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 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, 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, stigma ± decurrent, dry [not secretory]; P deciduous in fruit; seed exotestal; pollen germinating in less than 3 hours, tube elongated, growing at 80-600 µm/hour, with callose plugs and callose-based walls, penetrating between cells, siphonogamy, penetration of ovules within ca 18 hours, distance to first ovule 1.1.-2.1 mm; 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....

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with 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.

SANTALALES [CARYOPHYLLALES + ASTERIDS]: ?

SANTALALES Dumortier  Main Tree, Synapomorphies.

Mycorrhizae absent; polyacetylenes [triglycerides with C18 acteylenic acids], triterpenic sapogenins + [Loranthaceae?]; cork subepidermal; perforation plates not bordered; intervascular pits alternate; tension wood?; pericyclic fibers 0; (cuticle waxes with annular rodlets, palmone common); petiole/mesophyll with astrosclereids; lamina entire; inflorescences cymose; K often reduced, C valvate; A opposite petals, epipetalous, anthers basifixed, pollen colpate or porate, disc +; G [3], 1 pendulous apotropous tenuinucellate ovule/carpel, micropyle endostomal, style +, stigma small, globose; fruit a drupe, 1-seeded, K persistent; seed coat crushed; chalazal endosperm and embryo sac haustoria +, embryo minute, green. - 8 families, 151 genera, 1985 species.

Evolution. Anderson et al. (2005) date stem group Santalales at 115-113 million years before present, crown group members at 108-101 million years before present (sampling is adequate).

Caterpillars of some Pieridae-Pierinae (ca 440 species recorded, but on only 9+ genera; 2/5 of all host-plant records) and Lycaenidae-Lycaeninae-Iolaini in particular are found on members of this order, Loranthaceae (especially), "Olacaceae" (= Ximenia, Olax: Lycaeninae), Opiliaceae and Santalaceae being recorded hosts (Ehrlich & Raven 1964; Fiedler 1991, 1994; Congdon & Bampton 2000). The ancestors of the pierine butterflies seem for the most part to have eaten members of Brassicales and their initial santalalean hosts may have been Loranthaceae; again, there are no reports of caterpillars on free-living Santalales (Braby 2005; Braby & Trueman 2006; Braby et al. 2006: I thank M. F. Braby for information). Interestingly, a number of the adults of these butterflies have warning colourations on the undersides of the wings, and some caterpillars may also have warning colourations. However, it is unclear what compounds the insects might pick up from their santalalean hosts that would discomfit potential predators (Braby & Trueman 2006), although movement of alkaloids from host to parasite is known to occur in both Santalaceae and Loranthaceae (Cabezas et al. 2009).

It is clear from the phylogeny of the order that the plesiomorphic condition in it is the free-living habit, and hemiparasitism by attachment to the roots of the host is derived (Malécot 2002; Malécot et al. 2004). Aerial hemiparasitism has been derived some five times (Nickrent 2002), intermediate taxa perhaps being both root and stem parasites (Vidal-Russell & Nickrent 2008); photosynthesis in some aerial hemiparasites is largely in their stems. Aerial hemiparasites may have a single point of attachment to their host, or roots running over the surface of the bark may form both additional points of attachment and additional plantlets (as in Loranthaceae: Vidal-Russell & Nickrent 2006, 2008). Some Santalales are largely endophytic, even if the part of the plant that finally appears is chlorophyllous (Santalaceae, e.g. some species of Viscum and Arceuthobium), while Balanophoraceae are holoparasitic (Nickrent et al. 2005). Some Loranthaceae are hyperparasites, parasitizing other members of that family, while some species of Phoradendron (Santalaceae) are obligate parasites on other members of the genus (Calvin & Wilson 2009). For some information on the physiological details of parasitism in Santalales, see Stewart and Press (1990).

Although little is known about mycorrhizae in Santalales, the few taxa studied largely lack them (Landis et al. 2002), exceptions being Ongokea, Coula and Strombosia, scattered in ex-Olacaceae (Malécot 2002 for references). The absence of mycorrhizae, as well as that of root hairs which has been reported for the group (see below), could well be connected with the adoption of the hemiparasitic habit.

Chemistry, Morphology, etc. There are several other distinctive features in Santalales whose systematic significance is unclear. Absence of root hairs may be a synapomorphy (Judd & Olmstead 2004), but are they also absent from Erythropalaceae? The pits are notably variously bordered throughout the order (Herendeen et al. 1999b); Carlquist (2006) suggests that non-bordered perforation plates is a possible similarity with Caryophyllales. The foliar vascular bundles may lack fibers (but cf. "Olacaceae", Loranthaceae, ?some Opiliaceae). Terminal tracheids and cristarque cells are scattered, but their exact position on the tree is unclear (Baas et al. 1982; Kuijt & Lye 2005). Wax tubules with palmitone as the main wax occur in several members (Ditsch & Barthlott 1997). The vasculature of the inferior ovary of Darbya (= Nestronia, Santalaceae) and other members of the order suggests that they have become inferior by investment of tissue that is axial in origin (Smith & Smith 1942, 1943; Eyde 1975). The single perianth whorl found in some Santalales may represent the corolla of other members (Wanntorp & Ronse De Craene 2009), however, at least sometimes it has three vascular traces, two coming from commissural bundles (Smith & Smith 1943); what appears to the outer perianth whorl may be a caylculus of paired and prophyllar origin (Wanntorp and Ronse De Craene 2009). Whether the presence of a calyculus is a fairly high level apomorphy in the order, or not, depends on more extensive developmental studies. Tracheids in the nucellus have been reported from some species, as has vascular tissue directly reaching the embryo sac (Werker 1997). The mitochondrial coxII.i3 intron is absent in Comandra, the only member of the order to have been sampled.

For general information, see Barlow (1997), Calder and Bernhardt (1983), Reed (1955), and especially Mathiasen et al. (2008: an excellent survey and summary of the stem parasitic Santalales), for (poly)acetylenic and related fatty acids found in the seeds, see Badami and Patil (1981), for anatomy, see Baas et al. (1982), for hemi-parasitism, see Fineran (1991), and for additional information on relationships, see Nickrent and Duff (1996), Nickrent et al. (1998), for pretty much everything, see Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008).

Phylogeny. Malécot (2002) provides a phylogeny based on the analysis of variation in four genes that emphasises members of the old Olacaceae; he discusses variation of morphological characters in the context of this phylogeny and also provides analyses of a combined morphological-molecular data set. Although there is still little well-supported structure along the spine of basal Santalales (= "Olacaceae" s.l.: see the tree below), a number of clades appear to be fairly well supported. Hence Malécot's results and classification are largely followed here; they suggest i.a. that (hemi)parasitism is derived within the clade (see also Malécot et al. 2004), the Erythropalaceae, sister to all other Santalales, being free-living. Erythropalaceae, although poorly supported, differ in many features other than life style from other Santalales, and many of these are probably plesiomorphic (data from Michaud 1966; Malécot 2002 - see also Malécot et al. 2004 for a morphological phylogenetic analysis). However, confirmation of where they should be placed on the tree waits for a strongly-supported resolution of relationships within Santalales and between Santalales and other core eudicots. Malécot et al. (2004) found some support for Erythropalaceae, Ximenia plus some other genera, and most of the rest of the old Olacaceae (a very weakly supported clade) as three clades successively sister to the rest of Olacales in a morphological analysis. Recently, Malécot and Nickrent (2008) have found the old Olacaceae to form about eight clades basal to other Santalales, but relationships between these clades are still unclear. Molecular data place Brachynema, a genus that is so morphologically distinctive that its inclusion in the order was in some doubt (e.g. see versions 8 of this site and earlier), close to Maburea, in Erythropalaceae s. str. (K. Wurdack, pers. comm.). Within the Loranthaceae et al. clade, Misodendraceae are often sister to [Schoepfiaceae + Loranthaceae], especially in analyses that include many taxa, although when the number of taxa is reduced they may be sister to Schoepfia in particular (Malécot 2002, see also Nickrent et al. 1998; especially Der & Nickrent 2008 and Vidal-Russell & Nickrent 2008); this position is followed here. Opiliaceae (one genus) was strongly supported as being sister to a clade [Santalaceae + Viscaceae} in Soltis et al. (2007a), but this may in part be a sampling issue. Der and Nickrent (2008) show that Santalaceae are polyphyletic, a few genera being removed to Opiliaceae and Schoepfiaceae, while within Santalaceae there are eight well supported clades (see below).

Mystropetalum, Dactylanthus, and Hachettia, three members of Balanophoraceae, form a clade with 100% posterior probability that was sister to a clade made up of Schoepfia, Dendrophthoe and Santalum (almost 100%), the combined group having 100% support (Nickrent et al. 2005), so Balanophoraceae are included in Santalales here, but without any particular position in the clade (see also Nickrent 2002; Nickrent & Duff 1996; Barkman et al. 2007). Su and Hu (2008) analysing variation in B-class floral genes and with a quite good taxon sampling suggested that Balanophoraceae were basal or near basal (with respect to the other families) in the clade. Further work is needed to resolve details of all these relationships, especially increased sampling in Balanophoraceae, which are the only Santalales known to be holoparasitic. However, being holoparasitic, they lack most or all of the distinctive vegetative features of other Santalales.

Previous Relationships. Santalales have often been compared with Icacinaceae (now known to be polyphyletic), also with single-seeded fruits, often small calyx, valvate corolla, etc. (e.g. Takhtajan 1997), but there is little evidence suggesting such a relationship.

Includes Balanophoraceae, Erythropalaceae, Misodendraceae, Olacaceae, Opiliaceae, Loranthaceae, Santalaceae, Schoepfiaceae.

Synonymy: Anthobolales Dumortier, Balanophorales Dumortier, Erythropalales van Tieghem, Heisteriales van Tieghem & J. D. Hooker, Henslowiales Lindley, Loranthales Dumortier, Olacales Bentham & J. D. Hooker, Viscales van Tieghem, Ximeniales van Tieghem - Balanophoranae Reveal, Santalanae Reveal - Loranthopsida Bartling, Santalopsida Brongniart

ERYTHROPALACEAE Miquel, nom. cons.   Back to Santalales

Trees, shrubs or lianes; (plants Al-accumulators; arbuscular mycorrhizae +; (laticifers +); vessel elements with scalariform perforation plates; rays 7³ cells wide; sieve tubes with non-dispersive protein bodies; nodes 3:3 (5:5); petiole bundle annular (with adaxial plate); (epidermis lignified; with druses), stomata anisocytic (other), cuticular thickening +, large guard cell chamber; (hairs stellate); leaves spiral or two-ranked, conduplicate; (plant dioecious), inflorescence various; flowers small, 3-6-merous, hypanthium + or 0, K small, often cupular, (valvate - Heisteria), teeth inconspicuous, C basally connate and with adaxial hairs or not, stamens = or 2 (3) x C (some staminodial), connective massive (not), (pollen colporate), (disc 0; extrastaminal); G [(2-5)] (semi-inferior), opposite sepals (opposite petals) or odd member adaxial, septate (not), ovules (horizontal), (unitegmic), style short to long, stigma lobed or not; (K much accrescent); endosperm with starch or oil, cotyledons 1-2, connate or not; n = 16, 19, 20.

13/65. Pantropical, Southeast Asia, not Madagascar, New Guinea and to the S.E. (map: from Michaud 1966; Sleumer 1984a, b; Malécot 2002).

The stamens differ quite considerably in size, and the smallest stamens are opposite the petals, the largest stamens opposite the sepals (Michaud 1966). The gynoecium is often 10-ridged.

For some information on pollen, see Lobreau-Callen (1982).

The very distinctive Brachynema has vessel elements with scalariform perforation plates; nodes ?5:5; cristarque cells +; sclereids and sclereid nests +, pericyclic fibers +; pith [and in petiole] with diaphragms; petiole bundle annular; stomata anisocytic, cyclocytic, etc.; hairs unicellular; leaves spiral, margin with glandular teeth, stipules 0; inflorescence ± fasciculate, bracts and bracteoles 0?; flowers 5-merous, K connate, C long-tubular, valvate; A adnate to base of C, connective produced, pollen porate, nectary 0; G [3-5], 1 apical pendulous ?epitropous ovule/loculus, style 0; fruit subdrupaceous, K accrescent; ?testa undistinguished; endosperm with some starch and a yellowish sticky substance, embryo small, apical; n = ? [Photo - Flower.]

Brachynema has spirally-arranged leaves that are very unequal in size - particularly in petiole length, which varies from being about 20 cm to almost absent - in the one innovation and have glandular teeth, the petiole is pulvinate at both ends. The flowers are distinctive: the narrowly tubular corolla has valvate lobes and five stamens inserted at the base, and the spherical ovary has a sessile stigma. The connate calyx is accrescent in fruit, forming a cup under the single-seeded fruit; the seed is vertically channeled, vascular bundles running down the channels; I presume these vascular bundles are pericarpial in nature..

Baas et al. (1982: they examined Brachynema ramiflorum) recorded only infrequent and thin-walled sclereids. However, in the material examined there were numerous sclereid nests in the cortex, indeed, they sometimes formed an almost a continuous layer outside the pericycle. Furthermore, stem, petiole, and also, judging from the way young leaves had dried, even the midrib have strongly sclerified diaphragms in the pith; the inside of the xylem cylinder was strongly fluted. Sleumer (1984) described the inflorescences as being ebracteate corymbs. The seed coat is almost obliterated, and it is difficult to make out details of cell walls, etc. Sleumer (1984) described the endosperm as having amylum and fatty substances. The endosperm stains rather weakly for starch, and the cells contain yellowish globules, the "fatty" and "sticky" substances above.

Brachynema has often been associated with "Olacaceae" s.l. (Santalales), thus Lobreau-Callen (1980) placed it in Anacoloseae and Baas et al. (1982) placed it with Scorodocarpus in particular. It has also been linked with Ebenaceae (Ericales), as by Reed (1955) and others, while in a recent morphological phylogenetic analysis it appears close to Symplocaceae (Ericales; Malécot 2002). The stamens appear to alternate with the corolla members (see Sleumer 1984), rather unusual for Santalales, and indeed Brachynema has few of the more distinctive anatomical features of Santalales. However, its integument number - and indeed most details of its embryology, development, and chemistry - are unknown. Molecular data (K. Wurdack, pers. comm.) place it here, a position with which nodal anatomy and stomatal morphology, at least, are in agreement!

For vegetative anatomy, see Baas et al. (1982), and for general information, see Sleumer (1984). Brachynema axillare: floral morphology, Rimachi Y. 4465, fruit and vegetative anatomy, Liesener 16136.

The name Erythropalaceae for this clade may be incorrect, but I will keep it as it is, pending further studies to clarify the phylogeny of this part of Santalales.

Synonymy: Coulaceae van Tieghem, Heisteriaceae van Tieghem, Octoknemaceae Solereder, nom. cons. (cristarque cells +; ovary inferior; fruit drupaceous; seed longitudinally ruminate, embryo short, radicle very long, cotyledons 6), Scorodocarpaceae van Tieghem, Strombosiaceae van Tieghem, Tetrastylidiaceae van Tieghem (anthers polythecate).

"Olacaceae" [[[Misodendraceae + Schoepfiaceae] Loranthaceae] [Opiliaceae + Santalaceae]]: root hemiparasites; vessel elements with simple perforation plates; rays ³7 cells wide; nodes 1:1; sclerenchyma fibres of petiole and median vein 0; petiole bundle arcuate; stomata paracytic; silicification of some foliar mesophyll/epidermal cells; embryo sac with chalazal caecum and ± developed micropylar prolongation.

Chemistry, Morphology, etc. Graniferous tracheary elements are found in the haustoria of several unrelated members of the clade; the granules are usually proteinaceous, but are made up of starch in Ximenia (Fineran & Ingerfeld 1982). It is difficult to assign ovary position to a particular place on the tree. Olaceae have a superior ovary, and so do [Exocarpos + Omphalomeria] " a basal clade" in Santalaceae (Der & Nickrent 2005), Loranthaceae are inferior, Schoepfiaceae are half inferior. Either there are independent origins for the characters of inferior ovary, or reversals, or even both.

Ovule, embryo sac and embryo development of many Santalales, but probably not Erythropalaceae, is more or less remarkable. Distinct ovules may not be recognizable, the embryo sacs being borne in a spherical body, the mamelon; this consists of a basal placenta and everything else. Individual embryo sacs may elongate greatly and approach the apex of the mamelon or even the stigma at the end of a long style; Haig (1990) suggests that this may represent competition between female gametes given that their normal spatial constraints (i.e., being enclosed in an organised ovule) are absent. In any event, after fertilization the embryo is "planted" back down at the base of the mamelon by the development of a long suspensor (Fagerlind 1947a, 1948; Maheshwari 1950; Ram 1970; Bhatnagar 1970; Bhandari & Vohra 1983; Johri et al. 1992; Shamrov et al. 2001, and references). Cocucci (1983) outlines variation in ovary morphology and the distribution of starch-containing tissues (primarily in the style or the mamelon); these latter may be involved in the extraordinary growth of the embryo sacs.

"OLACACEAE" R. Brown, nom. cons.   Back to Santalales - note, probably paraphyletic.

Trees, shrubs or lianes; (plants Al-accumulators); sieve tubes with non-dispersive protein bodies; cuticle wax crystalloids 0 (platelets); cuticular thickening +, guard cell chamber small; leaves spiral or two-ranked, conduplicate; (plant dioecious), inflorescence various; flowers small, 3-6-merous, hypanthium + or 0, K small, often cupular, teeth inconspicuous, C (imbricate), basally connate and with adaxial hairs or not, stamens = or 2x C, (staminodes +), connective massive (not), (pollen colporate), (disc 0; extrastaminal); G [(2-5)] (semi-inferior), opposite sepals (opposite petals) or odd member adaxial, septate (not), ovules unitegmic, style short to long, stigma lobed or not; endosperm (helobial), with starch or oil.

14[list]/103. Pantropical (subtropics). [Photo - Flower, Fruit, Fruit.]

1. Olacoideae

SiO₂ bodies in ray cells; (nodes 3:3 - Dulacia); (K 0, but calyculus [bracteoles] +); A 1-2 x C, (staminodes 3-6); G [3], ridged or not, ovules unitegmic; (K much accrescent); cotyledons 0-1; n = 12.

3/57. Pantropical (also S.E. China, Formosa) (map: from Sleumer 1984a, b; George 1984; Malécot 2002).

Evolution. For the hemiparasitism of Olax phyllanthi, see Tennakoon et al. (1997 and references). Hibberd and Jaeschke (2001) provide a model of nutrient flow between host and parasite.

Chemistry, Morphology, etc. Again the smaller stamens may be opposite the petals, the larger stamens opposite the sepals. Olacoideae are ategmic, and Olax has endosperm haustoria reaching into the pedicel.

2. Anacalosoideae

(Arbuscular mycorrhizae + - Ongokea); (laticifers +); (bundle fibers +); flowers 4-5 merous, bracteoles ± connate; (anthers extrorse, porose or valvate; pollen 6-aperturate); G 2-3, ovules often bitegmic; K not/much accrescent, fruit surropunded by accesent disc or other strcutures; cotyledons 0-2, connate or not; n = ?

7/32. Pantropical (SE China, Formosa) (map: from Michaud 1966; van Balgooy 1993; Sleumer 1984a, b; Malécot 2002).

Evolution. For records of fossil pollen from the Upper Cretaceous (N. hemisphere) and Palaeocene (worldwide) onwards that are assignable to this clade, see Krutzsch (1988).

Synonymy: Aptandraceae Miers (A connate around style, anthers reflexed and so apparently extrorse - 3 genera. Ongokea has polyacetylenes, just like other "Olacaceae"), Cathedraceae van Tieghem, Chaunochitonaceae van Tieghem, Harmandaceae van Tieghem

3. Ximenioideae

Nodes 3:3; ovules uni- or bitegmic; Flowers 4-5-merous; A 1-2 x C; cotyledons 2, connate or not; n = 12, 13; germination hypogeal.

4/13. Pantropical, warm temperate (map: from van Balgooy 1993; George 1984; Sleumer 1984a, b; Malécot 2002).

Ximenia americana is crassinucellate.

Synonymy: Ximeniaceae Martinet

Within "Olacaceae", a number of taxa have green, zig-zag twigs; taxa with parallel tertiary venation are also quite common.

Cristarque cells are reported by Breteler et al. (1996). There is considerable discussion as to the number of integuments (e.g. information in Maas et al. 1992; Breteler et al. 1996; Malécot 2002), as well as cotyledon number. Some taxa may also have micropylar endosperm and embryo sac haustoria (Mickesell 1990).

Some data are taken from Baas et al. (1982: anatomy), Lobreau-Callen (1980: pollen), Robertson (1982: general) and Sleumer (1984: general).

[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]: guard cells not lignified; G not septate, ovules ategmic; testa 0; endosperm oily, starch 0.

Loranthaceae [Misodendraceae + Schoepfiaceae]: cambium storied; petiole astrosclereids 0; guard cell thickenings?; epidermal cells sclerified, with druses; K minute; G [3].

Misodendraceae + Schoepfiaceae: ?

MISODENDRACEAE J. Agardh, nom. cons.   Back to Santalales

Stem parasites; stem apex aborting; bundle fibers +; sieve tube plastids lacking starch and protein inclusions; plant dioecious; inflorescence (compound) raceme or spike; pedicels pubescent; staminate flowers: P 0; A 2-3, monothecal; pollen 4-12-colporate, spinuliferous; carpellate flowers: C 3; staminodes alternate with P; G superior; ovules straight; fruit dry, attached to 3 much accrescent staminodes growing from slits in the ovary to one side of the attachment of the C; seed coat with some sclereids; endosperm 0-copious, embryo short to large, cotyledons connate; n = ?; germination epigeal.

1/8. Cool temperate South America (map: from Heywood 1978). [Photos - Misodendron Flower, Misodendron Habit]

• Misodendraceae are dioecious stem parasites (their hosts are Nothofagaceae) that are recognizable by their stems, which are often thick, even when young, "giving the leafy species a rather elephantine appearance" (Kuijt 1969, p. 76). The leaves may be reduced, and those on flowering shoots are different in appearance from those on vegetative shoots; the two kinds of shoots are sharply distinguished. The flowers are small, and the small, nutlike fruits are very distinctive with their three, long, plumose attachments.

Evolution. Vidal-Russell and Nickrent (2006, 2007) estimate that stem parasitism in Misodendraceae evolved some time after the divergence of this clade, ca 75 million years before present, but well before stem parasitism in Loranthaceae, which occured ca 40 million years before present.

Chemistry, Morphology, etc. According to Takhtajan (1997) the pollen is colpate. For general information, see Kuijt (1969), for seeds and seedlings, see Kuijt (1982: corrections to earlier work), and for details of wood anatomy, see Carlquist (1985c).

Phylogeny. For a phylogeny of Misodendron, see Vidal-Russell and Nickrent (2007).

SCHOEPFIACEAE Blume   Back to Santalales

(Herbs); aliform confluent parenchyma +; hairs unicellular; bract and bracteoles immediately below and surrounding G; (flowers distylous), large, K ± 0[Aruna, or asymmetrical (Quinchmalium], C tubular, with adaxial hairs, pollen tetrahedral, heteropolar, colporate, apertures ± confluent, ektexine psilate; G (semi-)inferior, basally septate, ovules ?unitegmic, stigma lobed to capitate; embryo short; n = 12.

3/55: Quinchamalium (25). Central and South America, a few species in tropical South East Asia-Malesia (map: from Sleumer 1984, South East Asian mainland and South America only approximate distribution). [Quinchamalium flower.]

Chemistry, Morphology, etc. That Schoepfia is rather different from "Olacaceae" has often been remarked (e.g. Metcalfe & Chalk 1950; Sleumer 1984); the latter noted that the wood had aliform-confluent parenchyma. There are prominent bracteoles immediately below its flowers which look not unlike those of Loranthaceae, and the calyx and pollen of Schoepfia are also similar to those of Loranthaceae. However, pollen aperture development in Schoepfia follows Garside's Rule, there being three pores at four points in the tetrad (see Blackmore & Barnes 1995). Some information is taken from Smith and Smith (1943: floral morphology) and Dawson (1947: general), but some of the detail in the characterization above refers to Schoepfia alone; the family is very poorly known.

Phylogeny. Arjona, ex Santalaceae, is sister to Schoepfia (Malécot 2002), and Quinchamalium, another ex Santalaceae, is also to be included here (Smith & Smith 1943 noted relationships between these two genera). Support for this clade is strong (Vidal-Russell & Nickrent 2006; Der & Nickrent 2008).

Synonymy: Arjonaceae van Tieghem

LORANTHACEAE Jussieu, nom. cons.   Back to Santalales

Ellagic acid +; parenchyma apotracheal; cuticular epithelium developing; (stomatal orientation transverse); K 0, calyculus +, pollen usu. triradiate to triangular, apertures confluent or not; G 4-12 [number estimated from "ovules"], inferior, placentation basal, ovules 4-12, not clearly distinguished, gametophyte growing (to tip of style) or not; "hypostase" [= collenchymatous zone below the embryo sacs] +, mesocarp viscous, with rubber outside vascular bundles; endosperm copious, composite [derived from several ovules], suspensor long, first cleavage of zygote vertical [?distribution].

68[list]/950 - 2 groups below. World-wide.

1. Nuytsia

Leaves spiral; C free, yellow; fruit dry, winged; embryo size?, cotyledons 3-4, foliaceous; n = 12.

1/1: Nuytsia floribunda. S.W. Australia (map: from FloraBase 2006).

2. The Rest

Stem parasites, forming burl at point of attachment and with epicortical roots running over the surface and often forming secondary burls; indumentum quite often complex; leaves opposite (spiral); (plant dioecious); flowers (slit-monosymmetric; opening explosively), (3-)5-6(-9)-merous, C (0), connate, (A septate), (placentation axile - e.g. Lysiana); fruit also a berry (nut); (endosperm 0), embryo ± plug-shaped, medium to long?, (cotyledons connate; to 11 - Psittacanthus); no radicle, primary haustorium +; (germination cryptocotylar); n = (8-)12.

67/950: Tapinanthus (250), Psittacanthus (120), Amyema (95), Struthanthus (50), Phthirusa (40). World-wide; although common in Australia and apparently (one might have thought) easily dispersed, unknown from Tasmania (map: from Meusel et al. 1965; Jäger 1970; Barlow 1983; Polhill & Weins 1998). [Photo - Flower]

• Loranthaceae are usually stem parasites that form secondary points of attachment along the stem. They are recognizable by their more or less opposite, often rather thick and brittle (especially when dry) leaves with entire margins and inconspicuous venation born on stems that are not jointed. Their usually 4-5-merous flowers are often quite long, narrowly tubular and brightly colored - often red and/or orange - and lack much in the way of a calyx; the ovary is inferior and the fruits are fleshy. The flowers often have a bract/bracteoles at the base and immediately to one side of the ovary.

Evolution. the family started diversifying 28-40 million years before present (cf. Misodendraceae - Vidal-Russell & Nickrent 2006, 2008a), although the clade itself is possibly much older, ca 81 million years old (Vidal-Russell & Nickrent 2008a).

Kuijt (2009b) notes that floral variation in Neotropical Loranthaceae is far greater than in Palaeotropical members.

Dicaeidae are involved in the pollination of Malesian Loranthaceae, and in some taxa the flower will open only if it is pecked by the bird (hence their common name, "flower peckers"). Birds are very common pollinators in the family, and the groups involved and the evolution of bird-pollinated flowers are discussed in detail by Vidal-Russell and Nickrent (2008b). How loranthaceous seeds are dispersed, whether after moving through the gut, or by regurgitation, varies; the behaviour of the disperser is sometimes modified in distinctive ways. Dicaediae are also involved in dispersal, the seeds passing very quickly through the gut and being deposited on a branch, germination being almost immediate. The bird sometimes shows distinctive behaviour as it defecates, swinging its body parallel to the branch so the seed lands on the branch and germinates there (Docters van Leeuwen 1954 in particular; Polhill & Wiens 1998 and references; Restrepo 1987 for some South American species); the viscid covering of the embryo aids in its attachment to the branches. Overall, about 90 species of birds from 10 families are reported to be specialists on the fruit of Loranthaceae (and some Santalaceae: see Mathiasen et al. 2008).

Loranthaceae are the major hosts for caterpillars of pierid and lycaenid butterflies in Santalales (see introduction to Santalales for literature). Within Iolaini (Lycaenidae) caterpillar preferences show quite a good agreement with the classification of Pohill (1998), in particular, most Iolaini are found either on tapinanthoid or taxilloid genera, the two main African groups of the family (Congdon & Bampton 2000). Caterpillars of the pierid Delias occur on Malesian Loranthaceae (Docters van Leeuwen 1954).

The root parasitic habit, as in Nuytsia, is probably plesiomorphic in the family, since Nuytsia is sister to the rest of the family (Vidal-Russell & Nickrent 2005). It is also known from Atkinsonia (S.E. Australia) and Gaiadendron (Central and South America), other genera that may also be near the base of the phylogeny - hence the characterisation of "the rest" above is incorrect; it is "the rest" minus these two genera (Wilson & Calvin 2006a, b; cf. Vidal-Russell & Nickrent 2008b, but support there not very strong, either). It is estimated that the stem/branch parasitic habit evolved ca 28-40 million years before present (Vidal-Russell & Nickrent 2006, 2008a), about when the family started diversifying. In such parasites, the host-parasite junction may be much swollen, producing wood roses - ultimately split and branched cup-shaped vascular tissue - in the host. Details of the morphological nature of the association bewteen stem parasite and hosts varies, and the epicortical roots, which may be plesiomorphous in the aerial parasites, form either sympodial or monopodial systems (e.g. Polhill & Weins 1998; Calvin & Wilson 2006; Wilson & Calvin 2006b). Wilson and Calvin (2006a, b) discuss the evolution of the various kinds of host attachments, although given the weak support for relationships at the base of the tree it is premature to worry too much about how many times aerial parasitism has evolved, however, Vidal-Russell and Nickrent (2008b) suggest that aerial parasitism arose only once in the family. Some Loranthaceae are hyperparasites, parasitizing other Loranthaceae, while the endophytic Tristerix aphyllus can almost be considered holoparasitic, only the infloresence appearing on the cacti it inhabits (Amico et al. 2007). In Australia, the shapes of loranth leaves and of the eucalyptus host on which they grow are similar; explanations for this vary and this phenomenon is at most uncommon elsewhere (Barlow & Wiens 1977).

Mitochondrial genes from a presumably root-parasitic member of Loranthaceae seem to have been acquired by the fern Botrychium, perhaps via a common mycorrhizal associate (Davis et al. 2005b). However, in general mycorrhizae are not very common in Santalales and if the gene transfer took place in Asia, as is suggested, the apparent absence of root-parasitic Loranthaceae from that area is notable - perhaps they have gone extinct.

Economic Importance. Mathiasen et al. (2008) provide a list of Loranthaceae that harm crops - citrus and cocoa seem to be particularly susceptible.

Chemistry, Morphology, etc. The calyx-like structure on top of the flower of Struthanthus and Phthirusa is described as a calyculus by Wanntorp and Ronse De Craene (2009), and is thought to be of prophyllar origin. Polysymmetrical 6-merous flowers seem to be plesiomorphous in the family (Wilson & Calvin 2006). The embryo sac in Moquiniella is some 48 mm long, the longest in the angiosperms; it grows up the style and then may grow back downwards after reaching the stigma (this is sometimes called an embryo sac haustorium - see Mikesell 1990), and other members of the family have embryo sacs nearly as long (e.g. Cocucci 1990). Both Cronquist (1981) and Takhtajan (1997) describe the endosperm as being starchy, but it is not so scored in Malécot (2002). In many Old World Loranthaceae the cotyledons are connate, but not basally; the plumule emerges through the basal slit (Kuijt 1969).

For embryology, etc., see Raj (1970) and Johri and Bhatnagar (1972), for seedlings of neotropical Loranthaceae, see Kuijt (1982), for foliar anatomy, see Kuijt and Lye (2005: terminal tracheids and cristarque cells common), and for phylogeny, see Vidal-Russell and Nickrent (2005; summary).

Phylogeny. Relationships within Loranthaceae have recently been clarified. Nuytsia is sister to the rest of the family (Vidal-Russell & Nickrent 2005). There is some support for the root parasitic Atkinsonia (S.E. Australia) and Gaiadendron (Central and South America) may also be near the base of the phylogeny, although there is rather weak support for the stem parasite Notanthera being sister to all Loranthaceae except Nuytsia (Wilson & Calvin 2006a, b; cf. Vidal-Russell & Nickrent 2008b, but support there not very strong, either).

Classification. For a monograph of Psittacanthus, see Kuijt (2009a).

Previous Relationships. Loranthaceae and Viscaceae (here included in Santalaceae) have often been considered to be close, even being put in a single family, but there are numerous features separating the two; Kuijt (1969), Raj (1970) and Polhill and Wiens (1998) provide useful tables of differences, and see also Santalaceae here. Thus the viscous covering of the seeds is mesocarpial in origin, being outside the vascular bundles (cf. Viscaceae [= Santalaceae]). Furthermore, the fruits of Loranthaceae contain rubber (and may be used as bird lime), another difference between Loranthaceae and Viscaceae. Although some Loranthaceae such as Phthirusa have very small flowers and congested inflorescences, they still may readily be separated from Viscum and its relatives which also have these features. Plants of the latter group are often lighter green in color, they lack the roots running over the surface of the host, the flowers are often three-merous, and the endosperm is green, etc.

Synonymy: Dendrophthoaceae Nakai, Elytranthaceae Nakai, Gaiadendraceae Nakai, Nuytsiaceae Nakai, Psittacanthaceae Nakai

Opiliaceae + Santalaceae: P as a single whorl only.

Chemistry, Morphology, etc. The single perianth whorl is probably equivalent to the corolla of other members of the order, where the calyx is often small; Hiepko (1984) called this single whorl the perianth in Opiliaceae only because there was no obvious calyx.

OPILIACEAE Valeton, nom. cons.   Back to Santalales

Root parasitic trees or shrubs (lianes); tanniniferous?; wood often fluorescing; nodes 1:(1), 3, 5; mesophyll lacking sclerified cells; cystoliths +/0; stomata paracytic, transversely oriented on the stem [Anthoboleae]; leaves two-ranked to spiral; inflorescences axillary, (catkin-like, with relatively large bracts), (plant dioecious); flowers small, (3-)4-6(-8)-merous, hypanthium + or 0, calyculus +; P free to ± connate, (in carpellate flower of Gjellerupia 0); A adnate to P or not, pollen usu. colporate, microechinate, triangular, (nectaries alternating with A); G [2-5] (half inferior), placentation free central, 1(-few) embryo sacs only, (erect, basal - Agonandra), style short or 0, stigma ± capitate; (pedicel swollen, coloured - Anthoboleae); endosperm copious, also oily, embryo rather short, cotyledons 2-4; germination epigeal; n = 10.

?[list]/?:. Pantropical (map: from Stauffer 1959; Hiepko 1984, 2000). [Photo - Flower]

• Opiliaceae may be recognised by their leaves, which are often two-ranked, lack much in the way of venation, and may have small bumps because of the cystoliths. The flowers are small and are borne in inflorescences which are often almost catkin-like when young; there is only one perianth whorl. The ovary is superior.

Chemistry, Morphology, etc. Metcalfe and Chalk (1950) describe a branching system of lignified cells connecting veins in Olacaceae s. str., i.e. not including Anthoboleae. Agonandra and Anthoboleae have amphistomatic leaves and green twigs. Stauffer (1959) suggested that there might be viscin in the fruits of some Anthoboleae.

For embryology, see Ram (1970).

Phylogeny. The Australian Anthobolus, ex Santalaceae, belongs here (Der & Nickrent 2005, 2008, support strong), and it, like other members of the family, has a superior ovary. Other other Anthoboleae are close to Santalum and relatives (Der & Nickrent 2008: support strong).

Previous Relationships. Stauffer (1959), who monographed Anthoboleae, considered that they were closer to Santalaceae than to Opiliaceae.

Synonymy: Cansjeraceae J. Agardh

SANTALACEAE R. Brown, nom. cons.   Back to Santalales

Woody or herbaceous root (stem) parasites, (endophytic - Arceuthobium); ellagic acid 0; cuticular epithelium common; (cuticle waxes as rodlets); guard cell thickenings unknown; epidermal cells sclerified, with druses; stem stomata transversely oriented; leaves spiral to opposite, (margins with spines - Ionidium); flowers small, (3-)4-5(-8)-merous; hypanthium + or 0, calyculus 0 [?always]; P connate or not, nectary on inside, (prominent lobes alternating with P), frequently a patch of hairs when A are inserted, pollen various, (nectaries alternating with A); G [2-5], ± inferior, odd member abaxial, (placentation free central), ovules straight (anatropous), or not distinguishable, stigma often capitate or lobed; fruit [mesocarp stony] also baccate, (outer part exfoliating); endosperm (helobial; green), starchy or not, embryo short to long; n = 5-7.

44[list]/990: Thesium (325), Phoradendron (235), Viscum (65), Dendrophthora (65), Exocarpus (26). World-wide, esp. tropics (map: see Meusel et al. 1965; Hawksworth & Wiens 1972; George 1984; Jalas & Suominen 1976; Polhill & Weins 1998). [Photos - Acanthosyris fruit.]

Evolution. The Viscum clade itself may be some 72 million years old, perhaps being branch parasitic for much of that time (Vidal-Russell & Nickrent 2008).

The mistletoe Viscum minimum, from the eastern Cape, has aerial stems about 3 mm long only and with but a single internode (Don Kirkup, pers. comm.); these arise from the endophytic portion of the plant. It is also an indicator of elephant grazing; since it is succulent and nutrient-rich, the animals preferentially eat it (Germishuizen et al. 2007, and references). As Der and Nickrent (2008) and Vidal-Russell and Nickrent (2008) note, the branch-parasitic habit seems to have evolved three times in Santalaceae, in the Viscum, Eremolepis and Dendromyza groups; the latter two are in the Santalum and Amphorogyne clades respectively. Phacellaria is an obligate hyperparasite on a few other Santalaceae (Dendrophthoe) and especially Loranthaceae (esp. Taxillus: Li & Ding 2006; see also Mathiasen et al. 2008), while Phoradendron durangense and P. falcatum parasitize only other members of the same genus (Calvin & Wilson 2009). Some species of Arceuthobium are getting close to being holoparasites (Nickrent & García 2009); a number are largely endophytic. For root parasitism in Santalum album, see Tennakoon and Cameron (2006).

Molecular evolution has greatly speeded up in the Viscum clade (Vidal-Russell & Nickrent 2008).

Some ex-Viscaceae are wind pollinated. Many mistletoes and their relatives and other stem parasitic Santalaceae have fleshy fruits and are bird-dispersed in a rather similar fashion to fleshy fruits of Loranthaceae (Restrepo 1987 for some South American species). In Arceuthobium seed discharge is explosive, the seed leaving the fruit at some 1370 cm/second and travelling up to 20 meters (66 feet) in some cases (Hinds et al. 1963; Hawksworth & Wiens 1996; Ross Friedman & Sumner 2009 for embryo development); the seeds take two years to mature and the embryo lacks a plumule but has a well developed radicle.

Economic Importance. Mathiasen et al. (2008) provide a list of Santalaceae that harm crops and timber trees. Some mistletoes like species of Arceuthobium (e.g. A. americanum - the genus used to be placed in Viscaceae) are major pests on conifers in west North America in particular, causing extensive witches' brooms and the death of the host. Viscum crassulae is a pleasing horticultural subject with its bright red fruits; it must be about the only stem parasite so grown. Its preferred host is Portulacaria afra (Didieraceae) whose leaves its leaves are supposed to mimic.

Chemistry, Morphology, etc. When a cuticular epithelium develops, there is no cork cambium. Subepidermal cells divide irregularly, the outer walls being cutinised; the cuticular epithelium lacks both suberin (cf. cork) and lenticels (Wilson & Calvin 2003). It is present in the old Eremolepidaceae and Viscaceae, as well as some, but possibly not all Santalaceae s. str. Stomata in the stem and of leaf are commonly tranversely oriented (Butterfass 1987). Some Santalaceae have recurrent bundles in the gynoecium, perhaps evidence of receptacular epigyny (Eyde 1975, and references); however, Exocarpus and some other genera have a superior ovary. A number of Santalaceae have three traces in their perianth members, the two lateral traces coming from commissural bundles (Smith & Smith 1943). Thesium has starchy endosperm. Antidaphne seems to have three vascular traces in its cotyledons. A very large genome with a C value of some 350 picograms or more is found in Viscum alone of the Santalales examined (Leich et al. 2005).

See Wiens and Barlow (1971) for cytology, Leins (2000) for floral morphology of Viscum, Wilson and Calvin (2003) for some aspects of anatomy, and Norverto (2004: wood anatomy and evolution).

Viscaceae sensu stricto are indeed distinctive. They can be characterised as follows: Stem parasites often with haustoria ramifying through the host, no roots running over the surface of the host°; toxic polpypeptides +; cuticular epithelium developing; stems brittle and jointed°, stomata transverse; cuticle waxes usu. platelets with irregular margins; leaves opposite, 2ndary veins usu. ± palmate, petiole obscure; plant usu. monoecious°, no bract and bracteole immediately under the ovary°; K 0; P 3-4-merous°, short°, A (polythecate), opening by pores°, pollen spherical°; G 3-4, inferior, 2 "ovules"°, usu. mamelon +, embryo sac bisporic° (Allium type); "berry" sometimes explosive, viscous covering incomplete, inside the vascular bundles°, consisting of polysaccharide threads and mucilage°, thin endocarp +° (always?); suspensor short or 0, endosperm green°, starchy, zygote cleavage vertical, embryo green, apparently with 1 cotyledon [= 2 connate]; n = 10-14(-17): inc. Arceuthobiaceae, Bifariaceae, Ginalloaceae, and Phoradendraceae. Characters with ° after them differentiate Viscaceae s. str. from Loranthaceae - they are neither close nor morphologically very similar beyond superficialities! Expanded wood roses may be produced by the host at places where the parasite attaches. The development of the ovule and embryo is distinctive, e.g., there is no suspensor (Ross & Sumner 2005; Friedman & Sumner 2009 and references).

Phylogeny. Der and Nickrent (2005, esp. 2008) found eight well supported clades in Santalaceae (the Comandra, Thesium, Cervantesia, Nanodea, Santalum, Amphorogyne and Viscum clades), but relationships between these clades are poorly understood; there may be a clade including most of the family except the Cervantesia, Thesium and Comandra clades. The two genera of Eremolepidaceae, very often kept separate before, that were included in this study (Eremolepis itself was not included) are well embedded in the Santalum clade (Der & Nickrent 2008; see also Nickrent et al. 1998 for relationships). See Nickrent et al. (2004b: ?rooting) for a phylogenetic analysis of Arceuthobium, while for relationships within the large genus Thesium, see Nickrent et al. (2008). Santalum, the sandalwood genus, is centred on Australia and the Pacific, and there have perhaps been two migrations from Australia to Hawaii and also two migrations out of Hawaii (Harbaugh & Baldwin 2007).

Synonymy: Anthobolaceae Dumortier, Arceuthobiaceae Nakai, Bifariaceae Nakai, Canopodaceae C. Presl, Eremolepidaceae Nakai (cuticular epithelium developing; stem stomata transverse; leaves spiral; inflorescence catkin-like; pollen spherical, no obvious placenta, ovules in base of ovary, embryo sac bisporic; viscous covering complete or not; endosperm green - Eremolepis n = 10, Lepidoceras sister to Eubrachion, Antidapne n = 13 perhaps separate, one of the 5-6 "Santalaceae" s. str. lineages, with growth like Notanthera (Loranthaceae), some with green endosperm), Exocarpaceae J. Agardh, Lepidocerataceae Nakai), Ginalloaceae Nakai, Osyridaceae Rafinesque, Phoradendraceae H. Karsten, Thesiaceae Vest, Viscaceae Batsch

BALANOPHORACEAE L. C. & A. Richard, nom. cons.   Back to Unplaced

Echlorophyllous root parasites from underground tuber-like structures either parasite or parasite-host mixed, these rupture and leave a collar-like structure at ground level; tanniniferous; roots 0; cuticle wax crystalloids 0; stems endogenous; leaves spiral, two-ranked, whorled or 0; inflorescence ± capitate, spicate, or racemose, terminal, plant monoecious or dioecious; flowers small, (monosymmetric); staminate flowers: P 0, 3-4(-8), valvate, (basally connate), stamens equal and opposite perianth members, (1-2, esp when P = 0), extrorse, usu. connate, (thecae connate), pollen (trinucleate), tricolpate or tri- or pantoporate; pistillode 0; carpellate flowers: P 0 or minute; staminodes 0; G [2, 3(-5)], (inferior), [2 transverse - Rhophalocnemis], or acarpellate, ovules ategmic, 1 (bisporic [chalazal] 8-celled Allium type) embryo sac/ovary, antipodal cells 0 or short-lived, styles separate or style single, stigma ± expanded; fruits minute, drupes or nut-like; endosperm +, embryo short to undifferentiated; n = 14, ?16, 18; germination via germ tube.

17[list]/50: Balanophora (15). Mostly tropical (map: from Hansen 1972, 1980, 1986; van Balgooy 1975; Heide-Jørgensen 2008). [Photo - Flower]

• Balanophoraceae are echlorophyllous yellow to red or brown root parasites whose aerial stem arises from a collar-like structure borne at ground level. The dense inflorescence is racemose, bearing many minute flowers.

Chemistry, Morphology, etc. Langsdorffia, Thonningia and Balanophora have balanophorin, a wax-like substance, rather than starch as the main reserve. Weber (1986) noted several distinctive aspects of gross morphology and detailed anatomy of the haustoria of Mystropetalon such as runners that produced additional haustoria and graniferous tracheary cells in these haustoria that were similar to comparable structures in Santalales, however, graniferous cells occur in other root parasites including Krameriaceae and Orobanchaceae (Fineran & Ingerfeld 1982).

It often is very difficult to understand the morphology of the flower, whether the ovary is superior or inferior, etc., indeed, development of the gynoecium of Balanophora is perhaps best compared with that of the nucellus, hence the morphology of the "fruit" is unclear. Eberwein et al. (2009) note that the naked female flowers of Balanophora tend to be adnate to clavate bodies, perhaps modified bracts, borne in no particular order in the inflorecence. For cautionary comments on attempts to determine ovule type and orientation in the family, see Holzappel (2001) - but problems are hardly surprising, perhaps, if Balanophoraceae are to be compared with the hemiparasitic Santalales. Mystropetalon also has a clearly inferior ovary and cuboid pollen with pores at the eight corners and other variously angled pollen is known from other Santalales. Holzappel (2001) noted a pseudoendothelium was quite common in the family. Dactylanthus lacks any seed coat, and one of the cells produced by the first division of the endosperm never divides further - this is then perhaps to be compared with the chalazal haustorium in other Santalales. In Helosis the inner layer of cells of the seed coat is massively thickened on the inner and anticlinal walls, while in Balanophora it is the outer layer that is thickened; taxa like Hachettia are more complex. The mitochondral genes cox1, atp1 and matR showed massive divergence (Barkman et al. 2007: Ombrophytum only sampled).

Takhtajan (1988, 1997) provides much information under the segregate families mentioned below, including Hachettiaceae and Lathraeophyllaceae (= Helosidaceae); see also Harms (1935b), Kuijt (1969), and the Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008).

Phylogeny. The only phylogeny of the family (see Nickrent 1998: accessed 16.5.2009) based on nuclear SSU rDNA data suggest that Mystropetalon and relatives are sister to a clade containing the rest of the family examined.

Previous Relationships. Cronquist (1968) suggested relationships between Balanophoraceae and Santalales, later (1981) placing them all in his Santalales; Balanophoraceae include Cynomoriaceae. Takhtajan (1997) linked Balanophoraceae with Cynomoriaceae (here Saxifragales), Rafflesiales (here Malpighiales) and Hydnoraceae (here Piperales), including them all in his Magnoliidae; within Balanophorales he included all the families in synonymy below apart from Hachetteaceae as separate families.

Botanical Trivia. Balanophora has the smallest flowers of any angiosperm made up of as few as a mere 50 cells.

Synonymy: Dactylanthaceae Takhtajan, Hachetteaceae Doweld, Helosidaceae Bromhead, Langsdorffiaceae Pilger, Lophophytaceae Bromhead, Mystropetalaceae J. D. Hooker, Sarcophytaceae A. Kerner, Scybaliaceae A. Kerner