EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall with distinctive side chains; 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 its length [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band of microtubules [where cell plate will join parental cell wall], phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes, precursor for starch synthesis in plastid.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: xyloglucans in the primary cell wall with fucosylated subunits; gametophyte leafless; archegonia embedded/sunken [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte dominant, branched, branching apical, dichotomous, potentially indeterminate; vascular tissue +; stomata on stem; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response; (condensed or nonhydrolyzable tannins/proanthocyanidins +); plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xylans in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open; stele di- to pentarch [oligarch], pith relatively inconspicuous, lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry, extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, 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.
Evolution. Possible apomorphies for flowering plants are in bold. The actual level at which many characters, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, g-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial [extragynoecial compitum 0]; carpels plicate [?here]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / 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 m.y.a. (K. Bremer et al. 2004). Janssens et al. (2009) gave a date of 123±10.5 m.y.a., Lemaire et al. (2011b) one of (132-)128(-124) m.y., Moore et al. (2010: 95% highest posterior density) suggest substantially younger ages of (85-)81(-76) m.y., Bell et al. (2010) ages of (116-)108, 99(-93) m.y., Tank et al. (2015: Table S1) an age of ca 98.8 m.y., Magallón and Castillo (2009) and Magallón et al. (2013) an age of around 105.3 m.y., Magallón et al. (2015) an age of 112.3 m.y.; 132.6-122.1 m.y. is the age in Nylinder et al. (2012: suppl.), ca 137 m.y. in Z. Wu et al. (2014) and (126-)123(-113) m.y. 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 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 so do some Cornales (see Erbar & Leins 2011 for a recent survey). Although sampling 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 still 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]; 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, 11,545 species.
Age. Sytsma et al. (2006) proposed that diversification of Ericales began 109-103 m.y.a., Wikström et al. (2001: note topology) offered an age of (97-)92, 85(-80) m.y.a., Anderson et al. (2005) an age of 103-99 m.y., while Janssens et al. (2009) dated the crown group to 117±9.2 m.y. and K. Bremer et al. (2004) to 114 m.y.. Soltis et al. (2008: a variety of estimates) suggested an age of (126-)113(-85) m.y., Magallón and Castillo (2009) one of ca 98.85 m.y., Bell et al. (2010) an age of (102-)92 m.y., and Lemaire et al. (2011b) an age of (125-)118(-110) m.y.; around 103.6 m.y.a. is the age in Magallón et al. (2015) and (117-)109(-100) m.y. 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 m.y.o. (Li 2005), although this identification needs to be confirmed... Otherwise the oldest fossils assignable to Ericales are in rocks ca 90 m.y. old (Crepet et al. 2004; see also Martinez-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 fossils are quite unlike extant members of the clade, e.g. some have sepals with numerous huge abaxial and/or marginal glands (Crepet 2008). 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.
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Almost all families in Ericales had diverged by the early Eocene 50 m.y.a. (Sytsma et al. 2006; see also Magallón et al. 2015; Wikström et al. 2015).
Currently Ericales contain ca 5.9% of eudicot diversity (Magallón et al. 1999), of which one third is made up of Ericaceae alone, not a noteworthy component of tropical rainforests (see below).
Schönenberger et al. (2005) examined character evolution in Ericales, which now perhaps makes a little more sense, although there is still extensive homoplasy. For a good summary of the diverse Late Cretaceous fossils assigned to the order, see Friis et al. (2011).
Ecology. Ericales are an important component of the diversity of 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), whenever the clades now making it up initially diverged; members of Malpighiales are the other main component of this vegetation. Lens et al. (2007b: see also optimisation of characters of wood anatomy on to 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 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).
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). True parietal placentation does occurr (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 Jansen et al. (2004a, c), and for wood anatomy, see Lens (2005) and Lens et al. (2007b).
Phylogeny. Relationships within the order were for some time poorly understood, see R. J. Bayer et al. (1996) and Morton et al. (1997a - both largely molecular data) and Anderberg (1992: morphological data). However, Polemoniaceae + Fouquieraceae, Myrsinaceae and relatives, Ericaceae and relatives, and Balsaminaceae and relatives form 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). 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 shows rather weak [73% bootstrap] support for Lecythidaceae sister to most other Ericales - 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.
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, they also thought that Balsaminaceae and Marcgraviaceae might be sister taxa. 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 peregrinations of taxa that used to be included in or near Theaceae are interesting. There were suggestions that Pentaphylacaceae, placed close to Theaceae in both earlier systems, 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 be asociated with Theaceae s. str. in matK analyses, and although 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) - again, another member of Ericales - and found the two to be similar. On the other hand, Pentaphylacaceae were associated with Gonocaryum (Aquifoliales-Cardiopteridaceae) in Savolainen et al. (2000a); the latter are strongly associated with Aquifoliales in other studies (D. Soltis et al. 2000; Kårehed 2001; Lens et al. 2008b). However, Pentaphylax was placed sister to Ternstroemiaceae s. str. (Anderberg et al. 2001), and this is its resting place for now. Pelliciera was compared with Marcgraviaceae by Beauvisage (1920); details of wood anatomy suggest relationships with Tetrameristaceae (Baretta-Kuipers 1976; see also above); both Pellicieraceae and Tetrameristaceae were in the Theales of Cronquist (1981). Indeed, 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.
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 appeared in most analyses in Nickrent et al. (2004), and Hardy and Cook (2012) found that was 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, while its parietal placentation and inferior ovary are features found in many other parasitic angiosperms so they are not taxonomically particularly informative characters. Placing Mitrastemonaceae next to Ericaceae and their immediate relatives in the tree is partly for convenience.
Previous Relationships. Theales of Cronquist (1981) included mostly families now in Malvales, Ericales, and Malpighiales, Theaceae alone including genera here placed in Bonnetioideae (Malpighiales-Bonnetiaceae) and Asteropeioideae (Caryophyllales-Asteropeiaceae). Takhtajan's Theanae were largely equivalent (Takhtajan 1997). Both included Ternstroemia and relatives as a subfamily of Theaceae. 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's system. 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 65 m.y. by K. Bremer et al. (2004), to (66-)52, 49(-34) m.y. by Bell et al. (2010), ca 55.4 m.y. by Magallón et al. (2015) and ca 43.6 or 45.2 m.y. by Tank et al. (2015: Table S1, S2). With different topologies, the common ancestor of this clade was estimated at (52-)48, 44(-40) m.y. (Wikström et al. 2001: Balsaminaceae sister to the rest) or (85-)59(-38) m.y. (Wikström et al. 2015) and that of the [Balsaminaceae + Marcgraviaceae] clade was dated to the middle Palaeocene ca 58.9 m.y.a. (Janssens et al. 2009).
Evolution. Divergence & Distribution. Geuten et al. (2006) suggest that heterotopic SEP3-like gene expression in bracteoles and calyx in extant 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).
Phylogeny. Monophyly of this 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. Bremer et al. (2004) 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, 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.
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); bracts abaxially ascidiate, nectariferous; K quincuncial; A 4-40; G [2-8], opposite ?, placentation very intrusive parietal, stigma?, dry; ovules many/carpelfruit dehisces more or less irregularly, 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. New World tropics (map: from Heywood 1978). [Photo - Flowers, Fruits.]
1. Marcgravioideae Choisy
Phyllotaxis 2-ranked, leaves strongly heterophyllous; inflorescence umbellate; apical sterile flowers = nectaries; flowers 4-merous; C connate, forming a calyptra, thrown off at anthesis; 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; phyllotaxis spiral; inflorerscence also spike or umbel; nectaries associated with each flower; flowers 5-merous; C basally connate, reflexed; (style +); (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 prominent 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 taxa like Margravia are monosymmetric from the point of view of their avian pollinators, which get pollen dusted on their heads as they take nectar from the modified bracts which are held beneath the ring formed by the flower (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 easily (Simon et al. 2011).
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 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. (2004) dated this node to around 56 m.y., while around 50.5 m.y.a. was the age in Magallón et al. (2015), (77-)51(-30) m.y. in Wikström et al. (2015) and ca 42.7 m.y. in Tank et al. (2015: Table S2).
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, inverting during growth [resupinate]; functionally abaxial sepal with prominent nectariferous spur, K 3, C 5; anthers postgenitally ± connate and forming cap over stigma, (with trabeculae in loculi), filaments stout; tapetal cells 2(-4)-nucleate; cellulose threads from cell walls intermixed with pollen grains and holding them to anther, with raphides, starchy, pollen often rectangular in polar view, endexine lamellate; G [(4)], opposite petals, stigma fairly broad, wet; ovules (hemitropous), apotropous, outer integument 2-10 cells across, inner integument 2-6 cells across, parietal tissue 0-1 cells across, 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.
2[list]/1001: Impatiens (1000). 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) m.y.a. (Janssens et al. 2009).
1. Hydrocera Blume
K 5, C 5; G loculi divided longitudinally into three parts; fruit a drupe, stones 5, separating, each with two longitudinal air sacs; testa sclerotic, 6-8 layers thickened cells, ca 5 layers unthickened; n =
1/1: Hydrocera triflora. South India, Sri Lanka, Hainan to Peninsula Malaysia, Java, the Celebes.
Synonymy: Hydroceraceae Wilbred
2. Impatiens L.
(Plant woody); (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), (unitegmic, integument ? 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-)7-8(-10+).
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) m.y.a., but the speciation rate much increased in the early Pliocene within the last 5 m.y., climate change causing much population fragmentation, isolation, and migration (Janssens et al. 2009). Diversification began in the S.E. Asian/China region.
The combination of non-hydrolysable tannins and raphides, both of which are found in Balsaminaceae, is rarely found in herbs (Fischer 2004), but the family is likely to be primitively herbaceous. Increase in in width of the stem is by expansion of cells in the pith (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; duplication and probable subfunctionalisation of the class B DEF gene has occurred in this clade (Janssens et al. 2006b; Geuten et al. 2006).
Pollination Biology. 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.
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. 2006; 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 recent study by McAbee et al. (2007) shows that there is considerable plasticity in integument development in the family, although many species show 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), but Grey-Wilson (1980a) described it as a drupe with separate stones; see Leins (2000) for the fruit dehiscence of Impatiens. The micropylar endosperm haustorium is massive and may invade the funicle and even the placenta.
For general information, see Sandt (1921), Fischer (2004a) and Leins and Erbar (2010), for lamina epidermis, see X.-X. Zhang et al. (2013), for information on floral anatomy, development, etc., see Grey-Wilson (1980b) and Caris et al. (2006a) 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, Guignard (1893), Chandresekhara Naidu (1985) and Boesewinkel and Bouman (1991), for some embryology, see Dahlgren (1934a) and Narayana (1963), and for seed morphology, Utami and Shmizu (2005: variation considerable). For a revision and more of the African taxa, see Grey-Wilson (1980c).
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.) suggest a new classification, but it clearly has its limits (Ruchisansakun et al. 2015).
Previous Relationships. Balsaminaceae were included in Geraniales-Rosidae by Cronquist (1981) and in Geranianae-Rosidae by 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. W. Malesia, Central and N. South America. Two groups below.
Age. K. Bremer et al. (2004) estimated the age of crown-group Tetrameristaceae at 41 m.y.; (31-)28, 25(-22) m.y. was the age suggested by Wikström et al. (2001) and (53-31(-13) m.y. by Wikström et al. (2015). The age of this clade was estimated at (42-)30, 28(-15) m.y. by Bell et al. (2010).
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. Pelliciera Bentham
Vessels in multiples; petiole bundle more or less flat where it joins the stem, becoming annular; stomata ?paracytic; lamina vernation involute, base asymmetric, colleters?; flowers terminal, single, ca 10 cm across ["very large"]; bracteoles petal-like; K with two traces at base; 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 = ?; seed breaking the seed coat while still on the plant, germination phanerocotylar, hypogeal.
1/1: Pelliciera rhizophorae. Central and N. South America (map: from A. Graham 1977); mangroves. [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, but the identities of these fossils are questioned by Martínez-Millán (2010), while Manchester et al. (2015) note that pollen of Alangium (Cornales-Cornaceae) can be confused with that of Pelliciera.
Evolution. Divergence & Distribution. For the evolution of the mangrove habitat, to which Pelliciera is restricted, see Rhizophoraceae. The fossil history of the genus is uncertain; Martínez-Millán (2010) does 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).
Chemistry, Morphology, etc. Although the gynoecium apears to be two-carpellate 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), and Maas and Westra (1993).
Synonymy: Pellicieraceae Bullock
2. [Pentamerista + Tetramerista]
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) m.y. in age (Bell et al. 2010), around 99.7 m.y. (Magallón et al. 2015), or (106-)99(-94) m.y. (Wikström et al. 2015) - note topologies in all.
[Polemoniaceae + Fouquieriaceae]: kaempferol, quercetin +; cork cambium outer cortical; inflorescences terminal, determinate; K with scarious margins; A adnate to the corolla, thecal septum st most short and indistinct [septum 0]; gynoecial nectary +, with stomata; G , style hollow, style/stigma branched; ovules in two ranks, apotropous, micropyle zig-zag [abruptly tuned towards central axis]; fruit a loculicidal capsule, seeds on central columella; seeds winged; exotesta with circular/annular thickening; endosperm scanty; mitochondrial coxII.i3 intron 0.
Age. The age of this node is estimated at (77-)65, 61(-48) m.y. by Bell et al. (2010), ca 79.6 m.y. by Tank et al. (2015: Table S2), around 83 m.y. by Magallón et al. (2015), and (98-)51(-50) m.y. by Wikström et al. 2015).
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 - what is the general distribution of this feature?), anastomosing vascular bundles in sepals and petals, and details of gynoecial development.
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
Sugars accumulated as kestose and isokestose oligosaccharides, 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. 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 at (40-)36, 33(-29) (Wikström et al. 2001) or (47-)36, 31(-20) m.y.o. (Bell et al. 2010).
Gilisenium hueberi, perhaps close to Gilia, is known from the middle Eocene of Utah (Lott et al. 1998), at the upper end of the estimate above.
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; 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. There are several cases where predominantly western North American genera have a few species in the southern part of South America. [Photos - Collection (all except Cobaea).]
2. Cobaeoideae Arnott
Mostly mesic vines to small trees (herbs); (short shoots +): leaves usu. unequal-pinnate (palmate, simple); flowers large, (mostly positionally monosymmetric - Cobaea); (K basally connate only), 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 = [x = 7-9?], n = 15, 26, 27, 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, deciduous, lamina unlobed 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. Schönenberger (2009) lists other features that may be apomorphies for Polemoniaceae.
Pollination Biology & Seed Dispersal. For floral variation in the context of different pollinators, see 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 this genus 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. The pollen tube has callose plugs. In Cobaea the leaves are tendrillar and the basal pair of leaflets is foliaceous-stipuliform.
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 still unclear (Johnson et al. 2008 and references). 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 Phacelia, see Gilbert et al. (2005) and Hansen et al. (2009) and for that 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.]
Evolution. Divergence & Distribution. Schönenberger (2009) lists other features that may be apomorphies for Fouqueriaceae, including sepals and corolla lobes being similar in size and histology - the former, at least, they are not.
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 ovule morphology and embryology, see Mauritzon (1936b), and for seeds, see Corner (1976).
Phylogeny. For relationships within the family, see Schultheis and Baldwin (1999).
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 connate or not, 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]/350 - five groups below. Tropical, especially America and W. Africa.
Age. Crown-group diversification in Lecythidaceae may have begun (65-)84, 46(-30) m.y.a. (Bell et al. 2010) or (71-)65, 61(-55) m.y.a. (Wikström et al. 2001).
1. Napoleonoideae (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 glands or not, C valvate, connate, plicate, margin serrate; A adnate to C, 10, paired, opposite C, extrorse, monothecal, pairs 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, lateral parietal cells +; fruit a 1-several seeded drupe; testal bundle single; embryo curved; n = 16.
1/16. W. tropical Africa (map: from Liben 1971b; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]
Synonymy: Napoleonaceae 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.
2. Scytopetaloideae (Engler) O. Appel
Growth ?sympodial; plants Al-accumulators; nodes?, cortical bundles running two internodes before entering leaves; (cristarque cells +), sclereids +; ?crystal chains, crystals octahedral; leaves amphistomatous); leaves 2-ranked, stipules +, minute; inflorescence axilary, 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); seeds often 1, with unicellular hairs or not, ruminate or not; testa cells often with crystals, testal bundle single or branched; endosperm +, 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, N.E. Brasil (Asteranthos) (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]]: embryo usually starchy.
3. Lecythidoideae Beilschmied
Secondary xylem with crystal chains; leaves two-ranked or spiral, lamina involute; (inflorescence cauliflorous); (flowers monosymmetric via connate androecium); filaments contracted at the apex; pollen tricolp/oroidate, (fodder pollen +); nectary 0/+; style (long); ovules with 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<; embryo curved or not, hypocotylar or with long radicle and leaf-like (folded) or fat cotyledons; n = 17 (18).
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; fruit indehiscent.
4. Barringtonioideae Beilschmied
Secondary xylem without crystal chains; leaves spiral, vernation?, glands in the stipular position; K imbricate; pollen syntricolpate, strong colpus margin ridge; nectary annular; style long; ovules 1-many/carpel, endothelium 0 (+); fruit usu. 1-seeded; testal bundles 2<; embryo hypocotylar (long coiled radicle, cotyledons - Planchonia); n = 13; germination epigeal, or hypogeal, with reduced leaves.
6/88: Barringtonia (70). 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 of Barringtonia is reported from the Late Cretaceous Deccan Traps (Manchester et al. 2015 and references); its identity should be confirmed.
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; n = ?
1/18. E. Africa (Tanzania, Pemba), Madagascar, Comores, Mauritius and Reunion.
Synonymy: Foetidiaceae Airy Shaw
Evolution. 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. 2103). 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 that is usually produced by the anthers in the hood, but sometimes by some of those in the ring; 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 m.y.a. (Ramírez et al. 2010). 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); 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; 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, and the pollen may be heteromorphic. There is both centripetal and centrifugal androecial development in the family (Tsou 1994). There are differences in how carpel orientation is shown - 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 there apotropous ovules (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.)
For general information, see van Tieghem (1905b, as Rhaptopetalaceae), Prance and Mori (2004), Prance and Jongkind (2015: African taxa), andalso Scott Mori's The Lecythidaceae Pages, Appel (1996, 2004), Letousey (1961), all Scytopetalaceae, Liben (1971a) and Prance (2004), both as Napoleonaceae, also Endress (1994b: floral morphology), Mauritzon (1939a), Venkateswarlu (1952a), Vijayaraghavan and Dhar (1976: Scytopetaloideae), Tsou (1994: comprehensive, but not Scytopetaloideae), all embryology, and Tsou and Mori (2002: seed coat anatomy in Lecythidoideae); Takhtajan (1992) includes information on endothelium and testa vasculature. Lecythidoideae were monographed by Prance and Mori (1979) and Mori and Prance (1990), and for a revision of Foetidia, see Prance (2008).
Phylogeny. The set of relationships [Napoleonoideae [Scytopetaloideae [Lecythidoideae [Planchonoideae + Foetidioideae]]]] were recovered by Morton et al. (1998) and Mori et al. (2007). 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 Napoleonoideae (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 may collapse into another 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) founf lecythis and Eschweilera to be in eight clades among which Corythophora and Bertholettia were also interspersed.
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. (2015).
Previous Relationships. Scytopetalaceae were considered quite distinct until recently (e.g. Cronquist 1981, in Theales; 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. (2004: but note topology) estimated the age of this node at around 107 m.y.; ca 69.1 m.y. is the estimate in Tank et al. (2015: Table S1), but stem Pentaphylacaceae, which are included here, are 83.4 m.y.o. (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; 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. (2004) estimated this node to be ca 102 m.y.o., while (97-)92(-90) m.y.o. is the estimate in Wikström et al. (2015).
Pentapetalum trifasciculandricus is a fossil ca 91 m.y. old from New Jersey that is placed either with Theaceae or in the Pentaphylacaceae area depending on the analysis (Martínez-Millán et al. 2009).
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 (Ericales), 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
Exudate + [Ficalhoa]; chemistry?; cork pericyclic; vessels in radial groups [Sladenia] or not; intervessel pitting opposite-alternate; petiole also with wing bundles [Sladenia]; perulae 0/+ [Sladenia]; lamina vernation involute [Filcahoa], margins toothed (not); inflorescences cymose; flowers small [5³ mm long]; (C connate – Ficalhoa); A 10-15, anthers opening apically (sagittate – Sladenia), monocot anther wall development [Sladenia], exothecium thickened; microsporogenesis successive [tetrads tetragonal]; G [3, 5], opposite K, placentae apical or placentation axile, placentae bilobed, style short, with relatively long pointed lobes; ovules 2-many/carpel, outer integument ca 3 cells across; embryo sac tetrasporic, 8-nucleate [Adoxa type]; fruit also ?schizocarpic, endocarp crustaceous [Sladenia]; seeds winged [Sladenia]; testa crustose, exotesta cells ± polygonal, little thickened [Ficalhoa]; n = 24 [Sladenia].
2 [list]/3. S.E. Asia (Sladenia), tropical E. Africa (Ficalhoa) (map: see Verdcourt 1962; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; for fossil Sladenia [blue], see Giraud et al. 1992).
Age. The wood of extant Sladenia is distinctive, and matches fossil wood ca 100 m.y.o. from the ?Cretaceous-Albian/Cenomanian of northern Sudan remarkably closely (Giraud et al. 1992).
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. Sladenia has anthers dehiscing by pores, while in Ficalhoa the anthers open across the apex.
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]; mesotesta well developed; embryo U-shaped.
12[list]/345, three groups below. Tropical and subtropical, but few in Africa.
Age. Pentaphylax and Visnea are reported fossil from late Cretaceous (Maastrichtian, ca 69 m.y.) and Eurya from Santonian (ca 85 m.y.) deposits in Europe (Knobloch & Mai 1986). If the latter date is confirmed, it would suggest an age for this node of at least 90 m. years.
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; testa ± multioplicative, 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; (petals 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 (61-)55, 54(-48) (Wikström et al. 2001) or (69-)54, 51(-35) m.y. (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 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[Freziereae])
(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; 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.]
Evolution. Pollination Biology. Anneslea has remarkable petals that become narrowed, but a broadened apical portion surrounds the protruding style - buzz pollination?
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 m.y.a.; 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 on which they are borne is very much reduced, then the inflorescence is fasciculate. If the shoot of Pentaphylax does not develop expanded leaves after the flowers appear, it seems as if the inflorescence is racemose. For variation in seed type and pollen surface of Freziera, see Weitzman (1987). Cleyera, and also Eurya (for which see 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.
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, Ternstroemiaceae could include Theaceae (Beauvisage 1920) - but 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, etc..
[Sapotaceae [Ebenaceae + Primulaceae]]: ellagic acid 0; ovules apotropous.
Age. The age of this node is around 84.3 m.y. or 82.3 m.y. (Tank et al. 2015: Table S1 and S2), 94.4 m.y. (Magallón et al. 2015) or (101-)92(-79) m.y. (Wikström et al. 2015).
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; inflorescences cymose, fasciculate, pedicels not articulated; flowers (anisomerous); K ± connate at base, C 4-18, (variously lobed or divided), 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 much lignified cells; endosperm nuclear, + or 0; n = (10-)13(-14).
Age. Crown Sapotaceae have been dated to (105-)84.5(-67.1) m.y. (Richardson et al. 2014); ca 107 m.y. is the age used in Armstrong et al. (2014).
1. Sarcospermatoideae Swenson & Anderberg
Leaves ± opposite, (stipels +), stipules +, cauline; 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.
1/6. Indo-Malesia (map: from Aubréville 1964).
Synonymy: Sarcospermataceae H. J. Lam
[Sapotoideae + Chrysophylloideae]: (plants di- or monoecious); stamens = and opposite to 2x (-6x) C lobes, staminodes often ± petal-like (0); G 1-[2-14(-30)]; (amyloid in seed [xyloglucans] +). [Photos - Collection, Fruit].
Throughout the tropics (map: from Aubréville 1964).
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
Stipules 0; A high in the tube, (several stamens opposite each petal), (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) m.y.o. (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 these perhaps occurred in Africa in the Campanian 83-73 m.y.a., 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 that island 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 m.y.a. (Grandcolas et al. 2008; Swenson et al. 2014). 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. m.y.a. 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 m.y. or so (Smedmark & Anderberg 2007; for other taxa behaving similarly, see Hillebrandia [Begoniaceae], Psiloxylum [Myrtaceae], 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 disjunct distributions there, migration via the boreotropical route stopped around 33 m.y.a., and so it is suggested that long distance dispersal causes disjunct distributions like those in Manilkara (Armstrong et al. 2014).
Ecology & Physiology. Sapotaceae are notably common in terms of both numbers of species and individuals in the Amazonian tree flora, 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. 2013).
The New Caledonian Sebertia acuminata (sève bleue) is a nickel hyperaccumulator, its sap containing 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).
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 sometimes quite considerable increase in the number of carpels and parallel increases in the numbers of other parts (Swenson et al. 2008c; see also Wanntorp et al. 2011). Swenson and Anderberg (2005) suggested that the staminodes common in Chrysophylloideae were perhaps derived within the clade, being not 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. Kümpers et al. (2016) looked at floral variation, particularly meristicity, in Sapotaceae in considerable detail, and noted a variety of ways in which merism 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 meristicity.
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).
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). Within the rest of the family there are two major clades, the (Isonandreae + Mimusopeae + Sideroxyleae) and (Chrysophylleae + Omphalocarpeae). In a combined molecular + morphological analysis and after successive weighting the same three major clades were recognised, the latter still with only moderate support (79% jacknife) because of the inclusion of Xantolis (the rest of that clade minus Xantolis had 97% support); these were recognised formally as the subfamilies characterized above (Swenson & Anderberg 2005). Morphological characters are highly homoplasious and characters for the subfamilies are hard to come by. However, in a study that focussed on Isonandreae (Sapotoideae), relationships are messier, and Eberhardtia 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 general discussion of relationships and character evolution in Sapotoideae. For relationships in Sideroxylon, see Stride et al. (2014).
Xantolis may be sister to the other Chrysophylloideae (Anderberg & Swenson 2003; Bartisch et al. 2010). However, its inclusion weakened support for Chrysophylloideae (Swenson & Anderberg 2005). 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 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). 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), but 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). For a checklist and bibliography, see Govaerts et al. (2001), but generic limits are dated.
[Ebenaceae + Primulaceae]: K/C tube well developed; ovules bitegmic, inner integument thicker than the outer.
Age. This node is ca 81.1 m.y.o. (Tank et al. 2015: Table S2), around 87 m.y.o. (Magallón et al. 2015), or (99-)88(-74) m.y. (Wikström et al. 2015).
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, two subfamilies below. Tropical (to temperate).
Age. Crown-group Ebenaceae are estimated to be some (65-)54(-42) m.y.o. (Turner et al. 2013a).
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; 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, endothelium +; 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.
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) m.y. (Turner et al. 2013a).
Fossil flowers and associated leaves (Austrodiospyros) are known from the mid Eocene of southeastern Australia (Basinger & Christophel 1985).
Synonymy: Diospyraceae Vest, Guaiacanaceae Jussieu, nom. illeg.
Evolution. Divergence & Distribution. Duangjai et al. (2009) noted that there were four separate lineages of Diospyros in New Caledonia, while Turner et al. (2013a, b) noted that speciation there has occurred within the last 10 m.y., and resolution of relationships between species was often difficult. In the largest of these clades, with some 24 specis, 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).
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 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, although whether or not perfect flowers occur is unclear: At least some "perfect" flowers may not produce 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, 2004a). 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).
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. Duanjai 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. (1998). Since the two have morphologically much in common, it is reasonable to combine them (see A.P.G. III 2009).
For a monograph of Lissocarpa, see Wallnöfer (2004b).
PRIMULACEAE Borkhausen, nom. cons. Back to Ericales
(Schizogenous secretory canals [material yellow, red, brown: tannins, etc.]); saponins common; nodes ?3:3; (stomata anisocytic); inflorescence racemose; C and A from common primordia; A = C , opposite C, staminodes +, opposite K [represented by at least a vascular trace - ?Maesa]; 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 thick, pitted, with amyloid [xyloglucans]).
58/2590. World wide.
Age. Wikström et al. (2001) suggest a crown group age of around (52-)49, 46(-43) m.y.; this age is estimated at (74-)61, 57(-45) m.y. by Bell et al. (2010).
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 grow up around the ovules after fertilization, as in the image of the fruits of Stimsonia in Wanntorp et al. (2012).
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 on Maesa, but not so far on members of Theophrastoideae (Espeland et al. 2015); Ehrlich and Raven (1964) noted other records.
Chemistry, Morphology, etc. 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, there is commonly a staminodial vascular supply (e.g. Subramanyam & Narayana 1976; see also Saunders 1934).
The number of carpels is difficult to ascertain, 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), 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. Perhaps 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, is whether it is worth recognising families at all. A broader circumscription 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 Back to Ericales
Lianes, shrubs or trees; vessel element type?; 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 quite commonly in woody Theophrastaceae and Myrsinaceae); 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[?]; rays >5-seriate, uniseriate rays 0 [not herbaceous taxa]; bracteoles 0; C imbricate, subrotate; petals developing after the stamens.
Age. The age of this node is estimated at about 65 m.y. by K. Bremer et al. (2004), 42-40 m.y.a. by Wikström et al. (2001), (67-)55, 51(-40) m.y. by Bell et al. (2010) and (73-)55(-35) m.y. by Wikström et al. (2015).
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 taxa have capsular fruits with five apical teeth, presumably also plesiomorphic; in Primulaceae, nearly all taxa with capsular fruits are herbaceous (Wanntorp & Anderberg 2011). 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 mollecular evolution in the herbaceous taxa they examined was much greater than in the woody taxa.
2. Theophrastoideae A. de Candolle Back to Ericales
Bracts ± displaced up the pedicels; staminodes +, ± petal-like; ovule endothelium?
6-9[list]/105. Mostly New World and tropical, some also more temperate and Old World.
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.]
Evolution. Divergence & Distribution. Species of Samolus from SW North America are sister to the rest of the genus, and Theophrasteae, sister to Samolus, 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. The stomata are anomocytic. There are several petiole bundles forming an arc, and these seem to diverge very soon after the leaf trace departs from the central stele. The ovules completely cover the placenta, but fingers of placental tissue may poke up between them (but not seen in the material examined by Caris & Smets 2004); Ma and Saunders (2003) suggest that in this whole clade (i.e. Theophrastoideae) the ovules are not embedded in placental tissue (which would then be a synapomorphy for it). The valves of the capsule are opposite the calyx (Caris & Smets 2004).
For general information, see Ståhl (2004: as Samolaceae).
Phylogeny. For the phylogeny of Samolus, see Wanntorp and Anderberg (2011).
Synonymy: Samolaceae Rafinesque
2B. Theophrasteae Bartling
Woody, tending to be pachycaul; rays broad; 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 + or 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), Jacquinia (35 - perhaps to be divided). New World tropics (map: from Ståhl 1989, 1991, 1995). [Photos - Collection.]
Chemistry, Morphology, etc. The subepidermal fibres may not be lignified. For reports of glandular dots on calyx and corolla, see Mabberley (1997). Floral primordia may initially be quite strongly monosymmetric, as in Deherainia (Sattler 1962), even if the flower at anthesis is polysymmetric.
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 some (54-)44, 40(-30) m.y.o. (Bell et al. 2010: note topology) or (50-)32(-16) m.y. (Wikström et al. 2015).
Chemistry, Morphology, etc. For a distinctive triterpene saponin found at least scattered in this clade, see Podolak et al. (2013.
3. Primuloideae Kostelesky Back to Ericales
Cucurbitacins +; ?cork; 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.
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 m.y. (Strijk et al. 2014) or ca 33 m.y. (Boucher et al. 2016).
Evolution. Divergence and Distribution. Primula, Androsace and Soldanella have all radiated in alpine habitats, in Europe in particular, where they are the main radiations and with allopatric speciation common, but also elsewhere in the northern hemisphere (Comes & Kadereit 2003; L.-B. Zhang et al. 2004; Boucher et al. 2011, 2016; 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. Heterostyly is likely to be an apomorphy in Primula s.l. (de Vos et al. 2014a). 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). 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).
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. Dionysia (= Primula) are also mostly cushion-forming plants, and some are chasmophytes (Trift et al. 2004).
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 pollen variation, see Mast et al. (2001) and Y. Xu et al. (2015), for embryology, see Subramanyam and Narayana (1976: anther wall development varies within Primula), and for general information, see Anderberg (2004).
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). 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 relationships within Androsace, see Wang et al. (2004), Schneeweiss et al. (2004b) and Boucher et al. (2011). For Dionysia (= Primula), see Trift et al. (2004).
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). Richards (2003) provides good general descriptions of the species of Primula s. str.
Synonymy: Hottoniaceae Döll
4. Myrsinoideae Burnett Back to Ericales
Also trees to shrubs or lianes; benzoquinones +; (vessel elements with scalariform perforation plates); (wood rayless); (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 contorted, (margins ciliate); (petals developing before the stamens); nectariferous or oil-secreting hairs on C, G, or nectary 0; A (basally connate - e.g. Lysimachia), anthers dorsifixed or basifixed, sagittate, (anthers dehiscing by pores); style (0), (stylar canal +), 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; (antipodal cells large - Lysimachia); capsule also with irregular or circumscissile dehiscence, fruit also a berry or drupe, placentae ± pulpy; seeds 1-few, rounded, (ruminate; 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 cells wall thickening variable; embryo suspensor massive, (embryo slightly curved; medium; cotyledon single - Cyclamen); n = 10-13, 15, 17, 23.
41[list]/1435: Ardisia (450), Myrsine (155: inc. Rapanea, Suttonia, many species in the Pacific), Lysimachia (150), 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.]
Evolution. Divergence & Distribution. 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.
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) bees (Michez & Patiny 2005: see also Simpson et al. 1983; Michez et al. 2008). 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) m.y.a., and the stem clade to (52-)41(-28) m.y.; 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 deposits from the early Eocene some 53 m.y. old (the fossil macropid Eomacropis glaesaria is not 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 seeds of Cyclamen are dispersed by ants, and most species have rather local distributions (Yesson et al. 2009).
Ecology & Physiology. Aegiceras is restricted to the mangrove habitat, for the evolution of which, see Rhizophoraceae and Tomlinson (1986). 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).
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). The association involves a single strain/species of Burkholderia and there was a single origin of the bacteria/plant association; bacteria are also found in the shoot apex, and transmission is likley 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 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.
Some information is taken from Ståhl and Anderberg (2004); Lens et al. (2005a) provide much information about wood anatomy. For pollen, see Nowicke and Skvarla (1979), for some embryology, see Subramanyam and Narayana (1976), for the ovules of Cyclamen, see Woodcock (1926) and Corner (1976), and for floral morphology of the wind pollinated Myrsine, see Otegui and Cocucci (1999).
Phylogeny. The old Myrsinaceae included only woody taxa with fleshy often drupaceous fruits, but the clade that included these taxa (minus Maesa) was found also to include Anagallis, Ardisiandra, Asterolinon (?= Lysimachia), Coris, Cyclamen, Glaux (= Lysimachia - it lacks a corolla), Lysimachia, Pelletiera, Stimpsonia and Trientalis (Anderberg et al. 2000, 2001), all of which are herbaceous, capsular fruited, and ex-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 formed many basal pectinations within Myrsinoideae, Cyclamen (the focus of their study) was well embedded in the family, and 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
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).
Synonymy: Aegicerataceae Blume, Anagallidaceae Borkhausen, Ardisiaceae Jussieu, Coridaceae J. Agardh, Embeliaceae J. Agardh, Lysimachiaceae Jussieu, Myrsinaceae R. Brown, nom. cons.
[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) m.y. (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 mitochondral 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 (Bormham et al. 2013).
Chemistry, Morphology, etc. Watanabe (1936: V) talks a lot about a "Mitrastemon-Pilz" (c.f. 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 - and the latter both 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]) has been dated to 103 m.y. (K. Bremer et al. 2004), if including Ericaceae, etc., a date closer to 106 m.y.a. is more likely; Magallón et al. (2015) estimated the age of this node to be around 94.9 m. years, (103-)96(-88) m.y. is the estimate offered by Wikström et al. (2015).
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).
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; nectar from base of filaments or ovary; 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 present; 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, usu. slight, cotyledons longer than radicle, accumbent.
Ca 9[list]/195(-460!) - three groups below. Mostly South East Asia and S.E. U.S.A., Malesia and tropical South America. [Photo - Collection.]
Age. Crown-group Theaceae are some 49 m.y.o. (M.-M. Li et al. 2013).
Pentapetalum trifasciculandricus, a fossil ca 91 m.y. 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 Grote and Dilcher (1989).
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; n = 15, 17, 18.
1/9. East Asia, E. North America (map: from Hong 1993).
Age. Crown-group Stewarteae are around 18.7 m.y.o. (M. M. Li et al. 2013).
[Gordonieae + Theeae]: stomata anisocytic/cyclocytic; androecium whorled; capsule with persistent columella.
Age. This node has been dated to around 68 m.y.a. (K. Bremer et al. 2004).
[Gordonieae + Stewartieae]: ?
Age. This node is about 40.4 m.y.o. (M.-M. Li et al. 2013) or (77-)44(-14) m.y.o. (Wikström et al. 2015).
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; 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.y.o. (M.-M. Li et al. 2013).
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 with ribs; outer integument vascularized; (embryo sac bisporic [chalazal dyad], eight-celled [Allium-type]); 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), Pyrenaria (42), Laplacea, Polyspora (32), Pyrenaria (60). Southeast Asia, Malesia, tropical America (map: from Camp 1947, approximate). [Photo - Flower, Fruit.]
Synonymy: Camelliaceae Candolle
Evolution. Divergence & Distribution. 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).
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).
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) and 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) and Tsou (1997, 1998), all embryology, Gunathilake et al. (2015: testa surface) and Wang et al. (2006: Apterosperma, chromosomes and morphology).
Phylogeny. Major relationships within the family are still poorly understood. 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, family in broad sense, including Pentaphylacaceae). Relationships between these three clades remain unclear, although the clade [Gordonieae + Theeae] has some support (see also Prince 1999; Yang et al. 2004) and makes morphological sense. However, 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]) and M.-M. Li et al. (2013: several chloroplast genes, 11/20 species sampled were Stewartia).
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 Li et al. (2011).
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 (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), for which, see Caryophyllales. Pentaphylacaceae, Sladeniaceae and Pellicieraceae, also erstwhile Theaceae, are in separate families in Ericales, the last quite apart from the other two. Bonnetiaceae (see Malpighiales) have also been included in Theaceae s.l. (e.g. Cronquist 1981).
[[Symplocaceae [Styracaceae + Diapensiaceae]] [[Sarraceniaceae [Actinidiaceae + Roridulaceae]] [Clethraceae [Cyrillaceae + Ericaceae]]]]: ?
Age. If this clade exists, its crown-group age is around 93.2 m.y. (Magallón et al. 2015) or ca 83 m.y. (Tank et al. 2015: Table S1).
[Symplocaceae [Styracaceae + Diapensiaceae]]: shrubs to trees; lignans +; inflorescence racemose; style hollow; endosperm copious.
Age. The age of this node is some (68-)63, 61(-56) m.y. (Wikström et al. 2001), about 100 m.y. (K. Bremer et al. 2004), about 81.2 m.y. (Magallón et al. 2015) or (94-)92(-89) m.y.a. (Fritsch et al. (2015).
Evolution. Divergence & Distribution. 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, very large "water stomata" also present; (leaves two-ranked), lamina ± supervolute; (inflorescence branched), pedicels articulated (not - Cordyloblaste); K basally connate; A (= and opposite sepals)-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, 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. 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) m.y.o. (Fritsch et al. 2015).
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 diversication of [section Palura + The Rest], i.e., most of the family, is dated to only (41-)38(-35) m.y.a. (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). However, pollen germinates on the subapical lobes which are thus (and from their position) the 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 pericyclic; glandular hairs 0; leaves spiral, (margins entire); A 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) m.y. by Wikström et al. (2001), (78-)54, 51(-39) m.y. by Bell et al. (2010), about 52.7 m.y. by Magallón et al. (2015) and ca 73 m.y. by Tank et al. (2015: Table S2).
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 conduplicate-plicate or supervolute; bracteoles 0, pedicels articulated or not [Styrax]; flowers (4-)5(-7)-merous; K ± completely connate, open, C valvate or not; A 2 (3) x C, or = and alternate with C, adnate to C, often basally connate, (filaments as broad as anther - Styrax sect. Pamphilia), connective produced or not; 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 also drupaceous; testa vascularized, crushed; n = 8.
11[list]/160: Styrax (120). Warm N. temperate to tropical (map: from van Steenis 1949b; Sales & Hedge 1996; Fritsch 1999). [Photo - Flower].
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 (Cerataphidinae also produce soldiers - Stern 1995; Stern & Foster 1996; J. Chen et al. 2014 for a phylogeny of the aphids). Cecidomyids also produce galls on Styrax.
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); 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. 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 Rest on all three counts.
For relationships within Styrax see Fritsch (2001).
Synonymy: 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) perforations; 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. Circum-Arctic (Diapensia lapponica only) and scattered N. temperate, esp. East Asia and E. U.S.A. (map: from Diels 1914; Wood & Channel 1959; Hultén 1971).[Photo - Diapensia Flower, © J. Maunder; Diapensia Fruit, © J. Maunder.]
Age. Friis (1985) described Actinocalyx from the Upper Cretaceous of Sweden. 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).
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); 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; 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 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) m.y., 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 m.y.) 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) m.y., an age of ca 50.6 m.y. is the estimate in Ellison et al. (2012), of about 90.4 m.y. in Magallón et al. (2015), and (95-)86(-77) m.y. in Wikström et al. (2015).
Glandulocalyx upatoiensis, a small-flowered fossil from the Upper Cretaceous 86-84 m.y.a. in Georgia, the southeast United States, has been identified as near Actinidiaceae or Clethraceae (Schönenberger et al. 2012). 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 m.y.) 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 perhaps associated with Diapensiaceae or within Ericaceae (Crepet et al. 2013), but overall Glandulocalyx is morphologically heterogeneous and rather odd.
Paleoenkianthus is another interesting Late Cretaceous fossil from some 90 m.y.a. (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). 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 Friis et al. (2011) might be fungal hyphae. In fact, Nixon and Crepet (1993) were not that sure of their identification, while Friis et al. (2011) thought that although this fossil is 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, how to define the "character" - 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.).
[Sarraceniaceae [Actinidiaceae + Roridulaceae]]: route I secoiridoids +; K quincuncial, unequal, C quincuncial, stamens many [?here]at base thicker than sepals; nectary 0; stigma dry, papillate [?level]; ovule hypostase +; K persistent in fruit.
Age. The age of this node is estimated to be (53-)48.6(-43) m.y. (Ellison et al. 2012), ca 70.1 m.y. (Tank et al. 2015: Table S2), or about 88.1 m.y. (Magallón et al. 2015).
Evolution. Divergence & Distribution. See Löfstrand and Schönenberger (2015) and Löfstrand et al. (2016) for possible apomorphies within this clade. "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 +b>; mycorrhizae 0; cork?; vascular bundles separate; nodes ?; leaves with broad bases, ascidiate; 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 at base of style - Sarracenia); placentation intrusive parietal apically, style apically hollow or not, apex divided or peltate-expanded, stigmas small; ovules many/carpel, 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).
Age. Crown group Sarraceniaceae are estimated to be (44-)35(-25) m.y.o. (Ellison et al. 2012).
Although Archaeamphora (Sarraceniaceae) was described from rocks ca 124 m.y. old (Li 2005), the fossil is likely to be a gall of the conifer Liaoningocladus boii (W. Wong et al. 2015).
Evolution. Divergence & Distribution. Ellison et al. (2012) offered a vicariance-style that explained the relationships and disrribution of the three genera; Sarraceniaceae originated in South America, perhaps hopping across the proto-Caribbean on islands.
Ecology & Physiology. 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. It has also been suggested that the colouring on the flap of the pitcher may also attract insects, that is, it is a kind of pseudoflower (Cresswell 1993), although this is unlikely (Joel 1988; Ruxton & Schaefer 2011), however, the plants of both Sarracenia and Heliamphora are variously scented, so attracting potential prey (Fleischmann 2016). The pitcher varies in the amount of digestive enzymes it contains, indeed, these seem to come from the organisms there, and if so, this is a case of symbiotic digestion (Peroutka et al. 2008b). In Sarracenia 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; they then eat the pitcher; species of Exyra occur throughout the range of the genus (see e.g. McPherson & Schnell 2011).
The small mosquito Wyeomyia smithii breeds in the pitchers of Sarracenia purpurea. The larvae eat animal remains but they are not harmed by the fluid there. 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) and the Carnivorous Plants Database, for perforation plates, see Schneider and Carlquist (2004) and Carlquist (2012c: pores almost closed).
Phylogeny. R. J. Bayer et al. (1996), Neyland and Merchant (2006) and Ellison et al. (2012) provide more information about relationships within the family; the topology [Darlingtonia [Sarracenia + Heliamphora]] is well supported. See Stephens et al. (2015) for relationshipsfor 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 m.y. old (Warren & Hawkins 2006) or ca 38.1 m.y.o. (Ellison et al. 2012); the age for this node is about 84.8 m.y. in Magallón et al. (2015) and (85-)76(-72) m.y. 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), (± connate), anthers extrorse, 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)], style (unbranched), (grooved - Actinidia), (hollow), (stigma peltate, lobed); ovules 10</carpel, integument 6-9 cells across, parietal tissue ca 3 cells across, nucellar cap ca 3 cells across; (megaspore mother cells several); fruit usu. a berry; seeds embedded in placental pulp; integument multiplicative; endosperm haustoria?; n = 20, 29, 30; horizontal transfer of mitochondrial rps2 gene [Actinidia].
3[list]/380: Saurauia (300), Actinidia (54), Clematoclethra (25). Largely tropical, esp. South East Asia to Malesia, but not Africa (map: from Soejarto 1980).
Age. Parasuarauia was described from flowers of Early Campanian (Late Cretaceous) age ca 80 m.y.a. 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).
Evolution. Divergence & Distribution. Both separate styles and numerous stamens are probably derived within the family (Keller et al. 1996; Herendeen et al. 1999). For the fossil record, see Manchester et al. (2015).
Genes & Genomes. There is paternal transmission of the plastid genome in Actinidia at least (Chat et al. 2003).
Economic Importance. For the kiwi fruit, 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 vegetative anatomy, see Beauvisage (1920), the floral anatomy of Actinidia, see Schmid (1978), for floral development, see Schönenberger et al. (2012), for ovules, see Guignard (1882), for pollen, see Dickison et al. 1982), and for general information, see Dressler and Bayer (2004).
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 curved, 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 m.y. (Ellison et al. 2012).
Evolution. Divergence & Distribution. It was suggested that, given their age, ca 90 m.y., Roridulaceae must be very much a relictual (?Gondwanan) element in the Cape flora (e.g. Warren & Hawkins 2006). However, both well preserved fossils in Baltic amber dated to 47-35 m.y.a. were recently described by Sadowski et al. (2015), and the general distributions of families in this part of the ericalean tree are not Gondwanan; Roridulaceae might even have originated in the northern hemisphere; see also Givnish (2015a), also Cornales-Curtisiaceae for a comparable extant/fossil distribution.
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, 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 evident in the flowers (Anderson et al. 2003).
Bacterial/Fungal Associations. The plant lacks mycorrhizae (Brundrett 2004 and references).
Chemistry, Morphology, etc. Whether or not the roots are mycorrhizal is disputed (Conran 2004 for literature).
For general information, see Vani-Hardev (1972), Dahlgren in Dahlgren and van Wyk (1988: endosperm haustoria 0), Wilkinson (1998), Conran (2004), McPherson (2008, 2010) and the Carnivorous Plants Database.
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 pericyclic; pericyclic fibres absent; leaves spiral; inflorescence racemose, 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 m.y. (Naumann et al. 2013), ca 50.6 m.y. (Ellison et al. 2012) or (89-)71(-44) m.y. (Wikström et al. 2015); see sampling in all. Around 79.2 m.y.a. is the estimate in Magallón et al. (2015) and ca 70.4 m.y. in Tank et al. (2015: Table S2).
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 III 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
Mycorrhiza as modified ectendomycorrhiza?; sugars accumulated as kestose and isokestose oligosaccharides, iridoids?; (pits vestured); petiole bundle arcuate or annular with medullary bundle; stomata also paracytic and actinocytic; hairs stellate [sect. Clethra]; lamina vernation conduplicate-subplicate, margins toothed (entire); inflorescences terminal, branched or not; flowers spreading (pendulous), (bracts conspicuous - Purdiaea); K quincuncial, C basally connate or free; A ?obdiplostemonous, adnate to C or not, anthers ± sagittate, dehiscing by pores or short slits; pollen <20µm, oblate, psilate to rugulate; (nectary 0); G ?orientation, (placentation apical - Purdiaea), style not impressed, 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.]
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 Sai 1934 (mycorrhiza), Thomas (1960: Purdiaea), Sleumer (1967: Clethra), Anderberg and Zhang (2002: pollen), Schönenberger et al. (2012: floral morphology), and Schneider and Bayer (2004: general).
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 +; C connate, stigma wet.
Age. The age of this node is estimated to be ca 69.3 m.y. (Magallón et al. 2015) or ca 64.7 m.y. (Tank et al. 2015: Table S2).
CYRILLACEAE Lindley, nom. cons. Back to Ericales
Iridoids?; sieve tube plastids with protein crystalloids and fibres; petiole bundle annular, complex or deeply concave; lamina vernation supervolute, margins entire, petiole obscure; flowers spreading, (weakly monosymmetric), (6-7-merous); 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).
Chemistry, Morphology, etc. Goldberg (1986) notes the presence of small, scarious stipules; I have not seen them. However, some taxa have slight excavations in the leaf base enclosing the buds and the colleters may be sublateral, hence suggesting the presence of stipules; Thomas (1960, p. 15) described them as being bright red, ligulate and glandular, although it is not clear to what genera he was referring.
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 in the nectary, but apparently not in nectaries in Ericaceae (Brown 1938). Löfstrand et al. (2016: Cyrilla only examined) suggest that the style is impressed into the ovary.
For more information, see Copeland (1953: floral morphology and anatomy), Thomas (1960: monograph, 1961), and Vijayaraghavan (1970: ovule morphology, etc.), also Zhang and Anderberg (2002: pollen), and Anderberg and Zhang (2002) and Kubitzki (2004b), both general.
Previous Relationships. The old separation between Clethraceae and Cyrillaceae was based on fruit type (dehiscent versus indehiscent fruits), 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; (vessel elements with simple perforation plates); 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, with appendages, tapetal cells uni- or binucleate; pollen >26µm, surface ± rugulate; G , opposite C, style undivided, stigma expanded; integument 4-6 cells across; K persistent; testa with outer wall unthickened; chloroplast infA gene defunct.
Ca 126[list]/4,010 - 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 98-90 m.y. (Z.-W. Liu et al. 2014) or (123.9-)117.3(-109.4) m.y. (Schwery et al. 2014).
1. Enkianthoideae Kron, Judd & Anderberg
Pith with small, thick-walled and lignified and larger and thin-walled cells mixed [heterogeneous]; leaves pseudoverticillate; flowers pendulous; anthers 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 m.y.o., see above.
[[Pyroloideae [Monotropoideae + Arbutoideae]] [[Cassiopoideae + Ericoideae] [Harrimanelloideae [Epacridoideae + Vaccinioideae]]]]: plant ectendomycorrhizal, fungal 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; stigma dry to wet; vascular bundle in ovule absent; duplication of complete chloroplast ndhH-D operon.
Age. This node is dated at around 91 m.y.a. (Z.-W. Liu et al. 2014).
[Pyroloideae [Monotropoideae + Arbutoideae]]: Hartig net common [= pyroloid mycorrhizae], (clade A Sebacinales common).
Age. The age of this node is about 86 m.y. (Z.-W. Liu et al. 2014).
2. Pyroloideae Kosteltsky
Perennial herbs, rhizomatous, (plant myco-heterotrophic; leaves as scales); sugars accumulated as kestose and isokestose oligosaccharides; multicellular hairs 0; leaves pseudoverticillate; inflorescence a raceme; flowers more or less spreading, (mono-, asymmetric); C free; 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; 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) m.y. (Z.-W. Liu et al. 2014).
Synonymy: Pyrolaceae Lindley, nom. cons.
[Monotropoideae + Arbutoideae]: flowers pendulous.
Age. The two clades diverged ca 70 m.y.a. (Hardy and Cook 2012) or around 79 m.y.a. (Z.-W. Liu et al. 2014).
3. Monotropoideae Arnott
Perennial herbs, echlorophyllous, myco-heterotrophic, hyperparasitic; fungal hyphae with peg-like intrusions into the exodermal cells; sugars accumulated as kestose and isokestose oligosaccharides; sieve tube plastids lacking both starch and protein inclusions; multicellular hairs 0 [+ - Pterosporeae]; leaves sessile, ± scale-like; inflorescence a raceme, (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); seed winged or not, (walls thickened); embryo minute, undifferentiated; 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
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.]
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]; hyphal sheath and Hartig net 0; clade B Sebacinales common or not; (toxic andromedane diterpenes +); 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 m.y.a., but it is around 77 m.y.o. in Z.-Y. Liu et al. (2014).
[Cassiopoideae + Ericoideae]: leaves opposite, ericoid, lamina vernation revolute.
Age. Wagstaff et al. (2010: constraint age) give the age of this node as ca 40.5 m.y..
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; 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
(Epiphytes); (grayanotoxins + [cyclic diterpenes]); leaves also spiral, lamina flat (convolute); (pedicel articulated); flowers pendulous to erect, (monosymmetric); (median sepal abaxial), (C free); anthers lacking appendages (present - Ericeae); (tapetal cells multinucleate - Empetrum); (pollen with viscin threads, attached distally to the grains); capsule septicidal; (dust seeds +).
19/1790: Rhododendron (850: inc. Azalea, Ledum, Menziesia, Tsusiophyllum), Erica (765+). Most diverse in South Africa and Malesia to S.E. Asia, also general N. hemisphere to S. South America, inc. Tristan da Cuhna and Falkland Islands (map: from Meusel et al. 1978; Hultén & Fries 1986; Kron & Luteyn 2005). [Photo - Flower, Habit, Flower, Empetrum Fruit © J. Maunder.]
Synonymy: Azaleaceae Vest, Diplarchaceae Klotzsch, Empetraceae Hooker & Lindley, Ledaceae J. F. Gmelin, Menziesiaceae Klotzsch, Rhododendraceae Jussieu, Rhodoraceae Ventenat, Salaxidaceae J. Agardh
[Harrimanelloideae [Epacridoideae + Vaccinioideae]]: K in fruit not withering.
Age. The age of this node is about 77 m.y. (Z.-W. Liu et al. 2014).
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 67 m.y.o. in Z.-Y. Liu et al. (2014).
8. Epacridoideae Sweet [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.]
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) m.y.a., while (29.8-)22.3(-15.4 m.y.a. is the age in Schwery et al. (2014).
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) m.y. ago.
[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 also 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
(Epiphytes [ca 1/5 spp]); (grayanotoxins + [cyclic diterpenes]); (hyphal sheath and Hartig net +, hair roots short); axial parenchyma scanty paratracheal; stomata often paracytic; apical bud aborting; (lamina entire), (venation palmate; with parallel veins), (with marginal or surficial glands); inflorescence usually axillary; flowers usu. ± pendulous; pedicel often articulated, bracteoles +; anthers often with tubules, with spurs, 2 or 4 awns or appendages 0; (G inferior), stigma truncate; (integument ca 10 cells across - Andromeda); (calyx fleshy), (fruit fleshy); n = 12.
Ca 50/1580. Inferior-ovaried taxa: Vaccinium (450), but in Southeast Asia Agapetes (ca 400, inc. many Vaccinium), Dimorphanthera (ca 85), while in tropical America Cavendishia (155), Psammisia (60), Thibaudia (60), Macleania (55), and Gaylussacia (50). The rest: Gaultheria (240, inc. Pernettya, Diplycosia, Tepuia). 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.]
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 m.y.a. in Central Australia (Carpenter et al. 2015). Quite well preserved seeds of Rhododendron (R. newburyanum) were described from Paleocene deposits in southern England (Collinson & Crane 1978). For an evaluation of the fossil record of Styphelioideae, see Jordan and Hill (1996).
The inclusion of the largely Australian Epacridaceae within Ericaceae means that the distinctive rarity of Ericaceae s. str. in that area no longer presents a problem as it did in the 1970s - the clade is quite common there. 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, where Cassiopoideae are shown as being found throughout Greenland, perhaps in anticipation of the disappearance of the ice. 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.
The numerous African species of Erica (800+ in southern Africa - 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). Arbutoideae, now prominent in Mediterranean vegetation, may have moved from the New World to the Old World around 39.2-21.2 m.y. (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). Outlines of interesting biogeographical groupings in tropical Vaccinieae are developing (Kron et al. 2002a; see also Powell & Kron 2003; Pedraza-Peñalosa 2009), and these may be correlated with variation in wood anatomy (Lems et al. 2004c). Vaccinieae are diverse in the mountains of Central and South America and Malesia, Rhododendron is notably diverse in Malesia-South East Asia, with around 225 species in the Hengduan region of China alone (Boufford 2014). Empetrum is likely to have arrived in south South America in the Pleistocene, perhaps by long-distance dispersal from northwestern North America (Popp et al. 2011). 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. For the circumboreal species of Pyrola, a genus perhaps Asian in origin, and their places of origin, see Z.-W. Liu et al. (2014).
Another 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). Six radiations, including Richeeae, Rhodoreae, Vaccinieae, and some Gaultheria and Erica, including in total almost 80% of the family, are involved (Schwery et al. 2014; Bouchenak-Khelladi et al. 2015; Hughes & Atchison 2015). 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.
The speciose clade in Vaccinieae (inc. Vaccinium, Agapetes, Cavendishia) has been dated to (54.4-)45.6(-37.2) m.y.a. (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 (see also pollination, etc., below). Kron and Luteyn (2005) suggested that there were perhaps two migrations from the North to South America, and they dated diversification in Vaccinieae to Late Miocene. Vaccinieae from the Neotropics and North American may have had similar mycorrhizal Sebacinales in common (Setaro & Kron 2011). Indeed, around mid-Miocene times ca 24 m.y.a. connections between North and South America were established (see Bacon et al. 2015: c.f. Proc. National Acad. Sci. U.S.A. 112(43): E5765-E5668; Montes et al. 2015 for a re-evaluation of the geology), so some kind of synchronised island hopping of plant and fungus would not have been needed (c.f. Setaro & Kron 2011).
Diverse early Pleistocene Styphelioideae fossils 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 m.y. 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) m.y. ago. 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 m.y. 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 Styphelioideae 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 m.y. or so.
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 as being a megatherm family.
It can be difficult to interpret the floral morphology of Monotropoideae, as with other myco-heterotropic and parasitic groups, especially of Monotropeae. Seeds and embryos are usually very small, and Monotropa uniflora itself has a two-celled embryo (Olson 1991); much smaller than this you cannot get (except in Anemone). See also Francke (1935) for Monotropa hypopitys.
See Lens et al. (2003, 2004a, b, c) for some wood anatomical variation placed in a phylogenetic context; I have not attempted to place 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 Styphelioideae in West Australian kwongan vegetation - see Cowling et al. 1990), 3, taxa that are epiphytic (or epilithic) and often lianescent, ca 650 species, and 4, taxa with viscin threads, ca 900 spp.
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), 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 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).
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 some Ericaceae have notably small leaves (Cornwell et al. 2014). They are most commonly found in open, more or less acidic, nutrient-poor and nitrogen-limiting soils in cold to warm temperate climates, being characteristic and often common in heathlands world-wide (characteristic heathland families include the old Epacridaceae, Prionotaceae, Empetraceae and Vacciniaceae, all now in Ericaceae; Grubbiaceae and Diapensiaceae were the only other families listed: Specht 1979a; Read 1996; map: see Specht 1979b; White et al. 2000). In the Mediterranean heathlands of southern Africa and Australia Rhododendroideae and Styphelioideae respectively are common shrubs, e.g. the 600 or more species of Erica growing in the Cape region of South Africa alone (Oliver 2000). 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). See also Clade Asymmetries.
Many Ericaceae are noted for their distictive ericoid mycorrhize (ERM), ectendomycorrhizae in which fungal hyphae form complex, usually coiled intrusions into the exodermal cells of the distinctive and aptly-named very narrow hair roots, and sometimes also surround the roots with a hyphal sheath. Hair roots are as little as 40µm across, almost as thin as a root hair proper (these they lack). (At least in Vaccinium corymbosum, even low-order roots, i.e. not the ultimate rootlets, are also quite thin [Valenzuela-Estrada et al. 2008].) They consist of little more than endodermis, exodermis, tracheid, sieve tube, and companion cell, yet they are relatively long-lived.
The fungal intrusions in the exodermis are not broken down by the host (Frank 1887; Read 1996; Perotto et al. 2012[?]), but organic nitrogen and phosphorus taken up by the fungus move to the ericaceous associate; nitrogen in amino acids released by the fungus are also taken up by the plant (Cairney & Ashford 2002; Perotto et al. 2012). The protein-tannin complexes that come from Rhododendron, at least, may result in more nitrogen being in stable soil organic matter. This nitrogen is then more easily accessed by the ericoid fungus than by fungi in other kinds of mycorrhizal associations (Read 1991; Wurzburger & Hendrick 2009) by the saprotrophic activities of the fungi; the fine ericoid rootlets are very dense, if shallow, and efficiently permeate the soil (try digging up a rhododendron). ERM fungi show considerable metabolic diversity, 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). The ERM ascomycete Oidiodendron maius is saprotrophic, breaking down Sphagnum peat, and it has both cellulases and some lignin-decomposing enzymes (Kohler et al. 2015). Kohler et al. (2015 and references) found that the ERM ascomycete Oidiodendron maius retained a number of genes from its saprotrophic ancestors, and it itself could be saprotrophic on occasion.
An association with fungi may be an important element in the success of the family in the often rather acidic, nitrogen-poor and generally stressful habitats in which many of them grow, and also in their ability to grow in soils with toxic metals (Read 1991: useful summary, 1993; Cairney & Meharg 2003; Perotto et al. 2012; Garbaye 2013). They can grown 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 VAM 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 and a relatively few other species (Read 1991; Cornelissen et al. 2001). ERM hyphae have melanin, which, like lignin, is resistant to decay, and are an important component of the sequestered carbon in at least some older boreal forests; the nitrogen there is not so readily accessible to other plants (Read et al 2004; Clemmensen et al. 2014).
The relationship between fungi and Ericaceae is closest in the echlorophyllous and myco-heterotrophic Monotropoideae. Here the underground parts can be massive, and the roots are thick; basidiomycetes are the fungi often involved (Garbaye 2013). 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). Kranabetter and MacKenzie (2010) noted the distinctiveness of the nitrogen metabolism in Pyroloideae when compared with other Ericaceae with ERM, emphasizing their probably mixotrophic nutrition. Hashimoto et al. (2012) found that in Pyrola asarifolia from Hokkaido, Japan, non-ectomycorrhizal fungi (Sebacinales-B) were associated with the plant as it germinated, rather like the association of orchids and fungi, while fungi associated with roots of the adult plant were different, being ECM fungi also associated with Betulaceae growing in the same area. There was geographical variation in the extent of partial mycoheterotrophy in Moneses uniflora (Hynson et al. 2015).
The myco-heterotrophic habit (and probable hyperparasitism) has arisen at least twice, both in Monotropoideae and in Pyrola aphylla, which is also a myco-heterotroph at times (Zimmer et al. 2007; Hynson et al. 2009b; c.f. Cullings 1994); however, it 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). Monotropoideae are mixotrophic or fully heterotrophic (Hynson et al. 2009b; Selosse & Weiß 2009).
As with other mycorrhizae, relationships and pathways of nutrient flow can be complex. A member of Sebacinales group A found in Diphasiastrum alpinum (Lycophyta) 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 both the Indo-Malesian and the Andean regions many species of Vaccinieae are epiphytes, and they are a major component of the woody epiphytic flora there. Woody epiphytes (here I include the few epilithic taxa) are commonest in the fleshy-fruited tropical Vaccinieae, especially in the New Word, but are also quite common in the Old World Rhododendron, which has wind-dispersed seeds, and Ericaceae are one of the more important epiphytic families (Benzing 1990; Zotz 2013). 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. Interestingly, distinctive cavendishioid mycorrhizae - here the ericoid roots are short, and there is 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. (2008) also discuss the mycorrhizal fungi associated with epiphytic Ericaceae in the Andes.
Many taxa in Mediterranean climates in particular (Ericoideae in the South African Cape Region, Epacridoideae in Australia), and so with xeromorphic leaves, form starch-rich lignotubers with buds that allow the plants to resprout after fires, or they regenerate by seeding; germination is enhanced by heat and/or smoke (Bell & Ojeda 1999; Cairney & Ashford 2002 - 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 e.g. with latitude, but also with life form and precipitation.
Pollination Biology & Seed Dispersal. Although the anthers of most Ericaceae have functionally terminal pores, buzz pollination is not that common (c.f. in part de Luca & Vallejo-Marín 2013), although it is scattered in the family. In Pyroloideae, for instance, the lack of an endothecium and absence of a nectary are associated with this condition (Liu et al. 2011), as in other buzz-pollinated clades. Although vibrations of the anther that develop as bumble bees work the flowers of Rhododendron may facilitate pollination, the bees do not buzz the flowers (King & Buchmann 1995).
In most taxa nectar is the reward. Bird pollination is particularly common in the Andean Vaccinieae (Stiles 1981 and references) and may also occur in the large-flowered Indo-Malesian members of the tribe (= "Agapetes"). Ca 600 species of Vaccinieae occur 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 humming bids, which pollinate most of these species, are also maximally diverse (Luteyn 2002; see also Gesneriaceae-Gesnerioideae). Interestingly, it has been suggested that Ericaceae-Agapetes may originally have been pollinated by stem-group hummingbirds ca 45 m.y.a., although they are now pollinated by sunbirds, Nectariniidae, and their like (Mayr 2005, 2009). Several other factors have been implicated in this diversification, including the adoption of the epiphytic habitat by some of these plants, the uplift of the Andes, etc. (Luteyn 2002). A variety of pollinators visit Malesian vireya (= sect. Schistanthe) rhododendrons. 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 euvireyas (Goetsch et al. 2011), and there, too, bird pollination occurs - and nectar-eating mites use the birds to travel from flower to flower (Stevens 1976). In southern Africa it has been estimated that 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; Johnson 2010).
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 of very different floral morphologies, Vaccinium, Elliottia (polypetalous), Phyllodoce, Pieris, Chamaedaphne, Cassiope, Gaultheria (Ranta & Lunberg 1981; Tomono & Sota 1997; Kudo et al. 2011 and references), although other pollinators are also effective 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 Styphelioideae, where bee pollination is common, but there is also pollination by other insects and, in a few species, birds. Wind pollination has evolved at least twice, in Empetrum and its relatives, and also in taxa that were included in genera like Philippia, now Erica s.l.. Both groups of wind-pollinated plants have expanded stigmas.
Fleshy-fruited taxa, whether the calyx or the inferior ovary is fleshy, predominate in Vaccinieae, and in both the Old and New Worlds some species have seeds with a mucilaginous testa and a green embryo; plants with such seeds are generally epiphytic or epilithic (pers. obs.). Seeds of other Vaccinieae, and of other Ericaceae in general, have 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 tend to be a bit bigger than this.
Plant-Animal Interactions. Mirid bugs are associated with a sticky-leaved (glandular hairs) species of Rhododendron from Japan; only benefits to the insect from eating the carcasses of insects that had become stuck to the leaves was examined (Suguira & Yamazaki; for such mirids, see Wheeler & Krimmel 2015).
Bacterial/Fungal Associations. For Ericaceae-mycorrhizal associations in general, in which the fungi are often ascomycetes, see Cullings (1996) and Smith and Read (1997) and the discussion above. Many Leotiomycetes (ascomycetes) are ERM fungi and they increase in diversity towards the poles, where ericoid-dominated heath vegetation is conspicuous (Tedersoo et al. 2014b; Wardle & Lindahl 2014). A number of mycorrhizal "types" have been described for the family, but their discreteness needs to be be confirmed , and there may also be intermediates between mycorrhizae and dark septate endophytes, also known from Ericaceae (Vohnik & Albrechtova 2011; see also Walker et al. 2011); there is also melanin in the hyphae of the latter. Interestingly, ERM and ECM fungi may be quite different (Vohnik et al. 2012). For the mycorrhizae of Epacridoideae in particular, see Cairney and Ashford (2005).
In the echlorophyllous and myco-heterotrophic Monotropoideae mostly ECM basidiomycete fungi may be specifically associated with with individual species of Monotropoideae (Bidartondo and Bruns 2001, 2002; Bidartondo 2005: questions as to the identity of the plants compromise earlier literature). However, several species of Russula can be associated with Monotropa uniflora in a single area (S. Yang & Pfister 2006). Hashimoto et al. (2012) found that in Pyrola asarifolia from Hokkaido, Japan, non-ectomycorrhizal fungi (Sebacinales-B) were associated with the plant as it germinated, rather like the association of orchids and fungi, while fungi associated with roots of the adult plant were different, being ECM fungi also associated with Betulaceae growing in the same area. There was geographical variation in the mycorrhizal associate (same family, the basidiomycete Atheliaceae) in Moneses uniflora (Hynson et al. 2015; see also Massicotte et al. 2008 for Pyroleae).
Bougoure et al. (2007) detail the variety of ERM fungi associated with Vaccinium and Calluna - some may be ECM, although the distinction between the two mycorrhizal types is very slight (see above). Selosse et al. (2007a) described the association of Sebacinales, a "basal" order of basidiomycetes, with Ericaceae. They found that the non-mycorrhizal Sebacinales group A were largely associated with Arbutoideae, Pyroloideae and Monotropoideae, all now in the same immediate clade, as well as with fungi that were ectomycorrhizal or endophytic, while Sebacinales group B, in a major clade sister to the first and often ECM fungi, were associated with members of Ericoideae, Styphelioideae and Vaccinioideae; the fungi of Harrimanelloideae and Cassiopoideae are unknown (see also Setaro et al. 2006, 2008; Selosse & Weiß 2009; Selosse et al. 2009; Weiß et al. 2009, esp. 2011). Basidiomycete associates may be proportionally particularly common in Vaccinioideae (Bougoure et al. 2007; Setaro et al. 2006, 2008), and they are also common in myco-heterotrophic Monotropoideae (Hynson & Bruns 2010).
As sampling of tropical montane and southern hemisphere Ericaceae improves, we may expect to find more variation in Ericaceae-fungal relationships. Thus plant-fungal relationships in Argentinian species of Galtheria differs from those in the northern hemisphere Gaultheria (Bruzone et al. 2013), although Setaro and Kron (2011) found that some clades of Sebacinales were found on both North and South American Vaccinieae. (Andean Orchidaceae and Vaccinieae growing together were associated with different but closely related clades of Sebacinales - Setaro et al. 2013.) Fungal sheaths have been reported from a number of Vaccinieae (e.g. Setaro et al. 2006; Vohník et al. 2012), the so-called "cavendishioid" (see above) and "sheathed ericoid" mycorrhizae. Ascomycetous dark septate endophytes are found in the roots of alpine Ericaceae from the Rocky Mountains and also other plants from such habitate (Stoyke & Currah 1991).
Complex associations are formed. In western North America the arbutoid madrone, Arbutus menziesii, is a common subordinate tree in forests with ectomycorrhizal (ECM) Fagaceae and Pinales, occupying over 3.9x106 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). Taxa like A. menziesii resprout after fire, and they can be a source of fungal inoculum for associated Pinaceae, so facilitating their regeneration (Kennedy et al. 2012 and references); "C[omarostaphylis] arbutoides is a refuge plant for ectomycorrhizal fungi as it shares these fungi with ectomycorrhizal tropical trees such as Quercus costaricensis" (Kühdorf et al. 2015: p. 110). The ascomycete Rhizoscyphus ericae is a very common associate of the hair roots of North Temperate Ericaceae; this fungus can also be an ECM associate of Pinus growing with Ericaceae (Read 1996; Grelet et al. 2010; see also Villarreal-Ruiz et al. 2004), and it also forms mycorrhizal associations with Jungermanniales-Schistochilaceae and other leafy liverworts, often colonizing the rhizoids (Duckett & Read 1995; Upson et al. 2007; Pressel et al. 2008). Other ascomycetes are also involved, including Cenococcum and Geomyces.
Rinaldi et al. (2008) suggested that the diversity of fungi associated with Ericaceae may not be very high, but their figure of 15 species is a gross underestimate, more species than this being associated with Arbutus menziesii in a single site in Oregon and about the same number being found on three species of Ericaceae from Alaska (Kennedy et al. 2012; Walker et al. 2011); at least 150 species of fungi is the estimate in van der Heijden et al. (2014). The specificity of Arctic ERM fungi, at least, is low (Timling & Taylor 2012), and species of tropical American Sebacinales can form associations with more than one species of Ericaceae (Kottke et al. 2008; see also Weiß et al. 2011). Indeed, more recent studies that focus on Sebacinales (e.g. Weiß et al. 2011) suggest that quite high numbers of species in that group alone grow with Ericaceae.
Interestingly, Enkianthus has arbuscular mycorrhizae of the Paris type (Abe 2005; Obase et al. 2013), i.e. it is a VAM fungus and lacks hair roots. I have seen few accounts of mycorrhizae in Clethraceae or Cyrillaceae, but the distinctive mycorrhiza/root associations of Ericaceae became established only after Enkianthus diverged from the rest. ?Arbutus
Endophytes are common (Petrini 1988); Ngugi and Scherm (2006) discuss the pseudoflowers formed by some fungal associates of Vaccinium.
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. Leaf morphology in Ericaceae is very variable. For instance, linear leaves are found in Diplycosia, Rhododendron, Empetrum and relatives, Killipiella (= Sphyrospermum), Agarista, etc. "Ericoid leaves" are quite common, but they include a variety of morphologies. Typically such leaves are scleromorphic, narrow (less than ca 5 mm wide) and more or less linear, and often with recurved margins, as is common in Erica itself. Leaves of Epacridoideae do not have recurved margins, but are otherwise scleromorphic and often more or less ericoid. 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 m.y.a. (Hou et al. 2015).
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, and some of the changes there were the same as in Vaccinium macrocarpon (Martínez-Alberola et al. 2013). For the loss of chloroplast genes in myco-heterotrophic Ericaceae, see Braukmann and Stefanovic (2012).
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). For the distribution of grayanotoxenes, see Zhou et al. (2012).
Rays in some styphelioids can 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, anomocytic stomata, etc..
Members of the outer 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). 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. The "petals" of Empetrum are free (Vislobokov et al. 2012). 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]). Viscin threads are well known as occurring in Rhodoreae, and have also been reported from Gaultheria (Lu et al. 2009). 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 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 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 a phenetic analysis of some staminal characters, see Vander Kloet and Avery (2007); 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), and for New World taxa, see Luteyn (2000, 2002).
Phylogeny. Early studies are summarized by Kron et al. (2002b), and the structure of the tree immediately above Enkianthoideae was initially labile with Pyroloideae, Monotropoideae and Arbutoideae, variously arranged and forming a basal grade. Freudenstein et al. (2010) in a comprehensive phylogenetic study of the family suggested relationships [Enkianthoideae [[Pyroloideae [Arbutoideae + Monotropoideae]] The Rest]] (see also Z.-Y. Liu et al. 2011, 2014; Hardy & Cook 2012; Braukmann & Stefanovic 2012: PHYA, see below); 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, myco-heterotrophism apparently having evolved several times, Feldenkreis et al. (2011) suggested the relationships [Enkianthoideae [Pyroloideae [[Monotropoideae + Arbutoideae] The Rest]]], and Schwery et al. (2014) found Arbutoideae to be embedded in a paraphyletic Monotropoideae. In Braukmann and Stefanovic (2012) Pterospora, on a very long branch, was sister to all other Ericaceae except Enkianthus.
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 (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]]].
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, 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, 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, see 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; Milne 2004: subsection Pontica paraphyletic, includes subgenus Hymenanthes; Kron 2003; limits of genus, sections; Brown 2003; Brown et al. 2006a, b, c: section Vireya = sect. Schistanthe, biogeography; Craven et al. 2008, 2011; especially Goetsch et al. 2005, 2011). In Ericoideae-Rhodoreae, polypetaly is sporadic.
Characters like rust preferences (Savile 1979b) had linked the wind-pollinated and florally very distinctive Empetraceae with Ericoideae in particular, furthermore, both Rhodoreae and Empetreae have the flavonoid gossypetin. Molecular data also strongly associate Empetreae with Ericaceae.
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). See Wagstaff et al. (2010) for 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 (Puente-Lelièvre et al. 2015). Epacris has turned out to be paraphyletic (Quinn et al. 2015).
There has been some much-needed phylogenetic work in Vaccinioideae. 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. The majority of Gaultheria s. str. 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). See Y.-H. Wang et al. (2015) for a morphological analysis of numerous leaf epidermal characters of Gaultherieae and comparison of the groupings obtained with those from other studies on the group. 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 developing (Kron et al. 2002a) and these for the most part cut across the limits of the larger genera, these being based on floral (= variants of a bird pollination syndrome) characters. 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 studies currently offer 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 (Powell & Kron 2002; Tsutumi 2011). New Guinean Dimorphanthera is sister to Paphia, both primarily New Guinean; the latter used to be included in Agapetes s.l., 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 study, there was extensive polyphyly in the larger genera. A world-wide study of nferior-ovaried Vaccinieae is needed if we are to understand their relationships.
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), Albrecht et al. (2010) and Puente-Lelièvre et al. (2015) suggest some realignments - see e.g. the last for useful discussion about the merits and demerits of being broad or narrow. As Puente-Lelièvre et al. (2015) note, the limits of Leucopogon will have to be restricted - or Styphelia expanded to include much of the tribe, and they take the latter option (see also Taaffe et al. 2001; Johnson et al. 2012).
Still more substantial changes to generic limits are occurring 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. In particular, Vaccinium section Hemimyrtillus may be sister to all other Vaccinieae (Powell & Kron 2002). 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.