LIGNOPHYTA

Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm² (to 5 mm/mm²).

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm³], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; 2C genome size 1-8.2 pg [1 pg = 10⁹ base pairs], whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

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

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; 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]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/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 scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, "C" with a single trace; A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: ?

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; palaeohexaploidy [gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] 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.

[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?

[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?

[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.

ASTERIDS / Sympetalae redux? / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate, if evident only early in development and then petals often appearing to be free); anthers dorsifixed?; (nectary gynoecial); style +, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.

[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].

Evolution. Divergence & Distribution. The age of the stem group asterids may be ca 128 m.y. before present, mid Early Cretaceous, the Ericales diverging soon afterwards (K. Bremer et al. 2004). Magallón and Castillo (2009) offer estimates of ca 105.3 m.y. for the divergence of Ericales from other asterids, 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., and Magallón et al. (2013) an age of around 87.5 m.y..

Endress (2011a) suggested that a key innovation at this level was sympetaly.

ERICALES Dumortier  Main Tree, Synapomorphies.

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; pollen tricolporate; duplication of the PI gene. - 25 families, 346 genera, 11,545 species.

Note: Possible apomorphies are now being added throughout the site; they are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because there is very considerable homoplasy for many characters, with with variation within and between clades. Furthermore, basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

Evolution. Divergence & Distribution.Sytsma et al. (2006) proposed that diversification began 109-103 m.y.a.. However, Wikström et al. (2001) thought that the stem group was 114-106 m.y. old, divergence not beginning until 92-85 m.y.a. (if the clearly misplaced Roridulaceae are ignored, Ericales also sister to Cornales). Anderson et al. (2005: asterids other than Cornales and Ericales not sampled) suggested figures of ca 109 m.y. for stem group Ericales, 103-99 m.y. for the crown group, while Janssens et al. (2009) dated the stem group to 123±10.5 m.y.a. and the crown group to 117±9.2 m.y.. Soltis et al. (2008: a variety of estimates) suggested a crown-group age of (126-)113(-85) m.y., while Magallón and Castillo (2009) estimated ca 105.35 m.y. for the stem group age and ca 98.85 m.y. for the crown group; comparable figures in Lemaire et al. (2011b) are (132-)128(-124) and (125-)118(-110) m.y. respectively.

The fossil Archaeamphora and assigned to Sarraceniaceae has been described from rocks about the same age as those in which Archaefructus was found, i.e. ca 124 m.y. before present (Li 2005), although this attribution needs to be confirmed. Otherwise the oldest fossils assignable to Ericales may be ca 90 m.y. old (Crepet et al. 2004; see also Martinez-Millán 2010).

Almost all families in Ericales had diverged by the early Eocene (50 m.y. before present: Sytsma et al. 2006). Indeed, in the late Cretaceous of E. North America there is a great diversity of fossil flowers that may belong to Ericales, the oldest being some 90 m.y. old (Crepet et al. 2001, 2004; see also Herendeen et al. 1999), and some of these 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.

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 it still shows extensive homoplasy.

Ecology. Today Ericales are an important component of the diversity of the understorey 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. However, this forest may have developed only early in the Tertiary (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), however, suggest that the ancestors of Ericales-Cornales grew under more temperate and boreal-arctic conditions 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. For all taxa in which they found two copies of the PI gene, have connate filaments, however, Primulaceae-Theophrastoideae, with connate filaments, had only a single copy; they think that the PI gene may have facilitated floral diversification (Viaene et al. 2009).

Chemistry, Morphology, etc. Recent 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 asterid I clade: Oxelman et al. 2004). 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 a summary of some chemical features of Ericales, see Grayer et al. (1999), for aluminium accumulation, see Jansen et al. (2004a, c), and for wood anatomy, see Lens (2005) and Lens et al. (2007b: optimisation of characters on to a tree with rather different topology than that below). For details of ovary placentation, see Ng (1991); although true parietal placentation occurs in the order (e.g. Ericaceae - Pyroloideae), most other reports are incorrect.

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 formed distinct clades, and Styracaceae + Diapensiaceae were moderately (D. Soltis et al. 2000, 2007) or poorly (Albach et al. 2001b) supported, even if many other relationships were unclear. Many taxa lack the mitochondrial coxII.i3 intron, but it is known from the Maesaceae (and Balsaminaceae - plesiomorphic presence?) clades and also from Ebenaceae and Styracaceae (Joly et al. 2001). 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. 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, and Mitrastemon was sister to most of the family except the Marcgraviaceae-Tetrameristaceae-Balsaminaceae 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 suggest that Balsaminaceae and Marcgraviaceae may be sister taxa. Within the polytomy, Theaceae s. str. may be sister to Symplocacaeae, this clade being in turn sister to Styracaceae and Diapensiaceae, in turn related to the Ericaceae-Sarraceniaceae clade - all these relationships had strong support in some analyses - while Pentaphylacaceae and the Primulaceae group were sister taxa (Geuten et al. 2004). However, only 16 terminals were included in their analysis, 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 and relatives linked with Sapotaceae and Ebenaceae. However, Hao et al. (2010) note that the mitochondrial atp1 gene in species of Ternstroemia was highly chimaeric, transfer from Vaccinium having occurred ca 15-50 m.y.a.; this caused some of the odd findings in the Schönenberger et al. (2005) study.

Takhtajan's Theaceae were more narrowly drawn than Cronquist's (c.f. Takhtajan 1997, Cronquist 1981), but both included Ternstroemia and relatives as a subfamily of Theaceae. However, 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; 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 Cardiopteridaceae and Gonocaryum in Savolainen et al. (2000a); the latter are strongly associated with Aquifoliales in a three-gene analysis (D. Soltis et al. 2000: see Kårehed 2001). However, Pentaphylax was placed sister to Ternstroemiaceae s. str. (Anderberg et al. 2001), and this seems to be its resting place for now.

Independently of such studies, Barkman et al. (2004, also 2007, there sampling poor) had suggested that Mitrastemonaceae belong to Ericales, a suggestion that is followed here (placing them next to Ericaceae and their immediate relatives in the tree is partly for convenience). The mitochondral genes cox1 and matR showed considerable divergence, but not the atp1 gene (Barkman et al. 2007).

Previous Relationships. The circumscription and relationships of Theaceae have been particularly problematic in the past. Theales of Cronquist (1981) included mostly families now in Malvales, Ericales, and Malpighiales, Theaceae alone including Bonnetioideae (Malpighiales-Bonnetiaceae) and Asteropeioideae (Caryophyllales-Asteropeiaceae). Taktajan's Theanae were largely equivalent (Takhtajan 1997). Ericales 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: Primulineae Burnett, Sarraceniineae Reveal - 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]]: myricetin +, ellagic acid 0; raphide sacs +, druses 0; vessels in radial multiples; paratracheal parenchyma +; ± branched sclereids +; lamina lamina supervolute, elongating in bud, with obscure abaxial lines, toothed; inflorescence racemose; abaxial surface of C with stomata; stamens = and opposite sepals, free from C, anthers (near) basifixed, thread-like structures along the stomium, filaments broad; gynoecial nectary 0; mucilaginous secretion in the ovary, style short, stigma little expanded; ovules bitegmic, micropyle endostomal.

Evolution. Divergence & Distribution. The common ancestor of [Balsaminaceae + Marcgraviaceae] dates to middle Palaeocene ca 58.9 m.y.a.; the two families diverged ca 48.1 m.y.a. (Janssens et al. 2009).

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. Geuten et al. (2006) suggest that heterotopic SEP3-like gene expression in bracteoles and calyx in extant members was present in the common ancestor of the group; the gene is normally expressed in the corolla and other inner whorls. Most taxa in this clade have more or less petal-like sepals, bracts or bracteoles - Tetramerista and Pentamerista, derived members of the clade, lack such expression patterns. Schönenberger et al. (2010: see also Schönenberger & von Balthazar 2010) suggest that thread-like structures bordering the stomium, of varying morphological nature, are an apomorphy for the whole clade. Schönenberger et al. (2010) also emphasize that the nectary is situated in the periphery of the flower, that there are mucilage cells in the flower, etc.

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).

Phylogeny. Monophyly of the clade containing these three families 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 it, see e.g. 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 - except perhaps when one examines floral development closely (see Schönenberger et al. 2010; Schönenberger & von Balthazar 2010). Indeed, some of the similarities between Pellicieraceae and Marcgraviaceae may be because they are both woody, and may in fact be synapomorphies 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, shrubs (small trees), perhaps epiphytic; (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; heterophylly common, lamina margin entire, with marginal to abaxial cavities (black dots); inflorescence a raceme, spike or umbel; flowers 4- or 5-merous, bracts abaxially ascidiate, nectariferous; K quincuncial, C ± connate; A 4-40; G [2-8], opposite ?, placentation very intrusive parietal, stigma?, dry; ovules many/carpel, inner integument ca 3 cells across; embryo sac long; fruit dehisces more or less irregularly, placentae fleshy; seeds many, small; exotestal cells ± enlarged, inner walls much thickened; endosperm slight, haustoria 0, cotyledons large to small; n = 18 [one count!].

7[list]/130: Marcgravia (60). New World tropics (map: from Heywood 1978). [Photo - Flowers] [Photo - Fruits]

• Marcgraviaceae are often lianas and can be recognised by their often rather fleshy leaves with indistinct venation and minute abaxial cavities; their inflorescences have abaxially ascidiate bracts that function as nectaries. The fruits, with numerous small seeds borne on a fleshy, colored placenta, are distinctive. Heterophylly is common in Marcgravia, the climbing form of the plant often having orbicular leaves adpressed to the trunk.

Evolution. Pollination Biology & Seed Dispersal. The prominent inflorescences with nectar secreted in the cup-shaped (ascidiate) bracts attract a variety of large pollinators including humming birds and bats (e.g. Dressler 1999; Tschapka et al. 2006). 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 bat pollinated and 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 bats (Lobova 2009).

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" - 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 vegetative anatomy, see Beauvisage (1920), for general information, see Dressler (2004), 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. In the rest of the family both synapomorphies and generic limits are unclear.

Synonymy: Noranteaceae Martius

[Balsaminaceae + Tetrameristaceae]: K petal-like, nectariferous; filaments postgenitally united; stylar canal +, 5-radiate; endosperm with micropylar haustorium.

Chemistry, Morphology, etc. For characters of this clade, see Schönenberger et al. (2010) and Schönenberger and von Balthazar (2010).

BALSAMINACEAE A. Richard, nom. cons.   Back to Ericales

Fleshy herbs, (woody); non-hydrolysable tannins, naphthoquinones +; cork?; vessels single; sclereids 0; petiole bundle arcuate; mucilage sacs +; plant usu. glabrous; leaves (opposite), lamina vernation involute, lacking obscure abaxial lines, (extrafloral nectaries +, sometimes as paired glands or foliaceous lateral flaps on leaf base/stem), petiole normal; inflorescence axillary, (bracteoles 0); flowers vertically monosymmetric, inverting during growth; K 3 (5), functionally abaxial sepal with prominent nectariferous spur (spur 0), C 5, when K 3, adaxial C often with a sepaloid keel, lateral petals connate in pairs (free); anthers connate and forming cap over stigma, (with trabeculae in loculi), filaments stout, partly connate apically; tapetal cells 2(-4)-nucleate; pollen grains intermixed with cellulose threads coming from cell walls and holding them to anther, with raphides, starchy, 3- or 4-colpate (porate), often rectangular in polar view, endexine lamellate; G [(4-)5], opposite petals, stigma fairly broad, wet; ovules 1-several/carpel, uni- to biseriate, (hemitropous), apotropous, micropyle endostomal, outer integument 4-10 cells across, inner integument 3-6 cells across, (unitegmic, integument ? cells across); embryo sac (bisporic, 8-nucleate [Allium type]), becoming very long; fruit an explosive capsule, septifragal, walls inrolling from base, or a drupe/non-explosive schizocarp [Hydrocera]; seed pachychalazal, exotestal cells only thickened, ("hairs" with spiral thickenings; mucilaginous), (sclerotic testa of 6-8 layers thickened cells, 5 layers unthickened - Hydrocera); endosperm also with chalazal haustorium, scanty, (xyloglucans +), cotyledons large, n = (3-)7-8(9)10+.

2[list]/1001: Impatiens (1000). Mostly Old World, Africa (esp. Madagascar) to mountains of S.E. Asia (map: from Hultén 1971; Meusel et al. 1978; Grey-Wilson 1980a; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011). [Photo - Flower.]

• Balsaminaceae are fleshy herbs with more or less translucent stems and usually spiral, toothed leaves. The flowers are strongly monosymmetric and nearly always have a spur on the adaxial sepal, but since the flower is held upside-down the spur is on the lower (abaxial) part of the flower. The anthers cap the gynoecium (until they are dislodged) and the style is at most short. The fruit is usually an explosively-dehiscent capsule with the walls inrolling from the base.

Evolution. Divergence & Distribution. Impatiens is a genus that is most diverse in tropical and subtropical montane forests. Stem Balsaminaceae are ca 48 millions years old, crown diversification (Hydrocera diverged) began ca 31 m.y.a., more diversification may have begun in the Early Miocene ca 22.5 m.y.a., but the speciation rate much increased in the early Pliocene within the last 5 m.y., when climate change caused much population fragmentation, isolation, and migration (Janssens et al. 2009).

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).

Balsaminaceae are vegetatively rather 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).

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).

The flowers are protandrous. The abaxial-lateral sepal pair (non-inverted orientation) 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 five sepals there are only 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 cellulose threads produced as the anther walls break down and then retract hold the exposed pollen in a basketwork of these threads over the anther (Vogel & Cocucci 1988). 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 considerable platicisty 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). The fruit type of Hydrocera is unclear (see Wood 1975), and it may be a septicidal capsule or a several-seeded drupe; the latter is described by Grey-Wilson (1980a); see Leins (2000) for the fruit dehiscence of Impatiens. The micropylar haustorium is massive and may invade the funicle and even the placenta.

For some embryology, see Dahlgren (1934) and Narayana (1963), for information on floral anatomy, etc., see Grey-Wilson (1980b) and on the gynoecium, see Shimizu and Takao (1982, 1985), for a revision and more of the African taxa, Grey-Wilson (1980c), for cellulose threads in the anthers, see Vogel and Cocucci (1988), for ovule variation and seed anatomy and development, Guignard (1893) and Boesewinkel and Bouman (1991), for seed morphology, Utami and Shmizu (2005: variation considerable), for floral development, Caris et al. (2006a), for pollen morphology and evolution, see Janssens et al. (2012: African species more often porate, Asian species 4-aperturate), and for general information, see Fischer (2004a) and Leins and Erbar (2010).

Phylogeny. Hydrocera and Impatiens are clearly sister taxa (Yuan et al. 2004; esp. Janssens et al. 2006a). Taxa of Impatiens with five 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) for relationships.

Classification. The current infrageneric classification of Impatiens needs complete overhaul (Janssens et al. 2006a).

Previous Relationships. Balsaminaceae were included in Geranianae - Rosidae by Takhtajan (1997).

Synonymy: Hydroceraceae Wilbred, Impatientaceae Barnhart

TETRAMERISTACEAE Hutchinson   Back to Ericales

Evergreen trees; chemistry?; intervessel pitting opposite-alternate; petioles short; bracteoles rather large, ± caducous; K with adaxial nectar glands; ovule 1/carpel, ?orientation; fruit indehiscent.

3[list]/5. W. Malesia, Central and N. South America. Two groups below.

1. Pelliciera Bentham   Back to Ericales

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, large; bracteoles petal-like; A extrorse, anthers >4.5 cm long, ["very long"], connective prolonged into a point; pollen strongly verrucate; G [2], style long, stigma bifid, punctate; ovule pendulous, campylotropous; fruit ± dry, K and C caducous; seed coat?; endosperm 0, 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] [Photo - Fruit]

• Pelliciera is a tree in mangrove vegetation that may be recognised by its long, pointed terminal buds, more or less pseudoverticillate and toothed leaves with very short petioles and asymmetric bases, and their large, axillary flowers with conspicuous petal-like bracteoles. The adaxial glands on the sepals and the large, sharply-pointed, single-seeded fruits are also distinctive. Fluted buttresses formed by vertical series of adventitious roots form a conical mantle at the base of the trunk.

Evolution. Divergence & Distribution. From records of fossil pollen, 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). For the evolution of the mangrove habitat, to which Pelliciera is restricted, see Rhizophoraceae.

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"; flowers 4- or 5-merous (bracteoles persistent); K and C similar; filaments slightly connate at the base; G [4, 5]; ovule basal, ?epitropous; fruit a berry; testa several layers thick, walls thickened; endosperm copious, cotyledons small; n = ?

2/4. Malesia (Tetramerista), Venezuelan Guyana (Pentamerista).

• The two genera are rather small woody plants that can be recognised by their spiral, short-petiolate leaves with indistinct venation and marginal glands; there are clearly three separate bundles at the base of the petiole. The flowers are rather small, the sepals and petals being rather similar and spreading; at least the sepals have glands on their adaxial surfaces.

Chemistry, Morphology, etc. There are no reports that Pelliciera accumulates aluminium, again unlike Theaceae s.l., in which it has often been included. Pelliciera was compared with Marcgraviaceae by Beauvisage (1920); details of wood anatomy suggest relationships with Tetrameristaceae (Baretta-Kuipers 1976). Nodal anatomy is extrapolated from petiole scars; it is probably unilacunar. 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. Nodal anatomy of [Tetramerista + Pentamerista] was extrapolated from the petiole scars. In Tetramerista there are glistening dots on the adaxial surface of both calyx and corolla. The embryology, morphology and anatomy of Pellicieraceae s.l. are poorly known

For general information, see Kubitzki (2004b).

Previous Relationships. Tetrameristaceae s. str. were placed in Theales by Takhtajan (1997). 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.

[[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.

[Polemoniaceae + Fouquieriaceae]: cork cambium outer cortical; inflorescence terminal, determinate; K with scarious margins; A adnate to the corolla, anther thecae largely separate [septum 0]; gynoecial nectary +; G [3], style hollow, style/stigma branched; ovules in two ranks, apotropous; fruit a loculicidal capsule, seeds on central columella, sepals persistent in fruit; seeds winged; endosperm scanty; mitochondrial coxII.i3 intron 0.

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?), 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; stomata paracytic); leaves opposite to spiral (palmate, pinnate), 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; stamens = and opposite sepals, inserted at different levels or filaments of different lengths, anthers usu. ventrifixed; pollen pantoporate/stephanocolporate; nectary usu. not vascularized; G [(2-4)], median member adaxial, stigma dry, decurrent the length of the arms; ovules 1-many/carpel; 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 - two subfamilies below. N. temperate, W. North America, South America (map: from Hultén 1971; Meusel et al. 1978).

1. Polemonioideae Arnott

Mostly ± desert-dwelling herbs (subshrubs); (flowers monosymmetric, median petal ab- or adaxial); C veins usu. free or connected well above the base; filaments usu. merged with corolla; integument 3-20 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 +): flowers large; (flowers 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; leaves very dimorphic, as persistent branched spines on long shoots, deciduous and unlobed on short shoots; pollen stephanocolporate, exine coarsely verrucate; seeds few; n = 9, chromosomes 2-4 µm long.

1/1 [list]: Acanthogilia gloriosa. Baja California.

• Polemoniaceae are herbs, or sometimes shrubs or lianas, that may be recognised by their often opposite leaves; the plant may smell unpleasant. The calyx is more or less connate, the units of which it is made up often having a green central portion, the rest being whitish. The corolla is strongly sympetalous and the five stamens are frequently inserted at different levels in the tube (not in Loeselia, Collomia, Microsteris, etc.) and/or are of different lengths. The style is usually three-lobed, the fruit is a capsule and the seeds are mucilaginous when wetted.

Evolution. Divergence & Distribution. Gilisenium hueberi, perhaps close to Gilia, is known from the middle Eocene of Utah (Lott et al. 1998).

Schönenberger (2009) lists other features that may be apomorphies for Polemoniaceae.

Pollination Biology & Seed Dispersal. For floral variation in the context of flower 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.

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 some embryology, see Kapil et al. (1969), for inflorescence morphology, see Weberling (1989), for pollen, see Monfils and Prather (2004, and references), for seed morphology, see Johnson et al. (2004), for floral development, see Schönenberger (2009), 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 relative to the other two subfamilies 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 and xeromorphic, with long and short shoots; flavonols only, ellagic acid, route I secoiridoids +, myricetin 0; cuticle wax crystalloids 0; leaves heteromorphic, lamina margins entire, petiolar spines on long shoots; K ± scarious, separate; A 10(-23), only very shortly adnate to corolla; nectary tissue in base of ovary, vascularized; stigmas punctate; ovules 6-20/carpel, apotropous, bitegmic, micropyle endostomal, outer integument 3-4 cells across, inner integument (4-)7-8 cells across; testa and tegmen multiplicative, becoming crushed, testa hypodermis with banded thickenings; endosperm with micropylar and chalazal haustorium; n = 12.

1[list]/11. S.W. North America (map: Meusel et al. 1978). [Photo - Habit] [Photo - Branch] [Photo - Flowers]

• Fouquieriaceae are often little-branched shrubs with entire, spiral leaves, well developed short shorts, and petiolar spines on the long shoots. The flowers have free almost scarious sepals but a strongly connate corolla; the ten or more stamens are free from the corolla. The style is three-lobed.

Evolution. Divergence & Distribution. Schönenberger (2009) lists other features that may be apomorphies for Fouqueriaceae, including the fact that sepals and petal lobes are similar both in size and in histology.

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 asyymmetric 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).

For ovule morphology and embryology, see Mauritzon (1936b), also Corner 1976. See Kubitzki (2004b) for general information.

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; (cristarque cells +); petiole anatomy of 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 +; inflorescence various, often racemose, pedicels articulated; flowers large; K (2-)4-6(-12), variously arranged, connate or not, valvate; C 3-10(-16), (free); A many [15-1200], initiated as ring primordium, development centrifugal (centripetal), in concentric series or not, connate or not, latrorse, filaments not articulated, outer A staminodial; tapetum amoeboid, cells binucleate; pollen tricolpate, trinucleate; nectary +; G inferior, [2-8], opposite sepals, style short/0, stigma ± capitate (punctate, divided), wet or dry; ovules 1-many/carpel, (apical or basal), bitegmic, micropyle endostomal, outer integument 6-18 cells across, inner integument 3-7 cells across; megaspore mother cells several, 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]/340 - five groups below. Tropical, especially America and W. Africa.

1. Napoleonaeoideae Bentham

Secondary xylem with crystal chains; leaves distichous, lamina supervolute, often with glands abaxially at the base, margin serrate, stipules +/0; G initiated before A; C valvate, connate, plicate; A adnate to C, 2 whorls of staminodia, anthers long, (10, paired, opposite C, extrorse, monothecal - Napoleonaea, pairs alternating with staminodia); G opposite petals, style 0, stigma broad, pentagonal, flat; ovules 4/carpel, collateral in pairs [Napoleonaea], outer integument 5-7 cells across, inner integument 5-7 cells across, endothelium 0, lateral parietal cells; fruit a 1-several seeded drupe; embryo curved; n = 16.

2/11. W. tropical Africa (map: from Liben 1971b; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]

Synonymy: Napoleonaeaceae A. Richard

[Scytopetaloideae [Lecythidoideae [Barringtonioideae + Foetidioideae]]]: ?

2. Scytopetaloideae O. Appel

Plants Al-accumulators; nodes?, traces running two internodes before entering leaves; sclereids +; ?crystal chains; leaves 2-ranked, stipules +, minute; pedicels articulated; K connate, (C 0); A adnate to C, staminodes 6-28, connate, corolla-like, A basally connate, adnate to staminodes; tapetum cellular; (pollen tricolporoidate); (nectary 0); G superior (half superior), style relatively long, slender, stigma punctate; ovules with long micropyle, endothelium +, podium long, thin; fruit a capsule or indehiscent; seeds often 1, ± hairy, ruminate (not - Oubanguia), endosperm +, hemicellulosic, (embryo J-shaped); n = 11, 18, 21.

6/21. Africa, South America (N.E. Brasil) (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; (flowers monosymmetric via androecium); A with a basal ring, filaments contracted at the apex; pollen tricolp/oroid/ate, (fodder pollen +); nectary 0/+; style short (long); ovules (exostomal - Couroupita), lacking endothelium; fruit operculate (indehiscent); seed with swollen funicle, or aril (= wing), or neither; 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). [Photo - Flower, Fruit, Flower, Fruits.]

Synonymy: Gustaviaceae Burnett

[Barringtonioideae + Foetidioideae]: cortical bundles inverted; leaves supervolute; fruit indehiscent.

4. Barringtonioideae Beilschmied

Secondary xylem without crystal chains; leaves spiral, vernation?, glands in the stipular position; A with a basal ring; pollen syntricolpate, strong colpus margin ridge; nectary annular; style long; ovules lacking endothelium (+); fruit usu. 1-seeded; embryo hypocotylar or with long radicle and leaf-like cotyledons; n = 13.

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]

Synonymy: Barringtoniaceae F. Rudolphi, nom. cons.

5. Foetidioideae Engler

Secondary xylem with crystal chains; leaves elongating in bud; K woody, valvate, C 0; A free, introrse; nectary indistinct; style 3- or 4-fid; ovules in two rows, with endothelium; n = ?

1/18. E. Africa (Tanzania, Pemba), Madagascar, Comores, Mauritius and Reunion.

Synonymy: Foetidiaceae Airy Shaw

• Lecythidaceae are difficult to characterise. They are usually trees with spiral leaves in tufts at the ends of the branches, or the leaves are two-ranked and scattered along the stem. The leaves are minutely stipulate and/or the margins are serrate. The flowers are often large and have free petals or what appear to be petals. The numerous (up to 1200!) stamens are free to connate; when connate, they may form a complex, cochleate structure that obscures the style and top of the ovary. The ovary is inferior and crowned by the often persistent valvate calyx.

Evolution. Pollination Biology & Seed Dispersal. Monosymmetric Lecythidoideae are pollinated largely by euglossine bees and several taxa have fodder pollen 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); details of floral development, incuding the origin of monosymmetry, are to be found placed in a phylogenetic context in Tsou and Mori (2007). Monosymmetric flowers of Lecythidoideae 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 hood into which bees force their way. A rather close evolutionary association between euglossine bees and these monosymmetric Lecthyidoideae 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. 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 really 1:1. 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 that are involved in the expansion of the young leaves (Paiva 2012); are these glands of Barringtonia and the teeth of other Lecythidaceae 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. There are also differences in how carpel orientation is shown - opposite the petals (Ronse de Craene 2010, 2011) or opposite the sepals (Frame & Durou 2001).

The exact nature of the petal-like structures in the flower, especially in those of Napoleonaeoideae and Scytopetal-likeeae, is still a matter of 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; more developmental studies on Napoleonaeoideae 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.) Androecial variation in Lecythidoideae is extreme; the pollen may be heteromorphic. There is both centripetal and centrifugal androecial development in the family (ref.?). Are there apotropous ovules (Baillon 1877)?

For more information, see van Tieghem (1905b, as Rhaptopetalaceae, inc. anatomy), see also Appel (1996, 2004), Letousey (1961), all as Scytopetalaceae, general. For general information on Napoleonaeoideae, see Liben (1971a) and Prance (2004), both as Napoleonaeaceae, also Venkateswarlu (1952: embryology). See Tobe and Raven (1983a: embryology, general), Morton et al. (1997c, esp. 1998: phylogeny), Vijayaraghavan and Dhar (1976: embryology, Scytopetaloideae), Tsou (1994: ditto, Lecythidoideae), Endress (1994b: floral morphology) and Tsou and Mori (2002: seed coat anatomy in Lecythidoideae; Takhtajan (1992) includes information on endothelium and testa vasculature , and also Prance and Mori (2004: general), most are Lecythidaceae s. str. See also Scott Mori's The Lecythidaceae Pages (Lecythidoideae only).

Phylogeny.The relationships of Asteranthos have long been uncertain (e.g. Prance & Mori 1979; Mori & Prance (1990). The set of relationships [Napoleonaeoideae [Scytopetaloideae [Lecythidoideae [Planchonoideae + Foetidioideae]]]] were recovered by Morton et al. (1998) and Mori et al. (2007). Crateranthus rbcL sequences have not been obtained, but it is placed with Napoleonaea in joint analyses. In chemistry, morphology, etc., including androecium, Asteranthos is similar to Napoleonaeaoideae (but c.f. style, endosperm), yet sequence data align it with Scytopetaloideae...

Within Lecythidioideae, 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 includes the [Allantoma + Cariniana decandra] clade (= Allantoma s.l., see 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 [asterid I + asterid II] clade), but the current phylogeny does not yet provide strong support for this hypothesis. However, there is strong support for the hypothesis that the plesiomorphic condition for the flowers of Lecythidoideae is 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 (in this case, 52%) containing only six species (Huang et al. 2011).

Classification. Scytopetaloideae plus plus Asteranthos are placed in 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. Lecythidoideae were monographed by Prance and Mori (1979) and Mori and Prance (1990). For a revision of Foetidia, see Prance (2008).

Previous Relationships. Scytopetalaceae were considered quite distinct until recently (e.g. Cronquist 1981, in Theales; Takhtajan 1997, in Ochnales [both Dilleniidae]) - C valvate, basally connate or nor, calyptrate and deciduous.

[[Sladeniaceae + Pentaphylacaceae], [Sapotaceae [Ebenaceae + Primulaceae]], [Mitrastemonaceae, Theaceae, [Symplocaceae [Styracaceae + Diapensiaceae]], [[Sarraceniaceae [Roridulaceae + Actinidiaceae] [Clethraceae [Cyrillaceae + Ericaceae]]]]]: endothelium?

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; C ± campanulate, only basally connate, petals fairly small [1³ cm long]; 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 capsule, columella persistent, K persisting; endosperm +, embryo long.

Evolution. Divergence & Distribution. 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.

Baeuvisage (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 were included in Theales, and adding morphology 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; /APweb/ versions 1-3), and A.P.G. II (2003) suggested as an option recognising three families, i.e. separating Pentaphylacaceae and Ternstroemiaceae, as well as 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, part of the old Theaceae.

Previous Relationships. See Theaceae for a family that largely included this 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]; lamina toothed (not); inflorescences axillary, cymose; (C connate – Ficalhoa); A 10-15, anthers opening apically (sagittate – Sladenia), exothecium thickened; microsporogenesis successive [tetrads tetragonal]; G [3, 5], placentae apical or placentation axile, placentae bilobed, style short, with 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, 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).

• Sladeniaceae are evergreen trees with serrate, exstipulate leaves and distinctive axillary cymose inflorescences. The flowers are small, being less than 5 mm long.

Evolution. Divergence & Distribution. The wood of extant Sladenia is distinctive, and matches fossil wood from the ?Cretaceous-Albian/Cenomanian of northern Sudan remarkably closely (Giraud et al. 1992).

Chemistry, Morphology, etc. Sladenia is poorly known. Its pollen and wood anatomy is very much that of Pentaphylacaceae, but there are no sclereids. Ficalhoa is even more 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; inflorescence of axillary flowers or fasciculate; corolla greenish to yellowish [to orange-red in Balthazaria]; 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]/337, three groups below. Tropical and subtropical, but few in Africa.

1. Pentaphylaceae

Chemistry?; druses 0; buds perulate; stomata mostly paracytic; lamina margins entire; flowers in axils of reduced leaves; A 5, filaments very broad, narrowed and incurved apically, thecae each opening by a valve that lifts up; pollen smooth, tectum thin, columellae poorly developed, endexine thick; G [5], opposite petals, stigmas shortly radiate; ovules 2/carpel, apical, outer integument ca 3 cells across [check], crassinucellate; fruit a capsule, midrib ["teeth"] separating from rest of valves, endocarp cells transversely elongated; seeds flattened, exotestal cells slightly thickened, elongated, mesotestal cells large, ± thin-walled; endosperm development?, slight, cotyledons longer than the radicle; n = ?

1/1: Pentaphylax euryoides. Kwangtung and Hainan to Sumatra, scattered.

[Ternstroemieae + Frezierieae]: ellagic acid +, iridoids 0; (pits vestured); pith often with diaphragms; sclereids +; stomata anomocytic; perulae 0; filaments to 2x longer than anthers, latter variable in length, connective usu. prolonged; fruit ± fleshy; mesotestal cells also lignified, ± crystalliferous; endosperm +, ?nuclear, radicle longer than cotyledons, incumbent.

2. Ternstroemieae Candolle

Sclereids much branched; leaves pseudoverticillate, lamina often with black spots, margins entire to crenulate; flowers single from axils of reduced leaves; K opposite petals, filaments shorter than anthers; G [2-3], (inferior - Anneslea); ovules 4-12/carpel, apical, outer integument 6-9 cells across; fruit irregularly dehiscing; seeds few, ³3 mm long, brown, sarcotestal [either exotesta or pockets of fleshy cells on either side of seed], exotesta 10 cells across, sclerified 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; M. Sosef, pers. comm.). [Photo - Flowers & Fruits © Nick Turland.]

Synonymy: Ternstroemiaceae Candolle

3. Frezierieae

(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 fasciculate or flowers single, at least some from axils of expanded leaves; (K connate; C urceolate [Freziera]); 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), also styluli +; ovules 4-many/carpel, outer integument 3-4 cells across; fruit a berry (drupe); seeds (1-)many, <4(-6) mm long, brown or black, inner walls of exotesta thickened and lignified or not, sclerified mesotesta 1-5 cells across; (embryo curved); n = 12, 13(?), 15, 18, 21(commonest)-23, etc.

9/233: Adinandra (80), Eurya (75), Freziera (57). 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.]

• Pentaphylacaceae are shrubs or trees that often have two-ranked, serrate leaves which may remain rolled up as they elongate, so the lower surface of the blade has longitudinal markings. The flowers are medium-sized to smallish, and the numerous stamens usually have short filaments and long, basifixed anthers. The fruit, which has a persistent calyx, is usually a berry, and the embryo is curved. Ternstroemia, with its pseudoverticillate and usually entire leaves, can look rather unlike other Pentaphylacaceae.

Evolution. Divergence & Distribution. 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).

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. The flowers are basically single in the axils of reduced leaves; if the shoot on which they are borne is very much reduced, then the inflorescence is fasciculate. When the shoot of Pentaphylax does not develop expanded leaves after the flowers appear, it appears that the inflorescence is racemose. Although the leaves 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. The pericylic sheath of Pentaphylax consists of fibres alternating with lignified parenchymatous cells (Beauvisage 1920). Overall, however, Pentaphylax is poorly known; details of the ovules are taken from Mauritzon (1936). Cleyera (Freziereae) lacks pericyclic fibres in the petiole. It, and also Eurya (for which see Brown 1938), secrete nectary from the basal part of the ovary wall. Freziera shows considerable variation in nodal anatomy, stomatal morphology, seed type and pollen surface (Weitzman 1987). Pentaphylacaceae 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 floral development, see Tsou (1995) and Zhang et al. (2007), for pollen, see Lobreau-Callen (1977) and Wei (1997)

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: largely Theaceae only also 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 has 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, Strasbugeriaceae, etc.

[Sapotaceae [Ebenaceae + Primulaceae]]: ellagic acid 0; ovules apotropous.

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, 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 +, secreting gutta; sclereids +; hairs brownish, T-shaped, arms unequal or not, unicellular (not in Delpyodon); leaves (two-ranked, opposite), lamina vernation conduplicate, margins entire (toothed), secondary veins often rather close, ?stipules; (plants di- or monoecious), inflorescences cymose, fasciculate, pedicels not articulated; flowers (anisomerous), K ± connate at base, C 4-18, (variously lobed or divided), stamens = and opposite C lobes, introrse to extrorse, staminodes +, ± petal-like, opposite K; tapetum 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, apotropous, 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).

53[list]/1100. Pantropical.

1. Sarcospermatoideae Swenson & Anderberg

Leaves ± opposite, (stipels +), stipules cauline; inflorescence axis apparently well developed [actually a reduced branch]; staminodes short, broad, scale-like; G 1[-2], style stout; endosperm 0.

1/6. Indo-Malesia (map: from Aubréville 1964).

Synonymy: Sarcospermataceae H. J. Lam

[Sapotoideae + Chrysophylloideae]: stipules cauline/0; stamens = and opposite to 2x (-6x) C lobes, staminodes often ± petal-like, opposite sepals (0); G 1[2-14(-30)], opposite sepals; (amyloid in seed [xyloglucans] +).

Throughout the tropics (map: from Aubréville 1964).

2. Sapotoideae Eaton

(K in two whorls of 2-4 valvate members in each, petals with three segments); 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); endosperm copious, cotyledons foliaceous, radicle exserted.

25/550: Pouteria (235), Chrysophyllum (80), Planchonella (70), Micropholis (38). Pantropical.

• Sapotaceae are woody plants that may be recognized by their rather small, naked terminal buds with adpressed, brownish, often T-shaped unicellular hairs, axillary branches often with prominent, basal prophyllar buds and then long internode(s), leaf blades that tend to have rather closely parallel secondary veins and entire margins, and petioles that are bottle-shaped - i.e. swollen at the base - when fresh. The twigs usually exude copious gutta. The flowers, with their persistent sepals and often protruding style, are distinctive, as are their seeds, which are large and have a thick, shiny, brown testa with a very large, pale-colored hilum.[Photo - Collection], [Photo - Fruit].

Evolution. Divergence & Distribution. Bartish et al. (2010) discuss the historical biogeography of Chrysophylloideae, and find long distance dispersal to dominate when explaining the current distribution of the group. Initial diversification perhaps occurred in Africa in the Campanian 83-73 m.y.a., although much diversification in the subfamily in Tertiary. 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.). Dating in Chrysophylloideae suggests that the largely New Caledonian Niemeyera clade reached that island in the latter part of the Oligocene (Swenson et al. 2008c, c.f. Ladiges & Cantril 2007). In Sideroxylon (Sapotoideae) there seems to have been ancient hybridisation 43-36.6. m.y.a. between a basically African clade and a basically American clade. The descendents, previously segregated as Nesoluma and found on very young islands in the Pacific, may have persisted hopping from island to island ever since (Smedmark & Anderberg 2007; for other taxa behaving similarly, see Hillebrandia [Begoniaceae], Psiloxylum [Myrtaceae], etc.).

Seed Dispersal. For the cautionary tale of the dodo and the tambalacoque, see Herhey (2004).

Economic Uses. Chicle, a complex rubber, 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.

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) for a good summary of floral variation. Floral variation is considerable and most characters are very homoplasious (e.g. Swenson et al. 2008a, b, c). 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) suggest that the staminodes common in Chrysophylloideae, but derived within the clade, are perhaps 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. Amyloid is also known from the seeds of Omphalocarpum, a clade that is close to sister to the rest of Chrysophylloideae (see Kooiman 1960).

The mitochondrial coxII.i3 intron is absent in Chrysophyllum, at least (Joly et al. 2001).

For more information on Sapotaceae, Ebenaceae, etc., see Franceschi (1993), and Ng (1991). For general information, see Pennington (1991, 2004).

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, and also a conspicuous hilar scar; the genus was placed in Sideroxyleae by Pennington.

Within the rest of the family there are two major clades, the (Isonandreae + Mimusopeae + Sideroxyleae) and (Chrysophylleae + Omphalocarpeae). Xantolis may be sister to the latter clade (Anderberg & Swenson 2003). In a combined molecular + morphological analysis and after successive weighting the same three 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 listed above (Swenson & Anderberg 2005). Morphological characters are highly homoplasious, more so than the molecular data, and characters for the subfamilies are hard to come by. See Smedmark et al. (2006) for general discussion of relationships and character evolution in Sapotoideae. Swenson et al. (2007a, 2008a) discuss generic limits in Australasian members of Chrysophylloideae (the whole lot are monophyletic); 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). See Swenson et al. (2007b) for Planchonella and Swenson et al. (2008c) for its sister group, the largely New Caledonian Niemeyera complex. 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. Clade limits in e.g. New Caledonian Sapotaceae are now becoming clear enough so that species can be described in appropriate genera (Swenson et al. 2008b, esp. c).

Classification. For a checklist and bibliography, see Govaerts et al. (2001).

[Ebenaceae + Primulaceae]: ovules bitegmic, inner integument thicker than the outer.

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; stamens adnate to corolla, in two series, basifixed, anthers long; style ± divided; ovules 2/carpel, pendulous, apotropous; fruit a berry, K persistent; testa vascularized; endosperm copious, mannose-rich polysaccharides +, radicle long.

4[list]/548, two subfamilies below. Tropical (to temperate).

1. Lissocarpoideae Wallnöfer

Iridoids, etc.?; cork?; (vessel elements with scalariform perforation plates); (petiole bundle arcuate but with recurved edges and wing bundles); stomata anomocytic and cyclocytic; plant glabrous; flowers axillary, or inflorescences subfasiculate; bracteoles large, apical; flowers 4(-5)-merous, C with an 8-lobed corona; A 8, filaments connate, anther connective prolonged; pollen 3-porate, 40-70 µm across, psilate; nectary?; G inferior, [4], stigma clavate, hairy apically; ovule morphology?; seeds 1-2; testa?; endosperm very hard; cotyledons foliaceous; n = ?

1/8. Tropical South America (map: from Wallnöfer 2004b).

Synonymy: Lissocarpaceae Gilg, nom. cons.

2. Ebenoideae Thorne & Reveal

Saponins, C-30 oxidised triterpenes, naphthoquinone derivatives of 7-methyljugone and plumbagin, flavonols, leucodelphinidin, myricetin +, ellagic acid 0; (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; (C valvate), nectary 0; staminate flowers: A (3-)12-20(-many), anthers extrorse, often hairy; pollen 25.9±6.4 µm across, infratectum granular; pistillode +; carpellate flowers: staminodes + (0); G [2-8], opposite C or K, loculi often divided, stigmas little expanded, dry; ovule often 1/carpel, 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, (vascularized), (radicle surrounded by ingrowth of coat [not in 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.

3/540: Diospyros (500+). Tropical (to temperate) (map: from Morley & Toelken 1983; Wickens 1976; White 1988). [Photo - Carpellate flower, Fruit, Collection.]

Synonymy: Diospyraceae Vest, Guaiacanaceae Jussieu, nom. illeg.

• Ebenaceae are woody plants that may be recognised by their usually two-ranked, entire leaves that may have flat, dark-colored glands on the lower surface of the blade. The corolla is contorted. In Diospyros and relatives the flower buds have adpressed brown indumentum (sometimes of T-shaped hairs) and are distinctively pointed; the calyx is usually much accrescent in fruit. The bark (including that of Lissocarpus), even of twigs, is black and very hard, its undersurface is yellow; the heartwood is also black and the leaves, too, may dry blackish - because of the naphthoquinones that are common in the family. The flowers of Lissocarpa are glabrous and have a rather narrow sympetalous corolla and an inferior ovary below which are two well-developed bracteoles.

Evolution. Divergence & Distribution. Fossil flowers and associated leaves (Austrodiospyros) are known from the mid Eocene of southeastern Australia (Basinger & Christophel 1985).

Duangjai et al. (2009) noted that there were four separate lineages of Diospyros in New Caledonia.

Ecology & Physiology. Diospyros is about the most diverse genus in West Malesian t.l.r.f. (Davies et al. 2005).

Chemistry, Morphology, etc. Ellagic acid may occur in Ebenaceae-Ebenoideae (Bate Smith 1962). Since I do not know of details the chemistry of Lissocarpoideae, whether the presence of ellagic acid or naphthoquinones is a synapomorphy of Ebenaceae as a whole or just part of them remains to be established. 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. 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 Diospyros and relatives and carpel orientation, see Baillon (1891), Eichler (1875) and Le Maout and Decaisne (1868), for some seed anatomy, see Quisumbing (1925). For general information, see Wallnöfer (2001, 2004a), and on this and putatively related families, see Francheschi (1993). Some information on Lissocarpa is taken from Schadel (1978: leaf morphology) and Wallnöfer (2004a, b), but that genus is poorly known.

Phylogeny. 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 are unclear. Geeraerts et al. (2009) suggest apomorphies - especially palynological - for these genera, while Duanjai et al. (2009: eight genes, 119 species) provides a more detailed phylogeny of Diospyros itself with good Bayesian support for relationships along the backbone of the tree.

Previous Relationships. Lissocarpaceae have often been placed in or close to Ebenaceae, but they were unassigned in A.P.G. (1998). Rather degraded rbcL sequences suggested that Lissocarpa was to be included in Sapindales - Rutaceae (Savolainen et al. 2000a), however, it is well supported (rbcL only) as sister to Ebenaceae s. str. (Berry et al. 2001), with which it also has much morphologically in common, so it is reasonable to combine the two.

Classification. For a monograph of Lissocarpa, see Wallnöfer (2004b).

PRIMULACEAE Borkhausen, nom. cons.   Back to Ericales

(Schizogenous secretory canals [material yellow, red, brown: tannins, etc.]); nodes ?3:3; (stomata anisocytic); inflorescence racemose; C and A from common primordia; stamens = and opposite C, staminodes +, opposite K, represented by at least a vascular trace [?Maesa]; nectariferous tissue on G; G [5], 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.

• Primulaceae can be recognised by their usually spirally arranged leaves sometimes with dark dots or lines. Their flowers are sympetalous with stamens borne opposite to the petals and an ovary with several to many ovules and free-central placentation; the stigma is not lobed.

Evolution. Divergence & Distribution. Wikström et al. (2001) suggest a stem group age of 75-72 m.y. before present, with crown group divergence beginning 49-46 m.y. before present.

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 (see 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 Lycaenidae-Riodininae-Hamearini and a few Riodinini (see also Abisara) are found on them, especially on Maesa but not so far on members of Theophrastoideae (Ehrlich & Raven 1964).

Chemistry, Morphology, etc. Leaves of Theophrasteae and Myrsinoideae are often described as being involute (?supervolute, c.f. Cullen 1978) or conduplicate.

There are common stamen/corolla primordia born on a ring primordium in this clade, but there is variation in the position/relative development of these primordia. In some cases such as Cyclamen the stamens are initiated as adaxial outgrowths of a common primordium, i.e. the petal primordia are early larger than the stamen primordia, as also in Myrsine and Aegiceras (see especially Ma & Saunders 2003), whereas in other taxa the stamen primordia may initially be 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 how fast they initially develop, 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 1936). The number of carpels can be also 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, the diagrams presented by Dickson (1936) mostly 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 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 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), for wood anatomy, see Lens et al. (2005a), for floral morphology and ontogeny, Dickson (1936: esp. gynoecial arrangement), Sattler (1962), Sundberg (1982), Ronse Decraene (1992), Ronse Decraene et al. (1995) and especially Ma and Saunders (2003), and for seed and endosperm, for the most part poorly correlated with major clades, see Morozowska et al. (2011: no Maesa). For general morphology, see Anderberg et al. (2000) and especially Ståhl and Anderberg (2004).

Phylogeny. The monophyly of the group 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), and available subfamilial and tribal names fit well with the phylogeny here.

Previous relationships. Plumbaginaceae (see Caryophyllales here) were often associated with Primulaceae because of having features like apparently similar placentation and oppositipetalous stamens in common (see Cronquist 1981 for discussion).

1. Maesoideae de Candolle   Back to Ericales

Evergreen lianes or trees; vessel element type?; petiole bundles all annular; glands/canals throughout the plant; leaves spiral or two-ranked, lamina vernation induplicate, margin toothed to entire; inflorescence often branched; flowers small; C 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.

1/150. Old World tropics to Japan, the Pacific, and Australia (map: from Palgrave 2002).

• Maesoideae are woody plants that can be recognised by their serrate, exstipulate leaves that often lack much venation, even when dry, and which have well-developed and conspicuous canals in the leaf blades, sepals and petals. The small, obviously bracteolate flowers have a connate corolla, stamens opposite the petals and an inferior ovary; the many-seeded fruit is drupaceous.

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 ³5-seriate, uniseriate rays 0 [not herbaceous taxa]; small ± immersed often peltate/glandular hairs +; bracteoles 0; C imbricate, subrotate; petals developing after the stamens.

Evolution. 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 Myrsinaceae). Many of these taxa have capsular fruits with apical teeth, presumably also plesiomorphic (Wanntorp & Anderberg 2011). Herbaceous taxa of Myrsinoideae such as Stimpsonia, Ardisiandra and Coris are more basal on the tree to woody taxa; variation in habit is very extensive in this part of Primulaceae. 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 (map: from Hultén 1971).

2A. Samoleae Reichenbach

Nodes ?1:1; lamina margins entire; flowers small; K connate; (staminodes 0); (anthers with prolonged connective); G [5], 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).

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; scale leaves +; lamina vernation conduplicate, margins spiny-toothed to entire, subepidermal fibres +; 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]

• Theophrasteae have sympetalous flowers with stamens opposite the petals and five, petal-like staminodes opposite the sepals. Most taxa are woody plants with broad rays and often pseudoverticillate leaves with toothed or spiny margins or a pungent apex. The extrorse anthers form a cone in the center of the flower when it opens, but later they spread. The subepidermal fibers are visible in the dried leaf as fine striations - use a hand lens!

Chemistry, Morphology, etc. The subepidermal fibres may lack lignification. 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]: tapetal cells uninucleate; (exotegmic cells elongated, with band-like thickenings); two ndhF deletions.

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; immersed glandular hairs 0 0, trichomes articulated; lamina (odd pinnate), vernation involute or revolute, margins entire to dentate or serrate; inflorescence scapose; (bracts 0); flowers medium-sized; K often connate, C hypocrateriform, (lobes fringed); A attached at or above middle of C tube; pollen syn- or polycolpate; style usu. long, (heterostyly +), stigma dry; ovules not immersed in placenta (immersed - Dionysia), (integument single, 6-10 cells across - Douglasia); fruit a capsule; 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: inc. Cortusa, Dionysia [some chasmophytes, for which see Trift et al. 2004, relationships, biogeography; Lidén 2007, revision), Dodecatheon), Androsace (160: inc. Douglasia, Vitaliana, see Schneeweiss et al. 2004b). Northern hemisphere, scattered elsewhere (map: from Hultén 1971; Meusel et al. 1978). [Photo - "Dodecatheon" flower © R. Kowal, Primula flower.]

• Primuloideae are usually rosette herbs with a scapose inflorescence and medium-sized flowers with connate sepals, obviously connate petals, hypocrateriform corolla and stamens borne opposite the corolla lobes; the placentation is free-central and the capsular fruits have numerous, angular seeds.

Evolution. Pollination Biology & Seed Dispersal. Heterostyly is common, although it is unlikely to be an apomorphy for the subfamily; it is sometimes lost, as in those Primula with buzz pollination, members of the erstwhile genus, Dodecatheon (Mast et al. 2001, 2006). Thrum plants are heterozygous Ss, while pin plants are the homoxygous recessive, ss (e.g. Li et al. 2011). 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-Lebrun et al. 2012).

Myrmecochory is common in Primula (Lengyel et al. 2010).

Ecology & Physiology. Boucher et al. (2011) discuss the evolution of life forms in Androsace s.l., which turns out to be very labile. The cushion habit has evolved several times since the Miocene, perhaps a "key innovation" enabling life at high altitudes.

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 occur 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), for embryology, see Subramanyam and Narayana (1976: variation in anther wall development within Primula), and for general information, see Anderberg (2004).

Phylogeny. For ITS-based relationships within Primuloideae, see Martins et al. (2003), and for relationships within Primula, see also Trift et al. (2002), Mast et al. (2004, 2006) and Yan et al. (2010), for relationships within Androsace, see Wang et al. (2004), Schneeweiss et al. (2004b) and Boucher et al. (2011).

Classification. The limits of Androsace will have to be extended (Boucher et al. 2012). 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 perforations); (nodes 3:3 - unnamed taxon from Atlantic Forest; Ardisia densiflora); glands/canals throughout the plant (0); 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; (bracts foliaceous); (median sepal abaxial); C often contorted; (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); fruit a berry, drupe or capsule [latter in herbaceous taxa], 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), Embelia (100), Oncostemum (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.]

• Myrsinoideae are trees to herbs, and many have distinctive yellowish to blackish dots or streaks on the often spiral leaves and also often obvious on the persistent calyx and on the fruit - I have not seen them on genera like Trientalis, Anagallis (but there may be pigmented spots on the abaxial surface of the lamina), Cyclamen, or some species of Lysimachia. The sympetalous corolla is often contorted, the five stamens are antepetalous, the ovary is superior, and the ovules and/or seeds are immersed in the placenta. In many woody taxa the point of insertion of the branches on the main stem is vertically elongated; growth is often sylleptic.

Evolution. Pollination Biology & Seed Dispersal. Vogel (1986, 1997) discussed pollination in Lysimachia, which is 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 oil is secreted by trichomes, and the bees also collect 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 (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 likely to be 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. For the evolution of the mangrove habitat, to which Aegiceras is restricted, see Rhizophoraceae and Tomlinson (1986). Hardly surprisingly, Aegiceras has a number of anomalous anatomical and morphological features, and the seed characters in particular are those that might be expected from a mangrove plant, since 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). It is unclear what role they might be playing (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). 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). Cyclamen has one cotyledon and one integument. 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 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, but the immediate clade with these taxa (minus Maesa) was found 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 herbaceous and ex-Primulaceae. However, the limits of this 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 clade as a whole had moderate support as being monophyletic (72% jacknife), and Cyclamen, the herbaceous taxa, and the woody taxa then formed a trichotomy. Hao et al. (2004) also provide a phylogeny of much of the group, although focusing on Lysimachia. Yesson et al. (2012) found that herbs formed many basal pectinations within Myrsinoideae, Cyclamen (the focus of this study) was well embedded in the family, and Coris (note nectary morphology) was sister to the whole of the rest of the subfamily when Stimpsonia (another herb, moving between Primuloideae and Myrsinoideae) did not occupy that position.

For the phylogeny of Badula, which may make Oncostemum paraphyletic, see Bone et al. (2012).

• Coris is particularly distinctive morphologically. It is a small ericoid sub-shrub with monosymmetric flowers that have a spine-tipped epicalyx. There is a nectary at the base of the ovary and there are only 5-6 ovules that are ± sunken into the placenta. Monosymmetry is expressed early in development by the calyx, but monosymmetry of the corolla becomes evident only later (Ronse Decraene et al. 1995: they suggest that the median sepal is abaxial, i.e. that the orientation of the flower is inverted or oblique).

• Aegiceras is a mangrove plant: vascular rays relatively narrow; ovules unitegmic, integument 4-5 cells across; no vascular bundle in the funicle; seed 1/fruit; embryo large, to 8 cm long; germination starts on the plant; etc. (Carey & Fisher 1932: embryology, Staåhl å Anderberg 2004; Lens et al. 2005).

• Cyclamen is also distinctive morphologically: plant cormous; inflorescence axis 0; flowers large; style hollow; integument single, ca 2 cells across, parietal tissue ca 4 cells across; pedicel coiling or otherwise bringing the mature capsule close to the ground; endosperm with thick and pitted walls, perhaps hemicellulosic, embryo long, lying diagonally in the seed, cotyledon single (Woodcock 1933, but c.f. Corner 1976).

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.

MITRASTEMONACEAE Makino, nom. cons.   Back to Ericales

Root parasites, 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 with 8-20 intrusive parietal placentae, 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.

1/2. 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]

• Mitrastemonaceae are root parasites, often found on Fagaceae, with opposite, scale-like leaves. The single, terminal flowers are surrounded at the base by the perianth, the stamens are completely connate, forming a conspicuous cone entirely surrounding the gynoecium except for a terminal opening, and the anthers are extrorse. The ovary has parietal placentation and the fruit contains many minute seeds.

Evolution. Genes and Genomes. A mitochondrial gene has moved from the parasite to its host, Quercus (Systma et al. 2008).

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 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. Along with Cytinaceae and Rafflesiaceae, relationships with of Mitrastemonaceae to Malvales have also been suggested (Nickrent 2002). Barkman et al. (2004) use mitochondrial sequences to place Mitrastemonaceae in Ericales, a position that appeared in most analyses in Nickrent et al. (2004: for further discussion, see Rafflesiaceae). Its cellular endosperm is certainly compatible with a position in Asterids, and its extrorse anthers are perhaps comparable with those of Ericaceae and their relatives. Since its parietal placentation is found in many other parasitic angiosperms, as well as in the echlorophyllous hyperparasitic Ericaceae-Monotropoideae, this is not necessarily a taxonomically informative character. 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.

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 and mucilage cells common; 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 (basal)/carpel, bitegmic, micropyle endostomal, outer integument 4-10 cells across, inner integument 4-11 cells across, hypostase present; fruit a capsule, central axis often persistent, 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.]

1. Stewartieae Choisy

(Plant deciduous); pith heterogeneous; androecium fasciculate; pseudopollen type?; embryology?; capsule lacking columella; seeds narrowly winged or not, ?vascularization; n = 15, 17, 18.

1/9. East Asia, E. North America (map: from Hong 1993).

[Gordonieae + Theeae]: androecium whorled; capsule with columella.

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 proliferates - Schima); n = (15), 18.

3/4-30. Franklinia, Gordonia, Schima. Southeast Asia, West Malesia, S.E. United States (map: from Camp 1947; Bloembergen 1952).

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; (cotyledons much folded); n = 15.

5/ : Camellia (120-180), Pyrenaria (42), Laplacea, Polyspora, Pyrenaria (60). Southeast Asia, Malesia, tropical America (map: from Camp 1947, approximate). [Photo - Flower, Fruit.]

Synonymy: Camelliaceae Candolle

• Theaceae are shrubs or trees that are recognised by their quite thick and serrate exstipulate leaves, they often turn red just before falling. The plant has sclereids that may be visible as minute punctations, e.g. in the leaf blades. The flowers are usually medium-sized to large, and the bracteoles, calyx and corolla are quite often in a single spiral and are not clearly distinguishable one from another. The numerous stamens have quite long filaments and short, dorsifixed anthers. The fruit is usually capsular and with a columella, and the seeds, often flattened, have straight embryos.

Evolution. Divergence & Distribution. 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).

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. In some species of Camellia, at least, a cyclocytic arrangement of cells may be surrounded by anisocytic arrangement (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; the basic orientation of the gynoecium is the same as that of Gordonia, where the carpels are clearly opposite the petals (Eichler 1878).

For further information about Theaceae s.l., see Beauvisage (1920: vegetative anatomy), Keng (1962: general), Grote and Dilcher (1989: fossil record), Liang and Baas (1991), Leins and Erbar (1991: floral morphology), Fagerlind (1939c: embryo sac development), Yang and Min (1995a, b: embryology and systematics), Tsou (1997, 1998: embryology), Stevens et al. (2004b: general), Wang et al. (2006: Apterosperma, chromosomes and morphology), Zhang et al. (2009: sclereids in Camellia) and Jiang et al. (2010: lenticels on Camellia leaves); for pollen, see Wei (1997).

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). However, the relationships between the three clades is unclear, although the clade [Gordonieae + Theeae] has some support (see also Prince 1999) and makes morphological sense. 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]), while Yang et al. (2004) found Stewartieae to be sister to the rest, although not with very strong support.

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). Generic limits in other Theaceae are difficult, but for useful notes on the genera, see Prince (2007). The iconic Franklinia hybridizes with Schima, and perhaps Gordonia and even Camellia (Ranney et al. 2003), while 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 all in separate families in Ericales. Bonnetiaceae (see Malpighiales) have also been included in Theaceae (Cronquist 1981).

[Symplocaceae [Styracaceae + Diapensiaceae]]: shrubs to trees; inflorescence racemose; style hollow; endosperm copious.

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, subgenus Hopea common as fossils in Europe (Eocene) (map: see Nooteboom 1975). [Photo - Symplocos chinensis Flowers]

• Symplocaceae are shrubs or trees that can be recognised by their serrate, exstipulate leaves which often dry yellowish and racemose inflorescences with rather small flowers. The petals are only basally connate, there are often many stamens, and the ovary is inferior - indeed, the flowers look superficially rather like those of Rosaceae-Maloideae. The fruit is drupaceous and the stone has germination pores.

Evolution. Divergence & Distribution. Symplocos is locally very abundant as both pollen and fruits in the Tertiary fossil record of Europe; it is also known from the southern USA and East Asia (Krutzsch 1989), as well as New Zealand (Lee et al. 2001).

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); section Cordyloblaste appears to be sister to the rest. The infrageneric taxonomy needs reworking, but it has been suggested that two genera in the family should 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.

Phylogeny. There is also fairly good support for this clade in B. Bremer et al. (2002). 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.

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; lamina conduplicate-plicate or supervolute; bracteoles 0, (pedicels articulated); 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, apotropous [Pamphilia], integument 12< cells across (bitegmic - Styrax, micropyle endostomal), placental obturator +, (endothelium + - Alniphyllum, Styrax); fruit also drupaceous; testa vascularized, crushed; n = 8.

11[list]/160: Styrax (120 - benzoin, gum bejamin [sic], pedicels not jointed). Warm N. temperate to tropical (map: from van Steenis 1949b; Sales & Hedge 1996; Fritsch 1999). [Photo - Flower, Fruit.]

• Styracaceae may be recognised by their stellate or lepidote indumentum; spiral, serrate, exstipulate leaves; and sympetalous flowers with a more or less completely connate and/or small calyx and a more or less inferior ovary. The filaments are stout and not sharply distinguished from the anthers.

Evolution. Divergence & Distribution. For the early Tertiary fossil history of Styracaceae that are now East Asian endemics, see Manchester et al. (2009).

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). Cecidomyids also produce galls on Styrax.

Chemistry, Morphology, etc. The floral vasculature suggests that although the stamens are in a single whorl, they are basically obdiplostemonous (Dickison 1993; see also Wang et al. 2010). Van Tieghem (1898) shows 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) describe the fruit, ovule, etc. of Styrax camporum.

Phylogeny. For relationships within Styracaceae, see Fritsch et al. (2001) and within Styrax Fritsch (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 possible additional synapomorphies for Styracaceae, see Fritsch et al. (2001).

Synonymy: Halesiaceae D. Don

DIAPENSIACEAE Lindley, nom. cons.   Back to Ericales

Shrublets or herbs, ecto- and endomycorrhizae + [?ectendomycorrhiza]; plants Al-accumulators; ellagic acid +, iridoids?; (cork superficial); vessel elements with simple (scalariform) perforations; secondary wood rayless; pericyclic fibres 0 (+ - Shortia); nodes (1:1 - Pyxidanthera) - 3:3; 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 flattened filaments, lobes serrate or not; stamens = and opposite sepals, (connate - Galax), anthers ± incurved, thecae horizontal, staminodes + (0); G [3], median member adaxial, stigma shortly 3-lobed, wet; ovules lacking endothelium; 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.]

• Diapensiaceae are herbs or subshrubs with moderately-sized and weakly sympetalous flowers; the five stamens with their flattened filaments alternate with the petals and the anthers are incurved. There are usually staminodes, the stigma is shortly three-lobed, and the fruit is a loculicidal capsule with small seeds.

Evolution. Divergence & Distribution. 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 smaller (7-9.5 µm, versus 17-40 µm), and the styles are separate.

Chemistry, Morphology, etc. The mycorrhizal association in Diapensiaceae may be a distinctive ectendomycorrhiza as is found in many Ericaceae (see Asai 1934, although at that time the distinctiveness of the ericaceous mycorrhizal association was not fully understood). For ellagic acid, see Harborne and Williams (1973). The integument is 5-7 cell layers thick, and seems to consist of an outer and inner part in some taxa. An endothelium may 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), for pollen and a morphological phylogeny, see Xi and Tang (1990).

Phylogeny. Galax and Pyxidanthera are successively sister taxa to the rest of the family (Rönblom & Anderberg 2002); if this series of relationships hold, the presence of staminodes is a derived feature within the family.

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 extrorse, inverting during development, opening by pores or short slits, pollen ± rugulate ["cerebellar"], tectum and foot layer solid, infratectum with granular elements; G [3], median member adaxial, also [5], opposite C, style impressed; ovules many/carpel, endothelium +; fruit a capsule; testa with much thickened inner wall [?higher level], endosperm copious; mitochondrial coxII.i3 intron 0.

Evolution. Divergence & Distribution. 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 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 slightly 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, or perhaps associated with Diapensiaceae or within Ericaceae (Crepet et al. 2013).

Wikström et al. (2001) had suggested a stem group age of 74-71 m.y., the crown group being 67-59 m.y., however, relationships between members of the group are other than those shown here, and Roridulaceae are sister to all other Ericales... Later, Wikström et al. (2004) suggested an age for the clade of 58-50 m.y., although they noted the considerable difference between their estimate and the substantially older (ca 89 m.y.) fossil-based estimate of Magallón et al. (1999).

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). For a summary of pollen variation, see Zhang and Anderberg (2002). When the anther inverts varies within this clade, and also the direction in which it occurs; thus in Sarraceniaceae) inversion is introrse -> extrorse, but usually it is in the opposite direction (Schönenberger et al. 2012).

Phylogeny. The whole clade may be sister to ((Theaceae s. str. + Symplocacaeae) (Styracaceae + Diapensiaceae)) (Geuten et al. 2004). Bracteole presence is rather variable (Anderberg & Xiaoping (2002).

[Sarraceniaceae [Actinidiaceae + Roridulaceae]]: route I secoiridoids +; nectary 0; stigma dry; ovule hypostase +.

Evolution. Pollination Biology. Buzz pollination is likely to be common in this clade, but nectaries are found in some taxa, whether on the overy or anther.

SARRACENIACEAE Dumortier, nom. cons.   Back to Ericales

Herbs, carnivorous [insectivorous], rosette-forming; O-methyl flavonols only +; mycorrhizae 0; cork?; vascular bundles separate; nodes ?; leaves with broad bases, ascidiate; inflorescence scapose (flowers solitary), bracteoles + [Heliamphora]; K (3-6), ± petal-like, C (0 - Heliamphora, 4), free; A 8-10 [Heliamphora] or many, centrifugal, anthers introrse, with slits (basal pores), inverting late and becoming extrorse; pollen 5+ colporoidate, surface verrucose-vermiculate, with small granules; (nectary at base of style - Sarracenia); placentation intrusive parietal apically, style hollow [?always], (apex divided; peltate-expanded), stigmas small; integument ca 4 cells across; 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).

• Sarraceniaceae are herbaceous, insectivorous pitcher plants. The pitchers are long, with short petioles, and are borne in a rosette. The flowers are quite large, with free sepals and petals, the former being petal-like, and there are usually numerous stamens. The capsules have many small seeds. [Photo - Inflorescence © J. Maunder, Flower, Flower.]

Evolution. Divergence & Distribution. Archaeamphora (Sarraceniaceae) has been described from rocks ca 124 m.y. old (Li 2005) - this is perhaps an unlikely identification.

Ecology & Physiology. There are nectar glands on the pitcher which attract insects that fall into the pitcher and drown - alternatively, the nectar may take up water increasing the possibility of an insect's hydroplaning into the pitcher (see Bauer et al. 2008). 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). 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 and nutrients from the entrapped animals are made available to the plant by the activity of detritivores that break up the prey that is further decomposed by bacteria, in turn eaten by rotifers and protozoa and ultimately by mosquito larvae - all forming a microcosm in the liquid of 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).

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).

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).

Pollination Biology. Flowers of Heliamphora lack a nectary and are buzz pollinated; Sarracenia has ten nectaries on the ovary wall above the stamen fascicles.

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 midib area. When there are many stamens, development is centrifugal from initially 10 primordia. The ovules may be unitegmic or bitegmic; the integuments are thin. Is the style hollow?

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) and Neyland and Merchant (2006) provide more information about relationships within the family; the topology [Darlingtonia [Sarracenia + Heliamphora]] seems well supported.

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]: ?

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 +); raphide sacs +; 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 basally connate or not, (nectar at base of petals), A 10-many, centrifugal, (in groups opposite petals), inflexed in bud (not - Saurauia; ± connate), inverting rather late, anthers dehiscing by pores or ± short slits; pollen rugulate and transversely striate; G [(-20)], style (impressed), single, or branched to the base, (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]/355: Saurauia (300), Actinidia (30), Clematoclethra (25). Largely tropical, esp. South East Asia to Malesia, but not Africa (map: from Soejarto 1980).

• Actinidiaceae are usually shrubs or lianes with spiral, serrate, exstipulate leaves and often rather flattened setose hairs. The flowers have apparently free sepals and petals and many stamens that invert just before anthesis; the anthers dehisce by a slit that is much broader towards the apex. The styles are short and separate and the fruit is a berry. [Photo - Flowers, Collection.]

Evolution. Divergence & Distribution. Parasuarauia was described from flowers of Campanian (Late Cretaceous) age 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).

Both separate styles and numerous stamens are probably derived within the family (Keller et al. 1996; Herendeen et al. 1999).

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. There is paternal transmission of the plastid genome in Actinidia at least (Chat et al. 2003).

For vegetative anatomy, see Bauvisage (1920), information on the floral anatomy of Actinidia, see Schmid (1978), for ovules, see Guignard (1882), 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]; C free, quincuncial; stamens = and opposite sepals, connective swollen at base of anther, conspicuous and nectariferous, anthers early inverting, fibrous endothecium 0; pollen densely and minutely spinose; placentation apical, stigma capitate, ?surface; ovules 1-4/carpel, pendulous; testa mucilaginous; micropylar haustorium +; n = 6.

1[list]/2. Southern Africa.

• Roridulaceae are small shrubs with linear leaves that have resin-secreting capitate hairs especially along the margins and abaxial midrib; the leaves are neither circinate in bud nor are the hairs sensitive (c.f. Droseraceae, Drosophyllaceae, and Byblidaceae). The flowers are medium-sized with free sepals and petals, only five stamens that invert early in development and that have a visually attractive, yellow, apparently nectariferous basal portion, and three carpels with an undivided style. [Photo - Roridula Flower © M. Schmidt].

Evolution. Divergence & Distribution. The age of Roridulaceae is ca 90 m.y., suggesting that they are very much a relictual element in the Cape flora (Warren & Hawkins 2006).

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. These bugs eat the insects that get stuck to the plant, and the plant absorbs nutrients from their excreta (Ellis & Midgley 1996; Anderson 2005). However, Plachno et al. (2009) suggest that Roridula is fully carnivorous, recording mineral uptake from Drosophila stuck on the leaves.

Pollination Biology. Pameridea may also be involved in pollinating Roridula (Ellis & Midgley 1996; Anderson 2005).

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). There are bracteoles.

For general information, see Vani-Hardev (1972), Dahlgren and van Wyk (1988), 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; flowers pendulous; stamens = 2x K; 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.

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, and I have not worked out where - perhaps 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, (bracts conspicuous - Purdiaea); K quincuncial, C basally connate or free; A ?obdiplostemonous, adnate to C or not, inverting late, anthers ± sagittate, dehiscing by pores or short slits; pollen <20µm, oblate, psilate to rugulate; (nectary 0); G ?orientation, (placentation apical - Purdiaea), stigma lobed or not; (ovule 1/carpel, 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 or subtropical (map: from Sleumer 1971d; Good 1974; Heywood 1978).

• Clethraceae are woody plants that can be recognised by their medium-sized, spiral, often toothed leaves that tend to be clustered at the ends of branches, their racemose inflorescences, and their rather small flowers with quincuncial sepals, free or basally connate petals, and ten late-inverting stamens with distinctive often sagittate anthers that open by pores. [Photo - Fruits & Flowers © A. Gentry], [Photo - Inflorescence], [Photo - 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) and especially Anderberg and Zhang (2002: pollen) 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.

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 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, mostly apotropous, integument 4-7 cells across; fruit a dry 1-4-seeded drupe or one-seeded, 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).

• Cyrillaceae are trees or shrubs that can be recognised by their spirally-arranged entire leaves with short petioles and often prominent, black colleters, and their long-racemose inflorescences. The flowers appear to be polypetalous, the style is short, and the stigma is often three-lobed. [Photo - Cliftonia Habit].

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 is 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).

For floral morphology, see Copeland (1953).

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. Clethra is sometimes included here (e.g. Mabberley 1997).

For more information, see Copeland (1953: general floral morphology and anatomy), Thomas (1960: monograph, 1961), and Vijayaraghavan (1970: ovule morphology, etc.), also Anderberg (1993), Zhang and Anderberg (2002: pollen), Anderberg and Zhang (2002: general) and Kubitzki (2004b: general).

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; lamina vernation involute, margins entire to toothed, teeth associated with multicellular hairs; inflorescence terminal; K connate basally, C connate; A obdiplostemonous, with appendages, inverting late, tapetal cells uni-, bi- or multinucleate [Empetrum}; pollen >26µm, surface ± rugulate; G [5], opposite C, stigma expanded; K persistent; testa with outer wall unthickened; chloroplast infA gene defunct.

Ca 126[list]/3995 - eight groups below. World-wide, but rare in lowland tropics (map: N. part of range, see Hultén 1971; Meusel et al. 1978; Luteyn 1995).

1. Enkianthoideae Kron, Judd & Anderberg

Pith with small, thick-walled and lignified and larger and thin-walled cells mixed [heterogeneous]; leaves pseudoverticillate; anthers with paired awns; pollen grains trinucleate, surface ± graulate; megagametophyte with "ears"; n = 11.

1/16. South East Asia: China, Japan and environs (map: from Kron & Luteyn 1995). [Photo - Habit.]

[[Pyroloideae [Monotropoideae + Arbutoideae]] [[Cassiopoideae + Ericoideae] [Harrimanelloideae [Epacridoideae + Vaccinioideae]]]]: plant ectendomycorrhizal, hair roots present [consisting of endodermis, epidermis, tracheid, sieve tube + companion cell], the fungal hyphae with complex coiled intrusions into the epidermal cells; anthers with exothecium, dehiscing by pores; pollen in tetrahedral tetrads; stigma dry to wet; chalazal vascular bundle in seed absent.

[Pyroloideae [Monotropoideae + Arbutoideae]]: Hartig net common, clade A Sebacinales common.

2. Pyroloideae Kosteltsky

Herbs, rhizomatous, (aphyllous, mycoheterotrophic); sugars accumulated as kestose and isokestose oligosaccharides; multicellular hairs 0; leaves pseudoverticillate; inflorescence a raceme; C free; anthers with short (0) tubules, appendages 0, (endothecium 0); (pollen in monads); nectary usu. 0; placentation intrusive parietal; 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.]

Synonymy: Pyrolaceae Lindley, nom. cons.

[Monotropoideae + Arbutoideae]: ?

3. Monotropoideae Arnott

Herbs, echlorophyllous, mycoheterotrophic, hyperparasitic; fungal hyphae with peg-like intrusions into the exodermal cells of hair roots; 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; K (0), sometimes quite large, C (0), free or connate; anthers usu. with slits, (thecae confluent), appendages 0 (spurs +); pollen in monads; (placentation parietal); (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; ovules 10³/carpel; 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 & Fries 1986; Kron & Luteyn 2005).[Photo - Flower (x-sec), Inflorescence.]

Synonymy: Arbutaceae Bromhead, Arctostaphylaceae J. Agardh

[[Cassiopoideae + Ericoideae] [Harrimanelloideae [Epacridoideae + Vaccinioideae]]]: mycorrhizae-forming fungi commonly ascomycetes, clade B Sebacinales common; (toxic andromedane diterpenes +); cauline pericyclic fibres well-developed, fibres associated with leaf bundles; stamens early inverting, anther wall without endothecium.

[Cassiopoideae + Ericoideae]: leaves opposite, ericoid, lamina vernation revolute.

5. Cassiopoideae Kron & Judd

Pith with large thin walled cells surrounded by smaller thick-walled and lignified cells [Calluna-type]; bud scales 0; inflorescences axillary; anthers with awns; embryo sac bisporic.

1/12. Circumboreal (map: from Meusel et al. 1978; Hultén & Fries 1986; Kron & Luteyn 2005). [Photo - Habit.]

The leaf midrib may lack associated fibres (Kron et al. 2002b), but this may be a plesiomorphy here and then apomorphic at higher levels.

6. Ericoideae Link

(Epiphytes); leaves also spiral, lamina flat (convolute); (pedicel articulated); flowers also held erect, (monosymmetric); (median sepal abaxial), (C free); anthers lacking appendages (present - Ericeae); (pollen with viscin threads); capsule septicidal.

19/1790: Rhododendron (850: inc. Azalea, Ledum, Menziesia, Tsusiophyllum), Erica (765+, 600+ in the S. Cape region: inc. Philippia, etc., see Oliver 2000). 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.

7. Harrimanelloideae Kron & Judd

Leaves acicular, lamina margins entire; flowers single; anthers with spurs.

1/2. Interruptedly circumboreal (map: from Hultén & Fries 1986; Kron & Luteyn 2005).

[Epacridoideae + Vaccinioideae]: ?

8. Epacridoideae Sweet [Tribes still being constructed]

Epidermis lignified; leaf bundles embedded, with well-developed abaxial fibrous vascular sheaths, no adaxial cap; epidermal cells ± rectangular, in longitudinally parallel ranks, anticlinal walls of abaxial [at least] epidermal cells sinuous; leaves xeromorphic, pungent, lamina with veins parallel or palmate; inflorescences often axillary, usu. spikes or multibracteolate axillary flowers; A = and opposite sepals, epipetalous (not), anthers bisporangiate, monothecal, with 1 (2) 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

Leaves with three veins from the base.

2/2. Chile, Tasmania.

Synonymy: Prionotaceae Hutchinson

[Archerieae [Oligarrheneae [Cosmelieae [Richeeae [Epacrideae + Styphelieae]]]]]: multicellular hairs 0; lamina serrations 0, midrib not evident.

8b. Archerieae

Abaxial epidermis plus associated hypodermis detach from mesophyll.

[Oligarrheneae [Cosmelieae [Richeeae [Epacrideae + Styphelieae]]]]: ?

8c. Oligarrheneae

Abaxial surface of lamina lacking ribbon wax and papillae; C lobes valvate to induplicate valvate; (A 2-5); G [2], style continuous, short; ovule 1/carpel; fruit a nut.

3/5. Australia.

[Cosmelieae [Richeeae [Epacrideae + Styphelieae]]]: ?

8d. Cosmelieae Crayn & Quinn

Leaves sessile, bases sheathing.

[Richeeae [Epacrideae + Styphelieae]]: ?

8e. Richeeae

Crystals in ray cells only; rays uniseriate + ³20-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). Australia, New Zealand, New Caledonia.

[Epacrideae + Styphelieae]: ?

8f. Epacrideae Kitt.

(Ovules apotropous - Lysinema).

Epacris (45).

Synonymy: Epacridaceae R. Brown, nom. cons.

8g. Styphelieae

Crystals in axial parenchyma only (0); rays uniseriate + 3-20-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.

Leucopogon (230, but perhaps to be split).

Synonymy: Stypheliaceae Horaninow

9. Vaccinioideae Arnott

(Epiphytes [ca 1/5 spp]); (hyphal sheath with inter/intracellular hyphae in cortex, basidiomycetes involved); apical bud aborting; stomata often paracytic; inflorescence usually axillary; pedicel often articulated; anthers with spurs, 2 or 4 awns or appendages 0, stigma truncate; 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 (235, 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; Kron & Luteyn 2005, still incomplete). [Photo - Psammisia Flowers, Gaultheria Flowers, Vaccinium Flower © J. Maunder.]

Chemistry, Morphology, etc. A group of genera around Lyonia has a lignified epidermis, bands of fibres in the secondary phloem, anomocytic stomata, etc.

For general information about New World taxa, see Luteyn (2000, 2002), for wood anatomy of superior-ovaried Vaccinoideae, see Lens et al. (2004a) and including many inferior-ovaried taxa, see Lens et al. (2004b: ecological correlations are mainly with latitude, also life form and precipitation).

Synonymy: Andromedaceae Döll, Oxycoccaceae A. Kerner, Vacciniaceae Perleb, nom. cons.

• Ericaceae are usually woody and shrubby and may be recognized by their flowers, which are often urceolate or tubular and are sympetalous; the ten stamens often dehisce by pores and sometimes have appendages on the anthers or the tops of the filaments. Vegetatively the family is very variable, but the leaves are always exstipulate and often spiral and rather mesomorphic, or they are xeromorphic, in that case being either opposite, ericoid, narrow and with a channel on the abaxial surface, or variable in size, thick, and with close parallel venation.

  Floral formula: * ⚥ K [5]; C [5]; A 10; N; G [5].

Evolution. Divergence & Distribution. For Paleoenkianthus, an interesting Late Cretaceous fossil from some 90 m.y. before present, see Nixon and Crepet (1993). It has many features of a bee-pollinated flower, and bees are likely to have been aorund by then (Cardinal & Danforth 2013).

There are diverse but much later (early Pleistocene) Stypheliodeae fossils from New Zealand (Jordan et al. 2007); indeed, there seems to be serious conflict between molecular and fossil estimates of clade ages. Thus leaves and pollen ascribed to Richeeae are ca 25-20 and 47-40 m.y. old, while in a molecular study Wagstaff et al. (2010) date stem Richeeae to (36.9-)33.4(-29.9) m.y., yet the stem age of the clade of Dracophyllum that now grows in New Zealand was a mere (7.2-)6.2(-5.2) m.y. Jordan et al. (2010) suggest 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 the identity of these fossils were accepted...

Kron and Luteyn (2005) discuss the historical biogeography of Ericaceae and give useful distribution maps for the subfamilies (Cassiopoideae are all over Greenland, perhaps in anticipation of the disappearance of the ice); an Eurasian origin of the family is likely. The inclusion of the largely Australian Epacridaceae within Ericaceae means that the distinctive rarity of Ericaceae s. str. from that area no longer is - the clade is quite common there. However, the biogeography of other newly proposed relationships are not so easy to understand, thus Gillespie and Kron (2010) found that the Guayanan Ledothamnus was sister to the northeast Asian Bryanthus. 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). 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).

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.

Hardy and Cook (2012) compared diversification in Monotropoideae (it has slowed) with that of Arbutoideae (exponential increase); the two diverged ca 70 m.y.a.

Ecology & Physiology. Ericaceae are most commonly found in open, more or less acidic habitats in cold to warm temperate climates, being common in heathlands world-wide (Read 1996; map: see Specht 1979; White et al. 2000). They can be abundant in montane shrubberies especially in the northern Andes, parts of the eastern Himalayan-Yunnan region, and Malesian mountains, and often in alpine and arctic tundra (Jonasson & Michelsen 1996; Michelsen et al. 1998). Tundra alone, the main component of heathland sensu Specht (1979), occupies ca 8% of the earth's surface and Vaccinium and Empetrum are two of the seven dominant biomass accumulators there (Gardes & Dahlberg 1996). In the Mediterranean heathlands of southern Africa and Australia Rhododendroideae and Styphelioideae respectively are common shrubs (e.g. the 600 or more spp. of Erica in the Cape region of South Africa alone). Boreal forests occupy ca 17% of the land surface (Lindahl et al. 2002), and there Ericaceae are often abundant in the understory (e.g. Villareal et al. 2004; Vrålstad et al. 2002; Vrålstad 2004; Kranabetter & MacKenzie 2010).in and in the mountains of South East Asia-Malesia and tropical America. See also Clade Asymmetries.

In terms of species numbers, there are four (partly overlapping) main ecological lines of diversification in the family: Taxa with fleshy fruits of one sort or another, ca 1,500 spp., taxa with xeromorphic leaves living in more or less Mediterranean or dry habitats, 1,300+ spp., taxa that are epiphytic (or epilithic) and often lianescent, ca 650 spp., and taxa with viscin threads, ca 900 spp. Many taxa in Mediterranean climates in particular (the South African Cape Region - Ericoideae, Australia - Epacridoideae), 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). Woody epiphytes (here I include the few epilithic taxa) are commonest in tropical Vaccinieae, especially in the New Word, but are also quite common in the Old World Rhododendron (Benzing 1990; Zotz 2013).

Ericaceae are particularly noted for their distictive ectendomycorrhizae (ERM). Fungal hyphae form complex coiled intrusions into the epidermal cells of the hair roots, which otherwise consist of little more than an endodermis, tracheid, sieve tube + companion cell; the fungal intrusions are not broken down by the host (Frank 1887; Read 1996; Perotto et al. 2012). Organic nitrogen and phosphorous are taken up by the mycorrhizal fungus associated with the plant, and they then move to the ericaceous associate; nitrogen in amino acids released by the fungus can be taken up by the plant (Cairney & Ashford 2002; Perotto et al. 2012). Indeed, protein-tannin complexes that come from Rhododendron, at least, may result in a higher nitrogen content in stable soil organic matter, nitrogen that is then more easily accessed by the ericoid fungus than by fungi in other kinds of mycorrhizal associations (Wurzburger & Hendrick (2009), either by the saprotrophic activities of the fungi, or by the fine ericoid rootlets that are simply very dense. ERM fungi show considerable metabolic diversity, being able to break down cellulose, and perhaps some even degrading lignin in a manner akin to brown rot fungi (Perotto et al. 2012 and references). Ericaceous leaves are well defended, 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 for the rather slow-growing plants (Cornelissen et al. 2001).

This association with fungi may be an element in the success of the family in the often rather acidic and nitrogen-poor habitats and generally stressful in which many of them grow, and also in their ability to grow in soils with toxic metals (Cairney & Meharg 2003; Perotto et al. 2012). 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). In western North America madrone, Arbutus menziesii, is commonly found as a subordinate tree in forests with ectomycorrhizal Fagaceae and Pinales, growing in over 3.9 x 10⁶ acres in California alone (Waddell & Barrett 2005). Its diverse fungal associates were also found on other angiosperms and in particular Pinaceae (Pseudotsuga) in Oregon (Kennedy et al. 2012). Indeed, Arbutoideae in western North America may facilitate regeneration of conifers after disturbances such as fire, taxa like A. menziesii resprouting and serving as a source of fungal inoculum for associated Pinaceae (Kennedy et al. 2012 and references).

Vaccinium and Empetrum are two of the dominant biomass accumulators in tundra, which occupies 8% of the land surface (Kranabetter & MacKenzie 2010; Gardes & Dahlberg 1996).

In both the Indo-Malesian and the Andean regions species of Vaccinieae are epiphytes; Vaccinieae represent a major component of the woody epiphytic flora (see also Rubiaceae). Interestingly, distinctive mycorrhizae (cavendishioid mycorrhizae) 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. Lignotubers are known from some of these epiphytic taxa; they lack buds and may be involved in water storage (Evans & Vander Kloet 2010).

The association of particular basidiomycete fungi with individual species of the echlorophyllous and myco-heterotrophic Monotropoideae is often close and specific (Bidartondo and Bruns 2001, 2002; Bidartondo 2005: problems with the identity of the plants examined make the earlier literature difficult), and 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 the probably mixotrophic nutrition. Hashimoto et al. (2012) found that in Pyrola asarifolia at least the fungi that were associated with the plant as it germinated (Sebacinales-B) were different from those associated with the adult plant (these were similar to fungi associated with Betulaceae growing in the same area).

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); 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 myco-heterotropic and parasitic groups, it can be difficult to interpret floral morphology, especially in Monotropeae. Seeds and embryos are also 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 Franke (1935) for Monotropa hypopitys.

Pollination Biology & Seed Dispersal. 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. 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). Several other factors are implicated in one way or another with this diversification, and these include 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, which seem 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). 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. 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 (Rebelo et al. 1984). 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 polinated by the marsupial mouse, Antechinus stuartii (McConchie et al. 1986). Buzz-pollination is scattered in the family, and in Pyroloideae, for instance, the lack of an endothecium and absence of a nectary are associated with this condition (Liu et al. 2011).

Fleshy-fruited taxa 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 (P.F.S., pers. obs.). Seeds of other Vaccinieae, and of other Ericaceae in general, have white embryos. In the New World, taxa with fleshy fruits are much eaten by tanagers (see also Myrtaceae), which will tend to remove seeds greater than 2 mm long from the fruits before ingesting them (Stiles & Rosselli 1993).

Bacterial/Fungal Associations. For ericoid mycorrhizae in general, in which the fungi are usually ascomycetes, see Cullings (1996) and Smith and Read (1997) and the discussion above. A number of mycorrhizal types have been described for the family, but their discreteness needs to be be confirmed, and there may also be intemediates between mycorrhizae and dark septate endophytes (Vohnik & Albrechtova 2011). Several clades of basidiomycete Sebacinales are involved in the distinctive mycorrhizae formed on the hemiepiphytic Cavendishia nobilis (Setaro et al. 2006), and this association has recently been described as a new mycorrhizal type, the cavendishioid type (Setaro et al. 2008). Massicotte et al. (2008 and references) discuss mycorrhizal associations in North American Pyroleae, and for the mycorrhizae of Epacridoideae in particular, see Cairney and Ashford (2005).

Bougoure et al. (2007) detail the variety of fungi associated with Vaccinium and Calluna - some may be ectomycorrhizal, although the distinction between the two mycorrhizal types is very slight (see above). Fungi on Arbutus menziesii probably form a common mycelial network with Pseudotsuga and Pinus in the same area (Kennedy et al. 2012). The ascomycete Rhizoscyphus ericae is very commonly an associate of the hair roots of North Temperate Ericaceae; this fungus can also be ectomycorrhizal on Pinus growing together with Ericaceae (Grelet et al. 2010; see also Villarreal-Ruiz et al. 2004), and it also forms mycorrhizal associations with Jungermanniales-Schistochilaceae, leafy liverworts (Pressel et al. 2008). Selosse et al. (2007a) described the association of Sebacinales, a "basal" order of basidiomycetes, with Ericaceae. They found that 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 were associated with members of Ericoideae, Epacridoideae and Vaccinioideae, in a major clade sister to the first; the fungi of Harrimanelloideae and Cassiopoideae are unknown (see also 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).

It has been suggested that the diversity of the fungi associated with Ericaceae may not be very high (Rinaldi et al. 2008), although 15 species is surely an underestimate; more species than this were associated with Arbutus menziesii in a single site in Oregon (Kennedy et al. 2012). 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 that group alone are associated with Ericaceae.

Interestingly, Enkianthus has arbuscular mycorrhizae of the Paris type (Abe 2005), i.e. it is endomycorrhizal, and it apparently lacks hair roots. I have seen few accounts of mycorrhizae in Clethraceae or Cyrillaceae, but the distinctive mycorrhizae/root assocation of Ericaceae may have become established only after Enkianthus diverged from the rest.

Endophytes are common (Petrini 1988); Ngugi and Scherm (2006) discuss the pseudoflowers formed by some fungal associates of Vaccinium.

Host preferences of the rust fungi Chrysomyxa and Exobasidium link Empetreae with other Ericaceae, perhaps Ledum with Rhododendron, etc.; Exobasidium is also found on Theaceae and Symplocaceae (Savile 1979b; see Jackson 2004 for possible codivergence). However, many characters other than rust preferences link Empetreae with Ericoideae in particular, e.g. both Rhodoreae and Empetreae have the flavonoid gossypetin. Molecular data also strongly associate Empetreae with Ericaceae, and the ericoid leaves of the former are common (?independently derived) in other Ericoideae.

Vegetative Variation. Leaf morphology in Ericaceae is very variable, for instance, linear leaves are found in Diplycosia, Rhododendron, Empetrum and relatives, Killipiella, 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 ericoid. Within the small genus Cassiope there 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).

Chemistry, Morphology, etc. For a survey of flavonoid and simple phenols, see Harborne and Williams (1973). Note that ellagic acid has been found in pollen of some European Ericoideae (Ferreres et al. 1996). The best developed pit membrane remnants in Ericaceae occur in Enkianthus of the genera sampled; 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? For some wood anatomical variation placed in a phylogenetic context see Lens et al. (2003, 2004a, b, c); I have not attempted to place all this variation on the tree, but there is extensive homoplasy in most of the characters even within a subfamily. The hair roots found in many (?nearly all) Ericaceae are distinctive, being barely wider than a root hair and consisting merely of endodermis, exodermis, tracheid, sieve tube, and companion cell; they are relatively long-lived. Even quite low-order root branches in Vaccinium corymbosum, at least, are quite thin (Valenzuela-Estrada et al. 2008: the ultimate root branches are first-order branches). Sylleptic branching is at best uncommon (Keller 1994).

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]; Lu et al. 2009 [Gaultheria and relatives]). Viscin threads are well known as occurring in Rhodoreae, and have recently been reported from Gaultheria (Lu et al. 2009). Carpels are opposite the calyx in Vaccinium, Dracophyllum and Monotropa (Schnizlein 1843-1870: fams 160, 161). There is considerable variation in integument thickness in Ericaceae, but I have not attempted to collate all the literature on this feature: Pyrola may have an integument only two cells across, while that of Epacris is three cells thick and of Vaccinium, Arctostaphylos, etc., ca 5 cells (e.g. Samuelsson 1913; Diels 1914).

For the distinctive embryology of the family, see Stushnoff and Palser (1969 and references), for oligosaccharide storage, Fouquieriaceae, Diapensiaceae, and Cyrillaceae (and Lennoaceae) also sampled, see Pollard and Amuti (1981); for protein crystals in the nucleus, see Speta (1977, 1979); for a phenetic analysis of some staminal characters, see Vander Kloet and Avery (2007); for wood anatomy of Epacridoideae, see Lens et al. (2003); for pseudotori, see Rabaey et al. (2006); for vegetative features of Epacridoideae, see Jordan et al. (2010); for venation patterns in neotropical Vaccinieae, see (Pedraza-Peñalosa et al. 2013), and for external seed morphology of Gaultherieae, see Lu et al. (2010a) and that of Erica - quite variable - see Szkudlarz (2010). For general information on the family, see Kron et al. (2002b) and Stevens et al. (2004a), for Oligarrheneae, see Albrecht et al. (2010).

Phylogeny. Early studies are summarized by Kron et al. (2002b); the structure of the tree immediately above Enkianthoideae was labile with Pyroloideae, Monotropoideae and Arbutoideae, variously arranged, forming a basal grade. Freudenstein et al. (2010) in a comprehensive phylogenetic study of the family suggest relationships [Enkianthoideae [[Pyroloideae [Arbutoideae + Monotropoideae]] The Rest]] (see also Liu et al. 2011; Hardy & Cook 2012); 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 Feldenkreis et al. (2011) suggested the relationships [Enkianthoideae [Pyroloideae [[Monotropoideae + Arbutoideae] The Rest]]].

For the phylogeny of Pyrola and its relatives (Pyroloideae), see Freudenstein (1999) and Liu et al. (2011); in the latter, the position of Orthilia was not stable, and there was a suggestion that allopolyploidy might be involved. Matsuda et al. (2012) found the well supported relationships of [[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) 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, while the Guyanan Ledothamnus was sister to the northeast Asian Bryanthus. For the phylogeny of Ericoideae-Ericeae, see McGuire and Kron (2005); the African species of Erica are probably monophyletic and are members of a lineage that originated within that part of the tree that otherwise includes taxa currently found in Europe. 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). Azalea, Ledum, Menziesia, Tsusiophyllum are all to be included, indeed, Menziesia hybridizes with related species of Rhododendron (de Riek et al. 2008). In Ericoideae-Rhodoreae, polypetaly is sporadic. The wind pollinated members of Empetreae are highly derived. Not only are their leaves opposite or whorled, small, and strongly revolute, but the plants are monoecious or dioecious, the flower parts in 2s or 4s, the perianth members free, the anthers without appendages, there is one basal apotropous ovule/carpel, the stigma is expanded, and the fruit is a few-seeded drupe. Ericeae usually have similar small, opposite or whorled, strongly revolute leaves - the prototypical ericoid leaf - and their flowers are 4-merous, the bracteoles are often recaulescent, the calyx and corolla are both more or less scarious, they wither in fruit, but do not fall off, and the anthers are often with spurs.

For the phylogeny of Epacridoideae, see Powell et al. (1996), Crayn and Quinn (2000) and Johnson et al. (2012). Within Epacridoideae, Prionoteae and Archerieae may be successively sister to remaining Epacridoideae - the former is distinctive in having plesiomorphic features such as multicellular hairs, leaves with serrate margins, pedicellate flowers, and anthers dehiscing by two slits. 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), and it is likely that the limits of Leucopogon will have to be restricted - or there will be a single genus including practically the whole tribe (see also Taaffe et al. 2001; Johnson et al. 2012).

Much-needed phylogenetic work is beginning 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). There may be a number of cryptic species in the high-altitude representatives of the genus (Lu et al 2010a). Outlines of relationships in tropical Vaccinieae are developing (Kron et al. 2002a) and these for the most part cut across the limits of the larger genera in particular, these being based on floral (= variants of a bird pollination syndrome) characters. A Vaccinium-type flower (i.e., small) is plesiomorphic in the whole clade and Vaccinium itself is paraphyletic (see also Powell & Kron 2002, 2003; Pedraza-Peñalosa 2009); Pedraza-Peñalosa (2010) explored the limits of Disterigma. Agapetes, a large genus centred in SW China-the Himalayas, is embedded in the group of Southeast Asian-Malesian Vaccinium with superficial cork cambium (Powell & Kron 2002; Tsutumi 2011).

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) modify tribal limits in Ericoideae. Argent (2006) provided an account of species of subgenus Vireya (= section Schistanthe); Craven et al. (2008, esp. 2011) list the subsections that it includes. Generic limits in Styphelieae and some other Epacridoideae are difficult (e.g. Cherry et al. 2001; Quinn et al. 2005 and Albrecht et al. 2010 suggest some realignments). 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), and Vaccinium itself is pretty wildly paraphyletic. In particular, the "Tethyan" Vaccinium section Hemimyrtillus, with species from the Mediterranean area, etc., may be sister to the rest of the Vaccinieae, although with only weakish support (Powell & Kron 2002), while in Southeast Asia the Agapetes clade probably also includes some 250+ species of Vaccinium and 90 or more species of Agapetes s. str., all having superficial phellogen and a falsely 10-locular ovary, both probably derived features. Dimorphanthera is sister to Paphia (18); the latter used to be included in Agapetes, but the two are not immediately related. However, if the Paphia clade really does include taxa of the old Vaccinium sect. Pachyantha, merging with Dimorphanthera might be best... Vander Kloet and Dickinson (2009) provide a sectional classification for Vaccinium - they recognize thirty sections.