EXTANT SEED PLANTS

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 rich in guaiacyl units; true roots present, apex multicellular, xylem exarch, branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; stem cork cambium superficial, root cork cambium deep seated; nodes ?; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, axillary buds +[?], prophylls [including bracteoles] two, lateral, veins -5 mm/mm² [mean for all non-angiosperms 1.8]; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, 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, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplication [N/O//A/C and P//BE lines], mitochondrial nad1 intron 2 and coxIIi3 intron present.

MAGNOLIOPHYTA

Plant woody, evergreen; lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], lignins derived from both coniferyl and sinapyl alcohols, containing syringaldehyde [in positive Maüle reaction, syringyl:guaiacyl ratio less 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; stem with 2-layered tunica-corpus construction; wood fibers and wood parenchyma +; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides; tracheids +; sieve tubes eunucleate, with a sieve plate and cytoplasm with P-proteins, companion cells from same mother cell that gave rise to the sieve tube; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves with petiole and lamina [the latter formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; flowers perfect, polysymmetric, parts spiral [esp. the A], free, development in general centripetal, numbers unstable; P not sharply differentiated, outer members not enclosing the rest of the bud, smaller than inner members; A many, with a single trace, introrse, filaments stout, anther ± embedded in the filament, tetrasporangiate, dithecal, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, binucleate at dispersal, trinucleate eventually, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, few [?1] ovules/carpel, ovules marginal, anatropous, bitegmic, [outer integument often largely subdermal in origin, inner integument dermal], micropyle endostomal, integuments 2-3 cells thick, nucellus at apex of ovule 1-3 cells thick, megasporocyte single, megaspore lacking sporopollenin and cuticle, chalazal, female gametophyte four-celled [one-modular, nucleus of egg cell sister to one of the polar nuclei], stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; P deciduous in fruit; seed exotestal; pollen germinating in less than 3 hours, siphonogamy, tube elongated, growing at 80-600 µm/hour, with callose plugs and callose-based walls, penetrating between cells, penetration of ovules within ca 18 hours, distance to first ovule 1.1.-2.1 mm; tube moves between nucellar cells, double fertilisation +, endosperm diploid, cellular [first division oblique, micropylar end initially with a single large cell, chalazal end more actively dividing], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, 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 PHYA + C/PHYB + E gene pairs.

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear, because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable variation between families 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 a 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), where on the tree a thicker nucellus and a stylar epidermal layer are acquired has not yet been indicated.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels + [one position], elements with elongated scalariform perforation plates; axial parenchyma diffuse or diffuse-in-aggregate; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

VITALES + ROSIDS: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].

ROSIDS: embryo long; genome duplication; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.

ROSID I/FABIDAE: Endosperm scanty.

FABALES [ROSALES [CUCURBITALES + FAGALES]] - "the nitrogen fixing clade" : (N-fixing by root-dwelling associates [usu. the actinomycete Frankia]); tension wood +; seed exotestal; embryo large.

ROSALES [CUCURBITALES + FAGALES]: 1-2 apical ovules/carpel.

CUCURBITALES + FAGALES: ovary inferior; fruit 1-seeded, indehiscent.

FAGALES Engler  Main Tree, Synapomorphies.

Ectomycorrhizal; (Frankia infection via root hairs); (flavononols), dihydroflavonols, ellagic acid +; (cork cambium outer cortical); vessel elements also with scalariform perforation plates; sieve tubes with non-dispersive P-protein bodies; bud scales +; leaf margins toothed, 2ndary veins proceeding straight to non-glandular teeth and higher-order veins convergent on those teeeth [urticoid]; plants monoecious, flowers in compact cymose clusters, very small, staminate inflorescence a spike or catkin; P +; A opposite P, tectum ± spinulate, infratectum granular [?here], nectary 0, 2 pendulous unitegmic ovules [with nucellar cap?]/carpel, poorly developed at pollination, integuments 3-13 cells across, fertilisation delayed, style undivided, ± 0, stigma ± decurrent, linear, dry; fruits dry; testa vascularised, not mechanical, exotesta often enlarged and persisting; cotyledons large. - 8 families, 55 genera, 1877 species.

Evolution. Wikström et al. (2001: relationships are [Fabales [Rosales [Cucurbitales + Fagales]]]) date the origin of Fagales to ca 84 million years before present (constrained), diversification beginning (65-)61(-57) million years before present. Most other ages are rather older. The age of crown group Fagales was estimated as (93-)90, 88(-84) million years (two penalized likelihood dates), the stem group age being (107-)103(-99) or (92-)88(-84) million years; Bayesian relaxed clock estimates were slightly older, to 100 or 109 million years respectively (Wang et al. 2009: note that relationships are [Rosales [Fabales [Cucurbitales + Fagales]]]), while Magallón and Castillo (2009: relationships are [Fabales + Rosales] [Cucurbitales + Fagales]) estimated ages of ca 102.3 and 102.6 million years for relaxed and constrained penalized likelihood datings for the age of stem Fagales, and an age of 93.5 million years for the crown group.

The pollen of Betulaceae, Rhoipteleaceae and Juglandaceae, and to a lesser extent that of Fagaceae, is rather like that of the Normapolles type abundant in the Turonian-Campanian of the Cretaceous, some 98-94 million years before present (Kedves 1989; Friis et al. 2003a, 2006a for a summary; Crepet et al. 2004 for a list of early records of Fagales fossils). Normapolles pollen is oblate in shape (i.e. it is a radially symmetrical grain in which the polar axis is shorter than the equatorial diameter) and triaperturate with protruding, elaborate and strongly thickened apertural regions, the apertures themselves often being formed from expansions of the granular infratectal layer; the result is that the pollen is more or less triangular in transverse section. The apertures have internal pores and externally short colpi or pores. The wall is usually tectate-granular, but sometimes with an atectate polar zone, the surface being almost smooth to finely spinulate to rugulate. The infratectum is granular (details from Friis et al. 2003a). Fossil flowers producing pollen of the Normapolles type are perfect, rarely imperfect (cf. extant Fagales), and with a simple, undifferentiated perianth. However, the pollination, at least, in fossil taxa assigned to Fagales (the fossils are ca 84 million years old - see Herendeen et al. 1999) may have been somewhat different from that of the extant members. Thus Antiquacupula appears to have nectaries at the base of the stamens (Sims et al. 1998; Herendeen et al. 1999). Other details of the the morphology of some of these fossil flowers are also distinctive. Normanthus, from the late Cretaceous of Portugal, has perfect flowers with five perianth members that alternate with the stamens, there are two collateral carpels with separate and quite long styles, and the placentation is described as being parietal (Schönenberger et al. 2001b). Endressianthus has imperfect flowers, and in the staminate flowers the stamens alternate with the tepals; Dahlgrenianthus has perfect flowers and a superior ovary with more or less separate styles (Friis et al. 2006a); while Archaefagacea has a tricarpellate gynoecium, two ovules per carpel and sometimes three-seeded fruits. Schönenberger et al. (2001b) and Friis et al. (2003a) give useful tables comparing the morphology of extant and fossil members of Fagales.

Wind pollination and monoecy now pervades the order, although taxa like Lithocarpus and probably some fossil Fagaceae are pollinated by insects. Delayed fertilisation, chalazogamy, and also intermittent pollen tube growth (e.g. Sogo & Tobe 2005, 2006a, b, d [the last for a summary]) are also common, although chalazogamy itself is perhaps unlikely to be plesiomorphic in the order (the situation is unknown for Nothofagaceae, Fagaceae are porogamous). Delayed fertilisation is associated with the immaturity of the ovules at pollination and competition between the ovules, indeed, in Corylus avellana the ovules do not even begin to develop until after pollination (Germain 1994). Fagales are hardly particularly speciose (e.g. Magallón & Sanderson 2001), but members - especially of Fagaceae - can dominate the forests in which they grow.

Lycaenidae caterpillars are quite commonly to be found on members of Fagales (see Fielder 1991). Phyllonorycter leaf-mining moths (Lepidoptera - Gracillariidae - Phyllocnistinae) are also especially speciose on Fagales, about half the known host records being from this group (Lopez-Vaamonde et al. 2003). However, diversification seems to have occured in the region of 50.8-27.3 million years before present, well after the order itself originated (see above), and after the leaf-miner clade itself evolved, some 76.3-50.3 million years before present (Lopez-Vaamonde et al. 2006). Both Heterobathmidae (Nothofagaceae) and Eriocraniidae (Fagaceae, Betulaceae), clades rather "basal" in the lepidopteran tree, are found on Fagales (Shields 1988).

Ectomycorrhizal associations are common in Fagales, and these may result in tuberculate structures (Smith & Pfister 2009); associations with N=nitriogen-fixing bacteria are sporadic. A particular Frankia clade involved in nitrogen fixation is restricted to Fagales, although members of another clade are also to be found here (Clawson et al. 2004). Rusts on Fagales are predominantly to be placed in Pucciniastraceae, also found on ferns (Savile 1979).

Chemistry, Morphology, etc. The leaf teeth in Juglandaceae, Rhoipteleaceae and Myricaceae are intermediate in "type", having a ± splayed, (non)glandular apex, and the main tooth vein is joined by branches that leave below, or one of the branches may proceed above the tooth (Hickey & Taylor 1991). Although the tepals in Fagales are small, they may have three traces, and petals with three traces are also found in some fossil taxa. Integument number is variable. Where change in infratectum structure is to be placed on the tree seems unclear when treated at the family level; either one gain, an ordinal apomorphy (see also Doyle 2009), and one reversion (Fagaceae), or two gains. Hopwever, since Fagus is also has a columellar infratectum, the former position is most reasonable - but Normapolles pollen also has a granular infratectum... Germination is often both hypogeal and epigeal in the one family, but not in Casuarinaceae and Nothofagaceae.

For cork cambium initiation, see Weiss (1890); flower and inflorescence morphology, see Abbe (1974): chemistry, see Giannasi (1986); pollen, Zavada and Dilcher (1986); vegetative morphology, Hickey and Taylor (1991); pollen, Feur (1991); embryology, Xing et al. (1998); and fossils, Friis et al. (2003a and references).

Phylogeny. The relationships within Fagales are becoming fairly well resolved (see tree), although the position of Myricaceae remains somewhat uncertain. Details can be found in Manos and Steele (1997), D. Soltis et al. (2000a: Rhoiptelea not included) and Li et al. (2002). Manos and Steele (1997) show Myrica as immediate sister to Betulaceae, etc., in a matK and combined matK + rbcL analysis, although support was weak, but sister to all Fagales except Nothofagaceae and Fagaceae in a rbcL analysis, the latter set of relationships also being found by Li et al. (2002) using trnL-F sequence data, but with only 61% bootstrap support. Li et al. (2004: six genes, all three genomes) found Myricaceae to be sister to [Juglandaceae + Rhoipteleaceae], although the support still was not strong; the tree here follows the topology in this last paper. Herbert et al. (2006: three genes) find the same set of relationships, but with little support for the position of Myricaceae, while the support was good in the Bayesian analysis of Soltis et al. (2007a, but sampling).

Previous Relationships. Fagales are the core of the old "Englerian" Amentiferae which have since been comprehensively demolished; a somewhat larger group, Juliflorae, included all "dicots" with very reduced flowers, so including Platanaceae, Lacistemaceae, Chloranthaceae, Piperaceae, etc. (e.g. Eichler 1878). Members have found resting places among many otherwise entirely unrelated groups within the Eudicots such as Malpighiales (Salicaceae, Lacistemaceae), Proteales (Platanaceae), and Rosales (Ulmaceae and relatives: e.g. Qiu et al. 1998), and even in or near the magnoliids (Piperaceae, Chloranthaceae). In the late 19th century and early twentieth century in particular, a number of botanists thought that Amentiferae were primitive, and the chalazogamy common in the order was even thought to be intermediate between fertilisation in some gymosperms and the porogamy that characterises most angiosperms (e.g. Nawaschin 1895). There are no immediate relationships with hamamelid taxa such as Altingiaceae and Hamamelidaceae (see Saxifragales here) that were previously thought to be intermediate between Amentiferae and more conventional broad-leaved angiosperms. Fagales comprise the Faganae and two and a half other superorders in Takhtajan (1997).

Includes Betulaceae, Casuarinaceae, Fagaceae, Juglandaceae, Myricaceae, Nothofagaceae, Rhoipteleaceae, Ticodendraceae.

Synonymy: Juglandineae Thorne & Reveal, Myricineae Thorne & Reveal - Betulales Bromhead, Casuarinales Lindley, Corylales Dumortier, Juglandales Dumortier, Myricales Engler, Nothofagales Doweld, Quercales Burnett, Rhoipteleales Reveal - Casuarinanae Reveal & Doweld, Faganae Takhtajan, Juglandanae Reveal

NOTHOFAGACEAE Kuprianova   Back to Fagales

Chemistry?; sclereid nests?; peltate glandular hairs +; leaves two-ranked (spiral), vernation various, margins also entire, stipules usu. peltate (0? - N. obliqua), enclosing colleters; staminate flowers: P connate, uniseriate; A 10-15(-many), basifixed, connective usu. produced, pollen 3-10-colpate, aperture margins raised; carpellate flowers: 1-3 together; P in 1 cycle, (A hairy); G [2-3], median member abaxial, chalazogamy?, (style short); cupule (2-)4-valved, lamellate (0), fruits (1) 3(-7), lenticular (central) or triangular; testa?; endosperm initially nuclear, cotyledons folded; n = 13.

1/35. New Guinea to South America (map: from Good 1974, slightly modified). [Photo - Branch]

Evolution. For the biogeography of Nothofagus, a much-discussed subject, see Swenson et al. (2001) and Knapp et al. (2005). The family is perhaps 90 million years old, and the current distribution of the genus has often been explained by vicariance, i.e. continental drift. Fossils of all four subgenera are known from the Late Campanian in Antarctica (Swenson et al. 2001). However, Knapp et al. (2005) suggest that Nothofagus reached New Zealand, at least, by long distance dispersal only ca 30 million years before present (see also Waters & Craw 2006).

The rust parasites of Nothofagaceae are rather different to those of other Fagales (Savile 1979). The inaperturate discomycete Cyttaria is found on Nothofagus in both the Antipodes and in South America, but not in New Guinea. Humphries et al. (1986: this work needs to be re-evaluated in the context of recent ideas of relationships) discuss the parasites and associates of Nothofagus, and suggest the possibility of some coevolution of the genus with Eriococcus scale insects that grow on it; the moth Heterobathmia, a genus perhaps 125 million years old, part of a clade (Micropterigidae) sister to all other Lepidoptera, makes its home exclusively on Nothofagus, both as an adult (it has jaws, and eats pollen) and as a larva (see also Futuyma & Mitter 1996).

Chemistry, Morphology, etc. Unlike Fagaceae, there is no obvious relationship between the number of fruits and the number of valves of the cupule. The central flower of the cupule often has two carpels, lateral flowers have three. Flowers that apparently have many stamens are interpreted as being the result of fusion of dichasia, so they are pseudanthia (see also Betulaceae). Nothofagus obliqua may have unilacunar nodes.

Further information may be found in Poole (1952), Hegnauer (1989, as Fagaceae: chemistry), Philipson and Philipson (1979, 1988), Hill and Jordan (1993, Kubitzki (1993b: general), Manos (1997: relationships), and Rozefelds (1998), Rozefelds and Drinnan (1998: stamens and staminate flowers), and Lersten and Horner (2008b: leaf crystals, etc., comparison with Fagaceae, similar).

Phylogeny. Knapp et al. (2005 and references) discuss relationships within the genus.

Classification. For checklist and bibliography, see Govaerts and Frodin (1998: in Fagaceae).

Previous Pelationships. Nothofagus has often been included in Fagaceae, as by Cronquist (1981) and Kubitzki (1993b).

Fagaceae [Myricaceae [Juglandaceae + Rhoipteleaceae]] [Casuarinaceae [Ticodendraceae + Betulaceae]: leaves spiral; anthers dorsifixed.

Evolution. Stem-group Fagales (excluding Nothofagus - not sampled) are estimated to be (107-)103(-99) or (92-)88(-84) million years old and the crown group is (93-)90, 88(-84) million years old (Wang et al. 2009).

FAGACEAE Dumortier, nom. cons.   Back to Fagales

Hairs often stellate/branched; sclereid nests in bark, cells with large rhomboidal crystals; stomata also cyclocytic; leaves (two-ranked, whorled), conduplicate-plicate, (margins entire, lobed; biserrate); inflorescence branched or not; flowers often trimerous; P biseriate [thus = T] or not, 4-6 (7)-lobed; staminate flowers: bract; A 4-20 (connective produced), pollen not spiny, tectum with ± flat-lying and fused rod-like elements [(micro)rugulate], pistillode +; carpellate flowers: staminode +; G [(2) 3-6(-15)], alternating with P, or median member abaxial, ovules (uni)bitegmic, epitropous, (nucellar tracheids +), (several archesporial cells); cupule of valves [one more than fruit number], ± spiny, fruit nut-like, trigonous; endocarp hairy inside; seed pachychalazal; (endosperm cellular); n = 12 (13, 21).

7[list]/670 - 2 subfamilies below. More or less worldwide (map: from Soepadmo 1972; Fl. N. Am. III. 1997).

1. Fagoideae K. Koch

Ellagic acid 0; inflorescence capitate; staminate flowers: pollen exine fine scabrate; carpellate flowers: ovule ?orthotropous ["unanatropous"], micropyle bistomal, elongate [Fagus], nucellar cap 0, pollen tube at ovule at dormancy, stigma capitate; cotyledons folded; germination epigeal.

1/10. Temperate N. hemisphere. [Photo - Fruiting Branch © M. Brand.]

2. Quercoideae Õrsted

Inflorescence spike or catkin, staminate and carpellate flowers on separate inflorescences or not; staminate flowers: pollen exine also (micro)verrucate or smooth, infratectum granular, (pistillode secreting nectar); carpellate flowers: ovule with single parietal layer, nucellar cap +, integuments the same length [micropyle endostomal?], pollen tubes in style at dormancy, (style relatively long, occupying most of the gynoecium), stigmas capitate, decurrent, or punctiform and with a terminal pore; cupule also cup-shaped, with scales; fruit also rounded, (endocarp glabrous inside - some subgenus Guercus); germination hypogeal or epigeal.

6/640: Quercus (400), Lithocarpus (120), Castanopsis (110). N. temperate, at higher elevations in the tropics, not S. Africa or New Zealand, barely in Australia. [Photo - Fruit]

Synonymy: Quercaceae Berchtold & Presl

• The family is readily recognisable in fruit. The distinctive cupules enclose one to three fruits, and the seed itself is often surrounded by dense hairs coming from the endocarp. The outer surface of the wood is characteristically furrowed, and the inflorescences are erect to pendant, spicate to catkinate. The leaves are stipulate and usually spirally inserted, serrate (if entire the venation is camptodromous - the secondary veins do not terminate at the margins), and rather leathery, and the hairs are stellate or branched.

Evolution. Some fossil taxa have a very different morphology to that of extant representatives, see e.g. the staminate and perfect flowers of Antiquacupula where there are also suggestions of nectary lobes between the stamens, the pollen has a perforate tectum, and the inner walls of the fruit loculi are glabrous (Sims et al. 1998). Flowers of Antiquacupula have a floral formula of P 3 + 3; A 12; G 3, the outer whorl of six stamens being opposite the tepals, the inner whorl alternating with them (Sims et al. 1998). The oldest fossils assignable to the family may be from some 90 million years before present (Crepet et al. 2004 for references).

Theclines (Lycaenini) are commonly found on this family (Ehrlich & Raven 1964). Indeed, oaks support the highest diversity of herbivores of all temperate holarctic forest trees. By some estimates half of all galls in the north temperate region are found on the family, especially on oaks (Mani 1964; Abrahamson et al. 1998), including an extensive radiation of perhaps 1,000 species of the species-rich gall wasps, Cynipini (perhaps two thirds of the species in the whole group: Csóka et al. 2005; Stone et al. 2009). These Cynipini show very considerable host plant conservatism that has persisted over the last ca 20 million years at least, members of major clades of gall wasps usually having associations with major clades of oaks (Stone et al. 2009).

The chestnut Castanea dentata, previously the dominant large tree in extensive areas of forest in eastern North America and an important source of food for humans and other animals, has been utterly devastated by the introduced ascomycete fungus Cryphonectria parasitica (Endothia parasitica) over a period of less than forty years. Castanea dentata may persist in the understorey for some time after infection because it continues to sucker from collars of the old trees or from stumps, but the suckers practically never reach reproductive age (Schlarbaum et al. 1997).

Fertilisation is porogamous, according to Johri et al. (1992), although it is much delayed (Sogo & Tobe 2006d and references; Deng et al. 2008). Quercoideae such as Castanea and Castanopsis are insect pollinated.

Members of Fagaceae are often very common in north temperate areas, but also on hills and mountains in Central America and Malesia, and they produce large numbers of fruits. When their abundance is combined with the tendency of a number of species to show masting behaviour, their effect on the animals that depend on these fruits is considerable. Red oaks (section Lobatae) take one and a half years to mature their fruits and the seeds are high in tannins and lipids; the fruits of white oaks (section Quercus) mature in about six months and their seeds are less rich in tannins and lipids, furthermore, their seeds tend to germinate faster. Much has been written about the behavior of animals that eat and disperse the acorns of these species. Thus squirrels tend to eat the embryos of white oaks before caching the fruits, although in general they prefer to eat acorns of white oaks in the fall and to cache those of red oaks (Wood 2005 for literature).

A mitochondrial gene has moved from the parasite Mitrastemon (Ericales) to its host, Quercus (Systma et al. 2008).

Chemistry, Morphology, etc. There has been infinite discussion over the morphological nature of the small protrusions surrounding the ovary, and the whole complex is often interpreted as a modified cymose inflorescence (e.g. Sims et al. 1998; Manos et al. 2001a; Pigg et al. 2001; Oh & Manos 2008 for references). When the cupule has valves, probably the plesiomorphic condition, there is one valve more than the number of fruits. Oh and Manos (2006, 2008) suggest that the apparently unitary scaly or spiny cup-shaped cupule that encloses a single, rounded fruit, the acorn, has evolved more than once within Quercoideae.

For intergeneric and -subfamilial graft hybrids, see Herrmann (1951). Denk and Grimm (2009) describe the pollen morphology in the family, focusing on Quercus; I follow the terms that they use. For the orientation of the carpels, see Endress (1977a), where the median member of outer P whorl in both staminate and carpellate flowers is shown as being abaxial, cf. Sims et al. (1998). Variation in ovule and fruit is extensive, and is conveniently tabulated by Deng et al. (2008); the polarity of some of this variation is unclear. The outer integument is vascularised.

See also Hegnauer (1966, 1989: chemistry), Loreto et al. (2009: terpenes - monoterpenes, isoprenoids - in Quercus), Axelrod (1983: distributional history), Nixon (1989), Kubitzki (1993b: general), Lersten and Horner (2008b: leaf crystals, etc., comparison with Nothofagaceae, similar) and Liu et al. (2009: stomata, hairs) for information.

Phylogeny. Fagus is sister to rest of Fagaceae (Manos et al. 1993); Quercoideae s. str. are paraphyletic, and Trigonobalanus is sister to the rest of Quercoideae + Castaneoideae, but all three are here combined as Quercoideae. For phylogeny, character evolution, and biogeography of Fagaceae, see e.g. Manos and Stanford (2001) and Manos et al. (2002).

Trigonobalanus was known from Fraser's Hill in Peninsula Malaya, but was described only some 40 years ago from Mt Kinabalu in Borneo, then it was found in South America 20 years ago, then from fossils in North America; the three extant species placed have been placed in three genera, but they form a single clade (Nixon & Crepet 1989 for information).

Recent studies (Oh & Manos 2006, 2008) suggest that Lithocarpus, which has fruits like those of Quercus, is polyphyletic, the South East Asian members grouping with Chrysolepis. However, the single species from the California floristic province of West North America, L. densiflorus (now = Notholithocarpus, is in a clade with Quercus, Castanopsis, and Castanea. For a phylogeny of Lithocarpus, see Li et al. (2009). Quercus contains species with fast-maturing acorns and a pericarp that is glabrous inside - both derived characters - and species in which the acorns take 1 1/2 years to develop and the endocarp is hairy inside. For phylogenetic relationships within Quercus, see Manos et al. (1999) and Oh and Manos (2008); New and Old World species are in separate clades.

Classification. Govaerts and Frodin (1998) provide a checklist and bibliography for the family.

[[Myricaceae [Juglandaceae + Rhoipteleaceae]] [Casuarinaceae [Ticodendraceae + Betulaceae]]]: myricetin +; pollen pororate, G [2]; fertilization chalazogamous.

Chemistry, Morphology, etc. At what level should "archesporium multicellular" be placed? Several features of wood anatomy, including the presence of chambered crystals in the axial parenchyma (although this may properly be a feature of Fagales as a whole), are also common in the group (Carlquist 2002c). A number of taxa have pollen walls with small granules clustered around the aperture near the inside (Feuer 1991).

[Myricaceae [Juglandaceae + Rhoipteleaceae]]: chains of crystal-containing cells in the wood; sieve tube P-protein bodies 0; peltate glandular hairs +; stipules 0; 1 flower/bract; ovule single [per flower], straight, stigma lamellular/laciniate.

Phylogeny. The evolution of features of inflorescence and ovule is particularly difficult to understand; they could be synapomorphies of the clade as a whole (as above), or be independent apomorphies of Myricaceae and Juglandaceae-Juglandoideae. Herbert et al. (2006) discuss possible synapomorphies of this clade.

MYRICACEAE Kunth, nom. cons.   Back to Fagales

Roots often with N-fixing Frankia, rootlets clustered, of limited growth [Proteoid roots]; nodes also 1:1; leaves (pinnatifid), conduplicate to curved, stipules 0 or ?foliaceous, lobed [Comptonia]; plants dioecious or monoecious; one flower/bract; P 0 (6-lobed - Canacomyrica), staminate flowers: A 1-8(-20) (opposite P); carpellate flowers: (staminodes + - Canacomyrica); G [(3)], ?superior to inferior, ovule basal, straight, (bitegmic, ?micropyle - Canacomyrica), fertilisation porogamous; fruit a drupe; seed ?pachychalazal, testa ± thickened; n = 8, 12.

3[list]/57: Myrica (55). ± Cosmopolitan, including New Caledonia but not Australia (map: Hultén 1958; van Balgooy 1974). [Photos - Collection.]

• Myricaceae are woody plants recognisable by the aromatic glands that cover the plant coupled with the spiral, simple, rarely deeply lobed leaves.

Evolution. Myricaceae are associated with nitrogen-fixing Frankia and the rootlets are clustered and of limited growth; mycorrhizae appear to be absent.

Although fertilisation is porogamous, it is delayed as in other Fagales, the growth of the pollen tubes as it were pausing on the nucellar surface; this method of fertilization, described as pseudoporogamy, may be derived (Sogo & Tobe 2006a, b). The flowers of plants of some species differ in sex from year to year (Jurzyk 2005 and references).

Chemistry, Morphology, etc. Bracteoles may be present or not. Although the ovary appears to be superior, as in Comptonia, it is often so highly reduced that any traces of its inferior construction would be lost, however, in Canacomyrica, from New Caledonia, staminodes are borne on top of the ovary and there is a six-lobed perianth. In some species of Myrica the ovary is invested by tissue from a meristem developing below the flower, even below the bracteoles, which are then borne on the flower. The flowers of Canacomyrica have three "bracts" (Herbert et al. 2006) - do these represent a floral bract plus two bracteoles/prophylls? Kubitzki (1993b) draws the ovule of Canacomyrica as being basal, straight, and with a much elongated integument forming an apical tube; Herbert et al. (2006) simply describe the ovules as being bitegmic.

For chemistry, see Hegnauer (1969, 1990), for the staminate flowers, see Macdonald (1978), for general information, see Kubitzki (1993b), and for wood anatomy, see Carlquist (2002c).

Synonymy: Canacomyricaceae Doweld

Juglandaceae + Rhoipteleaceae: leaves odd-pinnate; P 4; endosperm 0; x = 16.

Including Rhoipteleaceae in Juglandaceae s.l. is optional in A.P.G. II (2003); the two were merged in A.P.G. III (2009).

For karyomorphology, see Oginuma (1999).

JUGLANDACEAE Perleb, nom. cons.   Back to Fagales

Flavones, naphthoquinones, raffinose and stachyose [phloem exudate] +; nodes also 5:5; leaves spiral, leaflets subopposite, (involute or ± conduplicate [Alfaroa]; margins entire); (inflorescence branched), one flower/bract, bracts and/or bracteoles ± adnate to flower or not, (P 0-3); staminate flowers: A 2-many, opposite P, pollen porate, apertures usu. elongate, pistillode +; carpellate flowers: G [(3, 4)], median or transverse, median member adaxial, apically 1-locular, loculi often divided [false septae], ovule erect, born at the top of the incomplete septum, (fertilisation porogamous), (stigmas not decurrent); fruit drupaceous, nut, samaroid, or winged by persistent bracts, pericarp intrusive; seed large, pachychalazal, cotyledons much folded.

7-10[list]/50 - 2 groups below. North temperate, S. to Argentina and Malesia. [Photo - Collection.]

1. Engelhardioideae Iljinskaya

Leaf parenchyma with druses [basal - none]; buds lacking scales; leaves (opposite), even-pinnate, leaflets usu. entire; bracts 3-lobed, bracteoles 0-2, adnate to lower half of ovary; nuts with a layer of fibrous cells.

3-4/14. Himalayas to Malesia, Mexico to Colombia (map: see Meusel et al. 1965; Manchester 1987).

Platycarya (Engelhardioideae) is distinctive in having cone-like infructescences, male and female flowers are in the same spike, bracts are not part of the fruit, the sticky pollen and strongly scented flowers suggest insect pollination, etc. (Li et al. 2005 and references).

Synonymy: Engelhardtiaceae Reveal & Doweld, Platycaryaceae Doweld

2. Juglandoideae Eaton

Vessel elements with simple perforation plates alone; buds usu. with scales; staminate flowers: bracts 1-lobed, pollen usu. at least 26 µm [17-26 µm is the plesiomorphic condition] (with 4 or more pores); carpellate flowers: bracts unlobed, bracteoles usually lateral and adnate to the ovary; nuts with sclereids in shell, (endocarp with lacunae; outer part of fruit dehiscing [Carya]); (n = 15).

3-6/35. Temperate N. hemisphere, only 1 sp. in Europe, Central America and Andes (map: see Meusel et al. 1965; Manchester 1987).

• Juglandaceae are evergreen or deciduous trees that may be recognised by the small, aromatic glands on the young parts of the plant; the compound, estipulate, usually spiral leaves the leaflets of which are often serrate; and the spicate inflorescences with single, axillary flowers. The endocarp of the drupaceous fruit often has complex intrusions.

Evolution. The oldest fossils assignable to Juglandaceae may be from some 83-98 million years before present (Crepet et al. 2004 for references) or 78 million years before present (Manos et al. 2007, based on the age of Caryanthus). However, details of timing of diversification in the family are unclear, there being great variation of estimates in Juglandoideae in particular (Manos et al. 2007). Several genera are fossil in North America and especially Europe that are not found there now (Manchester 1987 - for the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. 2009), and several extinct genera, some showing very interesting combinations of characters, are known from early Tertiary deposits in North America - clearly the family was very diverse there (Elliott et al. 2006). It seems that taxa with biotic means of dispersal evolved in the early Tertiary from taxa that were probably dispersed by wind (Tiffney 1986).

Chemistry, Morphology, etc. Triads of flowers are found as abnormalities (Manning 1940). Perfect flowers are known from Platycarya (Li et al. 2005, for which see floral development). Genera with opposite leaves (Alfaroa, Oreomunnea) have spiral leaves in seedlings. The stigma may be commissural or not and the orientation of the carpels varies (Manos & Stone 2001 for a summary). Pororate pollen in Juglandaceae is unlike that in other Fagales (Feuer 1991).

For chemistry, see Hegnauer (1966, 1989), for general information, see Stone (1993), for fertilisation, Luza and Polito (1991 and references), for relationships in the family, Gunter et al. (1994), for the fossil record, which is particularly well-known, Manchester (1991 and references).

Phylogeny. Manos and Stone (2001) provide a phylogeny and revised classification of the family; adjustments to current generic limits are needed. Engelhardia may be paraphyletic (Manos & Stone 2001).

RHOIPTELEACEAE Handel-Mazzetti, nom. cons.   Back to Fagales

Chemistry?; cork?; sieve tube protein bodies?; buds lacking scales; leaves two-ranked, stipules asymmetrically caudate; inflorescence branched, flowers in triads; A 6, pollen 3-colporate, [ectoapertures elliptic, not round]; G [2], ovule campylotropous, bitegmic, micropyle ?, fertilisation unknown, stigmas flattened, commissural, recurved; fruit a samaroid nut; P persistent; testa?.

1[list]/1: Rhoiptelea chiliantha. China, northern Vietnam, but fossil pollen from E. North America (map: from Fu 1992).

• Rhoipteleaceae may be recognised by their stipulate and odd-pinnately compound leaves with serrate leaflets, indumentum of peltate scales, and branched, pendulous inflorescences with flowers in triads, the central flower apparently being perfect and having a superior ovary.

The ovary of Rhoiptelea is presumably secondarily superior.

For chemistry, see Hegnauer (1990), for the breeding system, Sun et al. (2006), and for general information, see Wu and Kubitzki (1993).

Casuarinaceae [Ticodendraceae + Betulaceae]: dihydroflavonols +[?]; stigmas elongate.

Evolution. Sogo and Tobe (2008) suggest that the chalazogamous fertlization that occurs in all families of this clade is similar down to the details of where the pollen tube growth is temporarily delayed.

CASUARINACEAE R. Brown, nom. cons.   Back to Fagales

Roots with N-fixing Frankia, rootlets clustered, of limited growth [Proteoid roots]; flavonols, biflavonoids +, flavones, myricetin 0; nodes 1:1; stomata usu. tetracytic [hidden], transversely oriented [?sampling]; leaves 4-16-whorled, scale-like, margins entire, stipules 0; plant monoecious or dioecious, inflorescence capitate-spicate, one flower/bract, bracts and bracteoles ± well-developed; staminate flowers: P ["inner bracteoles"] 2, median, A 1, filaments incurved in bud, anthers ± longer than connective, granular layer 0, pollen tube branched, pistillode 0; carpellate flowers: bracteoles large; P 0; G median, naked, only abaxial fertile, ovules straight, bitegmic, micropyle endostomal, archesporium multicellular, embryo sac with micropylar and chalazal caecum/haustoria, nucellar tracheids +; fruit a samara, freed as the much accrescent bracteoles separate; seed coat adnate to pericarp, testa vascularised?; endosperm 0; n = 8[Gymnostoma]-14.

4[list]/95. South East Asia and Malesia to the S.W. Pacific, esp. Australia (map: from Coetzee & Muller 1984; George 1989). [Photo - Collection.]

• Casuarinaceae are easily recognised, looking as they do rather like a conifer. The minute leaves are whorled, and the carpellate inflorescence forms a small cone. The bracteoles that gape widely at maturity to release the samara fruits are very distinctive.

Evolution. Casuarinaceae fossils are known from Tertiary deposits in South Africa and Argentina (Coetzee & Muller 1984); material from the Eocene of Patagonia has been identified as Gymnostoma (Zamaloa et al. 2006). Some diversification in Allocasuarina may be associated with the aridification of the Nullarbor Plain some 14-13 million years ago separarting eastern and western clades (Crisp & Cook 2007).

Chemistry, Morphology, etc. Do flavananols occur in this family? The texture of what some have called the outer and inner bracteoles is very different; the latter is called the perianth above. The starch grains are distinctive (Czaja 1978). The ovules are described as being ascending by Takhtajan (1997).

See Hegnauer (1964, 1989: chemistry), Rogers (1982a), Johnson and Wilson (1993: general) and Sogo et al. (2001: fertilization) for further information.

Phylogeny. Steane et al. (2003) provide a phylogeny of the family. Although the monophyly of Causarina has never been in doubt, it has been split into four genera, themselves probably monophyletic; Gymnostoma is sister to the rest of the family and has many plesiomorphous features. Both carpels are fertile (although this feature is likely to be an apomorphy, given the situation in the rest of the order), with 2 ovules/carpel, its stem stomata are not hidden, and perhaps n = 8.

Ticodendraceae + Betulaceae: sclereid nests in bark, cells with large rhomboidal crystals; mucilage cells +; leaves two-ranked.

TICODENDRACEAE Gomez-Laurito & L. D. Gomez P.   Back to Fagales

Bud scales 0?; foliar idioblasts +; hairs T-shaped, unicellular, not glandular; stipules encircling the stem; plant (polygamo-)dioecious; staminate flowers: P 0; A 8-10+, thecae almost separate; carpellate flowers: single, ?P minute, connate; G with divided loculi, ovules epitropous, hemitropous, integument 20-30 cells across; fruit drupaceous; exotestal cells initially radially elongated, all cells ± thick-walled and tanniniferous; endosperm development?; n = 13.

1[list]/1: Ticodendron incognitum. Central America (map: from Hammel & Burger 1991). [Photo - Fruit]

• Ticodendraceae are wind-pollinated trees that may be recognised by their doubly-serrate leaves that have stipules encircling the stem and carpellate flowers with two, long stigmas.

Evolution. Fruits assignable to Ticodendron have been found in Eocene deposits from Oregon and in the London Clay (Manchester & Renner 2005).

Chemistry, Morphology, etc. The nodes are trilacunar, judging from the condition in the outer cortex. Lersten and Horner (2008c) describe hypodermal idioblasts (they also occur below the midrib); these sometimes contain druses, and the authors suggest that they may be an apomorphy for the family. Almost all the leaf teeth are vascularised directly by secondary veins, unlike Betulaceae. The bracteoles of the carpellate flowers have groups of vascularised scales in their axils, suggesting that the carpellate inflorescence has a fundamentally cymose construction.

For information, see Carlquist (1991: wood), Feuer (1991: pollen), Tobe (1991: floral morphology), Kubitzki (1993b: general), and Sogo and Tobe (2008: fertilization).

Classification. For a checklist and bibliography, see Govaerts and Frodin (1998).

BETULACEAE Gray, nom. cons.   Back to Fagales

Trees or shrubs; flavones +; stratified phloem +; sieve tube P-protein usu. 0; leaves usu. laterally or vertically conduplicate, colleters +; plant monoecious or dioecious, catkinate; P 0-6, staminate flowers: (filaments ± divided), anthers longer than connective, pollen starchy, tube branched; G 0; carpellate flower: A 0; G [(3)], transverse (median), septae incomplete, (1-4 ovules/carpel), (short style +); n = 8, 11, 14; horizontal transfer of rps11 gene; sporophytic incompatibility system present.

6[list]/145 - 2 groups below. North Temperate, to Andes and Sumatra (map: from Meusel et al. 1965; Hultén 1971). [Photo - Flower]

1. Betuloideae Arnott

No spirally-thickened vessel elements; peltate glandular hairs +; (leaves spiral Alnus); carpellate flowers: P 0; infructescence with woody or scaly bracts separate from small, ± flattened and samaroid nut.

2/95: Betula (60). N. hemisphere, to South America; montane in tropics.

2. Coryloideae J. D. Hooker

Spirally-thickened vessel elements, tracheids +; cymule with <3 flowers; staminate flowers: P 0; A hairy; carpellate flowers: P +, (embryo sac with chalazal caecum); infructescence with leafy bracteoles [from one or two orders of branching] remaining associated with the fruit; nuts large, not or little flattened.

4/50. N. Temperate, South East Asia, Central America.

Synonymy: Carpinaceae Vest, Corylaceae Mirbel

• Betulaceae are usually deciduous trees that may be recognised by their stipulate, doubly serrate leaves, catkinate inflorescences (both staminate and carpellate), and fruits are that are either small and flattened or associated with large, leafy bract-like structures.

Evolution. The oldest fossils assignable to the family are from 94-83 million years before present (Crepet et al. 2004 and Forest et al. 2005 for references). Normanthus and Endressanthus, from the late Cretaceous of Portugal, may be close to the root of the Betulaceae clade (Friis et al. 2005); the former has has perfect flowers with five perianth members that alternate with the stamens, and the placentation is described as being parietal (Schönenberger et al. 2001b; Friis et al. 2003a).

Alnus is well known as a N-fixing plant, and may be used in land remediation; cluster roots have been reported from the genus (Shane & Labers 2005).

In Corylus avellana in particular there may be three to five months between pollination and fertilisation, ovules starting to develop about half way through this period and the nuts being 7-10 mm across at the time of fertilization. If pollination does not occur, the stigma may remain receptive for up to three months (Germain 1994).

Chemistry, Morphology, etc. Alnus has a single adaxial prophyll. Staminate flowers in Coryloideae are sometimes reported as being single (e.g. Mabberley 1997), however, as Abbe (1935) noted, there are usually three together; the staminate "flower" of Ostrya, with some 15 pairs of half stamens, is pseudanthial in origin, also being derived from three flowers (Abbe 1935, 1974; Macdonald in Sattler 1973: see also Nothofagaceae). In staminate flowers of Corylus the perianth is reduced to a ridge. see Endress (2008c) for the structural lability of female flowers of Carpinus betulus. The ovary of Corylus is not always obviously inferior. Betula has three carpellate flowers per bract.

See Horne (1914), Heller (1935), Abbe (1935: flowers, inflorescences), Hegnauer (1964, 1989: chemistry), Crane (1989), Kubitzki (1993b: general), Manchester and Chen (1998), Chen et al. (1999: phylogeny and evolution) for more information.

Phylogeny. Although Li et al. (2004) suggested that Betuloideae were paraphyletic, with Alnus and Betula being successively sister to the rest of the family, Forest et al. (2005), analysing variation in ITS and the 5S spacer, recovered the two subfamilies as monophyletic. The monophyly of Ostrya and Carpinus is unclear, as are many of the basic characters of Coryloideae (see Yoo & Wen 2002, 2007, 2008).

Classification. The two subfamilies are sometimes recognised as families, as by Brummitt (1992). For a checklist and bibliography, see Govaerts and Frodin (1998: as Corylaceae and Betulaceae).