowers: A 8, filaments basally connate; pollen 3-porate, 40-70 µm across, psilate; carpellate flowers: ovary inferior, , stigma clavate, hairy apically; ovule morphology?; seeds 1-2; testa?; endosperm very hard; cotyledons foliaceous; n = ?
1/8. Tropical N.W. South America (map: from Wallnöfer 2004b).
Synonymy: Lissocarpaceae Gilg, nom. cons.
2. Ebenoideae Thorne & Reveal
Saponins, C-30 oxidised triterpenes, naphthoquinones [derivatives of 7-methyljugone and plumbagin], flavonols, leucodelphinidin, myricetin +; (cork pericyclic); cambium storied; (nodes 1:3); SiO2 bodies + [not in Diospyros]; secretory cells common; cuticle wax crystalloids 0; stomata usu. paracytic; hairs (T-shaped), unicellular; terminal bud aborts; leaves (opposite, spiral), lamina conduplicate; inflorescence cymose, axis short; flowers 3-7-merous, urceolate to campanulate, rather small [usu. <1 cm long]; (C valvate), nectary +/0; staminate flowers: A (3-)12-20(-many), (inner anthers extrorse), often hairy; pollen 25.9±6.4 µm across, infratectum granular; pistillode?; carpellate flowers: (staminodes 0); G [2-8], opposite C or K, loculi often divided, stigmas little expanded, dry; micropyle bi/endostomal, outer integument 3-7 cells across, inner integument 5-10 cells across; K often accrescent; seed pachychalazal, often ruminate, testa multiplicative, radicle in pocket formed by testa (not - Diospyros), ± parenchymatous, or exotesta fibriform or mucilaginous, cells cuboid to palisade, endotesta crystalliferous or not, walls thickened or not; endosperm ± hard, cells thick-walled; n = 15; nuclear genome [1C] (1171-)1903(-2814) Mb.
3/545: Diospyros (500+). Tropical (to temperate) (map: from Morley & Toelken 1983; Wickens 1976; White 1988; Autralia's Virtual Herbarium iii.2014). [Photo - Carpellate flower, Fruit, Collection.]
Age. Crown-group Ebenoideae have been dated to (50-)42(-35) Ma (Turner et al. 2013a) or ca 38 Ma (Rose et al. 2018).
Fossil flowers and associated leaves (Austrodiospyros) are known from Middle Eocene rocks of southeastern Australia ca 33.9 Ma (Basinger & Christophel 1985; Martínez-Millán 2010), while fossil pollen from western Europe suggests that diversification in this subfamily had begun by ca 56 Ma (Hofmann 2018).
Synonymy: Diospyraceae Vest, Guaiacanaceae Jussieu, nom. illeg.
Evolution: Divergence & Distribution. Duangjai et al. (2009) found four separate lineages of Diospyros in New Caledonia, Turner et al. (2013a, b) noting that speciation there has occurred within the last 10 Ma. Resolution of relationships between species was often difficult, even when looking at a combination of whole plastid genomes and ribosomal DNA (Turner et al. 2016). In the largest of these clades, with some 24 species, initial divergence seems to have been mediated by climate or other features affecting the macrohabitat, but latterly differences in substrate/soils triggered speciation (Paun et al. 2015).
Geeraerts et al. (2009) suggested apomorphies - especially palynological - for genera of Ebenoideae. The chemistry of Lissocarpoideae is unknown, so whether the presence of naphthoquinones is a synapomorphy of Ebenaceae as a whole or just part of them remains to be established.
Diospyros is about the most diverse genus in West Malesian l.t.r.f. (Davies et al. 2005).
Plant-Animal Interactions. Extrafloral nectaries occur widely in Ebenaceae (Weber & Keeler 2013).
Chemistry, Morphology, etc. Ellagic acid may occur in Ebenaceae-Ebenoideae (Bate Smith 1962). Vessels sometimes occur in radial multiples. Both Massart's model (rythmic monopodial branches) and variants (e.g. Roux - continuous branching) occur in Diospyros. The terminal bud of each innovation frequently aborts. The flat foliar glands are extrafloral nectaries and they are quite often closely associated with vascular bundles; they probably occur in about three quarters of the species in the family (Contreras & Lersten 1984).
The morphology of the inflorescence of Lissocarpoideae is unclear; one interpretation is that the flowers are axillary, whether on short or long shoots. The flowers seem to be imperfect, at least some "perfect" flowers not producing fertile pollen despite having well developed anthers (Wallnöfer 2004a). In Diospyros s.l., both integuments appear to be very thick, although the inner is only three cells across at the endostome (van Tieghem 1898). There is variation in germination - foliaceous cotyledons and alternate subsequent leaves vs thick cotyledons and opposite leaves.
For general information, see Franceschi (1993), Ng (1991), and Wallnöfer (2001). For Diospyros and relatives and carpel orientation, see Baillon (1891), Eichler (1875) and Le Maout and Decaisne (1868), for some seed anatomy, see Quisumbing (1925). Some information on Lissocarpa is taken from Schadel (1978: leaf morphology) and Wallnöfer (2004a, b), but that genus is poorly known.
Phylogeny. Rather degraded rbcL sequences initially suggested that Lissocarpa was to be included in Rutaceae (Sapindales) (Savolainen et al. 2000a). However, it is well supported (rbcL only) as sister to Ebenaceae s. str. (e.g. Berry et al. 2001; Rose et al. 2018).
Duangjai et al. (2006a and especially b), sequencing six plastid genes, found extensive phylogenetic structure in Ebenoideae; the African(-Arabian) Euclea and Royena were sister to Diospyros, and within Diospyros there were a number of well-supported clades, although relationships between them were unclear. Duangjai et al. (2009: eight genes, 119 species) provided a more detailed phylogeny of Diospyros s. str. with good Bayesian support for relationships along the backbone of the tree.
Classification. Lissocarpaceae have often been placed in or close to Ebenaceae, but they were unassigned in A.P.G. I (1998). Since the two have morphologically much in common, it is reasonable to combine them (see A.P.G. III 2009).
PRIMULACEAE Borkhausen, nom. cons. - Back to Ericales
(Schizogenous secretory canals [material yellow, red, brown: tannins, etc.]); saponins common; rays 1-3 cells across; nodes ?3:3; peltate trichomes +; stomata paracytic; inflorescence racemose; C and A from common primordia; A = C , opposite C, staminodes +, opposite K; nectariferous tissue on G; G , opposite C, placentation free-central, with sterile apical projection, style short, hollow, stigma ± capitate; ovules at least partly immersed in swollen placenta, apotropous, micropyle bistomal, outer integument ca 2 cells acrooss, inner integument 3-4 cells across, endothelium tanniniferous; seeds angled; endotesta crystalliferous; endosperm nuclear, copious, cell walls with xyloglucans [thick, pitted - amyloid).
58/2,590 - four subfamilies below, for synonymy, see under the subfamilies. World wide.
Age. Wikström et al. (2001) suggest a crown group age of around (52-)49, 46(-43) My; this age is estimated at (74-)61, 57(-45)Ma by Bell et al. (2010) and ca 79.5Ma by Rose et al. (2018).
Evolution: Divergence & Distribution. Wanntorp et al. (2012) discuss the evolution of a number of characters of floral development in this clade. Where on the tree the character "ovules embedded in the placenta" should be placed is unclear; the placenta sometimes seems to envelope the ovules after fertilization, as in the image of the fruits of Stimsonia in Wanntorp et al. (2012).
Ecology & Physiology. Aegiceras is quite often to be found in mangroves; its seeds tend to sink quite quickly (Clarke et al. 2001). For the evolution of the mangrove habitat, see Rhizophoraceae
Plant-Animal Interactions. Plants of this group are not often eaten by butterfly larvae, but the 110 species of the largely Old World (there are two species from the Caribbean) Lycaenidae-Riodinidae-Nemeobiinae are known only from Primulaceae, especially Maesa, but so far they have not been found on members of Theophrastoideae (Espeland et al. 2015); Ehrlich and Raven (1964) noted other records.
Chemistry, Morphology, etc. For wood anatomy (not Primuloideae!) see de Luna et al. (2018). There are small often peltate/glandular hairs; these may be stalked (Primuloideae) or more or less immersed (Theophrastoideae), while there are both kinds in Myrsinoideae (Große 1908). Leaves of Theophrasteae and Myrsinoideae are often described as being involute (?supervolute, c.f. Cullen 1978) or conduplicate.
There are common stamen/corolla primordia in turn born on a ring primordium in this clade, but the position/relative development of these primordia varies. In some cases such as Cyclamen the stamens are initiated as adaxial outgrowths of a common primordium, i.e. the petal primordia are initially larger than the stamen primordia, as also in Myrsine and Aegiceras (see especially Ma & Saunders 2003), whereas in other taxa it is the stamen primordia that are early larger, as in Samolus (e.g. Sattler 1962). However, this is a tricky character, since there are really two variables, the relative positions of these primordia and the relative speed of their development, and, as with evicted terminal inflorescences, initial topological relationships between parts can speedily become disrupted by post-initiation growth. The staminodes of Samolus and Theoprasteae are developmentally rather different (Caris & Smets 2004); even in taxa lacking staminodes such as Maesa there is commonly a staminodial vascular supply (e.g. Subramanyam & Narayana 1976; see also Saunders 1934).
The number of carpels is difficult to ascertain (see especially Sokoloff et al. 2017a), but five seems to be a common number; although their orientation is often unclear, they might be expected to be opposite to the sepals. However, several of the diagrams presented by Dickson (1936) suggest that the carpels are opposite the petals, but in Primula, at least, the carpels appear to be opposite the sepals - although not always (Subramanyam & Narayana 1976).
For general information, see Anderberg et al. (2000) and especially Ståhl and Anderberg (2004). For wood anatomy, see Lens et al. (2005a) and de Luna et al. (2017, 2018), for the hollow style, see Guéguen (1901: is the condition in Maesa known?), for nectaries and nectar/oil, variously produced, see Vogel (1986, 1997) and Caris and Smets (2004), for floral morphology and ontogeny, see Dickson (1936: esp. gynoecial arrangement), Sattler (1962), Sundberg (1982), Ronse Decraene (1992), Ronse Decraene et al. (1995) and especially Ma and Saunders (2003), for embryology, etc., especially of the herbaceous taxa, i.e. Primulaceae in the old sense, see Dahlgren (1916) and Subramanyam and Narayana (1976), and for that of other taxa, see Warming (1913), and for seed and endosperm, for the most part poorly correlated with major clades, see Morozowska et al. (2011: no Maesa).
Phylogeny. The monophyly of Primulaceae s.l. is not in doubt (see Anderberg & Ståhl 1995; Anderberg et al. 1998; and especially Källersjö et al. 2000): support values for Samolus as sister to Theophrasteae are reduced when morphological and molecular data are combined. In the morphological analysis of Anderberg and Ståhl (1995) herbaceous taxa grouped together, and Theophrastaceae were sister to the rest, i.e., relationships were basically conventional.
Classification. This group was often recognised as Primulales in the past. The only question, particularly in light of the break-up of Primulaceae, the removal of Maesa from Myrsinaceae, the placement/addition of Samolus as sister to the old Theophrastaceae, the many herbaceous ex-Primulaceae that are sister to the old-style, woody Myrsinaceae rather than being in a clade with other Primulaceae, and the numerous features shared by the group as a whole, was whether it was worth recognising families at all. A broad circumscription of Primulaceae was proposed in A.P.G. III (2009); Primulaceae s.l. are well characterized, and available subfamilial and tribal names fit well with the phylogeny here.
Previous relationships. Plumbaginaceae (see Caryophyllales here) were often associated with Primulaceae, both having features like apparently similar placentation and stamens opposite the petals in common (see Cronquist 1981 for discussion).
1. Maesoideae de Candolle
Lianes, shrubs or trees; (vessels with scalariform perforation plates); petiole bundles three, annular; glands/canals throughout the plant; leaves spiral or two-ranked, lamina vernation induplicate, margin toothed to entire; inflorescence often branched; flowers small [<7 mm across]; C urceolate, induplicate-valvate; petals developing before the stamens; A basally connate, attached at the middle of the C tube; G [3-4], semi-inferior, stigma truncate or capitate and lobed; fruit a many-seeded drupe, K persistent; testa 2-layered, inner layer with rhombic crystals; n = 10.
1 [list]/150. Old World tropics to Japan, the Pacific, and Australia (map: from Coates Palgrave 2002).
Chemistry, Morphology, etc. Vessels are in radial multiples as is quite common in woody Theophrastoideae and woody Myrsinoideae; there may be groups of druses in the abaxial epidermis; the fibres are septate; and the lateral bundles arise about half an internode below the leaf they supply.
Information on floral development is taken from Caris et al. (2000); the ovules are often separated by and partly sunken in placental tissue (see also Warming 1913; Utteridge & Saunders 2001).
Synonymy: Maesaceae Anderberg, B. Ståhl & Kallersjö
[Theophrastoideae [Primuloideae + Myrsinoideae]]: herbs[?]; bracteoles 0; C imbricate, subrotate; petals developing after the stamens.
Age. The age of this node is estimated to be 42-40Ma by Wikström et al. (2001), (67-)55, 51(-40)Ma by Bell et al. (2010), (73-)55(-35)Ma by Wikström et al. (2015), about 65Ma by K. Bremer et al. (2004a), and ca 72.1Ma by Rose et al. (2018).
Evolution: Divergence & Distribution. For the suggestion that rosette herbs might be the plesiomorphic condition for this part of the clade, see Anderberg et al. (2001); however, Lens et al. (2005a) find no evidence from wood anatomy that this is likely (apart from in a few Myrsinoideae). Many of these herbaceous taxa have capsular fruits with five apical teeth, presumably also plesiomorphic. Herbaceous taxa of Myrsinoideae such as Stimpsonia, Ardisiandra and Coris are more basal on the tree than woody taxa.
Smith and Donoghue (2008) found that the rate of molecular evolution in the herbaceous taxa they examined was much greater than in the woody taxa.
2. Theophrastoideae A. de Candolle
Bracts ± displaced up the pedicels; staminodes +, ± petal-like; ovule endothelium?
6-9[list]/105 - two tribes below. Mostly New World and tropical, some also more temperate and Old World.
Age. Crown-group Theophrastoideae are ca 70 Ma (Rose et al. 2018).
2A. Samoleae Reichenbach
Nodes ?1:1; lamina margins entire; flowers small [<7 mm across]; K connate, C rotate; (staminodes 0); (anthers with prolonged connective); G , semi-inferior, style impressed; inner integument ca 2 cells across; fruit a capsule with 5 teeth; seeds many; coat undistinguished, exotesta and endotegmen tanniniferous, the latter crystalliferous; endosperm cell walls thin to slightly thickened; n = (12) 13.
1/15. America, the Antipodes, Europe, tropical to temperate (map: from Hultén 1971; Meusel et al. 1978; FloraBase 2005; red, Samolus valerandi only - Wanntorp & Anderberg 2011). [Photo - Flowers.]
Synonymy: Samolaceae Rafinesque
2B. Theophrasteae Bartling
Woody, tending to be pachycaul; rays >10 cells across; nodes also 1:1 [Jacquinia, dividing into three], 5:5 [Clavija]; secretory system?; petiole bundle deeply arcuate or annular, with small adaxial inverted bundles; (subepidermal fibres +); perulae +; lamina vernation conduplicate, margins spiny-toothed to entire, plant dioecious or flowers bisexual; flowers medium-sized; ?petal development; anthers extrorse, with calcium oxalate crystals, etc. at apex and base, initially incurved over stigma; nectariferous hairs +/nectary 0; G?, style long, stigma dry or wet; outer integument 2-4 cells across, ?inner; fruit a (rather dry) berry, placentae ± pulpy, (drupe); seeds 1-few, rounded; testa multiplicative, exotestal cells flattened, thick-walled, (hypodermal cells with thickened anticlinal walls), other mesotestal cells crystalliferous; cotyledons usu. foliaceous; n = 18, 20, 24.
4/90: Clavija (50). New World tropics (map: from Ståhl 1989, 1991, 1995). [Photos - Collection.]
Evolution: Divergence & Distribution. Species of Samolus from SW North America are sister to the rest of the genus, and Theophrasteae are a tropical New World clade (Wanntorp & Anderberg 2011), perhaps suggesting a New World origin for Samoleae.
Chemistry, Morphology, etc. Ståhl (2004) suggests that a secretory system is present, if not always conspicuous in Samolus; the stomata are anomocytic and there are several petiole bundles forming an arc which seem to diverge very soon from the leaf trace after it departs from the central stele. The subepidermal fibres of Jacquinia may not be lignified; for reports of glandular dots on calyx and corolla, see Mabberley (1997).
The floral primordia may initially be quite strongly monosymmetric, as in Deherainia (Sattler 1962), even if the flower at anthesis is polysymmetric. In Samolus, the ovules completely cover the placenta, but fingers of placental tissue can poke up between them (but not seen in the material examined by Caris & Smets 2004); Ma and Saunders (2003) suggest that in Theophrastoideae in general the ovules are not embedded in placental tissue (which would then be a synapomorphy for it). The capsule valves of Samolus are opposite the calyx (Caris & Smets 2004).
Phylogeny. For the phylogeny of Samolus, see Wanntorp and Anderberg (2011).
For general morphology, etc., see Ståhl (2004) and in particular Caris and Smets (2004), for anther cryslas, see Pohl (1941).
Phylogeny. Phylogenetic relationships suggested by Källersjö and Ståhl (2003) imply that some generic realignments are needed.
Synonymy: Theophrastaceae G. Don, nom. cons.
[Primuloideae + Myrsinoideae]: herbs[?]; tapetal cells uninucleate; (exotegmic cells elongated, with band-like thickenings); fruit a capsule, dehiscing by apical valves; two ndhF deletions.
Age. This node may be ca 57.6 Ma (Rose et al. 2018), (54-)44, 40(-30) Ma (Bell et al. 2010: note topology) or (50-)32(-16) Ma (Wikström et al. 2015).
Chemistry, Morphology, etc. For a distinctive triterpene saponin that is at least scattered in this clade, see Podolak et al. (2013.
3. Primuloideae Kostelesky
Cucurbitacins +; ?cork; ray width?; trichomes articulated; lamina (odd pinnate), vernation involute or revolute, margins entire to dentate or serrate; inflorescence scapose; (heterostyly +); (bracts 0); flowers medium-sized; K often connate, C salverform, (lobes fringed); A attached at or above middle of C tube; pollen syn- or polycolpate; style usu. long, stigma dry; ovules not immersed in placenta (immersed - Primula [Dionysia]), (integument single, 6-10 cells across - Androsace [Douglasia]); seeds many, angled, exotesta ± persistent, walls thickened or not, (endotesta with inner walls thickened [Primula]), (endotegmen crystalliferous); endosperm cell walls thick and pitted (somewhat thickened, thin); n = 8-12; nuclear genome [1C] (460-)2777(-10352) Mb [?level].
9 [list]/900: Primula (490-600), Androsace (160). Northern hemisphere, scattered elsewhere (map: from Hultén 1971; Meusel et al. 1978). [Photo - "Dodecatheon" flower © R. Kowal, Primula flower.]
Age. The age of crown-group Primuloideae is around 51 (Rose et al. 2018), (Strijk et al. 2014) or 33 (Boucher et al. 2016a) Ma.
Evolution: Divergence and Distribution. Primula, Androsace and Soldanella have all radiated in alpine habitats in Europe where allopatric speciation has been common, but they also grow elsewhere in the northern hemisphere (Comes & Kadereit 2003; L.-B. Zhang et al. 2004; Boucher et al. 2011, 2016a; Roquet et al. 2013; see also Hughes & Atchison 2015). Extensive dispersal between these isolated alpine areas has also occurred (e.g. Boucher et al. 2011; Roquet et al. 2013). Southwestern China and adjacent regions harbours the bulk of the diversity of the speciose Primula (Y.-J. Liu et al. 2015 and references).
Pollination Biology & Seed Dispersal. Heterostyly is common, although it is unlikely to be an apomorphy for the subfamily although it is likely to be an apomorphy for Primula s.l. (de Vos et al. 2014a). Heterostyly may reduce the chances of the extinction of older clades, at least; over shorter time spans, homostylous clades may show accelerated diversification (de Vos et al. 2014b). Primula section Primula contains European species that have been subjects of many of the studies on heterostyly; relationships in this isolated section are complex and species limits unclear (Schmidt-Lebuhn et al. 2012). Thrum plants are heterozygous Ss, while pin plants are the homozygous recessive, ss (e.g. Li et al. 2011). The condition is sometimes lost, as in those Primula with buzz pollination, i.e. members of the erstwhile genus Dodecatheon (Mast et al. 2001, 2006), and in a number of other small clades (de Vos et al. 2014a, b).
Myrmecochory is common in Primula (Lengyel et al. 2010).
Ecology & Physiology. Boucher et al. (2011; see also Roquet et al. 2013) discuss the evolution of life forms in Androsace (incl. the North American Douglasia), which turns out to be very labile. Probably initially annuals, the perennial cushion habit has evolved several times in alpine habitats since the Miocene, and it is perhaps a "key innovation" enabling life at high altitudes - cold and dry. Dionysia (= Primula) are also mostly cushion-forming plants, and some are chasmophytes (Trift et al. 2004). With over 60 species of cushion plants, Primuloideae include a disproportionatey large number of them (Boucher et al. 2016b).
Chemistry, Morphology, etc. The involute leaves can be sharply bent rather than incurved (for vernation, see Conti et al. 2000; Mast et al. 2001). Solereder (1908) reported that secretory tissues occurred in Androsace lactea.
The corolla epidermal cells are isodiametric. Saunders (1936) suggested that some of the lobing of the corolla of Soldanella might be staminodial.
For general information, see Anderberg (2004) and Richards (2003: species descriptions of Primula); see also Harborne (1968: chemotaxonomy of Primulaceae in the old sense), Colombo et al. (2017: phytochemistry of Primula), Mast et al. (2001) and Y. Xu et al. (2015) for pollen, and Subramanyam and Narayana (1976: embryology, anther wall development varies within Primula).
Phylogeny. For ITS-based relationships within Primuloideae, see Martins et al. (2003); overall relationships are shown by de Vos et al. (2014a: suppl. Fig. 1) and also - Chineae species - by Z.-D. Chen et al. (2016). For relationships within Primula, see also Trift et al. (2002), Mast et al. (2004, 2006), Yan et al. (2010) and Y.-J. Liu et al. (2015); for Dionysia (= Primula), see Trift et al. (2004). Wang et al. (2004), Schneeweiss et al. (2004b) and Boucher et al. (2011) discuss relationships within Androsace.
Classification. Primula will include Cortusa, Dionysia (see Lidén 2007 for a revision), and Dodecatheon. The limits of Androsace will have to be extended to include Douglasia and Vitaliana (Schneeweiss et al. 2004b; Boucher et al. 2011).
Synonymy: Hottoniaceae Döll
4. Myrsinoideae Burnett
Also trees to shrubs or lianes; benzoquinones +; (vessel elements with scalariform perforation plates); (wood rays 0), (with breakdown areas); (nodes 3:3 - unnamed taxon from Atlantic Forest; Ardisia densiflora); glands/canals throughout the plant (0); inner wall of epidermis ± mucilaginous; leaves (opposite), lamina also supervolute (curved), margins entire (crenate to serrate, teeth cartilaginous); (plant dioecious); inflorescence often fasciculate/corymbose; flowers (3-)4-5(-7)-merous, small to medium-sized; (bracts foliaceous); (median sepal abaxial); flowers protogynous [?sampling]; C often right-contorted [?level], (margins ciliate); (C developing before the A); nectariferous or oil-secreting hairs on C, G, or nectary 0; A with anthers dorsifixed or basifixed, sagittate, (dehiscing by pores); style (0), (stylar canal 0), stigma (punctate), dry or wet; ovules (micropyle endostomal - Coris), outer integument 2-3 cells across, inner integument 2-3(-7 - Cyclamen) cells across, (unitegmic - ca 2 cells across), (endothelium 0), parietal tissue ca 4 cells across; fruit a capsule (dehiscence irregular/circumscissile), also berry or drupe, placentae ± pulpy; seeds 1-few, rounded, (hilum depressed) [woody taxa], or many, small, angular; seed coat undistinguished, testa multiplicative, (endotesta crystalliferous, thickening U-shaped - Cyclamen), tegmen ?multiplicative, becoming crushed, (endotegmen crystalliferous - ?woody taxa); endosperm (ruminate), cell wall thickening variable; embryo suspensor massive, (embryo slightly curved; medium; cotyledon single - Cyclamen); n = 10-13, 15, 17, 23; nuclear genome [1C] ca 841 Mb [Aegiceras].
41 [list]/1,435: Ardisia (450), Myrsine (155: inc. Rapanea, Suttonia, many species in the Pacific), Discocalyx (115: inc. Tapeinosperma), Oncostemum (110), Embelia (100), Parathesis (85), Stylogyne (60). Pantropical and N. Temperate (map: from Hultén 1958, 1971; FloraBase 2008: S. Hemisphere a bit notional). [Photos - collection woody members, Cyclamen flower © H. Schneider, fruit © H. Schneider, collection of ex Primulaceae.]
Age. Myrsinoideae began radiating ca 53.1 Ma (Rose et al. 2018).
C (0); A basally connate, nthers porose); (antipodal cells large - Lysimachia).
5/250: Lysimachia (150). Widely scattered, but few in South America, Australia or Africa.
Synonymy: Lysimachiaceae Jussieu
Synonymy: Aegicerataceae Blume, Anagallidaceae Borkhausen, Ardisiaceae Jussieu, Coridaceae J. Agardh, Embeliaceae J. Agardh, Myrsinaceae R. Brown, nom. cons.
Evolution: Divergence & Distribution. The rare, monotypic Pleiomeris (P. canariensis) is restricted to the Canary Islands - it is sister to Heberdenia, which also grows on the Azores - Stimsonia may be close (Martins et al. 2003). Note that Palaeo-Macaronesia is likely to be 60 Ma or more old, the oldest currently emergent Canary Island dating to ca 21 Ma (Gelmacher et al. 2005; Fernández-Palacios et al. 2011). Strijk et al. (2014) discussed the evolution of the Madagascan and Mascarene Oncostemon-Badula complex. Much speciation is quite recent, but Badula on Rodrigues may be older than the island. Lysimachieae in Eastern Asia are quite diverse, and this is ascribed to a combination of how long the clade has been there and high diversification rates (Yan et al. 2018).
Ecology & Physiology. Aegiceras is restricted to the mangrove habitat, for the evolution of which, see Rhizophoraceae and Tomlinson (1986, 2017); see also articles in Ann. Bot. 115(3). 2015. Hardly surprisingly, Aegiceras has a number of anomalous anatomical and morphological features. The seeds in particular are those that might be expected from a mangrove plant; they lack endosperm and contain a large embryo that breaks the seed coat before the seed falls from the tree (c.f. Rhizophoraceae-Rhizophoreae, Acanthaceae-Acantheae-Acanthus ilicifolius, etc.: Juncosa 1982).
Pollination Biology & Seed Dispersal. Vogel (1986, 1997) examined pollination in Lysimachia, a largely herbaceous group with a few woody species. Pollination of about 70 or more species with yellow flowers is by 16 species of Macropis (Mellitidae-Macropodini) bees (Michez & Patiny 2005: see also Simpson et al. 1983; Michez et al. 2008; Possobom & Machado 2017 and references). The bees collect the oil that is secreted by trichomes, as well as pollen. There are also buzz-pollinated taxa, and in species that have white flowers there are nectariferous hairs. Renner and Schaefer (2010: summary) date the crown clade of Lysimachia to (41-)31(-8) Ma, and the stem clade to (52-)41(-28) My; Michez et al. (2007) described a fossil bee Palaeomacropis eocenicus, with hairs on its legs very similar to those of Macropis itself, from France in amber from the early Eocene some 53 Ma (the fossil macropid Eomacropis glaesaria is not likely to have been an oil collector: Michez et al. 2008). Anderberg et al. (2007) suggested that Lysimachia with buzz-pollinated flowers and those with nectar-producing hairs formed separate clades and were both derived from oil-producing ancestors, but the pattern of gain and loss of oil flowers is complex (Renner & Schaefer 2010); there are some selfers (Vogel 1986).
The stigma of Cyclamen is wet, and is just inside the punctate tip of the hollow style (Reinhardt et al. 2007).
The pedicels of Cyclamen twist spirally as the fruits mature, the capsules ending up close to the ground, and the seeds are dispersed by ants; most species of Cyclamen have rather local distributions (Yesson et al. 2009).
Bacterial/Fungal Associations. About 35 species of Ardisia (and perhaps other genera) have pustules along the edge of the leaf blade inhabited by Burkholderia; the association is quite recent, and the symbionts may be close to leaf-nodulating bacteria in Rubiaceae (Lemaire et al. 2011b, c). The association involves a single strain/species of Burkholderia and there was a single origin of the bacterium—plant association; bacteria are also found in the shoot apex, and transmission is likely to be vertical (Ku & Hu 2014 and references). It is unclear what role the bacteria might play (Miller 1990).
Chemistry, Morphology, etc. The presence of coloured glands may well not be a synapomorphy of Myrsinoideae (Hao et al. 2004). There are breakdown areas in the rays of woody members, and these may be filled with dark contents (Lens et al. 2005); for secretory structures in Myrsinoideae, see de Luna et al. (2014 and references). Discocalyx has three traces in the petiole base, and some other taxa may be trilacunar; nodal anatomy needs study.
Floral variation is quite considerable. In late buds of some species of Lysimachia the as yet tiny corolla encloses only the base of the massive anther. The epidermal cells of the corolla are often elongated; this is a derived feature within the family. Does Lysimachia sometimes have staminodes? Trientalis has anisomerous flowers (Swenson et al. 2008c). See Oh et al. (2008) for the seed morphology of herbaceous taxa around Lysimachia. Interestingly, Maesa has less xyloglucans than other Primulaceae (Kooiman 1960).
Some information is taken from Ståhl and Anderberg (2004); see also Lens et al. (2005a) and de Luna et al. (2017), both wood anatomy, for floral morphology of Myrsine, see Otegui and Cocucci (1999), for pollen, see Nowicke and Skvarla (1979), for some embryology, see Subramanyam and Narayana (1976), and for the ovules of Cyclamen, see Woodcock (1926) and Corner (1976).
Phylogeny. The old Myrsinaceae included only woody taxa with fleshy and often drupaceous fruits, but the clade that included these taxa (minus Maesa) was also found to include Anagallis, Ardisiandra, Asterolinon (?= Lysimachia), Coris, Cyclamen, Glaux (= Lysimachia, although it lacks a corolla), Lysimachia, Pelletiera, Stimpsonia and Trientalis (Anderberg et al. 2000, 2001), all of which are herbaceous, capsular fruited, and used to be in Primulaceae. However, the limits of this extended clade were not so clear in Martins et al. (2003: ITS data alone). Anderberg et al. (2007) was particularly interested in the relationships of the herbaceous taxa; the monophyly of Myrsinoideae s.l. had moderate support (72% jacknife), and Cyclamen, the herbaceous taxa, and the woody taxa then formed a tritomy. Hao et al. (2004) also provide a phylogeny of much of the group, although focusing on Lysimachia. Yesson et al. (2009) found that herbs occupied basal pectinations within Myrsinoideae, and Cyclamen (the focus of their study) was well embedded in the family. The subshrub Coris (for nectary morphology, see below) was sister to the whole of the rest of the subfamily when Stimpsonia (moving between Primuloideae and Myrsinoideae) did not occupy that position. Both genera have capsules opening by apical valves. The clade [Coris + Stimpsonia] was sister to other Myrsinoideae in the phylogeny recovered by Rose et al. (2018). For Chinese taxa, see Z.-D. Chen et al. (2016).
For the phylogeny of Badula, recognition of which may make Oncostemum paraphyletic, see Bone et al. (2012) and especially Strijk et al. (2014); for a morphological phylogeny of Chinese Ardisia, see J. Wang and Xia (2013).
Classification. Generic limits in the woody Myrsinoideae in particular are unsatisfactory, but the limits of genera like the herbaceous Lysimachia are also unclear (Anderberg et al. 2007).
[Mitrastemonaceae, Theaceae, [Symplocaceae [Styracaceae + Diapensiaceae]], [[Sarraceniaceae [Roridulaceae + Actinidiaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]]]: testa with outer wall unthickened.
Age. The age of this node is (98.4-)78.4(-55.8) Ma (Naumann et al. 2013: [Clethraceae + Ericaceae] sister).
MITRASTEMONACEAE Makino, nom. cons. - Back to Ericales
Root parasites, plant endophytic; ?anatomy; leaf waxes hummocky; leaves opposite, scale-like; flowers single, terminal; P uniseriate, 4; anthers extrorse, completely connate and surrounding G except for small apical pore, polythecate; pollen 2-porate [?colpate], ektexine reduced to tuberculae; G 8-20, placentation intrusive parietal, style stout, stigma hemispherical; ovules many/carpel, unitegmic, integument ca 2 cells across, funicular obturator +; fruit berry-like, circumscissile; funicle sticky; exotestal cells with massive U thickenings; endosperm 1-layered, embryo undifferentiated, 4-celled; n = 20.
1 [list]/2. South East Asia, Malesia, Central America, N.W. South America, scattered (map: from van Steenis and van Balgooy 1966; Meijer & Veldkamp 1993). [Photo - Habit © S. Hsiao.]
Evolution: Genes and Genomes. A mitochondrial gene has moved from host to the parasite (Barkman et al. 2007: atp1) and from the parasite to its host, Quercus (Systma et al. 2009). The mitochondrial genes cox1 and matR showed considerable divergence, but not the atp1 gene (Barkman et al. 2007). The rate of genome evolution in Mitrastemon is rather slower than that of other parasitic taxa ().
Chemistry, Morphology, etc. Watanabe (1936: V) talks a lot about a "Mitrastemon-Pilz" - c.f. the ectomycorrhizae of Ericaceae?
The pollen may have three or four pores - see Watanabe (1936: III). Cronquist (1981) and Meijer and Veldkamp (1993) describe the fruit as being a berry or berry-like and opening via a transverse slit, i.e., it is also some sort of circumscissile capsule, while Meijer and Veldkamp (1993) described the ovule as being unitegmic and the seed coat as as being formed from the inner integument (the latter following Watanabe 1937: VII).
For general information (including a more extensive list of hosts) and references, see Meijer and Veldkamp (1993), the Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008).
Previous Relationships. Mitrastemonaceae were included in the old Rafflesiales (e.g. Cronquist 1981). Cocucci and Cocucci (1996) suggested that Mitrastemonaceae had relationships with Annonaceae.
[Theaceae, [Symplocaceae [Styracaceae + Diapensiaceae]], [[Sarraceniaceae [Actinidiaceae + Roridulaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]]]: cork?; vessel elements with scalariform perforation plates; lamina margin serrate.
Age. This node (as [Theaceae + Styracaceae] or equivalent) has been dated to 103 Ma (K. Bremer et al. 2004a) and (101.5-)91.5(-80) Ma (Yu et al. 2017), if including Ericaceae, etc., a date closer to 106 Ma is more likely; Magallón et al. (2015) estimated the age of this node to be around 94.9 Ma, (103-)96(-88) Ma is the estimate offered by Wikström et al. (2015) and ca 101.9Ma by Rose et al. (2018).
Evolution: Ecology & Physiology. Plants in this clade have relatively low leaf nitrogen, and other major shifts in this part of the tree (see also Ericaceae, and [[Sarraceniaceae [Actinidiaceae + Roridulaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]) suggest slow carbon and nutrient cycling (Cornwell et al. 2014).
Genes & Genomes. A genome duplication, Ad-β, that is somewhere around here has been dated to ca 75.9 or 101.4-72.9 Ma (Shi et al. 2010 and S. Huang et al. 2013 respectively).
THEACEAE Ker Gawler, nom. cons. - Back to Ericales
Trees or shrubs; plants Al-accumulators; myricetin, ellagic acid +; cork pericyclic; (pits vestured); intervessel pitting opposite-scalariform; pericyclic fibres +/0; petiole bundle arcuate; sclereids +, mucilage cells +; stomata paracytic, anisocytic or cyclocytic; hairs unicellular; leaves also two-ranked, lamina involute or supervolute (conduplicate), margins toothed (entire); flowers single, axillary; bracteoles +; C ± free; A usu. 40<, development centrifugal, ± basally connate, anthers versatile, articulated, connective usu. not prolonged, filaments variable in length; pseudopollen produced from connective; pollen tricolporoidate; nectary?; G [(3-)5(-10)], opposite petals, (styles +, separate), stigma wet; ovules 2-few/carpel, (basal), bitegmic, micropyle endostomal, outer integument 4-10 cells across, inner integument 4-11 cells across, hypostase +; fruit a loculicidal capsule, K persistent or not; seeds few, often >4 mm long, flattened; testa massive, exotesta lignified or not, mesotesta lignified (fibrous; with sclereids), endotesta lignified or not; endosperm nuclear, cotyledons longer than radicle, accumbent.
Ca 9 [list]/195(-460!) - three groups below. Mostly Subtropical South East Asia and Malesia, some in the Americas, Africa none. [Photo - Collection.]
Age. Crown-group Theaceae are some 49 Ma (M.-M. Li et al. 2013), (74.7-)57.3(-39.6) Ma (Yu et al. 2017, q.v. for several other dates) or ca 63.1 Ma (Rose et al. 2018).
Pentapetalum trifasciculandricus, a fossil ca 91 Ma old from New Jersey, may belong to Theaceae or be in the Pentaphylacaceae area (Martínez-Millán et al. 2009: c.f. analyses). For other information on the fossil record of Theaceae, see Martínez-Millán (2010).
1. Stewartieae Choisy
(Plant deciduous); pith heterogeneous; androecium fasciculate; pseudopollen type?; embryology?; capsule lacking columella; seeds narrowly winged or not; surface of testa with ± detailed sculpturing; integument vascularization?; endosperm +; n = 15, 17, 18.
1/9. East Asia, E. North America (map: from Hong 1993).
Age. Crown-group Stewartieae are around 18.7 Ma (M. M. Li et al. 2013) or (24.7-)14.8(-8.3) Ma (Yu et al. 2017).
[Gordonieae + Theeae]: stomata anisocytic/cyclocytic; androecium whorled; capsule with persistent columella; endosperm slight to 0.
Age. This node has been dated to around 68 Ma (K. Bremer et al. 2004a), ca 60 Ma (Rose et al. 2018), or (66.9-)49.8(-33.8) Ma (Yu et al. 2017).
2. Gordonieae de Candolle
(Plant deciduous - Franklinia); cork superficial; androecium in 3-5 whorls [?is this a character], connective with stomata; pseudopollen with pores; (ovule campylotropous), inner integument vascularized; dehiscence also septicidal; seeds apically winged (not – Franklinia]; testa proliferating, surface with irregular protrusions, tegmen also proliferating; (embryo curved - Schima); n = (15), 18.
3/4-30. Franklinia, Gordonia, Schima. Southeast Asia, West Malesia, S.E. United States (map: from Camp 1947; Bloembergen 1952).
Age. Crown-group Gordonieae are about 11.1 (M.-M. Li et al. 2013) or (32.2-)26.2(-23.3) Ma (Yu et al. 2017).
Grote and Dilcher (1992, also references) described Gordonia lamkinense from rocks of the Claiborne Formation of Kentuckey ca 40.4 Ma, as well as other Theaceae from there (see also Martínez-Millán 2010).
Synonymy: Gordoniaceae Sprengel
3. Theeae Szyszylowicz
Pith heterogeneous; pedicels multibracteolate; K and C intergrading; A in 2 whorls, obdiplostemonous; nectary at bottom of filaments; pseudopollen ribbed (0); outer integument becoming vascularized, (endothelium +), (hypostase 0); (embryo sac bisporic [chalazal dyad], eight-celled [Allium-type] - Camellia); seeds winged or not; surface of testa with narrow anticlinal walls of cells evident; (cotyledons much folded); n = 15.
5/230-420: Camellia (120-180), Laplacea, Polyspora (32), Pyrenaria (42-60). Southeast Asia, Malesia, tropical America (map: from Camp 1947, approximate). [Photo - Flower, Fruit.]
Age. Crown-group Theeae have been dated to (39.2-)27.1, 27(-18.4) (W Zhang et al. 2014) or (30-)19.4(-11.6) Ma (Yu et al. 2017).
Fossil leaves identified as Theeae are known from the Upper Eocene of Japan, woods (?= Camellia) from Lower Olicoene ca 30 Ma from both Bulgaria and Washington, W. U.S.A. (L.-L. Huang et al. 2016), and Camellia-type pollen perhaps 50 Ma is known from Europe (Hofmann 2018). On the other hand, crown-group Camellia is estimated to be (18.7-)15.9, 12.3(-7.3) Ma (W. Zhang et al. 2014).
Synonymy: Camelliaceae Candolle
Evolution: Divergence & Distribution. For some other dates in Theaceae, see Yu et al. (2017).
Ecology & Physiology. Theaceae, along with Magnoliaceae, Lauraceae and Fagaceae (Tang 2015), are a notably prominent component of the subtropical evergreen broad-leaved forests (EBLFs) of East Asia, over 55% (= 148 spp.) of the family growing there and another 33% being known from Tropical Asia (Yu et al. 2017).
Pollination Biology. The function of the pseudopollen is unknown, but it does not appear to be nutritious and it may be deceit pollen (Tsou 1997; Iqbal & Wijesekara 2002); not all taxa have it (Q. Zhang et al. 2017).
Seeds of Franklinia take about a year to mature, for although fertilization takes place soon after pollination in the autumn, the young fruits overwinter in a state where the endosperm is cellularized but the zygote is still undivided (Schoonderwoerd & Friedman 2015, esp. 2016).
Plant-Animal Interactions. For the remarkable interactions between Camellia japonica and its seed predator, the camellia weevil (Curculio camelliae), see Toju et al. (2011). The capsule of the plant may be the size of an apple, the pericarp being over 2 cm thick, but the snout of the weevil, used for boring into the fruit to make a hole for subsequent egg deposition in the seeds, may be over 2 cm long.
Chemistry, Morphology, etc. The cotyledons of (?all) Theaceae have three or more traces from a single gap. The stomata are often described as being "gordoniaceous", i.e. cyclocytic to anisocytic (see e.g. Lu et al. 2008).
For the basically obdiplostemonous construction of the androecium of Camellia japonica, see Sugiyama (1997). Although the carpels seem to be opposite the sepals in Camellia, this may be connected with the arrangement of the perianth, rather than that of the gynoecium per se; the basic orientation of the gynoecium with respect to the floral axis is the same as that of Gordonia, where the carpels are clearly opposite the petals (Eichler 1878).
For general information about Theaceae s.l., see Keng (1962) and Stevens et al. (2004b), also Beauvisage (1920) and Liang and Baas (1991), both anatomy, Zhang et al. (2009: sclereids in Camellia), Jiang et al. (2010: lenticels on Camellia leaves); also Leins and Erbar (1991: floral morphology), Wei (1997: pollen), Fagerlind (1939c), Yang and Min (1995a, b), Tsou (1997, 1998) and Q. Zhang et al. (2017), all embryology, Gunathilake et al. (2015: testa surface) and Wang et al. (2006: Apterosperma, chromosomes and morphology).
Phylogeny. An analysis of two chloroplast genes by Prince and Parks (2001) suggests that there are three major clades (see above) and that Polyspora and Laplacea should be separated from Gordonia (see also Airy-Shaw 1936; Yang et al. 2004: genes from all three genomes, 2006: mitochondrial gene only, study of Theaceae s.l., including Pentaphylacaceae). However, relationships between these three clades remain unclear. The clade [Gordonieae + Theeae] has some support (see also Prince 1999; Yang et al. 2004; Rose et al. 2018) and makes morphological sense, although an analysis of matK data alone suggested that Theeae were sister to the other two tribes, but there was a polytomy in the combined analysis (including rbcL data: Prince & Parks 2001); see also Su et al. (2011: Apterosperma sister to [Tutcheria + Camellia]), M.-M. Li et al. (2013: several chloroplast genes, 11/20 species sampled were Stewartia) and Z.-D. Chen et al. (2016: Stewartia sister to the rest, but support weak). W. Zhang et al. (2014) found that Polyspora was sister to other Theeae using the LEAFY gene (see also Rose et al. 2018), Camellia was paraphyletic, but there was little resolution along the spine of the tribe in a matkK + rbcL analysis; Apterosperma may be of ancient hybrid origin. Details of relationships differed again in the plastome and n-ribosome analysis of Yu et al. (2017); the relationships [Stewartieae [Gordonieae + Theeae]] were usually obtained, but in single analyses there was weak support for Theeae and for Gordonieae being sister to the rest of the family.
For relationships within Camellia, see Vijayan et al. (2009); current sectional limits need overhauling, and for the limits of Pyrenaria, which are best broadly drawn, see R. Li et al. (2011). Within Stewartia, S. malacodendron is sister to the rest of the genus (Yu et al. 2017). however, relationships in the genus may be obscured by ancient introgression (Lin et al. 2019). Laplacea turned out to be wildly polyphyletic, L. grandis being sister to Gordonia lasiantha and L. fruticosa being embedded in Theeae (Yu et al. 2017).
Classification. Stewartia is to include Hartia (e.g. Prince 2002; M.-M. Li et al. 2013). Generic limits in other Theaceae are difficult, but for useful notes on the genera, see Prince (2007). Franklinia hybridizes with Schima, and perhaps Gordonia and even Camellia, i.e. taxa scattered throughout Gordonieae and Theeae (Ranney et al. 2003); genera may have to be reduced.
Species limits in Camellia (see Vijayan et al. 2009) and also Schima (Bloembergen 1952) in particular are unclear.
Previous Relationships. Theaceae s.l. have in the past been associated with Asteropeiaceae (e.g. Takhtajan 1997), now in Caryophyllales, and Bonnetiaceae (see Malpighiales) (e.g. Cronquist 1981). Pentaphylacaceae, Sladeniaceae and Pellicieraceae, also erstwhile Theaceae, are in separate families in Ericales, the last quite apart from the other two. 1).
[[Symplocaceae [Styracaceae + Diapensiaceae]] [[Sarraceniaceae [Actinidiaceae + Roridulaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]]]: ?
Age. If this clade exists, its crown-group age is around 101.6 Ma (Rose et al. 2018), 93.2 Ma (Magallón et al. 2015) or ca 83 Ma (Tank et al. 2015: Table S1).
[Symplocaceae [Styracaceae + Diapensiaceae]]: shrubs to trees; lignans +; inflorescence racemose; A (obdiplostemonous); style hollow; endosperm copious.
Age. The age of this node is some (68-)63, 61(-56) Ma (Wikström et al. 2001), about 100 Ma (K. Bremer et al. 2004a), 99.3 Ma (Rose et al. 2018), 81.2 Ma (Magallón et al. 2015), (94-)92(-89) Ma (Fritsch et al. 2015) or (95.5-)84(-71.5) Ma (Yu et al. 2017).
Evolution: Divergence & Distribution. In the context of the floral morphospace of Ericales, Chartier et al. (2017) thought that this clade was morphologically rather homogeneous.
Characters like presence of ellagic acid and a vascularized integument could be optimized to this node, but they would later have to be lost.
SYMPLOCACEAE Desfontaines, nom. cons. - Back to Ericales
Plants Al-accumulators, O-methyl flavonols, route II decarboxylated iridoids, ellagic acid +, myricetin 0; true tracheids +; crystal sand +; stomata usu. paracytic, also very large water stomata +; (leaves two-ranked), lamina ± supervolute; (inflorescence branched), pedicels articulated (not - Cordyloblaste); K basally connate; A (= and opposite K)-many, in bundles, (connate), adnate to C; anthers globose; pollen angular, spinuliferous; G [2-5], (half) inferior, median member abaxial, style hollow [?all], stigma ± capitate, wet or dry; nectary on ovary; ovules 2-4/carpel, pendulous, epitropous, endothelium +; fruit drupaceous, stone with as many pores as fertile carpels, K persistent; seed usu. 1; testa vascularized, (exotestal cells with inner walls thin); embryo large, (curved); n = 11 (12); mitochondrial coxII.i3 intron 0.
2 [list]/320 (260): Symplocos (318). Tropical to subtropical, inc. New Caledonia, not Africa (map: see Nooteboom 1975, c.f. Fritsch et al. 2015 - nothing in Amazonia). [Photo - Symplocos chinensis Flowers.]
Age. Crown-group Symplocaceae are estimated to be (57-)52(-48) (Fritsch et al. 2015) or ca 47.8 Ma (Rose et al. 2018).
Symplocos fruits are common in the fossil record and have been dated up to ca 48.6 Ma ( Martínez-Millán 2010 and references).
Evolution: Divergence & Distribution. Symplocos is locally very abundant as both pollen and fruits in the Caenozoic fossil record of Europe; it is also known from western North America, the southern USA and East Asia (Krutzsch 1989; Fritsch et al. 2015), as well as New Zealand (Lee et al. 2001). The family may be Eurasian in origin, and diversification of [section Palura + The Rest], i.e., most of the family, is dated to only (41-)38(-35) Ma (Fritsch et al. 2015, q.v. for much information on biogeography).
Pollination Biology. There are subapical lobes on the style just below and alternating with commissural "stigmatic" lobes in the ca 145 species of the New World Symplocos subg. Symplocos sect. Symplocastrum; the papillae on these lower lobes are rich in lipid that may help the pollen stick to the pollinators (Kriebel et al. 2007). Pollen germinates on these subapical lobes which are thus (and from their position) true stigmatic lobes (Kelly & Nicholson 2009).
Chemistry, Morphology, etc. Although the placentation is described as being fully axile, in material seen it is parietal at the apex. The androecium is basically obdiplostemonous (Caris et al. 2002).
For testa anatomy, see Corner (1976) and Huber (1991), and for general information, see Nooteboom (2004).
Phylogeny. For a phylogeny of Symplocos s.l., see Y. Wang et al. (2004) and Fritsch et al. (2006, 2008, 2015); section Cordyloblaste, with two species, appears to be sister to the rest of the genus and section Palura sister to the remainder (one node up in Wang et al. 2004).
Classification. The infrageneric taxonomy needs reworking, and two genera should perhaps be recognised (Fritsch et al. 2008).
[Styracaceae + Diapensiaceae]: cork cambium pericyclic; glandular hairs 0; leaves spiral, (margins entire); anthers basifixed; nectary 0; style continuous with ovary; ovules many/carpel; fruit a loculicidal capsule.
Age. The age of this node is estimated at (60-)55, 45(-40)Ma by Wikström et al. (2001), (78-)54, 51(-39)Ma by Bell et al. (2010), about 52.7Ma by Magallón et al. (2015), ca 73Ma by Tank et al. (2015: Table S2), and as much as 93.2Ma by Rose et al. (2018).
Evolution: Divergence & Distribution. Scott (2004) and Fritsch (2004) suggest that there are embryological features in common between the two families; I do not know if any of them are really synapomorphies.
Phylogeny. There is also fairly good support for this clade in B. Bremer et al. (2002).
STYRACACEAE Candolle & Sprengel, nom. cons. - Back to Ericales
Trees or shrubs; ellagic acid, myricetin 0, iridoids?; (vessel elements with simple perforations); wood siliceous; resin canals often +; petiole bundle arcuate or D shaped (medullary and/or wing bundles +; complex - Parastyrax); indumentum stellate or scaly; (buds perulate); lamina vernation conduplicate-plicate or supervolute; bracteoles 0, pedicels articulated or not [Styrax]; flowers (4-)5(-7)-merous; K ± completely connate, open, (1 trace), C valvate or not; A 2 (3) x C/= and alternate with C, adnate to C, often basally connate, anthers basifixed, connective well developed, running the length of the anther, (filaments as broad as anther - Styrax sect. Pamphilia); pollen spinuliferous; G [2-5], ± inferior, alternate with K, median member ?abaxial, often with hairs inside, (long style branches +), stigma punctate or lobulate, dry; ovule (1/carpel, basal - Pamphilia), in two ranks, often apotropous, integument 12< cells across, (bitegmic, micropyle endostomal - Styrax), placental obturator +, (endothelium + - Alniphyllum, Styrax); fruit drupaceous/nut-like; samara/loculicidal capsule; testa vascularized, crushed; n = 8.
11 [list]/160: Styrax (120). Japan to Malesia, esp. Southeast Asia, Mediterranean and thereabouts, North America, Styrax alone Central and South America (map: From van Steenis 1949b; Sales & Hedge 1996; Fritsch 1999). [Photo - Flower].
Age. Crown-group Styracaceae may be ca 56 Ma (Rose et al. 2018) and pollen of Styrax a little younger than his is reported from Europe (Hofmann 2018).
Evolution: Divergence & Distribution. For the early Caenozoic fossil history of Styracaceae that are now East Asian endemics, see Manchester et al. (2009).
Fritsch et al. (2001) suggest possible additional synapomorphies for Styracaceae.
Plant-Animal Interactions. Van Steenis (1949b) illustrates the remarkable galls found on Malesian species of Styrax. There is a rather close association between the aphids involved (Cerataphidinae) that cause some of these galls and individual species of Styrax; the morphology of the galls is ultimately determined by the aphids (Stern 1995; Stern & Foster 1996; J. Chen et al. 2014 for a phylogeny of the aphids). Cecidomyids also produce galls on Styrax.
Genes & Genomes. There is a 20kb inversion in the large single copy region of the chloroplast genome in the [Bruinsma + Alniphyllum] clade and the accD gene has become a pseudogene, which is quite common in this part of Ericales (Yan et al. 2016, 2018).
Chemistry, Morphology, etc. Benzoin or gum benjamin, which contains benzoic acid but not polysaccharides, is exuded from the resin canals of Styrax (c.f. storax, from Altingiaceae).
The floral vasculature suggests that although the stamens are in a single whorl, they are basically obdiplostemonous (Dickison 1993; c.f. H.-C. Wang et al. 2010). Van Tieghem (1898) showed Halesia as having two ascending epitropous ovules and two descending apotropous ovules. Pterostyrax (and Styrax?) lack endothelium. There are no septal bundles, as in many Ericales (but details of the distribution of this character?).
For general information, see Fritsch (2004), for pollen, see Morton and Dickison (1992); Julio and Oliveira (2007) described the fruit, ovule, etc., of Styrax camporum.
Phylogeny. For relationships within Styracaceae, see Fritsch et al. (2001). The main phylogenetic structure in the family is [[Huodendron + Styrax] [[Alniphyllum + Bruinsmia] [The Rest]]]; both main clades, especially the second, are well supported, however, the rather scanty sampling in Rose et al. (2018) suggests different relationships. Members of the former clade have entire leaf blades, members of the latter have dentate blades, an inferior ovary, and bud scales, with the exception of the [Alniphyllum + Bruinsmia] clade which differs from the others on all three counts. In an analysis of chloroplast genomes Yan et al. (2018) obtained the well-supported relationships [Styrax [Huodendron [[Alniphyllum + Bruinsmia] [The Rest]]]]; both Pterostyrax and Halesia were poly-/paraphyletic. Things are still somewhat unclear.
For relationships within Styrax see Fritsch (2001).
Synonymy: Alniphyllaceae Hayata, Halesiaceae D. Don
DIAPENSIACEAE Lindley, nom. cons. - Back to Ericales
Shrublets or perennial herbs; ecto- and endomycorrhizae + [?ectendomycorrhiza]; plants Al-accumulators; ellagic acid +, iridoids?, lignans?; (cork superficial); vessel elements with simple (scalariform) perforation plates; secondary wood rayless; pericyclic fibres 0 (+ - Shortia); nodes 3:3 (1:1 - Pyxidanthera); petiole bundle(s) arcuate to annular (medullary bundles +); (stomata anisocytic); lamina margins toothed or entire, secondary veins subpinnate to palmate; (flowers axillary); K free or connate, C forming tube along with filaments, lobes serrate or not; stamens 5, opposite sepals, (connate - Galax), anthers ± incurved, thecae horizontal, filaments flattened, staminodes + (0); G , median member adaxial, stigma shortly 3-lobed, wet; ovules with integument 5-7 cell layers across, endothelium 0/+; endosperm copious, embryo terete; n = 6.
6 [list]/18. Scattered N. temperate, esp. East Asia and E. U.S.A., Diapensia lapponica circum-Arctic (map: from Diels 1914; Wood & Channel 1959; Hultén 1971).[Photo - Diapensia Flower, © J. Maunder; Diapensia Fruit, © J. Maunder.]
Age. Crown-group Diapensiaceae are ca 59.9 Ma (Rose et al. 2018).
Friis (1985) described Actinocalyx from Upper Cretaceous rocks in Sweden dated to ca 83.5 Ma (see also Martínez-Millán 2010). It has a number of similarities with extant Diapensiaceae, although the anthers are rather different, the pollen is much smaller (7-9.5 µm, versus 17-40 µm), and the styles are separate.
Evolution: Bacterial/Fungal Associations. The mycorrhizal association in Diapensiaceae may be an ectendomycorrhiza like that of many Ericaceae (see Asai 1934: the distinctiveness of the ericaceous mycorrhizal association was not fully understood then; Brundrett & Tedersoo 2018).
Genes & Genomes. For extensive rearrangements in the chloroplast genomes of Diapensia and Berneuxia, see Yan et al. (2018).
Chemistry, Morphology, etc. For ellagic acid, see Harborne and Williams (1973). The absence of rays from the family should be confirmed; there is only one old reference in Carlquist (2015b).
The integument seems to consist of an outer and inner part in some taxa, and an endothelium does not always develop (Samuelsson 1913; Diels 1914; Kapil & Tiwari 1978). Schnizlein (1843-1870: fam. 160) shows Galax with the median G abaxial.
For general information, see Scott (2004); also Xi and Tang (1990: pollen).
Phylogeny. Galax and Pyxidanthera are successively sister taxa to the rest of the family (Rönblom & Anderberg 2002; Rose et al. 2018); if this set of relationships holds, the presence of staminodes may be a derived feature within the family. For a morphological phylogeny, see Xi and Tang (1990).
Previous relationships. Diapensiaceae have often been considered close to Ericaceae, but the anthers of some genera of the former which appear to be inverted, are not.
Synonymy: Galacinaceae D. Don
[[Sarraceniaceae [Actinidiaceae + Roridulaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]]: inflorescence racemose; K quincuncial; anthers inverting late during development, initially extrorse, opening by pores or short slits; pollen ± rugulate ["cerebellar"], tectum and foot layer solid, infratectum with granular elements; G , median member adaxial, also , opposite C, style impressed, branched; ovules many/carpel, endothelium +; fruit a loculicidal capsule; testa with much thickened inner wall [?higher level], endosperm copious; mitochondrial coxII.i3 intron 0.
Age. Wikström et al. (2001) suggested a crown group age for this clade of around (72-)67, 59(-54) Ma, although relationships within the group are other than those shown here and Roridulaceae are way elsewhere on their tree, being sister to all other Ericales. Later, Wikström et al. (2004) noted the considerable difference between their estimate and the substantially older (ca 89 My) fossil-based estimate of Magallón et al. (1999). Bell et al. (2010: internal topology) estimated an age for this node of (68-)53, 51(-43) Ma, an age of ca 50.6 Ma is the estimate in Ellison et al. (2012), (95-)86(-77) Ma in Wikström et al. (2015), about 90.4 Ma in Magallón et al. (2015), and ca 98.2 Ma in Rose et al. (2018).
Glandulocalyx upatoiensis, a small-flowered fossil from the Upper Cretaceous 86-84 Ma in Georgia, S.E. United States, has been placed near Actinidiaceae or Clethraceae (Schönenberger et al. 2012) or in a tritomy with Roridulaceae and Actinidiaceae (Martínez 2016). Florally it does seem quite a good match: It has extrorse anthers that may become introrse, placentation that becomes intrusive parietal apically, the placentae being pendant basally, hollow style branches, etc.; the 24-28 stamens are in a single whorl, but an odd feature is the dense perhaps glandular hairs on the outside of the sepals (Schönenberger et al. 2012; see also Crepet et al. 2013). Three rather older (98-94 My) species of Glandulocalyx have been described from New Jersey; the flowers are also very small, less than 2.2 mm long, and with five stamens and clawed petals, some species have nectariferous staminodes, one species has viscin threads, another stellate hairs, there is a single style and expanded stigma, and so on, again, there are usually remarkable glands on the abaxial surface of the calyx. These latter species come out somewhere in this part of the tree in morphological analyses, or associated with Diapensiaceae or even within Ericaceae (Crepet et al. 2013), but overall Glandulocalyx is both morphologically heterogeneous and rather odd.
Paleoenkianthus is another interesting Late Cretaceous fossil from some 90 Ma (Nixon & Crepet 1993). It, too, has tiny flowers; many of its features are those of a bee-pollinated flower, and bees are likely to have been around by then (Cardinal & Danforth 2013; Sann et al. 2018). Its floral morphology is odd - K5 C(5) A 8 G (4), with "four, short slightly unequal styles/stigmas" (Nixon & Crepet 1993: p. 620), and viscin threads which, however, Friis et al. (2011) suggested might be fungal hyphae. In fact, Nixon and Crepet (1993) were not that sure of their identification, and while Friis et al. (2011) thought that this fossil was probably Ericalean, they were loath to place it more precisely.
Evolution: Divergence & Distribution. Löfstrand et al. (2016) suggest several apomorphies for/within this clade.
Ecology & Physiology. A considerable increase in leaf mass per area (SLA) can be placed at this node (Cornwell et al. 2014).
Chemistry, Morphology, etc. There are pit membrane remnants in the perforations of vessels in several families of this clade (Schneider & Carlquist 2003, 2004; Carlquist & Schneider 2005).
Bracteole presence is variable around here (Anderberg & Xiaoping 2002). For a summary of pollen variation, see Zhang and Anderberg (2002). The particular time during development that the anther inverts varies within this clade, and even the direction in which it occurs - thus in Sarraceniaceae the inversion is introrse → extrorse, but usually it is in the opposite direction (Schönenberger et al. 2012). How this character evolved - indeed, what this character "is" - are both unclear (Löfstrand & Schönenberger 2015; Löfstrand et al. 2016).
Phylogeny. Family-level relationships within this clade are well supported (e.g. Löfstrand et al. 2016, etc.), however, Z.-D. Chen et al. (2016) found the grouping [Clethraceae [Actinidiaceae + Ericaceae]] in a study of Chinese taxa.
[Sarraceniaceae [Actinidiaceae + Roridulaceae]]: route I secoiridoids +; K unequal, C quincuncial, at base thicker than sepals; stamens many [?here]; nectary 0; G opposite K [when 5], stigma dry, papillate [?level]; ovule hypostase +; K persistent in fruit.
Age. The age of this node is estimated to be (53-)48.6(-43) Ma (Ellison et al. 2012), ca 70.1 Ma (Tank et al. 2015: Table S2), 88.1 Ma (Magallón et al. 2015) or ca 93.4 Ma (Rose et al. 2018).
Evolution: Divergence & Distribution. Chartier et al. (2017) thought that this clade was morphologically rather homogeneous in the context of the general floral morphospace of Ericales; this would obviously not have been the case if vegetative variation had been examined.
See Löfstrand and Schönenberger (2015) and Löfstrand et al. (2016) for possible apomorphies. "Many stamens" is probably a feature derived independently within Sarraceniaceae and Actinidiaceae.
Pollination Biology. Buzz pollination is scattered throughout this clade, but nectaries are found in some taxa, whether on the ovary or anther.
Chemistry, Morphology, etc. For a detailed study of floral morphology of the whole clade, see Löfstrand and Schönenberger (2015). They describe all three families as having hydrolyzable tannins in the floral tissue and condensed tannins in vescicles; I do not know what these are chemically.
SARRACENIACEAE Dumortier, nom. cons. - Back to Ericales
Herbs, carnivorous [insectivorous], rosette-forming; O-methyl flavonols only +, monoterpene sarracenin +; mycorrhizae 0; cork?; vascular bundles initially separate; nodes ?; leaves with broad bases, pitcher +, terminal [epiascidiate]; inflorescence scapose (flowers solitary), bracteoles + [Heliamphora]; K ± petal-like, (3-6), C (0 - Heliamphora, 4), free; A 8-10 [Heliamphora] or many, centrifugal, anthers introrse, inversion late/unclear, with slits (basal pores); pollen (3-)4+ colporate, surface verrucose-vermiculate, with small granules; (style not impressed), nectary (on ovary wall - Sarracenia); placentation intrusive parietal apically, style apically hollow or not, apex divided or peltate-expanded, stigmas small; ovules many/carpel, unitegmic, integument 9-10 cells across, (bitegmic, micropyle endostomal, outer integument 3-4 cells across, inner integument 4-5 cells across - Heliamphora), "incompletely tenuinucellar"; seeds small, with wings or hairs, exotesta ± thickened; endosperm haustoria?, embryo medium; n = 13, 15, 21.
3 [list]/32: Heliamphora (23). E. and W. U.S.A. and the Guayana Highlands (map: from Uphof 1931; Schnell 2002). [Photo - Inflorescence © J. Maunder, Flower, Flower.]
Age. Crown group Sarraceniaceae are estimated to be (44-)35(-25) (Ellison et al. 2012) or ca 48.5 (Rose et al. 2018) Ma old.
Archaeamphora was described from rocks ca 124 Ma and thought to be Sarraceniaceae (Li 2005), however, it is likely to be a gall of the conifer Liaoningocladus boii (W. Wong et al. 2015; see also Herendeen et al. 2017).
Evolution: Divergence & Distribution. Ellison et al. (2012) offered a vicariance-style explanation that integrates the relationships and distributions of the three genera; Sarraceniaceae originated in South America, perhaps hopping across the proto-Caribbean on islands.
Ecology & Physiology. Carnivory: There are nectar glands on the pitcher which attract insects that then fall into the pitcher, alternatively, the nectar may take up water increasing the possibility of an insect's hydroplaning into the pitcher (see Bauer et al. 2008); either way, death by drowning is the result. Suggestions that the colouring on the flap of the pitcher may attract insects, that is, it is a kind of pseudoflower (Cresswell 1993), seem unlikely (Joel 1988; Ruxton & Schaefer 2011), however, the plants of both Sarracenia and Heliamphora are variously scented, so attracting potential prey (Fleischmann 2016); for more on pitcher morphology, see Thorogood et al. (2017). The pitcher varies in the amount of digestive enzymes it contains, although these seem to come from the organisms in it; if so, this is a case of symbiotic digestion (Peroutka et al. 2008b). In S. purpurea, for example, there are few enzymes. Nutrients from the entrapped animals are made available to the plant by the activity of detritivores that break up the the animals, further decomposition is carried out by bacteria, and these in turn are eaten by rotifers and protozoa and ultimately by mosquito larvae - all forming a microcosm in each pitcher (Kitching 2000; Ellison et al. 2003; Butler & Ellison 2007; Adlassnig et al. 2011). For general information on carnivory, see especially Lloyd (1942) and Juniper et al. (1989).
Pollination Biology. Flowers of Heliamphora have nectaries and are buzz pollinated; Sarracenia has ten nectaries on the ovary wall above the stamen fascicles.
Plant-Animal Interactions. Caterpillars of the moth Exyra fax drain the pitchers of Sarracenia by opening up a hole at the base, and they then eat the pitcher. Exyra occurs throughout the range of Sarracenia (see e.g. McPherson & Schnell 2011).
For the microcosm inside the pitcher, see Bittleston (2018 and references). The small mosquito Wyeomyia smithii breeds in the pitchers of Sarracenia purpurea, and the larvae eat animal remains in the pitcher although they are not harmed by the fluid there (Bradshaw 1983; Istock et al. 1983). The recent range expansion of the mosquito as the climate warms and its adaptation to the changing daylengths it consequently faces have been much studied (Mathias et al. 2007 and references). Interestingly, the diversity of animals, whether invertebrates or bacteria, in the pitchers increases with increasing latitude, the reverse of the normal trend (see elsewhere), perhaps because the numbers of Wyomyia larvae that eat them decrease (Buckley et al. 2003; Kindlmann et al. 2007).
Bacteral/Fungal Associations. The plant lacks mycorrhizae (Brundrett 2004 and references).
Chemistry, Morphology, etc. Jensen (1992) suggests the family has route I iridioids. In Sarracenia, at least, the leaves have an adaxial flange, but the pitcher develops from the midrib area - see Fukushima et al. (2015) for patterns of cell division and development of the leaf and Franck (1976) for an evaluation of classical work on the nature of the pitcher.
Löfstrand and Schönenberger (2015) suggested that the perianth of Heliamphora is biseriate and is made up of calycine and corolline whorls. Outside the petaloid calyx of Sarracenia there are three "bracts". When there are many stamens, development is sometimes centrifugal from initially 10 primordia.
For general information, see Kubitzki (2004b), McPherson (2006, 2010), papers in Ellison and Adamec (2018), esp. Naczi (2018), and the Carnivorous Plants Database, for perforation plates, see Schneider and Carlquist (2004) and Carlquist (2012c: pores almost closed), and for pollen, see Takahashi and Sohma (1981).
Phylogeny. R. J. Bayer et al. (1996), Neyland and Merchant (2006), Ellison et al. (2012) and Rose et al. (2018) provide more information about relationships within the family; the topology [Darlingtonia [Sarracenia + Heliamphora]] is well supported. See Stephens et al. (2015) for relationships and species limits in Sarracenia.
Classification. McPherson and Schnell (2011) and McPherson et al. (2011) provide an account of the family. There is extensive interspecific hybridization in both Heliamphora and Sarracenia.
Thanks. I thank D. Hoekman for information.
Synonymy: Heliamphoraceae Chrtek, Slavíková & Studicka
[Actinidiaceae + Roridulaceae]: raphides + [in sacs]; mucilage in stylar canal/on placentae, inner surface of carpels secretory, lateral carpellary vascular bundles absent [no synlaterals].
Age. Stem-group Roridulaceae have been estimated to be ca 90 Ma old (Warren & Hawkins 2006) or ca 38.1 Ma (Ellison et al. 2012); the age for this node is about 84.8 Ma in Magallón et al. (2015), 79.5 Ma in Rose et al. (2018), and (85-)76(-72) Ma in Wikström et al. (2015).
Chemistry, Morphology, etc. See Löfstrand et al. (2016) for a discussion on synlateral vascular bundles and gynoecial mucilage.
ACTINIDIACEAE Engler & Gilg, nom. cons. - Back to Ericales
Trees, shrubs or twining lianes; (vessel elements with simple perforation plates); (nodes 3:3); petiole bundle deeply arcuate with wing bundles [Actinidia] or annular (medullary bundles +); stomata anomocytic; hairs multiseriate, often ± (flattened) setose; leaves (opposite), lamina vernation conduplicate, apex of tooth expanded, clear, not deciduous, (secondary veins subpalmate); plant usu. dioecious; C ± connate or not, (?nectar at base of C); A 10-many, centrifugal, (in groups opposite petals), inflexed in bud (not - Saurauia), (basally connate), anthers extrorse, inverting [?always], dehiscing by pores or ± short slits; pollen tectum ± psilate to rugulate and transversely striate, columellae reduced, (equatorial bridge of ektexine over endoaperture); (?nectary on G); G [(-20)], styluli, or style, ± branched (unbranched), (grooved - Actinidia), (hollow), (stigma peltate, lobed); ovules 10</carpel, integument 6-9 cells across, endothelium +, parietal tissue ?0-ca 3 cells across, nucellar cap 0-ca 3 cells across; (megaspore mother cells several), embryo sac protruding from nucellus; fruit usu. a berry (loculicidally dehiscent); seeds embedded in placental pulp; integument multiplicative; endosperm haustoria?; n = 20, 26, 29, 30, chromosomes ca 1μm long [Actinidia]; nuclear genome [1C] (680-)1242(-2176) Mb; (plastid transmission biparental); horizontal transfer of mitochondrial rps2 gene [Actinidia].
3 [list]/430: Saurauia (350), Actinidia (54), Clematoclethra (25). Largely tropical, esp. South East Asia to Malesia, but not Africa (map: from Soejarto 1980).
Age. The crown-group age of this family is ca 46.5 Ma (Rose et al. 2018).
Parasaurauia was described from flowers of Early Campanian (Late Cretaceous) age ca 80 Ma from the eastern USA. It has impressed, separate styles and numerous stamens and may belong to crown group Actinidiaceae (Keller et al. 1996; Herendeen et al. 1999; see also Martínez-Millán 2010).
Evolution: Divergence & Distribution. For the fossil record, see Manchester et al. (2015).
Both separate styles and numerous stamens are probably derived within the family (Keller et al. 1996; Herendeen et al. 1999).
Genes & Genomes. For a genome duplication around here, Ad-α, perhaps in Actinidia only, see Shi et al. (2010: ca 28.3 Ma) and S. Huang et al. (2013: ca 26.7 Ma).
There is paternal transmission of the plastid genome in Actinidia (Chat et al. 2003), maternal in Clematoclethra, and the clP gene is missing in both (W.-C. Wang et al. 2018).
Economic Importance. For the vitamin C-rich kiwi fruit, Actinidia delicosa, see H. Huang (2014).
Chemistry, Morphology, etc. Anthers of staminodes in Saurauia contain sterile pollen; in general, dioecy in the family is cryptic. For androecium development in Actinidia, see van Heel (1987), the synascidiate carpels are in a single whorl, and there is a large, flat, residual floral axis.
For general information, see Dickison (1972), Dressler and Bayer (2004) and Wong (2017: Saurauia), for vegetative anatomy, see Beauvisage (1920), the floral anatomy of Actinidia, see Schmid (1978), for floral development, see Schönenberger et al. (2012), for pollen, see Dickison et al. 1982), and for ovules, see Guignard (1882) and Schnarf (1924).
Phylogeny. Rose et al. (2018) suggest the relationships [Saurauia [Clematoclethra + Actinidia]].
Synonymy: Saurauiaceae Grisebach, nom. cons.
RORIDULACEAE Martinov, nom. cons. - Back to Ericales
Shrub, carnivorous [insectivorous]; unspecified iridoids +, ellagic acid?; cork?; pericyclic fibres 0; hairs dense, glandular; leaves ± U-shaped in t.s., sessile, lamina linear, margins entire or laciniate; inflorescence with a terminal flower [?always; sometimes looking racemose], bracteoles +; C free; stamens = and opposite sepals, connective swollen at apex of anther, conspicuous and nectariferous, anthers latrorse; pollen densely and minutely spinose, or surface irregular; placentation apical, style unbranched, apical part of style/stigma clavate, densely long-papillate; ovules 1-4/carpel, pendulous, integument 10-11 cells across, funicle prominent; testa mucilaginous [?]; endosperm with micropylar haustorium +; n = 6.
1 [list]/2. Southern Africa (map: fossil locality in green). [Photo - Roridula Flower © M. Schmidt.]
Age. The age of crown-group Roridulaceae is estimated at ca 10.7 Ma (Ellison et al. 2012) or ca 20.2 Ma (Rose et al. 2018).
Evolution: Divergence & Distribution. It was suggested that, given their age, ca 90 Ma, Roridulaceae must be very much a relictual (?Gondwanan) element in the Cape flora (e.g. Warren & Hawkins 2006). However, well preserved fossils in Baltic amber dated to 47-35 Ma were recently described by Sadowski et al. (2015), furthermore, the general distributions of families in this part of the ericalean tree are not Gondwanan. Indeed, Roridulaceae might even have originated in the northern hemisphere; see also also Cornales-Curtisiaceae for comparable extant/fossil distributions. In any event, this is definitely a low-diversification clade (Magallón et al. 2018)!
Ecology & Physiology. Although the family may not be carnivorous in a conventional sense, digestive enzymes not having been recorded from it (e.g. Hartmeyer 1997), its two species live in a very close mutualistic association with two species of the hemipteran mirid bug, Pameridea (see Wheeler & Krimmel 2015 for the bug). These bugs eat the insects that get stuck to the hairs that cover the plant, and the plant absorbs nutrients from their excreta via tiny holes in the cuticle, a form of indirect carnivory (Ellis & Midgley 1996; Anderson 2005). However, Plachno et al. (2009) suggest that Roridula is directly carnivorous because they recorded mineral uptake from Drosophila stuck on the leaves.
Pollination Biology. The bug Pameridea may also be involved in pollinating Roridula (Ellis & Midgley 1996). Most pollination is by autonomous selfing or (25-68%) selfing or geitonogamy by immature bugs, buzz pollination being at most uncommon and unimportant despite the apparent buzz pollination syndrome of the flowers (Anderson et al. 2003).
Bacterial/Fungal Associations. The plant may lack mycorrhizae (Brundrett 2004; Conran 2004 and references; c.f. Adlassnig et al. 2005).
For general information, see Vani-Hardev (1972), Dahlgren in Dahlgren and van Wyk (1988: endosperm haustoria 0), Conran (2004), McPherson (2008, 2010), papers in Ellison and Adamec (2018), and the Carnivorous Plants Database, also Wilkinson (1998: anatomy) and Takahashi and Sohma (1981: pollen).
Previous Relationships. Roridula was included in Byblidaceae by Cronquist (1981); for further information on relationships, see that family (Lamiales!).
[Clethraceae [Cyrillaceae + Ericaceae]]: ellagic acid +; cork cambium ± pericyclic; pericyclic fibres absent; leaves spiral; bracteoles 0; stamens = 2x K, anthers extrorse; nectary in basal part of ovary wall; placentation intrusive parietal apically, basal part of placenta free, pendulous, style hollow; endosperm with micropylar and chalazal haustoria, embryo terete.
Age. The age of this node is estimated to be ca 58 Ma (Naumann et al. 2013), ca 50.6 Ma (Ellison et al. 2012) or (89-)71(-44) Ma (Wikström et al. 2015); see sampling in all. Around 93.9 Ma is the estimate in Rose et al. (2018), 79.2 Ma in Magallón et al. (2015) and ca 70.4 Ma in Tank et al. (2015: Table S2).
Rariglandula jerseyensis, a 92-85 Ma fossil from New Jersey, has dense multicellular hairs on the abaxial surface of the calyx; in an analysis of 13 morphological characters (anther apical protrusion is what in the three species so coded?) it was placed with the single species of Clethra in the analysis (Martinez et al. 2016). If correctly placed, most molecular ages proposed in this clade will have to be reconsidered.
Evolution: Divergence & Distribution. In the context of the floral morphospace of Ericales, Chartier et al. (2017) thought that this clade was rather homogeneous.
Chemistry, Morphology, etc. It is possible that the accumulation of sugars as ketose and isokestose oligosaccharides is of systematic significance; fructoses may be involved in membrane stabilization and cold- and/or drought tolerance in plants (Livingston et al. 2009). Bracteoles have to be regained somewhere in this clade, but I have not worked out where - perhaps it is not that important.... Van Tieghem (1903) noted that both Clethraceae and Ericaceae had ovules with an epistase.
Phylogeny. The relationships [Cyrillaceae [Clethraceae + Ericaceae]] are sometimes recovered (Morton 2011: nuclear Xdh gene).
CLETHRACEAE Klotzsch, nom. cons. - Back to Ericales
Plant (deciduous); mycorrhiza a modified ectendomycorrhiza?; fructan sugars accumulated as kestose and isokestose oligosaccharides [levans and inulins], iridoids?; (pits vestured); petiole bundle arcuate or annular with medullary bundle; stomata also paracytic and actinocytic; hairs stellate [Clethra sect. Clethra]; lamina vernation conduplicate-subplicate, margins toothed (entire); inflorescences terminal, branched or not; flowers spreading (pendulous), (bracts conspicuous - Purdiaea), pedicels articulated; C basally connate or free; A obdiplostemonous [?all], adnate to C or not, anthers ± sagittate, dehiscing by pores or short slits; pollen <20µm, oblate, psilate to rugulate; nectary +, not vascularized/0; G ?orientation, (placentation apical - Purdiaea), stigma lobed or not; (ovule 1/carpel, pendulous, straight - Purdiaea); K persistent in fruit; seeds winged or not, or fruit dry, indehiscent, testa undistinguished, ± disappearing [Purdiaea]; endosperm hemicellulosic; n = 8.
2 [list]/75: Clethra (65). E. Asia to Malesia, S.E. U.S.A. (sect. Clethra), Mexico southwards, Cuba, 1 sp. on Madeira (Clethra sect. Cuellaria); largely tropical montane to ± warm temperate (map: from Sleumer 1971d; Good 1974; Heywood 1978). [Photos - Fruits & Flowers © A. Gentry, Inflorescence, Purdiaea Inflorescence.]
Age. Crown-group Clethraceae are ca 82.8 Ma (Rose et al. 2018).
Evolution: Divergence & Distribution. Grehan (2017) suggested that the distribution Clethra arborea/Macaronesia — C. alnifolia/east North America reflects vicariance events as the North Atlantic opened 120-100 Ma. Dates around here seem particularly unclear (for more in Clethra, see Rose et al. 2018), however, Palaeo-Macaronesia is likely to be 60 Ma or more old, the oldest currently emergent Canary Island dating to ca 21 Ma (Gelmacher et al. 2005; Fernández-Palacios et al. 2011) so at least some role for dispersal is likely.
Ecology & Physiology. Purdiaea nutans locally dominates in ridge-line vegetation in Ecuador (Mandl et al. 2008).
Chemistry, Morphology, etc. Iridoids were described as being absent but scored as being present in Hufford (1992); they are not mentioned by Schneider and Bayer (2004). In Clethra, there is a prominent endodermis in the stem and the pith tends to be heterogeneous.
Some information is taken from J. L. Thomas (1960: Purdiaea), Sleumer (1967: Clethra), and Schneider and Bayer (2004), all general, Sai 1934 (mycorrhiza), Giebel and Dickison (1976: wood anatomy), Kavaljian (1952) and Schönenberger et al. (2012), both floral morphology, and Anderberg and Zhang (2002: pollen).
Phylogeny. See Fior et al. (2003) for a phylogeny of Clethra; they suggest that the Macaronesian C. arborea may be sister to the E. North American C. alnifolia.
[Cyrillaceae + Ericaceae]: myricetin +; colleters +; K ?imbricate, C connate; stigma wet.
Age. The age of this node is estimated to be ca 93.9 Ma (Rose et al. 2018), 69.3 Ma (Magallón et al. 2015) or ca 64.7 Ma (Tank et al. 2015: Table S2).
CYRILLACEAE Lindley, nom. cons. - Back to Ericales
Shrub (deciduous), shooting from roots; iridoids?; sieve tube plastids with protein crystalloids and fibres; petiole bundle annular, complex or deeply concave; colleters + [Cyrilla]; lamina vernation supervolute, margins entire; flowers spreading, (weakly monosymmetric), (6-7-merous), pedicels articulated; K connate basally, C connate basally; A diplostemonous, or = and opposite sepals [Cyrilla], anthers ellipsoid, introrse, not inverting, dehiscing by slits; pollen >16µm, spherical, smooth; G [2-5], placentation apical, style 0 or short, continuous with ovary, stigma lobed; ovules 1-3/carpel, pendulous, mostly apotropous, integument 4-7 cells across; fruit indehiscent, 1-4-seeded, a dry drupe or 2-5-winged samara; testa undistinguished, ± disappearing; endosperm moderate; n = 20.
2 [list]/2. S. U.S.A. to N. South America (map: from Thomas 1960). [Photo - Cliftonia Habit].
Age. Crown-group Cyrillaceae may be ca 19.6 Ma (Rose et al. 2018).
Chemistry, Morphology, etc. Goldberg (1986) notes the presence of small, scarious stipules; I have not seen them. J. L. Thomas (1960: p. 15) described "bright red, ligulate, glandular structures" associated wuith the axillary buds, and there were perhaps similar structures paired at the bases of the bracts and even sepals; he was unsure of their nature. Although it is unclear to what genera he was referring, it was probably Cyrilla.
Goldberg (1986) also shows a floral diagram in which the median K is abaxial. The sepals are small and do not overlap, except perhaps very early in development. Anderberg and Zhang (2002: see also Copeland 1953) draw the anthers as being introrse and also suggest that the stamens do not invert during development. Cyrilla was described as having its five stamens opposite the petals by Thomas (1960). There are stomata on the nectary, but apparently not on the nectaries of Ericaceae (W. H. Brown 1938).
For general information, see J. L. Thomas (1960: monograph, 1961), Anderberg and Zhang (2002) and Kubitzki (2004b), also Copeland (1953: floral morphology and anatomy), Zhang and Anderberg (2002: pollen), Vijayaraghavan (1970: ovule morphology, etc.)..
Previous Relationships. The old division between Clethraceae and Cyrillaceae was based on fruit type (dehiscent versus indehiscent fruits), but the new limits correlate better with general floral morphology.
ERICACEAE Jussieu, nom. cons. - Back to Ericales
Benzo- and naphthoquinones, route I secoiridoids +, ellagic acid 0; petiole bundle arcuate; pericyclic fibres in leaf and stem poorly/not developed; buds perulate [?level]; lamina vernation involute, margins entire to toothed, teeth associated with multicellular hairs; inflorescence terminal; K connate basally, C connate; A obdiplostemonous, appendages +, (resorbtion tissue/granular pouches +); tapetal cells uni- or binucleate; pollen >26µm, surface ± rugulate; G , opposite C, style undivided, stigma expanded; integument 4-6 cells across; K persistent; exotesta with outer wall unthickened; chloroplast infA gene defunct.
Ca 126 [list: to tribes]/4,1800 (4,426: Schwery et al. 2014) - eight main groups below. Boreal to warm temperate, also montane tropics, very rare in lowland tropics (map: N. part of range, see Hultén 1971; Meusel et al. 1978; Luteyn 1995).
Age. The age of this node may be around ca 90.5 Ma (Rose et al. 2018), 98-90 Ma (Z.-W. Liu et al. 2014) or (123.9-)117.3(-109.4) Ma (Schwery et al. 2014), although many estimates of the age of core eudicots are similar to this last age...
1. Enkianthoideae Kron, Judd & Anderberg
(Plant deciduous); pith with small, thick-walled and lignified and larger and thin-walled cells mixed [heterogeneous]; leaves pseudoverticillate; flowers pendulous; anthers dehiscing by slits broadening towards the apex, with paired awns; pollen grains tricellular, surface ± granulate; suprachalazal nucellar tissue; megagametophyte with "ears"; n = 11.
1/16. South East Asia: China, Japan and environs (map: from Kron & Luteyn 1995). [Photo - Habit.]
Age. For Paleoenkianthus, ca 90 Ma, see above.
[[Pyroloideae [Monotropoideae + Arbutoideae]] [[Cassiopoideae + Ericoideae] [Harrimanelloideae [Epacridoideae + Vaccinioideae]]]]: plant ectendomycorrhizal, [fungal sheath; Hartig net; hyphae with complex coiled intrusions in the exodermal cells], root hairs 0; (K with single trace); anthers with exothecium, dehiscing by pores; pollen in tetrahedral tetrads, tetrads calymmate, cohesion simple; stigma dry to wet; vascular bundle in ovule absent; nuclear genome [1C] (577-)735(-1252) Mb; duplication of complete chloroplast ndhH-D operon.
Age. This node is dated at around 91 Ma (Z.-W. Liu et al. 2014).
[Pyroloideae [Monotropoideae + Arbutoideae]]: root with hyphal mantle, Hartig net common, ECM-type fungi, commonly inc. Sebacinales-Sebacinaceae.
Age. The age of this node is about 86 Ma (Z.-W. Liu et al. 2014).
2. Pyroloideae Kosteltsky
Perennial herbs, rhizomatous, (plant mycoheterotrophic; leaves as scales); fructan sugars accumulated as ?kestose and isokestose oligosaccharides [levans and inulins]; multicellular hairs 0; leaves pseudoverticillate; flowers ± spreading, (monosymmetric, asymmetric); C free, ± rotate; anthers with short (0) tubules, appendages 0, (endothecium 0); (pollen in monads); nectary usu. 0; placentation intrusive parietal; integument 2-3 cells across; testa walls thin; embryo short, hardly differentiated; germination mycoheterotrophic; n = 8, 11, 13, 16, 19; protein crystals in nuclei.
4/40: Pyrola (35). N. hemisphere, temperate to arctic, in N. Sumatra (map: from Meusel et al. 1978; Hultén & Fries 1986); the distribution in E. Asia is rather unclear. [Photo - Chimaphila Flower, Pyrola Flower.]
Age. The age of crown-group Pyroloideae is estimated to be (70.9-)50.7(-33.5) Ma (Z.-W. Liu et al. 2014).
Synonymy: Pyrolaceae Lindley, nom. cons.
[Monotropoideae + Arbutoideae]: flowers pendulous.
Age. The two clades diverged ca 70 Ma (Hardy and Cook 2012) or around 79 Ma (Z.-W. Liu et al. 2014).
3. Monotropoideae Arnott
Perennial herbs, roots (coralloid/forming a tight ball); plant echlorophyllous, mycoheterotrophic, hyperparasitic; fungal hyphae with peg-like intrusions into the exodermal cells; fructan sugars accumulated as kestose and isokestose oligosaccharides [levans and inulins]; sieve tube plastids lacking both starch and protein inclusions; multicellular hairs 0 [+ - Pterosporeae]; leaves sessile, ± scale-like; (bracteoles +); flowers 3-8-merous; (bracts petaloid); K (0), sometimes quite large, C (0), free or connate; anthers usu. with slits, (thecae confluent), appendages 0 (spurs +); pollen in monads; (placentation parietal); integument 2-3 cells across; (fruit baccate); seeds minute, dust-like, winged or not, (walls thickened); embryo minute, undifferentiated; germination mycoheterotrophic; n = 8, (26); protein crystals in nuclei.
10/15. N. hemisphere, largely temperate (map: from Wallace 1975; Hultén & Fries 1986; to Colombia, Malaya and Sumatra). Photo - Monotropa Habit, Pterospora Habit, Flower.]
Synonymy: Hypopityaceae Klotzsch, Monotropaceae Nuttall, nom. cons.
4. Arbutoideae Niedenzu
(Plant deciduous); ellagic acid +, C-8 iridoid glucosides +; corolla urceolate; anthers with paired awns, without endothecium; style continuous with ovary; ovules 10>/carpel, integument ca 5 cells across; fruit fleshy, berry or drupe; testa cells rather thick-walled; n = 13.
1-6/ca 80: Arctostaphylos (60). Warm (cold) temperate, esp. S.W. North America, Mediterranean (map: from Meusel et al. 1978; Hultén 1962; Hultén & Fries 1986; Kron & Luteyn 2005).[Photo - Flower (x-sec), Inflorescence.]
Age. The age of the node [Arbutus + Arctostaphylos] is (25-)15, 14(-7) Ma (Bell et al. 2010), 17-12 Ma (Wikström et al. 2001) or (53.5-)40.9(-28.5) Ma (Schwery et al. 2014).
Synonymy: Arbutaceae Bromhead, Arctostaphylaceae J. Agardh
[[Cassiopoideae + Ericoideae] [Harrimanelloideae [Epacridoideae + Vaccinioideae]]]: ericoid hair roots + [± = endodermis, epidermis, tracheid, sieve tube + companion cell - 40-70 µm across]; non-ECM-type ascomycetes and basidiomycetes, inc. Sebacinales-Serendipitaceae; (toxic andromedane diterpenes +); (vessel elements with simple perforation plates [?here]); pericyclic fibres in leaf and stem ± developed; stamens early inverting, anther wall without endothecium.
Age. Wagstaff et al. (2010) date this node to ca 65 Ma, but it is around 76.9 Ma in Rose et al. (2018) and 77 Ma in Z.-Y. Liu et al. (2014).
[Cassiopoideae + Ericoideae]: leaves opposite, lamina vernation revolute.
Age. Wagstaff et al. (2010: constraint age) give the age of this node as ca 40.5 Ma, while ca 74.7 Ma is the estimate in Rose et al. (2018).
5. Cassiopoideae Kron & Judd
Pith with large thin walled cells surrounded by smaller thick-walled and lignified cells [Calluna-type]; pericyclic fibres in leaf and stem poorly/not developed; buds not perulate; leaves small, sricoid, sublinear, peltate; flowers single, axillary, pendulous; anthers with awns; embryo sac bisporic [Allium type] [?always].
1/12. Circumboreal (map: from Meusel et al. 1978; Hultén & Fries 1986; Kron & Luteyn 2005). [Photo - Habit.]
6. Ericoideae Link
(Pedicel articulated); stamens lacking appendages; style impressed; capsule septicidal; (dust seeds +).
19/1,950. Widespread, if scattered, not lowland tropics (map: from Meusel et al. 1978; Hultén & Fries 1986; Kron & Luteyn 2005).
Age. This node may be ca ca 67.9 Ma (Rose et al. 2018).
6a. Phyllodoceae Drude
(Grayanotoxins + [cyclic diterpenes]); leaves (opposite), (ericoid); C (free - Elliotia); A (held in C pockets - Kalmia).
7/. The Andes to North America, some Europe to Asia (Japan). Photo - Flower.
Age. There is Kalmia-type pollen from western Europe at least 40 Ma (Hofmann 2018).
6b. Bryantheae Gillespie & Kron
Shrubs; pith heterogeneous; leaves opposite/spiral, ericoid/flat; flowers 4-9-merous; C ± free; A = or 2X C, endothecium 0; x = ?
2/8. Japan, East Russia (Bryanthus), the Guayana highlands.
6c. Ericeae de Jussieu
Shrubs (to small tree); leaves ericoid (flat, linear); stamens with appendages (0).
3/800: Erica (765+). Western Europe, tropical African mountains, Madagascar, most South Africa. Habit, Flower.
Age. Pollen from western Europe about 56 Ma has been identified as Erica (Hofmann 2018).
Synonymy: Salaxidaceae J. Agardh
[Empetreae + Rhodoreae]: ?
6d. Empetreae Horaninow
Shrubs; leaves opposite (spiral - Diplarche), blades flat/ericoid; (plant mono-/dioecious); K 3-6, C 0 (5); A 3-10 (5A adnate to C - Diplarche); (tapetal cells multinucleate - Empetrum); G [-9], style short [shorter than the ovary]; (1 ovule/carpel; fruit often a drupe.
4/7. Scattered: N. temperate to Arctic, Azores and the Iberian Peninsula, E. North America, southern Andes, Tristan da Cuhna, E. Himalayas, SW China. Empetrum fruit, © J. Maunder.
Synonymy: Diplarchaceae Klotzsch, Empetraceae Hooker & Lindley
6e. Rhodoreae Bremekamp
Shrubs to small trees, plant (epiphytic), (deciduous); grayanotoxins +; leaf blade ± flat; flowers pendulous to erect, (monosymmetric); (median sepal abaxial), (C 0); (pollen with viscin threads, attached distally to the grains); plastid transmission biparental [Rhododendron]; n = .
1/1,010: Rhododendron (inc. Azalea, Ledum, Menziesia, Tsusiophyllum). Predominantly North Temperate, esp. montane Himalayas to Papua, the Arctic, to NE Australia.
Age. This clade (Thero sister) is around 65 Ma, but if the fossil seeds (see below) are stem Rhododendron, the clade may be less than 45 Ma (N. Shrestha et al. 2018).
Rhododendron-type pollen from western Europe is around 40 Ma or more (Hofmann 2018) while fossil seeds (R. newburyanum) are ca 54.5 Ma (Collinson & Crane 1978).
Synonymy: Azaleaceae Vest, Ledaceae J. F. Gmelin, Menziesiaceae Klotzsch, Rhododendraceae Jussieu, Rhodoraceae Ventenat
[Harrimanelloideae [Epacridoideae + Vaccinioideae]]: K in fruit not withering.
Age. The age of this node is about 77 Ma (Z.-W. Liu et al. 2014) or 71.7 Ma (Rose et al. 2018).
7. Harrimanelloideae Kron & Judd
Leaves acicular, lamina margins entire; flowers single, axillary, pendulous; anthers with spurs.
1/2. Interruptedly circumboreal (map: from Hultén & Fries 1986; Kron & Luteyn 2005).
[Epacridoideae + Vaccinioideae]: (multiseriate rays, wide and high).
Age. Wagstaff et al. (2010: constraint age) give the age of this node as ca 37.8 my., but it is around 65.3 Ma in Rose et al. (2018) and 67 Ma in Z.-Y. Liu et al. (2014).
8. Epacridoideae Arnott (Styphelioideae) [Tribes still being constructed.]
Axial parenchyma usu. diffuse (in aggregates); rays exclusively uniseriate; epidermis lignified; cells ± rectangular, in longitudinally parallel ranks, anticlinal walls of abaxial [at least] epidermal cells sinuous; leaf vascular bundles embedded, with well-developed abaxial fibrous tissue, no adaxial cap; leaves xeromorphic, pungent; inflorescences often axillary, usu. spikes or multibracteolate axillary flowers; flowers often pendulous; A 5, opposite sepals, epipetalous, anthers bisporangiate, monothecal, dehiscing by slits, appendages 0; C persistent in fruit.
35/545. Australasia, Chile (map: Sleumer 1964; Kron & Luteyn 2005; FloraBase 2006; Australia's Virtual Herbarium xi.2012). [Photo - Flower, Fruit & Flowers.]
Age. Crown-group Epacridoideae are 89.3-68.7 (Schwery et al. 2014) or ca 65.3 Ma (Rose et al. 2018).
8a. Prionoteae Drude
Lamina with three veins from the base; anthers dehiscing by two slits.
2/2. Chile, Tasmania.
Synonymy: Prionotaceae Hutchinson
[Archerieae [Oligarrheneae [Cosmelieae [Richeeae [Epacrideae + Styphelieae]]]]]: multicellular hairs 0; lamina with parallel veins, [midrib not evident], margin lacking serrations; flowers often lacking a clear pedicel; anthers dehiscing by a single slit.
8b. Archerieae Crayn & Quinn
Rays also biseriate; abaxial epidermis plus associated hypodermis detach from mesophyll.
1/4: Australia (Tasmania), New Zealand.
[Oligarrheneae [Cosmelieae [Richeeae [Epacrideae + Styphelieae]]]]: ?
8c. Oligarrheneae Crayn & Quinn
Abaxial surface of lamina lacking ribbon wax and papillae; C lobes valvate to induplicate-valvate; (A 2-5); G , style continuous, short; ovule 1/carpel; fruit a nut.
[Cosmelieae [Richeeae [Epacrideae + Styphelieae]]]: ?
8d. Cosmelieae Crayn & Quinn
Vessels up to 500 mm2; axial parenchyma scanty paratracheal; leaves sessile, bases sheathing.
3/27: Andersonia (22). S.W., E. Australia, Tasmania.
[Richeeae [Epacrideae + Styphelieae]]: ?
Age. Wagstaff et al. (2010) date this node to (37-)34.3, 33.4(-26.9) Ma, (29.8-)22.3(-15.4) Ma is the age in Schwery et al. (2014) and ca 54.6 Ma in Rose vet al. (2018).
8e. Richeeae Crayn & Quinn
Vessels up to 500 mm2; axial parenchyma scanty paratracheal; crystals in ray cells only; rays also >20-seriate; nodes 3:3-several; lamina bundles transcurrent abaxially by fibrous bundle sheath extensions; stomata brachyparacytic, wax platelets on adaxial lamina 0; leaves sessile, bases sheathing; bracteoles 0.
2/68: Dracophyllum (62). E. (C.) Australia, New Zealand, New Caledonia.
Age. Wagstaff et al. (2010) date crown Richeeae to (23.5-)20.6, 16.5(-8.7) Ma.
[Epacrideae + Styphelieae]: ?
8f. Epacrideae Dumortier
Rays usu. also to 10-seriate; (ovules apotropous - Lysinema).
5/55: Epacris (45). E. Australia, Tasmania.
Synonymy: Epacridaceae R. Brown, nom. cons.
8g. Styphelieae Bartling
Crystals in axial parenchyma only (0); rays to 20-seriate; lamina bundles close to abaxial epidermis; stomata parallel to long axis of leaf, abaxial epidermal cells not sinuous, often papillae over stomata; pollen grains single, three cells of the meiotic quartet not developing; fruit a drupe.
Ca 16: Styphelia (210). Australia, to S.E. Asia, Hawaii.
Synonymy: Stypheliaceae Horaninow
9. Vaccinioideae Arnott
Plant (epiphytic [ca 1/5 spp]), (deciduous); (grayanotoxins [cyclic diterpenes], methyl salicylate +); (hyphal sheath and Hartig net +, hair roots short); (cork cambium subepidermal); axial parenchyma scanty paratracheal; stomata often paracytic; apical bud aborting; (lamina entire), venation (palmate), (veins parallel), (with marginal or surficial glands); inflorescence usu. axillary; flowers usu. ± pendulous; pedicel often articulated, bracteoles +; anthers often with tubules, with spurs/2 or 4 awns/appendages 0; (G inferior), stigma truncate; (integument ca 10 cells across - Andromeda); (calyx fleshy), (fruit baccate); (testa mucilaginous); (embryo chlorophyllous); n = 12.
Ca 50/1,580. Inferior-ovaried taxa 1563 spp. - Schwery et al. (2014): "Vaccinium" (450), in Southeast Asia Agapetes (ca 400, inc. many Vaccinium), Dimorphanthera (ca 85), in tropical America Cavendishia (155), Psammisia (60), Thibaudia (60), Macleania (55), Gaylussacia (50). The rest: Gaultheria (240, inc. Pernettya, Diplycosia, Tepuia), Lyonia (35). N. hemisphere, Malesia and montane Central and South America, Australia (Queensland), few in Africa (map: from Meusel et al. 1978; Hultén & Fries 1986; Fl. China 14. 2005; Kron & Luteyn 2005; Australia's Virtual Herbarium i.2014). [Photo - Psammisia Flowers, Gaultheria Flowers, Vaccinium Flower © J. Maunder.]
Age. The age of crown group Vaccinieae is estimated to be (54.8-)45.6(-37.2) Ma (Schwery et al. 2014), ca 46.3 Ma (Rose et al. 2018), ca 44 Ma (Rose et al. 2018: Ly), or ca 32.4 Ma (Rose et al. 2018: Gau.Vac).
Pollen from western Europe about 56 Ma has been identified as Gaultheria and Vaccinium (Hofmann 2018).
Synonymy: Andromedaceae Döll, Oxycoccaceae A. Kerner, Vacciniaceae Perleb, nom. cons.
Floral formula: * ⚥ K ; C ; A 10; N; G .
Evolution: Divergence & Distribution. Ericaceous pollen has been identified in heathland vegetation dated to 75-65.5 Ma in Central Australia (Carpenter et al. 2015); for an evaluation of the fossil record of Epacridoideae, see Jordan and Hill (1996). Pollen from Western Europe ca 56 Ma has been identified as Ericoideae (three genera), and perhaps somewhat younger pollen as Vaccinioideae (two genera) (Hofmann 2018), while there is Late Cretaceous ericaceous pollen from southern Africa (Scholz 1985: Namaqualand). Quite well preserved seeds of Rhododendron (R. newburyanum) were described from Palaeocene deposits in southern England (Collinson & Crane 1978), and pollen with viscin threads, quite possibly from Rhododendron, is known from several localities in the northern hemisphere in deposits as old as ca 45 Ma (see Zetter & Hess 1996). Maiella miocaenica, from 16.3-12.8 Ma deposits in Poland, is similar to Calluna in many respects, but not in seed micromorphology; thought to be the oldest fossil record for Ericeae (Kowalski & Fagúndez 2017), pollen of other genera appears to be older (Hofmann 2018). However, Comarostaphylis globula (Arbutoideae), of about the same age and also from Poland, is probably not ericaceous at al. (Kowalski & Worobiec 2018).
Ericaceae are prominent components of vegetation growing in often rather acidic, coolish and well-lit habitats. The majority of the family is likely to have ericoid mycorrhizae (ERM: see below), although other mycorrhizal types are known here, and this association with fungi is likely to be an important element in the ecological success of the family.
Kron and Luteyn (2005) discuss the historical biogeography of Ericaceae; an Eurasian origin of the family is likely. They give useful distribution maps for the subfamilies, Cassiopoideae being shown as growing throughout Greenland, perhaps in anticipation of the disappearance of the ice. However, the biogeographical connections of some newly proposed relationships are not easy to understand, for example, Gillespie and Kron (2010) found that the Guayanan Ledothamnus was sister to the northeast Asian Bryanthus. A number of ages for major generic groupings in the family can be estimated from Fig 1 in Z.-W. Liu et al. (2014); some are given above.
One way of thinking about diversification in the family is to focus on clades in montane habitats, often shrubby and with low SLA (specific leaf area = relatively high mass/surface area, see below). Bouchenak-Khelladi et al. (2015) thought that being shrubby and with a low SLA, features that evolved at/below the base of the family, were essential for the later radiations to occur, while moving into montane environments where taxa in general tend to have a low SLA might sometimes trigger diversification; Schwery et al. (2014) noted also the association of Ericaceae with distinctive mycorrhizal types and oligotrophic, acidic conditions (see below) might also be contributing factors to these montane radiations. More specifically, there are six radiations, including Epacridoideae-Richeeae, Ericoideae-Rhodoreae and -Ericeae, and Vaccinioideae-Vaccinieae (both Gaultheria and inferior-ovaried taxa on both sides of the Pacific), in total almost 80% of the family, that have diversified greatly in mostly montane habitats (Schwery et al. 2014; Bouchenak-Khelladi et al. 2015; Hughes & Atchison 2015).
The inclusion of the largely Australian Epacridaceae within Ericaceae as Epacridoideae means that the rarity of Ericaceae in Australia no longer presents a biogeographical problem as it did in the 1970s - Ericaceae are indeed quite common there. Diverse early Pleistocene fossils of Epacridoideae are known from New Zealand (Jordan et al. 2007), but there are serious conflicts between molecular and fossil estimates of clade ages. Thus leaves and pollen from New Zealand and identified as Richeeae are ca 25-20 and 47-40 Ma old respectively, while in a molecular study Wagstaff et al. (2010) date the stem age of the clade of Dracophyllum that now grows in New Zealand at a mere (7.2-)6.2(-5.2) Ma. Indeed, Jordan et al. (2010) suggested that many of the fossil records in New Zealand may belong to extinct lineages, and this idea was seconded by Puente-Lelièvre et al. (2012) who noted that the age of Styphelieae would have to be some 210-120 Ma if these fossils were assumed to be members of the clades currently growing on the islands (see also Wagstaff et al. 2010). Puente-Lelièvre et al. (2012) found that seven of the eight New Zealand species of Epacridoideae that they examined all had closest relatives in Australia (that of the other species was in New Guinea) and had arrived in New Zealand within the last 4 Ma or so.
Within Ericoideae the numerous African species of Erica (659 spp. in the Cape Floristic Region - Linder 2003; see also S. D. Johnson 2010) form a clade that originated within a part of the Erica tree that otherwise includes taxa currently found in Europe (Pirie et al. 2011; see also McGuire & Kron 2005). Erica is the most diverse genus in the hyperdiverse Cape Floristic Region (Linder 2003; Pirie et al. 2017). 71-64 Ma pollen identified as Ericaceae has been found in Namaqualand, South Africa (Linder 2003); knowing what plant produced it would be of more than passing intereat. Rhododendron, which grows through much of the northern hemisphere, is notably diverse in Malesia-South East Asia. There are around 225 species in the Hengduan region of China alone (Boufford 2014), and two increases of diversification in the genus there are dated to 15-9 Ma, perhaps at the beginning of the uplift of the Hengduan mountains (Xing & Ree 2017). Lack of seasonality (N. Shrestha et al. 2017) and environmental heterogeneity may play roles in diversification in Rhododendron (see also orchids), which may have started in NE Asia, the genus then moving around the northern hemisphere and latterly into the Southeast Asian tropics, where the species are young and are nearly always to be found in montane habitats (N. Shrestha et al. 2018). There are around 290 species of Rhododendron in Malesia (Sleumer 1966), nearly all members of sect. Schistanthe (the old Vireya). Empetrum is likely to have arrived in southern South America in the Pleistocene, perhaps by long-distance dispersal from northwestern North America (Popp et al. 2011).
Vaccinieae are particularly diverse in the mountains of Central and South America and of Southeast Asia-Malesia. As is clear below, many of these species are epiphytic and/or lianes, some have distinctive seeds probably associated with the epiphytic habitat, and bird pollination is likely important in both hemispheres, however, depressingly little is known about diversification in Vaccinieae. The hyperspeciose clade in Vaccinieae (inc. "Vaccinium", Agapetes, Cavendishia) has been dated to (54.4-)45.6(-37.2) Ma (Schwery et al. 2014), although given the relationships of "Vaccinium" to other Vaccinieae, a major effort is needed to put variation and evolution in the tribe as a whole in context. Kron and Luteyn (2005) suggested that there were perhaps two migrations from the North to South America, and they dated diversification in South American Vaccinieae to Late Miocene. Vaccinieae from the Neotropics and North America may have had similar mycorrhizal Sebacinales-Serendipitaceae in common, and some kind of synchronised island hopping of plant and fungus between the two continents may have been needed (Setaro & Kron 2011; see also below). Although it has been suggested that connections between North and South America were established around the middle of the Miocene ca 24 Ma (see Bacon et al. 2015 and the discussion of that paper; Montes et al. 2015: geology re-evaluated), a recent comprehensive refutation of this idea should be consulted (see O'Dea et al. 2016). Outlines of interesting biogeographical groupings in neotropical Vaccinieae in particular are developing (Kron et al. 2002a; see also Powell & Kron 2003; Pedraza-Peñalosa 2009), and these may be correlated with variation in wood anatomy (Lens et al. 2004c).
Arbutoideae, now prominent in Mediterranean vegetation although hardly very diverse, may have moved from the New World to the Old World around 39.2-21.2 Ma (Hileman et al. 2001; Vargas et al. 2014) - Mediterranean vegetation is thought to be well under half that age (Vargas et al. 2014). Hardy and Cook (2012) compared diversification in Monotropoideae (it has slowed) with that of Arbutoideae (exponential increase). For the circumboreal species of Pyrola, a genus perhaps Asian in origin, and their places of origin, see Z.-W. Liu et al. (2014).
Note that Heads (2003) suggested that the main elements of the distribution patterns in the family were best explained by vicariance. The diverse Malesian Ericaceae in particular were, he thought, largely derived from taxa that lived in the mangroves, their current prevalance in higher-altitude vegetation being the result of rapid tectonic uplift. However, Ericaceae are hardly noted for being a megatherm family.
Lens et al. (2003, 2004a, b, c) place variation in wood anatomy in a phylogenetic context. I have not attempted to put this variation on the tree, but there is extensive homoplasy in most of the characters even within a subfamily.
Ecology & Physiology. There are four (partly overlapping) main ecological groupings in the family: 1, Taxa with fleshy fruits of one sort or another, ca 1,500 species, 2, taxa with xeromorphic leaves living in more or less Mediterranean or dry habitats, 1,300+ species (this includes about 675 species of Erica in the Cape fynbos vegetation and 120 species of Epacridoideae in West Australian kwongan vegetation - see Cowling et al. 1990), 3, taxa that are epiphytic (or epilithic) and often lianes, ca 650 species, and 4, taxa with viscin threads, ca 900 species. Most Ericaceae are shrubby plants and have associated ericoid mycorrhizae (ERM) growing in the ultimat branches of their roots.
Ericaceae are often common in alpine and arctic tundra (e.g. Jonasson & Michelsen 1996; Michelsen et al. 1998). Tundra alone, the main component of heathland sensu Specht (1979a, b; map: see end-papers in Specht 1979a; White et al. 2000), occupies ca 8% of the earth's surface (Kranabetter & MacKenzie 2010; Gardes & Dahlberg 1996) and Vaccinium and Empetrum are two of the seven major biomass accumulators there (Chapin & Körner 1995). Boreal forests occupy ca 17% of the land surface of the earth (Lindahl et al. 2002), and there the trees (Pinaceae, some Salicaceae and Betulaceae) are all ectomycorrhizal (ECM) while ERM Ericaceae often dominate in the understory (e.g. Villareal et al. 2004; Vrålstad et al. 2002; Vrålstad 2004; Kranabetter & MacKenzie 2010). However, in many of these habitats mosses like Sphagnum are very common, and they may dominate in overall carbon accumulation (e.g. Ragoebarsing et al. 2005; Flanagan 2014). Note that the map here differs considerably from that showing the distribution of ERM in Soudzilovskaia et al. (2017) where ERM records are absent from nearly all Africa, India, Asia and Malesia, but that was based on GBIF records, and the authors noted other problems.
In terms of functional distinctiveness, Ericaceae are in a clade that has notably low leaf nitrogen and a notably high leaf mass per area (i.e. a low specific leaf area - SLA), and a good number of Ericaceae, especially in Ericoideae-Ericeae and Epacridoideae, have notably small and often tough leaves (Cornwell et al. 2014). In the Mediterranean heathlands of southern Africa and Southwest Australia Ericoideae and Epacridoideae respectively are common shrubs, most with small leaves, thus there are 600 or more species of Erica growing in the Cape region of South Africa alone (Oliver 2000). In California Arctoctaphylos is a conspicuous component of the vegetation (see Rundel et al. 2016 for Mediterranean biomes). Ericaceae may dominate in montane shrubberies, especially in the northern Andes, parts of the eastern Himalayan-Yunnan region, and in Malesia, and are a prominent feature of alpine and arctic tundra and boreal forests (e.g. Chapin & Körner 1995; Jonasson & Michelsen 1996; Michelsen et al. 1998; Sistla et al. 2013), and Gerz et al. (2017) comment on the relatively broad niches of ERM plants (see also Clade Asymmetries). For variation in potentially ecologically important leaf and root traits and the evolution of Rhododendron, see Medeiros et al. (2017).
Connected with their ability to grow in such heathland habitats, many Ericaceae have distinctive ERM, ectendomycorrhizae in which fungal hyphae form complex and usually coiled intrusions in the exodermal cells of the distinctive very thin and aptly-named hair roots and sometimes also surround the roots with a sheath - such mycorrhizae are not known from other land plants. Hair roots are as little as 40 µm across, getting close to as thin as a root hair proper (hair roots lack root hairs), and in Vaccinium corymbosum, at least, even low-order roots, i.e. not the ultimate rootlets, are also quite thin (Massicotte et al. 2005; Valenzuela-Estrada et al. 2008). Hair roots consist of little more than endodermis, exodermis, tracheid, sieve tube, and companion cell, yet they are relatively long-lived. (Although Medeiros et al. (2017) note that the first order roots in the Rhododendron they studied were 0.1-0.8 mm. across, "on the larger side compared with most plants" (ibid.: p. 11), Valverde-Barrantes et al. (2017) show the diameter of ericoid roots as being substantially below the mean diameter for seed plants as a whole.) There are other ERM-type morphologies in Ericaceae, and one can think of them as showing various combinations of the development of a fungal sheath or mantle, a Hartig net (and if this is just between epidermal cells or the hyphae penetrate more deeply into the cortex), and hyphal protrusions into the cell (Imhoff 2009: see Bacterial/Fungal Associations below).
Overall, ERM Ericaceae make up ca 1.4% of all seed plants (Brundrett & Tedersoo 2018). They are most commonly found in open, more or less acidic, nutrient-poor and nitrogen-limiting soils in cold to warm temperate climates, that is, in generally rather stressful habitats, and they can also grow on soils with toxic metals (Read 1991: useful summary, 1993; Vrålstad et al. 2000; Cairney & Meharg 2003; Perotto et al. 2012; Garbaye 2013). They are often common in heathlands world-wide - in the past, characteristic families of such heathlands were thought to include Epacridaceae, Prionotaceae, Empetraceae and Vacciniaceae, but all these are now in Ericaceae (Grubbiaceae and Diapensiaceae were the only other families listed, see Specht 1979b; Read 1996). Indeed, if you see Ericaceae when in the field, it is a sign that the soil is likely to be acidic. They can grow on old soils where ERM compete successfully for phosphorus with microbes (Turner et al. 2012). Enzymes, etc., produced by the ERM plant/fungus association contribute to the formation of acidic mor humus that ERM plants like and AM plants do not (Read 1991). Ericaceous leaves are well defended chemically, often long-lived, and the plants are efficient at removing N and P from them when they die, and the result is persistent, nutrient-poor humus suitable only for the rather slow-growing Ericaceae, their fungal associates, and a relatively few other species (Read 1991; Cornelissen et al. 2001; see also Peay 2016). The hyphae of ERM fungi also have melanin, which, like lignin, is resistant to decay, and is an important component of the sequestered carbon in at least some older boreal forests (Read et al. 2004; Clemmensen et al. 2014; Fernandez et al. 2014, 2015; Lindahl & Clemmensen 2017).
Soils with acid mor humus may not be suitable for most plants, but many Ericaceae thrive under such conditions. The protein-tannin complexes that come from Rhododendron, at least, may result in nitrogen being held in the stable soil organic matter. This nitrogen is then more easily accessed by the saprotrophic activities of the ericoid fungi than by AM fungi in particular (Read 1991; Wurzburger & Hendrick 2009); the fine ericoid rootlets are very dense, if shallow, and efficiently permeate the soil (try digging up a rhododendron). In ERM, the fungal intrusions in the exodermis are not broken down by the host (Frank 1887; Read 1996; Perotto et al. 2012), but organic N and P taken up by the fungus move to the ericaceous associate; N in amino acids released by the fungus are also taken up by the plant (Cairney & Ashford 2002; E. A. Hobbie & Hobbie 2008; Perotto et al. 2012). ERM fungi show considerable metabolic diversity, having Plant Cell Wall Degrading Enzymes (PCWDs) and being able to break down cellulose and some perhaps even degrading lignin in a manner akin to brown rot fungi (e.g. Perotto et al. 2012 and references; Vohník et al. 2012; Martino et al. 2018); for some details of the movement of nutrients and photsynthesates between Ericaceae and other plants and their associated fungus, see Bacterial/Fungal Associations below. The ERM ascomycete Oidiodendron maius is saprotrophic and can break down Sphagnum peat; it has both cellulases and some lignin-decomposing enzymes that came from its saprotrophic ancestors (Kohler et al. 2015). ERM are not involved in carbon uptake by the host (Kohler & Martin 2017), indeed ECM fungi may use .
The adoption of the ERM habit can perhaps be dated to at least 72-66 Ma, Leucothoe eocenica (Vaccinioideae) being known from deposits of that age in Europe (Knobloch & Mai 1986; Strullu-Derrien et al. 2017). Indeed, if the identification is correct - the fruits are tiny, ca 1.8 x 1.8 mm, although apparently ripe - the clade characterized by ERM plants, the [[Cassiopoideae + Ericoideae] [Harrimanelloideae [Epacridoideae + Vaccinioideae]]] clade, must be considerably older. Indeed, Martino et al. (2018) dated the age of the common ancestor of the four ERM fungi (ascomycetes, Leotiomycetes) that they sequenced at ca 118 Ma, agreeing with the age of the family - ca 117 Ma - in Schwery et al. (2014), but the origin of the ERM association would in fact have to be younger (the AM Enkianthus is sister to the rest of the family and the mostly ECM [Arbutoideae [Monotropoideae + Pyroloideae]] make the next branch up), not to mention that the 117 Ma age itself is a remarkably high estimate. Wagstaff et al. (2010) date the ERM clade to ca 65 Ma and the estimate is around 77 Ma in Z.-Y. Liu et al. (2014).
The mycoheterotrophic habit (and probable hyperparasitism: see Björkman 1960) has arisen at least twice in Ericaceae, in Monotropoideae and Pyroloideae (Zimmer et al. 2007; Hynson et al. 2013; Lallemand et al. 2016; Tedersoo & Brundrett 2017; c.f. Cullings 1994). The relationship between fungi and Ericaceae is closest in the echlorophyllous and mycoheterotrophic Monotropoideae. Here the underground parts can be massive and the roots are thick, some 200-600 µm across, often with a thick fungal mantle (evident even in germinating seedlings), a Hartig net, and fungal pegs (Imhof et al. 2013). Basidiomycetes are often the fungi involved (Bruns et al. 2002; Garbaye 2013). In Pyroloideae Pyrola aphylla is a mycoheterotroph at times, other members of the subfamily are mixotrophic or fully heterotrophic (Hynson et al. 2009b; Selosse & Weiß 2009; Bowler et al. 2017), indeed, P. aphylla (a form of P. picta) may have small green leaves and the fungi associated with it show no particular specificity, as in other more photosynthetically conventional species of Pyrola (Hynson & Bruns 2009; Johansson et al. 2017). Both carbon and nitrogen move from the fungal associate to chorophyllous Pyroloideae and echlorophyllous Monotropoideae alike (Zimmer et al. 2007; Tedersoo et al. 2007a; Matsuda et al. 2012; Johansson et al. 2015; Lallemand et al. 2016); see also Hynson et al. (2016) for nitrogen metabolism, and Kranabetter and MacKenzie (2010) noted the distinctiveness of the nitrogen metabolism in Pyroloideae when compared with that of other Ericaceae with ERM, emphasizing their probably mixotrophic nutrition. Lallemand et al. (2016) discussed the evolution of the mycoheterotrophic habit and of mixotrophy in this clade (which includes Arbutoideae) in terms of predispositions, although it was unclear what these might be.
Hashimoto et al. (2012) found that in Pyrola asarifolia from Hokkaido, Japan, non-ECM fungi (Sebacinales-Serendipitaceae: Weiß et al. 2016) were associated with the plant as it germinated, at that stage the plant-fungus relationship being rather like that between orchids and fungi; different fungi were associated with the roots of the adult plant, being ECM fungi also associated with Betulaceae growing in the same area. However, the duration of this subterranean, non-photosynthetic stage and other details of this early relationship are poorly known (Hynson et al. 2013; see Johansson et al. 2017 and references for some details). Pyrola japonica s.l. included more or less aphyllous and mycoheterotrophic and leafy, "normal" haplotypes (Shutoh et al. 2016). Moneses uniflora showed geographical variation in the extent of partial mycoheterotrophy it showed (Hynson et al. 2015). See also Johansson et al. (2017) for discussion about Swedish taxa. Of course, mixotrophic and mycoheterotrophic species are also found in Orchidaceae (q.v. for more discussion), as are echlorophyllous seedlings.
Many species of Vaccinieae are epiphytes, and they are a major component of the woody epiphytic flora in both the Indo-Malesian and the Andean regions, indeed, Ericaceae are one of the more important epiphytic families among broad-leaved angiosperms, along with Gesneriaceae, Piperaceae and Melastomataceae (Benzing 1990; Zotz 2013). Woody epiphytes (here I include the few epilithic taxa in the family) are commonest in the fleshy-fruited tropical Vaccinieae, especially in the New Word, but are also quite common in Old World Rhododendron, which has wind-dispersed seeds, especially in section Schistanthe. Species of section Schistanthe commonly have large, mucilaginous hypodermal cells, perhaps involved in buffering the lamina against changes in water availability (Tulyananda & Nilsen 2017); such cells also occur elsewhere in the family. Lignotubers are known from some epiphytic taxa; they lack buds and may be involved in water storage (Evans & Vander Kloet 2010). Some epiphytic Vaccinioideae may also be lianes, especially in the New World (300 epiphytic/scandent species: Gentry 1991), and lianes are quite common in South East Asian/Malesian Vaccinioideae such as Vaccinium s.l. (including Agapetes) and Dimorphanthera. Note that distinctive cavendishioid mycorrhizae - here the ericoid roots are short, and there is both a fungal sheath and a Hartig net - have been found in (hemi-)epiphytic Vaccinieae from Andean South America (Setaro et al. 2006, 2008). Kottke et al. (2008a) also discuss the mycorrhizal fungi associated with epiphytic Ericaceae in the Andes, interestingly, bushy Ericaceae growing in open habitats have ordinary ERM, but the fungal associations in the forest-dwelling species differ (Kottke et al. 2008b).
Interestingly, Enkianthus has arbuscular mycorrhizae of the Paris type (Abe 2005; Obase et al. 2013), and it lacks hair roots. I have seen few accounts of mycorrhizae in Clethraceae or Cyrillaceae, but it is likely that the distinctive ERM became established only after Enkianthus and the [Arbutoideae [Monotropoideae + Pyroloideae] clades diverged. Diapensiaceae have ERM fungi (Brundrett & Tedersoo 2018), but their presence there is likely to be independant of that in Ericaceae.
Many taxa in Mediterranean climates in particular (Ericoideae in the South African Cape Region, Epacridoideae in Australia; Arctostaphylos in California), have xeromorphic leaves. Some species form starch-rich lignotubers with buds that allow the plants to resprout after fires, while others, like Arctostaphylos, regenerate by seeding; germination is enhanced by heat and/or smoke (Bell & Ojeda 1999; Cairney & Ashford 2002; Rundel et al. 2016 - c.f. Restionaceae).
Lens et al. (2003, 2004a, b, c) looked at ecological aspects of the woody anatomy of various members of the family. They found correlations between aspects of anatomy with latitude, and also with life form and precipitation.
Pollination Biology & Seed Dispersal. Although the anthers of most Ericaceae have functionally apical pores, nectaries are also common, and little is known about pollination in general and buzz pollination in particular in the family (c.f. in part de Luca & Vallejo-Marín 2013). There are some reports of buzz pollination. In Pyroloideae, for instance, the lack of an endothecium and absence of a nectary are associated with buzz pollination (Liu et al. 2011), and as in other such clades pollen is the reward. Buzz pollination is also reported from Conostephium (Styphelioideae), and here the pollen comes out of a narrow opening at the apex of the corolla tube, and again, there is no nectary (in Styphelioideae the anthers open by slits). Buzz pollination also occurs in genera like Sprengelia, although here the petals are spreading (Houston & Ladd 2002). However, most taxa (also) offer nectar as a reward. Although vibrations of the anther that result from bumble bees working the nectariferous flowers of Rhododendron may facilitate pollination, the bees do not buzz the flowers (King & Buchmann 1995). On the other hand, in Vaccinium and Erica growing in temperate heaths in Europe and both with nectar, buzz pollination and nectar foraging may occur on the same plant (Andrena and Bombus are the bees), and both may result in effective pollination (Moquet et al. 2017a, b). Viscin threads are well known in Rhodoreae, and have also been reported from Gaultheria (Lu et al. 2009). Although it would seem that such threads should increase the efficiency of placement of pollen grains on the pollinator, little is known about their role in pollination (e.g. Zetter & Hesse 1996).
Bird pollination is particularly common in the Andean Vaccinieae (Stiles 1981 and references). There are ca 600 species of Vaccinieae in the tropical Andes, over 500 species being found above 1,000 m., and the center of their diversity is the Colombia-Ecuador region, where hummingbirds, which pollinate most of these species, are also maximally diverse (Luteyn 2002; see also Gesneriaceae-Gesnerioideae, Bromeliaceae and Zingiberales-Heliconiaceae; for further details of hummingbird pollination, see elsewhere). Gentry (1982) discussed the diversity of bird-pollinated taxa of Gondwanan origin in tropical and premontane parts of the northern Andes. Several other factors have been implicated in this Andean diversification, including the adoption of the epiphytic habitat by some of these plants, the microtopographic diversity associated with the uplift of the Andes, etc. (Luteyn 2002) - but remember, little is known about their phylogeny. For an interesting mutualism involving the hummingbird Basilinna xantusii and Arbutus peninsularis in Baja California, see Abrahamczyk et al. (2017). Bird pollination also occurs in the large-flowered Indo-Malesian Vaccinieae Dimorphanthera and Paphia (Malesia) and Agapetes s. str. (mainland Southeast Asia). Interestingly, it has been suggested that "Agapetes" may originally have been pollinated by stem-group hummingbirds in the Old World ca 45 Ma, although "Agapetes" is now pollinated by sunbirds, Nectariniidae, and their like (Mayr 2005, 2009). In southern Africa perhaps 100 species of Erica in the Fynbos are pollinated by a few species of nectariniids, particularly by Nectarinia (= Anthobaphes) violacea, the orange-breasted sunbird (Rebelo et al. 1984; Rebelo 1987; S. D. Johnson 2010).
A variety of pollinators visit Malesian vireya rhododendrons (= Rhododendron sect. Schistanthe). This clade seems to have moved through the archipelago west to east, New Guinea and places south and east being inhabited by a separate and very speciose clade of vireyas (Goetsch et al. 2011), and there, too, bird pollination occurs - and nectar-eating mites may use the birds to travel from flower to flower (Stevens 1976). Bees are also common pollinators of the genus (references in Berry et al. 2017). Monosymmetry is quite common in Rhododendron, whether the flowers are tubular or infundibular and the colour is patterned or plain, and there is also variation in the direction of the curvature of the style and of the stamens - correlations between such features was examined by Berry et al. (2017). Indeed, bee, especially bumble bee, pollination is common in temperate and arctic-alpine members of the family, almost regardless of their floral morphology. Thus bumble bees pollinate alpine species of Rhododendron, Vaccinium (both polypetalous to tubular urceolate-campanulate), Elliottia (polypetalous), Phyllodoce, Pieris, Chamaedaphne, Cassiope, Gaultheria (all mostly urceolate to campanulate), etc. (Heinrich 1979; Ranta & Lundberg 1981; Tomono & Sota 1997; Kudo et al. 2011 and references), although other pollinators are also effective (in the northeast U.S.A. oligolectic bees are notable visitors of Vaccinium - Fowler 2016) and selfing also occurs.
Secondary pollen presentation - the pollen sticking on the hairs of the recurved corolla tips by its copious pollenkitt - occurs in the Australian Acrotriche, which is probably pollinated by the marsupial mouse, Antechinus stuartii (McConchie et al. 1986). Keighery (1996) outlined pollination in western Australian Epacridoideae, where bee pollination is common, but there is also pollination by other insects and, in a few species, birds. Wind pollination in Ericaceae has evolved at least twice, in Empetrum and its relatives and in taxa that were included in genera like Philippia (= Erica). Both these groups have expanded stigmas.
Fleshy-fruited taxa, whether the calyx or the walls of the inferior ovary are fleshy, predominate in Vaccinieae. In both the Old and New Worlds some species have seeds with a mucilaginous testa and a chlorophyllous embryo; plants with such seeds are generally epiphytic or epilithic (pers. obs.). Seeds of other Vaccinieae, and of other Ericaceae in general, have a hard testa and white embryos. In the New World, Vaccinieae with fleshy fruits are much eaten by tanagers (see also Myrtaceae), which tend to remove seeds greater than 2 mm long from the fruits before ingesting them (Stiles & Rosselli 1993); the seeds of Vaccinieae are often a bit bigger than this. Seeds in fleshy fruits of the mycoheterotroph Monotropastrum humile in Japan are dispersed by camel crickets (Rhaphidophoridae: Tachycines elegantissima), as are the seeds of unrelated mycoheterotrophs (Suestsugu 2017).
Plant-Animal Interactions. Mirid bugs are associated with a sticky-leaved (glandular hairs) species of Rhododendron from Japan; the benefits to the insect from eating the carcasses of other insects that had become stuck to the leaves were examined (Sugiura & Yamazaki; for such mirids, see Wheeler & Krimmel 2015).
Bacterial/Fungal Associations. For Ericaceae-mycorrhizal associations in general, see also Cullings (1996) and Smith and Read (1997) and the discussion above. Note that Rayner (1915: p. 128), who worked on the association of Ericaceae with fungi, had early observed that many of the family had "solved the problem of growth upon the poorest and most unpromising soils, but have solved it at a price of their independence".
Arbutoideae, Pyroloideae and Monotropoideae, all in the same immediate clade above, are commonly associated with the largely ECM basidiomycete Agaricomycete-Sebacinales-Sebacinaceae (Selosse et al. 2007; Toju et al. 2016; Weiß et al. 2016; see also Brundrett 2017a; Tedersoo 2017b; Tedersoo & Brundrett 2017 for literature, ages, etc.). Although there are hyphal coils in the root cortical cells, the sheath and Hartig net make the association quite ECM-like (Hynson et al. 2013). ECM Agaricales were found associated with Arctostaphylos alpina (Toju et al. 2016), while suilloid basidiomycetes such as Rhizopogon may be associated with Arbutoideae and Monotropoideae - and as ECM on co-occuring Pinaceae (Bruns et al. 2002 and literature). Fungi associated with individual species of the echlorophyllous mycoheterotrophic Monotropoideae are mostly ECM basidiomycetes (Bidartondo & Bruns 2001, 2002; Bidartondo 2005: questions as to the identity of the plants compromise earlier literature; Hynson & Bruns 2010). Several species of the basidiomycete Russula can be associated with Monotropa uniflora in a single area (S. Yang & Pfister 2006), although considerable fungus-monotropoid specificity, the specificity being more on the side of the monotropoid, was reported by Bruns et al. (2002). Indeed, the specificity of the fungal associations here increases during juvenile ontogeny - and this may also happen in some partly mycoheterotrophic species of Pyrola (Johansson et al. 2017). Hashimoto et al. (2012) found that in Pyrola asarifolia from Hokkaido, Japan, non-ECM Sebacinales-Serendipitaceae were associated with the seedling, while the fungi of the adult plant were ECM fungi that were also associated with Betulaceae growing in the same area, a switch also found in Orchidaceae.
A number of ERM "types" have been described for the family, but their discreteness needs to be be confirmed. Fungal sheaths have been reported from a number of Vaccinieae (e.g. Setaro et al. 2006; Vohník et al. 2012; Yagame et al. 2016). These include the so-called "cavendishioid" (see above) and "sheathed ericoid" mycorrhizal types, and as the sampling of tropical montane and southern hemisphere Ericaceae improves, we may expect to find yet more variation in Ericaceae-fungal relationships there. Ascomycetous dark septate endophytes (the dark colour = melanin) are found in the roots of alpine Ericaceae from the Rocky Mountains (Stoyke & Currah 1991), and there are intermediates between ERM (and ECM) and dark septate endophytes in Rhododendron (Vohník & Albrechtova 2011; Lukesová et al. 2015). Fungi in both ericoid and cavendishioid mycorrhizae are Sebacinales-Serendipitaceae, often saprophytic or endophytic (Setaro et al. 2006; Selosse et al. 2007; Weiß et al. 2016: the two families of Sebacinales are sister taxa, but the particular groups of fungi under discussion are not very close; Weiß et al. 2016: Fig 3), indeed, the route to mycorrhizal associations here may be via an endophytic stage (Strullu-Derrien at al. 2018). Many Leotiomycetes (ascomycetes) are ERM fungi and they increase in diversity towards the poles where Ericaceae-dominated heath vegetation is conspicuous (Tedersoo et al. 2014b; Wardle & Lindahl 2014).
Note that some ERM fungi may also be ECM on different hosts, and the distinction between the two mycorrhizal types, although at first sight quite substantial, is within the capacity of a single fungal isolate to express (e.g. Grelet et al. 2009: ECM Pinus silvestris/ERM Vaccinium vitis idaea; Imhoff 2009; Martino et al. 2018; see elsewhere). Similarly, ERM fungi in Epacridoideae may be dark septate endophytes when growing on other plants (Chambers et al. 2008). Toju et al. (2016) described the numerous fungi associated with Ericaceae growing in extreme Alpine environment in Japan. The ascomycete Helotiales dominated, although Sebacinales-Serendipitaceae were also common, and they are also associated with members of Ericoideae, Epacridoideae and Vaccinioideae (see also Setaro et al. 2006, 2008; Selosse & Weiß 2009; Selosse et al. 2009; Weiß et al. 2009, esp. 2011; Toju et al. 2016); the fungi associated with Cassiopoideae are unknown. Bougoure et al. (2007) detail the variety of ERM fungi associated with Vaccinium and Calluna. Basidiomycete associates may be proportionally particularly common in Vaccinioideae, including the tropical members (Bougoure et al. 2007; Setaro et al. 2006, 2008; Yagame et al. 2016). Interestingly, the basidiomycete isolated from the sheathed ERM roots of Vaccinium myrtillus was quite distinct from other fungi associated with Ericaceae (Vohník et al. 2012). For the mycorrhizae of Epacridoideae in particular, see Cairney and Ashford (2002) and Chambers et al. (2008) and references; the latter emphasize that dark septate endophytes on a variety of plants in southeast Australian sclerophyll vegetation may also be ERM fungi on epacrids.
Within a particular locality, fungi particularly common on individual species of Ericaceae may differ, that is, there is some host specificity, and species shared fewer fungal associates than might be expected by chance (Toju et al. 2016: "anti-nestedness"). There was geographical variation in the mycorrhizal associates of Moneses uniflora, although they were in the same family, the basidiomycete Atheliaceae (Hynson et al. 2015; see also Massicotte et al. 2008 for Pyroleae). Furthermore, plant-fungal relationships in Argentinian species of Gaultheria differ from those in the northern hemisphere Gaultheria (Bruzone et al. 2013). However, Setaro and Kron (2011) found some clades of Sebacinales-Serendipitaceae on both North and South American Vaccinieae, while Andean Orchidaceae and Vaccinieae growing together were associated with different but closely related clades of Serendipitaceae (Setaro et al. 2013). The specificity of Arctic ERM fungi, at least, is low (Walker et al. 2011; Timling & Taylor 2012), different ericaceous genera in the one place being linked by an ERM network - even if plots only 2-3 m apart had rather different fungi (Kjøller et al. 2010). Similarly, species of tropical American Serendipitaceae can form associations with more than one species of Ericaceae (Kottke et al. 2008; see also Weiß et al. 2011).
Rinaldi et al. (2008) suggested that the diversity of fungi associated with Ericaceae might not be very high, but their figure of 15 species is a gross underestimate, more species than this being found with Arbutus menziesii in a single site in Oregon (Kennedy et al. 2012), while 224 OTUs were detected from three species of Ericaceae from Alaska, of which there were 14 distinct clades in the ascomycetan Helotiales alone (Walker et al. 2011; Timling & Taylor 2012). At least 150 species of fungi is the estimate in van der Heijden et al. (2014), but clearly this is still far too low. Recent studies that focus on Sebacinales (e.g. Weiß et al. 2011, see also 2016) suggest that quite a number of species in that group also grow with Ericaceae. However, overall rather little is known about the fungi associated with Ericaceae and their distributions, a situation not helped by uncertainty over fungal species limits (Kohout 2017: see e.g. Oidiodendron).
As with other mycorrhizal associations, the relationships between the partners and the pathways of nutrient flow can be complex, and mycorrhizal networks involve other than the echlorophyllous Pyroloideae and Monotropoideae. For example, a member of Sebacinales-Sebacinaceae found in Diphasiastrum alpinum (Lycopodiaceae) and also on Calluna vulgaris growing in the same habitat may allow the movement of nutrients from the latter to the former (Horn et al. 2013). In western North America the arbutoid madrone, Arbutus menziesii, is a common subordinate tree in forests with ECM Fagaceae and Pinales that occupies over 3.9 x 106 acres in California alone (Waddell & Barrett 2005). Its diverse fungal associates are also found on other angiosperms and in particular Pinaceae (Pseudotsuga and Pinus) in Oregon (Kennedy et al. 2012). Arbutus menziesii resprouts after fire and it can be a source of fungal inoculum for newly-germinated seedlings of associated Pinaceae, so facilitating their regeneration (Kennedy et al. 2012 and references), although many temperate, but not Arctic, ECM associations develop from propagules in the soil (Hewitt et al. 2017). As Kühdorf et al. (2015: p. 110) noted, the arbutoid "C[omarostaphylis] arbutoides is a refuge plant for ECM fungi as it shares these fungi with tropical ECM trees such as Quercus costaricensis". The ascomycete Rhizoscyphus ericae (c.f. also Meliniomyces) is a very common associate of the hair roots of ERM North Temperate Ericaceae; this fungus can also be an ECM associate of Pinus and Abies growing with Ericaceae (Read 1996; Grelet et al. 2009, 2010; see also Villarreal-Ruiz et al. 2004; Martino et al. 2018), and it also forms mycorrhizal associations with Jungermanniales-Schistochilaceae and other leafy liverworts, often colonizing their rhizoids (Duckett & Read 1995; Upson et al. 2007; Pressel et al. 2008); other ascomycetes are also involved, including Cenococcum and Geomyces. (See Lofgren et al. 2018 for cautionary comments about host specificity.) Furthermore, some ERM fungi form endophytic associations (ERM-Epacridoideae/other families-dark septate endophytes: Chambers et al. 2008; ERM-Vaccinium myrtillus/ECMPicea abies: Vohnik et al. 2013), and some endophytic fungi are physiologically quite similar to ERM fungi (Martino et al. 2018). For additional information, see papers in Martin (2017).
Ericaceae like Vaccinium may also have ascomycetous dark septate endophytes which form microsclerotia in the roots, but some of these fungi, like Phialocephala glacialis, formed structures approaching ERM, while Acephala species produced both similar intermediate structures and full-blown ERM (Lukesová et al. 2015). Ngugi and Scherm (2006 and references) discuss fungal associates of Vaccinium including Monilinia vaccinii-corymbosi (an ascomycete, Helotiales; other species also involved). Conidia are produced on the leaves and the conidial patches may seem like floral calyxes to the pollinator, which moves spores to flowers where they behave just like pollen grains but parasitize the fruits (mummy berries); they can cause serious losses of the berries.
Endophytes are common (Petrini 1988; Sieber & Grünig 2013: general summary), Koudelková et al. (2017) for the ability of endophytes to tolerate the essential oils of Rhododendron tomentosum.
Host preferences of the basidiomycete rust fungi Chrysomyxa and Exobasidium link the old Empetraceae with Ericaceae, perhaps Ledum with Rhododendron, etc.; Exobasidium is also found on Theaceae and Symplocaceae (Savile 1979b; see Jackson 2004 for possible codivergence). Fruits of Ericaceae are a food source for Monilinia (polyphyletic - ascomycete-Sclerotiniaceae), also found on Rosaceae (Holst-Jensen et al. 1997).
Vegetative Variation. Variation in leaf morphology in Ericaceae is extensive. For instance, linear leaves are found in Diplycosia (+ Gaultheria), Rhododendron, Empetrum and relatives, Killipiella (= Sphyrospermum), Agarista, etc.. "Ericoid leaves" - typically scleromorphic, narrow (less than ca 5 mm wide), more or less linear, and often with recurved margins - are quite common, as in Erica itself. Within the small genus Cassiope leaf morphologies vary from flat and more or less linear, or with strongly recurved margins, or like the finger of a glove (hypoascidiate), or peltate (Stevens 1970), but the different morphologies do not map simply on to the recent phylogeny of the genus, where divergence is dated to ca 17 Ma (Hou et al. 2015). Leaves of Epacridoideae do not have recurved margins, but are otherwise scleromorphic and often more or less ericoid.
Genes & Genomes. Fajardo et al. (2013) found a number of inversions in the long single copy area of the chloroplast genome of Vaccinium macrocarpon; more sampling in the Ericaceae-Ericales area in particular is needed to evaluate the significance of this. There were also extensive changes in the chloroplast genome of Arbutus unedo, including gene losses, tandem repeats, etc.. Some of the changes there were the same as in Vaccinium macrocarpon, thus even in these autotrophic Ericaceae the small single copy region, at a little over 3,000 bp, is very short (Martínez-Alberola et al. 2013). For the loss of chloroplast genes in mycoheterotrophic Ericaceae, see Braukmann and Stefanovic (2012) and Braukmann et al. (2017). The genome in such plants is very small and the inverted repeat is lost in six genera, including Pterospora, or it is very small, as in Monotropa, although it may have been secondarily regained there (Braukmann et al. 2017). Collinearity/synteny of the chloroplast genome of perhaps all Ericaceae when compared to that of other Ericales, etc., is low (Martínez-Alberola et al. 2013; Braukmann et al. 2017).
Chemistry, Morphology, etc. For a survey of flavonoids and simple phenols, see Harborne and Williams (1973); note that ellagic acid has been found in the pollen of some European Ericoideae (Ferreres et al. 1996) even though the family is generally considered to lack the tannin. For the distribution of grayanotoxin, a polyhydroxylated diterpene, see C. Zhou et al. (2012) and S. A. Jansen et al. (2012) and references. For hydroxycinnamates, diverse and showing some correlation with taxonomy in Rhododendron, see A. Shrestha et al. (2017).
Rays in some styphelioids may be very low and narrow (Carlquist 2015b). The best developed pit membrane remnants in Ericaceae occur in Enkianthus. They are more poorly developed in other genera, but are well developed in other families in this part of Ericales (Carlquist & Schneider 2005) - a plesiomorphy? Sylleptic branching is at best uncommon (Keller 1994). The leaf midrib of Cassiopoideae may not have associated ("pericyclic") fibres (Kron et al. 2002b), but details of the distribution of this feature are not clear. A group of genera around Lyonia can be characterized by having a lignified epidermis, bands of fibres in the secondary phloem (i.e. stratified phloem), anomocytic stomata, etc.. Variation in indumentum in the family is considerable (e.g. Hubrecht & Bourguignon 2016: scales in Rhododendron, U.V. fluorescence).
It can be difficult to interpret the floral morphology of Monotropoideae, as with other myco-heterotrophic and parasitic groups, especially of Monotropeae. For instance, members of the outer perianth whorl of the flowers of Monotropoideae such as Monotropa itself have small buds in their axils and are interpreted as being modified bracts by Freudenstein and Brow (2015). Seeds and embryos are usually very small, and Monotropa uniflora itself has a two-celled embryo (Olson 1991), and much smaller than this you cannot get (except in Anemone); see also Francke (1935) for Monotropa hypopitys.
Monosymmetric flowers in Rhodoreae have inverted symmetry, the median sepal being abaxial. Any speckling of the corolla occurs on the adaxial petal - as in Lupinus, also with inverted flowers. Obdiplostemony is reported from some Ericaceae (Ronse De Craene & Bull-Hereñu 2016). Anther pores form in two ways. In one, resorbtion tissue, crystals of uncertain nature develop in the cells and the walls break down; this process is similar to what goes on in the granular pouches on the backs of the anthers of some species. In the other, collapse tissue, the cells vacuolate, flatten, and break down, but no crystals form (Hermann & Palser 2017). For the development of the distinctive pollen of many Epacridoideae in which only a single cell of the tetrad persists, see Furness (2009) and Lemson (2011). A common surface morphology of pollen grains in Ericaceae is faintly cerebellar, although there are some notable exceptions, as in Vaccinium japonicum - indeed, pollen is somewhat more variable than one perhaps might have thought (Sarwar et al. 2006: Vaccinium, 2008: Arbutoideae; Sarwar & Takahashi 2006a: Vaccinioideae excl. Vaccinieae, 2006b: Enkianthus, 2007: Vaccinieae, 2009: Cassiopoideae and Harrimanelloideae, 2014; Erica; Lu et al. 2009: Gaultheria and relatives). Carpels are opposite the calyx in Vaccinium, Dracophyllum and Monotropa (Schnizlein 1843-1870: fams 160, 161). For variation in integument thickness in Ericaceae, see Samuelsson (1913). For more on the distinctive embryology of the family, also floral anatomy, see Stushnoff and Palser (1969 and references).
For oligosaccharide storage, Fouquieriaceae, Diapensiaceae, and Cyrillaceae (and Lennoaceae) also sampled, see Pollard and Amuti (1981); for protein crystals in the nucleus, see Speta (1977, 1979); for epidermal variation in Gaultherieae, see Y.-H. Wang et al. (2015), and for wood anatomy of Epacridoideae, see Lens et al. (2003) and for that of superior-ovaried Vaccinoideae, see Lens et al. (2004a); for pseudotori, see Rabaey et al. (2006); for vegetative features of Epacridoideae, see Jordan et al. (2010); for venation patterns in some neotropical Vaccinieae, see Pedraza-Peñalosa et al. (2013); for a phenetic analysis of some staminal characters, see Vander Kloet and Avery (2007); for floral morphology of Empetrum, see Vislobokov et al. (2012), for nectaries, see Erbar (2014), for seed anatomy, see Peltrisot (1904), for external seed morphology of Gaultherieae, see Lu et al. (2010a) and that of Erica - quite variable - see Szkudlarz (2010), and for seeds and seedlings of Rhododendron, seed Hedegaard (1980). For general information on the family, see Kron et al. (2002b) and Stevens et al. (2004a), for Oligarrheneae, see Albrecht et al. (2010), for Rhododendron, see Milne (2017), and for New World taxa, see Luteyn (2000, 2002).
Phylogeny. Early studies are summarized by Kron et al. (2002b). The structure of the tree immediately above Enkianthoideae was initially labile with Pyroloideae, Monotropoideae and Arbutoideae variously arranged and often forming a basal grade, although support values were low (e.g. Cullings 1994). Freudenstein et al. (2010) in a comprehensive phylogenetic study of the family suggested relationships [Enkianthoideae [[Pyroloideae [Arbutoideae + Monotropoideae]] [The Rest]]] (also Z.-Y. Liu et al. 2011, 2014; Hardy & Cook 2012; Braukmann & Stefanovic 2012: PHYA, see below; esp. Freudenstein et al. 2016a; Lallemand et al. 2016; Lam et al. 2018: some caveats); these relationships are followed here. However, in early versions of this site (pre-August 2010), Monotropoideae (including Pyroloideae) and Arbutoideae were successively sister to the remainder of the family (other than Enkianthus), while Brundrett (1994) found a very different set of relationships, mycoheterotrophy apparently having evolved several times, Feldenkreis et al. (2011) suggested the relationships [Enkianthoideae [Pyroloideae [[Monotropoideae + Arbutoideae] [The Rest]]]], Schwery et al. (2014) found Arbutoideae to be embedded in a paraphyletic Monotropoideae, while in Rose et al. (2018) [Enkianthoideae [[Monotropoideae + Arbutoideae] [Pyroloideae [The Rest]]]] were the relationships, although the position of Pyroloideae had little support. In Braukmann and Stefanovic (2012) Pterospora, on a very long branch, was sister to all other Ericaceae except Enkianthus, and subfamilial relationships in Z.-D. Chen et al. (2016) are also rather different than those above.
Cullings examined relationships within Monotropoideae, and although the subfamily as a whole had poor support, a clade [Sarcodes [Hypopitys + Pterospermum were sister to the rest, the two clades being well supported. Genera are becoming ever more finely split (see e.g. Q.-R. Zhao et al. 2018).
For the phylogeny of Pyrola and its relatives (Pyroloideae), see Freudenstein (1999) and Z.-W. Liu et al. (2011, 2014). The position of Orthilia was not stable, and there was a suggestion that allopolyploidy might be involved in its origin (Z.-W. Liu et al. 2011). Matsuda et al. (2012) found the well supported relationships of [[Orthilia + Pyrola] [Moneses + Chimaphila]], while relationships in Z.-W. Liu et al. (2014) are [Orthilia [Pyrola [Moneses + Chimaphila]]]; the former set of relationships is preferred hetre (see also Lallemand et al. 2016).
Arbutus sometimes appears to be paraphyletic with respect to the other genera of Arbutoideae (Hileman et al. 2001; see also Kron et al. 2002b), but broader sampling with the ITS gene yields a topology compatible with conventional delimitations of genera, in particular, Arctuos is not sister to Arctostaphylos (Greg Wahlert, pers. comm.). For relationships within Arctostaphylos s. str., see Wahlert et al. (2009); the genus may be monophyletic, but no taxa outside the subfamily were included.
Gillespie and Kron (2010: four chloroplast, 2 nuclear markers) studied relationships across Ericoideae and found i.a. that the distinctive Himalayan Diplarche, previously of uncertain relationships, was sister to Empetreae (see also Z.-D. Chen et al. 2016), in which they thought it should be included, and the Guyanan Ledothamnus was sister to the northeast Asian Bryanthus. However, separate analyses of the two nuclear markers placed Diplarche as sister to Corema alone, and even in the combined analysis relationships along the spine of Ericoideae were poorly supported, while an earlier two chloroplast marker study had linked Diplarche with Rhododendron, etc. (Kron et al. 2002b). Something does not seem quite right. For the phylogeny of Ericoideae-Ericeae and the circumscription of Erica, see e.g. Oliver (1994), McGuire and Kron (2005) and Pirie et al. (2011); the African species of Erica are probably monophyletic. The circumscription of Rhododendron and relationships within it have been the subjects of much recent work (Kurashige et al. 2001; Gao et al. 2002; Kron 2003: limits of genus, sections; G. K. Brown 2003; Milne 2004: subsection Pontica paraphyletic, includes subgenus Hymenanthes; Brown et al. 2006a, b, c: section Vireya = sect. Schistanthe, biogeography; de Riek et al. 2008: Therorhodion sister to Rhododendron; Craven et al. 2008, 2011; especially Goetsch et al. 2005, 2011) - genera like Azalea, Ledum and Menziesia are well embedded in Rhododendron.
For the phylogeny of Epacridoideae, see Powell et al. (1996), Crayn and Quinn (2000) and Johnson et al. (2012). Within Epacridoideae, Prionoteae and Archerieae are successively sister to remaining Epacridoideae, and this is consistent with morphology (see above). Wagstaff et al. (2010) looked at relationships within the distinctive Richeeae; however, relationships between this tribe and Cosmelieae remain uncertain (Johnson et al. 2012). Relationships in Styphelieae are being disentangled (e.g. Powell et al. 1997: morphology), Cherry et al. 2001; Quinn et al. 2003, 2005; Puente-Lelièvre et al. 2012). In a five-gene (two compartments)-207 taxon study focusing on Styphelia, it and Leucopogon popped up all over the place - with obvious taxonomic implications (Puente-Lelièvre et al. 2015). Epacris has turned out to be paraphyletic (Quinn et al. 2015).
Within Vaccinioideae, Z.-D. Chen et al. (2016) found the relationships [[Lyonia, Pieris, etc.] [[Gaultheria, Leucothoe, Andromeda] [inferior ovaried taxa]]] among the Chineae taxa (see also Rose et al. 2018). Within Gaultheria s.l. the epiphytic Diplycosia with some 100 species and Tepuia (Powell & Kron 2001; Bush et al. 2006; Bush & Kron 2008; Fritsch et al. 2011) may form a clade along with a few species of Gaultheria, while the majority of Gaultheria forms a sister clade (Bush et al. 2009: see also optimisation of fruit and inflorescence characters); the position of G. procumbens is unclear (Fritsch et al. 2011). Y.-H. Wang et al. (2015) carried out a morphological analysis of numerous leaf epidermal characters of Gaultherieae and compared the groupings obtained with those from other studies; there may be a number of cryptic species in the high-altitude representatives of the genus (Lu et al 2010a). Outlines of relationships in the tropical inferior-ovaried Vaccinieae are slowly developing (Kron et al. 2002a) and for the most part they cut across the limits of the larger genera; these are based on floral characters, often variants of a bird pollination syndrome. However, a Vaccinium-type flower (i.e., small, ± urceolate) appears plesiomorphic in the whole clade and Vaccinium itself is very paraphyletic (see also Powell & Kron 2002, 2003; Pedraza-Peñalosa 2009). In particular, the "Tethyan" Vaccinium section Hemimyrtillus, from the Mediterranean area, etc., may be sister to other Vaccinieae, although there is currently only weakish support for this position (Powell & Kron 2002), while in Southeast Asia the Agapetes clade, with 90 or more species centred in the SW China-the Himalayan region, will probably need to be extended to include some 250+ species of Vaccinium, all having superficial phellogen and a falsely 10-locular ovary, both probably derived features, and forming a single clade (Powell & Kron 2002; Tsutumi 2011; Z.-D. Chen et al. 2016; Ghandforoush & Kron 2016). New Guinean Dimorphanthera is sister to Paphia, both primarily New Guinean; the latter used to be included in Agapetes, but the two are not immediately related. Pedraza-Peñalosa (2010) explored the limits of Disterigma and Pedraza-Peñalosa et al. (2015) those of Colombian Vaccinieae in general. In the latter, extensive polyphyly in the larger genera was found. The bottom line? A world-wide study of inferior-ovaried Vaccinieae is badly needed.
For additional information on relationships, see Anderberg (1993), Cullings (2000), Judd and Kron (1993), Kron and Chase (1993), Kron et al. (1999a, b), and Crayn et al. (1998).
Classification. The infrafamilial classification outlined by Kron et al. (2002b) is largely followed here; Gillespie and Kron (2010) modified tribal limits in Ericoideae, but see above.
Argent (2006) provided an account of species of Rhododendron subgenus Vireya (= section Schistanthe); Craven et al. (2008, esp. 2011) listed the subsections that it includes. Azalea, Ledum, Menziesia, Tsusiophyllum, and perhaps even Diplarche (Craven 2011) are all to be included, indeed, Menziesia hybridizes with related species of Rhododendron (de Riek et al. 2008). Erica has been expanded to include the wind-pollinated Philippia and several small segregate genera (Oliver 2000). Generic limits in Styphelieae and some other Epacridoideae are difficult, but Quinn et al. (2005) and Albrecht et al. (2010) suggest some realignments - see e.g. Puente-Lelièvre et al. (2015) for a useful discussion about the merits and demerits of having broad or narrow generic limits. As Puente-Lelièvre et al. (2015) note, the limits of Leucopogon will have to be restricted, or those of Styphelia expanded to include much of the tribe, and they have taken the latter option, so whereas most of the diversity in Styphelieae used to be in Leucopogon, it is now in Styphelia... (see also Taaffe et al. 2001; Johnson et al. 2012; Hislop & Puente-Lelièvre 2017).
There are yet other substantial changes to generic limits in Vaccinioideae. Gaultheria is to include Pernettya, Diplycosia as well as Tepuia, and intrageneric relationships are being disentangled (Powell & Kron 2001, 2002; Bush et al. 2006; Bush & Kron 2008; Bush et al. 2009). Generic limits in the epiphytic Vaccinieae in particular are in a mess (Powell & Kron 2003; Pedraza-Peñalosa 2009, Pedraza-Peñalosa et al. 2015). In Southeast Asia the Agapetes clade is made up of some 250+ species of Vaccinium and 90 or more species of Agapetes s. str.. Dimorphanthera is sister to Paphia, however, if the Paphia clade really does include taxa of the old Vaccinium sect. Pachyantha, merging with Dimorphanthera might be best... (c.f. Stevens 2004). Vaccinium itself is pretty wildly paraphyletic. Indeed, given the relationships of "Vaccinium" to the rest of the Vaccinieae, nomenclatural changes in the tribe as a whole must await a comprehensive phylogenetic analysis. Vander Kloet and Dickinson (2009) provide a sectional classification for Vaccinium - they recognize thirty sections.
Previous Relationships. Ericaceae here are basically the Ericales of Cronquist and Takhtajan. However, even then there were suggestions that relationships might be more entwined, thus characters like rust preferences (Savile 1979b) had linked the wind-pollinated and florally very distinctive Empetraceae with Ericaceae-Ericoideae in particular, furthermore, both Rhodoreae and Empetreae have the flavonoid gossypetin.
Botanical Trivia. Mad honey disease is the result of eating honey containing the neurotoxin grayanotoxin - such honey incapacitated some of Xenophon's troops in Asia Minor, although the effects of this poison are only transitory (S. A. Jansen et al. 2012).