LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and 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 and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; 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, developing after pollination, 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 duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [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; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally 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, 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, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

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

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

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

Evolution. Although Soltis et al. (2008) give the ages of divergence of a number of branches below asterids, this is based on a topology [Berberidopsidales [[Caryophyllales + Dilleniales] Santalales, asterids]], and the ages of (131-)120, 117(-112) million years in Bell et al. (2010) are based on a similar topology. Moore et al. (2010: 95% highest posterior density) suggest ages of (107-)103(-97) million years for this clade, the superasterids.

Phylogeny. Relationships between asterids and other core eudicots - prior to the seventh version of this site asterids were part of a major polytomy that included rosids, Berberidopsidales, Santalales, and Caryophyllales - have long been uncertain, but the study by Moore et al. (2008, esp. 2010) using whole chloroplast genomes with moderately good sampling bids fair to clear up this confusion, although the order of branching below the asterids is still not clear (e.g. Soltis et al. 2011). For further discussion, see the Dilleniales page.

SANTALALES Berchtold & J. Presl  Main Tree, Synapomorphies.

Mycorrhizae absent; polyacetylenes [triglycerides with C18 acteylenic acids], triterpenic sapogenins + [Loranthaceae?]; cork subepidermal; vessel elements with scalariform perforation plates [E]; perforation plates not bordered; intervascular pits alternate; axial parenchyma strands ³7 cells wide [E], rhombic crystals in ray cells [E]; tension wood?; nodes 3:3 [E]; pericyclic fibres 0; (cristarque cells +); petiole bundle annular [E], (cuticle waxes with annular rodlets, palmone common); petiole/mesophyll with (astro)sclereids; lamina margins entire; inflorescences cymose; K small, open, cupular, teeth ± inconspicuous, C valvate, large and protecting bud, with adaxial hairs; anthers basifixed; nectary [sometimes as "disc"] +; G [3], style +, stigma small; ovule 1/carpel, pendulous, apotropous, tenuinucellate, outer and inner integuments ca 4 cells across, (unitegmic), micropyle endostomal; embryo sac curved, with chalazal caecum[?here]; fruit a drupe, 1-seeded, K persistent; seed coat crushed; chalazal endosperm haustoria +, first cleavage of zygote transverse [?sampling], embryo minute, green. - 13 families, 151 genera, 1985 species.

Evolution. Divergence & Distribution. 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). Magallón and Castillo (2009) suggest ages of ca 113.8 and 114.5 million years (relaxed and constrained penalized likelihood datings respectively) for the divergence of stem Santalales - but note that the positions of Berberidopsidales and Santalales are switched on their tree - and ages of 90.2 and 90.7 million years for crown divergence (relaxed and constrained again).

Note that where a number of the characters are to be placed on the tree is unclear; those with an "[E]" after them are found in the first three families below; if these form a single clade, their optimisation will need to be adjusted accordingly.

Ecology & Physiology. It is clear from the phylogeny of the order that the plesiomorphic life style in the clade is to be free-living, and hemiparasitism by attachment to the roots of the host is derived (Malécot 2002; Malécot et al. 2004; Nickrent et al. 2010). 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 occurs 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). A few Loranthaceae are hyperparasites, parasitizing other members of that family, and some species of Phoradendron (Santalaceae) are even obligate parasites on other members of the same genus (Calvin & Wilson 2009). For some information on the physiological details of parasitism in Santalales, see Stewart and Press (1990).

Plant-Animal Interactions. 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, Ximeniaceae (all Lycaeninae in particular, Opiliaceae and Santalaceae also being recorded as 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; there are no reports of pierine 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).

Floral Biology. The flowers of Santalales are for the most part (many Loranthaceae are notable exceptions, of course) rather small, with valvate petals that have hairs of various kinds adaxially, and a very small calyx. The corolla haits may be in small tufts where the stamens are inserted on the petals, as in Strombosia and Santalaceae.

There is some controversy over the morphology of the flower. What appears to the outer perianth whorl - often a minute, rim-like structure - has been interpreted as being a caylculus of paired and prophyllar origin in a number of Santalales (Wanntorp & Ronse De Craene 2009; Ronse de Craene 2010). The presence of such a calyculus might then be a fairly high level apomorphy in the order, but this depends on more extensive developmental studies, and for the time being it seems best to call any calyculus, a calyx. If the calyculus is interpreted as being prophyllar in nature, as by Wanntorp and Ronse De Craene (2009), then a shift in its position on to the top of an inferior ovary needs explanation, as does its presence in the terminal flower of a cymule (these would not be expected to have any prophylls at all associated directly with them). Finally, in Loranthaceae, a calyculus is described in flowers which are also shown as having a prophyll (Wanntorp & Ronse De Craene 2009). That being said, the calyx in Santalum and Loranthaceae like Struthanthus is unusual in that it initially does not completely encircle the flower, there being an interruption on the adaxial side. Furthermore, Johri and Bhatnagar (1971) also note that this structure is not regularly lobed and usually lacks a vascular supply, although it is vascularized in Nuytsia; it could also be a novel structure that is axial in origin. And in Santalaceae like Comandra there is absolutely no evidence of any calyx, as least from gross morphology.

Ovule variation in this clade is extreme, varying from fairly classic bitegmic ovules to structures which have no conventional ovular structure - embryo sacs alone! There is considerable discussion as to the number of integuments in "Olacaceae" (e.g. information in Johri & Bhatnagar 1960, Maas et al. 1992; Breteler et al. 1996; Malécot 2002; summary in Brown et al. 2010 and references), as well as cotyledon number. Some taxa may have both micropylar endosperm and embryo sac haustoria (Mickesell 1990), and variation in features of embryo sac morphology, embryo, etc., is considerable (see e.g. Johri & Bhatnagar 1960).

Bacterial/Fungal Associations. 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 (Malécot 2002 for references). The absence of mycorrhizae, as well as that of root hairs which has also been reported for the group (see below), is probably 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 and other free-living taxa? 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 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). 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); cf. calyculus above. The anther wall is monocotyledonous in development in Maburea (Erythropalaceae), and there may sometimes be two ovules per carpel (see Maas et al. 1992). 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 information on the first six families in particular, the old Olacaceae, see Baas et al. (1982: leaf anatomy), Sleumer (1984a: New World taxa, pollen, anatomy, etc., 1984b: Malesian taxa, general), Lobreau-Callen (1980, 1982: pollen), and Malécot et al. (2004: general information). For other information, see Roberston (1982), Barlow (1997), Calder and Bernhardt (1983), Reed (1955: esp. cotyledon number), Malécot et al. (2004: morphological phylogeny and data matrix), 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), and for hemi-parasitism, see Fineran (1991). For pretty much everything, see Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008).

Phylogeny. Malécot (2002) provided 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., Nickrent et al. 2010: see the tree below), a number of clades appear to be fairly well supported. Erythropalaceae s.l., including Strombosiaceae and Coulaceae (although Coulaceae were not included in all analyses, and their positionwas rather labile) are perhaps sister to all other Santalales and are free-living (Malécot 2002). These clades tend to 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 still 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 (see also Nickrent et al. 2010). 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 7 of this site and earlier), close to Maburea, in Erythropalaceae s. str. (K. Wurdack, pers. comm.); the genus is not mentioned by Nickrent et al. (2010). 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; Vidal-Russell & Nickrent 2008; Nickrent et al. 2010); this position is followed here. Opiliaceae (one genus) were strongly supported as being sister to a clade [Santalaceae + Viscaceae] in Soltis et al. (2007a), and this basic pattern is followed in Nickrent et al. (2010). 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) interrelationships of which are for the most part well supported.

Mystropetalum, Dactylanthus, and Hachettia, three members of Balanophoraceae, formed 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 being assigned (see also Nickrent 2002; Nickrent & Duff 1996; Barkman et al. 2007). Su and Hu (2008, 2011) analysing variation in B-class floral genes and with a quite good taxon sampling suggested that Balanophoraceae were basal or near basal in the clade since they found the euAP3 homologue in Balanaophora, but not in other Santalales. 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. Of course, being holoparasitic, they lack most or all of the distinctive vegetative and even floral features of other Santalales, but they do have a curved embryo sac (e.g. Fagerlind 1945c, d).

For additional information on relationships, see Nickrent and Duff (1996) and Nickrent et al. (1998).

Classification. For a detailed classification of all Santalales (except Balanophoraceae), see Nickrent et al. (2010). The seven small families for the seven clades of the basal poorly supported pectination are recognised pending resolution of relationships there; if any are sister taxa, they will almost certainly be combined. Families within the old Santalaceae are not recognised, despite the inclusion of highly autapomorphic Viscaceae there.

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

Includes Aptandraceae, Balanophoraceae, Coulaceae, Erythropalaceae, Loranthaceae, Misodendraceae, Octonemaceae, Olacaceae, Opiliaceae, Santalaceae, Schoepfiaceae, Strombosiaceae, Ximeniaceae.

Synonymy: Anthobolales Dumortier, Balanophorales Dumortier, Erythropalales van Tieghem, Heisteriales van Tieghem, Loranthales Link, Olacales Martius, Osyridales Link, Viscales Berchtold & J. Presl, Ximeniales van Tieghem

ERYTHROPALACEAE Miquel, nom. cons.   Back to Santalales

Trees, shrubs or lianes, (latter with branch tendrils); laticifers +/0; (vessel elements with simple perforation plates); ground tissue of fibre tracheids; sieve tubes with non-dispersive protein bodies; (nodes 5:5); (epidermal/stomatal cells lignified; with druses), stomata various, cuticular thickening +, large guard cell chamber; leaves spiral or two-ranked, lamina vernation conduplicate, (venation palmate), (petiole pulvinate, margin toothed); inflorescence fasciculate or cymose; flowers (medium-sized; 6-merous), K ± free; C (adaxial hairs 0); stamens = C, opposite K, C and with two lateral scales, 2X C; pollen tricolpate or tricolporoidate; (disc 0); G 10-ridged, ± inferior [Erythopalum], opposite sepals (opposite petals) or odd member adaxial, septate (not), style short, stigma ± lobed or not; ovules with micropyle exostomal; fruit 5-valved [Erythropalum], K much accrescent [Heisteria]/not; endosperm with starch or oil, (cotyledons orbicular, foliaceous); n = ?; germination phanerocotylar.

4/40: Heisteria (30). Pantropical, East Malesia to Talaud and Flores, not Madagascar or East Malesia and to the S.E.; most in Central and South America (map: from Sleumer 1984a, b; Malécot 2002). [Photo - Flower, Fruit.]

Chemistry, Morphology, etc. 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. The nectary is sometimes present, being described as adnate to the ovary (Sleumer 1984a) or on top of the ovary (Sleumer 1984b; cf. Nickrent et al. 2010). See Maas et al. (1992) for information on Maburea.

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 fibres +; 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 = ?

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.

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 (1984a) 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.

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; Maas et al. (1992) noted the similarity of Maburea and Brachynema in leaf anatomy.

The laticifers of Heisteria are both articulated and non-articulated (Baas et al. 1982).

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

Previous Relationships. Brachynema has often been associated with "Olacaceae" s.l. (Santalales), thus Lobreau-Callen (1980) placed it in Anacoloseae (Aptandraceae) and Baas et al. (1982) placed it with Scorodocarpus (Strombosiaceae) in particular (see also above). It has also been linked with Ebenaceae (Ericales), as by Reed (1955) and others, while in a morphological phylogenetic analysis it appeared close to Symplocaceae (Ericales; Malécot 2002).

Synonymy: Heisteriaceae van Tieghem

[Strombosiaceae [Coulaceae [Ximeniaceae, Aptandraceae, Olacaceae [Octonemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]]]: C ± connate, A adnate to C.

STROMBOSIACEAE van Tieghem   Back to Santalales

(Mycorrhizae +); (vessel elements with simple perforation plates); ground tissue of libriform fibres; (nodes 1:1, 5:5); (petiole bundle with adaxial bundles); groups of very narrow fibres associated with foliar vascular bundles); epidermal cells crystalliferous, with silica sand, stomata aniso-, cylco-, (helico)cytic; leaves spiral to distichous, (lamina venation palmate); inflorescence fasciculate; flowers 4-5 merous, (hypanthium +), (C fleshy); (nectary extrastaminal - Engogemona); A = and opposite C, 10, (filaments short, connective massive, anthers transversely multiseptate - Tetrastylidium; loculi dehiscing separately - Engomegoma); pollen tricolpate/tricolporoidate; G [3-6], (semi-inferior), septate at base, style short to long; ovules also unitegmic, integument ca 6 cells across, micropyle long; (megaspore mother cells several), (embryo sac caecum 0); endosperm starchy, chalazal endosperm haustorium unicellular.

6/18. Pantropical, but not Madagascar, East Malesia and to the S.E. (map: Sleumer 1984a, b; Malécot 2002). Photo - Fruit.]

Chemistry, Morphology, etc. For general information, see Sleumer (1984a, b); see Agarwal (1963b) for Strombosia and Breteler et al. (1996) for information on Engomegoma.

Synonymy: Scorodocarpaceae van Tieghem, Tetrastylidiaceae van Tieghem

[Coulaceae [Ximeniaceae, Aptandraceae, Olacaceae [Octonemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]]: ?

COULACEAE van Tieghem   Back to Santalales

(Mycorrhizae +); laticifers +; mesophyll lignified; epidermis lignified, with druses, stomata paracytic, epidermis with cork-warts [from stomatal complexes]; hairs dendritic; lamina venation scalariform; inflorescence spicate; (C adaxial hairs 0); A 10 (15); nectary 0?; G (3-)4-5), style 0-short; ovules bitegmic only, outer and inner integuments 5-6 cells across; endosperm amyloid.

3/3. Pantropical, not Madagascar or East Malesia and to the S.E. (map: Sleumer 1984a, b; Malécot 2002).

Chemistry, Morphology, etc. For general information, see Sleumer (1984a, b).

[Ximeniaceae, Aptandraceae, Olacaceae [Octonemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]: root hemiparasites; vessel elements with simple perforation plates; axial parenchyma strands 7³ cells wide; nodes 1:1; sclerenchyma fibres of petiole and median vein often 0; petiole bundle arcuate; cuticular thickening +, guard cell chamber small, stomata paracytic; silicification of some foliar mesophyll/epidermal cells; ovules unitegmic; embryo sac curved, with chalazal caecum and ± developed micropylar prolongation.

Evolution. Divergence & Distribution. Moore et al. (2010: 95% highest posterior density) suggest ages of (99-)96(-91) million years for a clade that includes Ximenia and Phoradendron.

Endress (2011a) thought that the inferior ovary in Santalales might be a key innovation for them. However, it is difficult to assign ovary position to a particular place on the tree. Many taxa in families above have a superior ovary, and so do [Exocarpos + Omphalomeria], a "basal clade" in Santalaceae (Der & Nickrent 2005), Loranthaceae are inferior, Schoepfiaceae are half inferior, and more or less inferior ovaries are found elsewhere in the clade. Either there are independent origins for the character of inferior ovary, or reversals, or both.

Floral Biology. Ovule, embryo sac and embryo development of many Santalales in this clade 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; Bhatnagar & Johri 1960; 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.

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).

Phylogeny. Details of lamina anatomy largely agree with the circumscription of this clade (Baas et al. 1982).

XIMENIACEAE Horaninow   Back to Santalales

Woody, (axillary thorns - Ximenia); rhombic crystals (and silica bodies) in ray cells; ground tissue of fibre tracheids; nodes 3:3; (stomata anomocytic); (lamina venation palmate); inflorescence ± umbellate; flowers 4-5-merous; A (= and opposite C), 2 (3) x C, (very long - Curupira); nectary 0; style short to long; (ovules unitegmic); 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).

Chemistry, Morphology, etc. Ximenia americana is crassinucellate. Some information is taken from Sleumer (1984a, b: general).

Aptandraceae, Olacaceae [Octonemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]: ovules unitegmic or ategmic.

Phylogeny. There is no strong evidence that this is a clade; I have simply optimized a character to this node.

APTANDRACEAE Miers   Back to Santalales

Branches plagiotropic [?many]; (arbuscular mycorrhizae + - Ongokea); laticifers +; rhombic crystals in ray cells; (petiole bundle fibres +); (epidermis with cork-warts [from stomatal complexes] - some Aptandra); twigs somewhat zig-zag; leaves distichous; (plant dioecious); flowers 4-5 merous, bracteoles ± connate; (C with apical thickenings); (A connate around style, anthers reflexed [e.g. Aptandra]), (extrorse), also dehiscing by pores or valvate, (3-valvate in Hondurodendron); (pollen breviaxial/oblate, 6-aperturate, tri-diporate); (nectary 0; outside A [Aptandra]; alternating wioth A); G [2(-3)]; ovules often bitegmic; K accrescent (fruit surrounded by accrescent disc or adjacent structures; fruit nut-like); cotyledons 0-2, connate or not; n = ?

8/34: Anacalosa (18). Pantropical (also SE China, Formosa) (map: from Michaud 1966; van Balgooy 1993; Sleumer 1984a, b; Malécot 2002). [Photo - Flower.]

Evolution. Divergence & Distribution. For records of distinctive breviaxial tri-diporate fossil pollen Anacalosidites, very similar to pollen of Anacalosa, Cathedra, and Phanerodiscus, from the Upper Cretaceous (Europe, Maastrichtian) and Palaeocene and particularly Eocene (worldwide) onwards, see Krutzsch (1988), Malécot (2002), and Malécot and Lobreau-Callen (2005).

Chemistry, Morphology, etc. In the anthers of Chaunochiton (Aptandra clade) each ovary loculus opens by a separate slit. Some information is taken from Sleumer (1984a, b: general); see also Ulloa Ulloa et al. (2010) for the remarkable Hondurodendron.

Phylogeny. There are two clades within Aptandraceae, which are easily characterization. The Aptandra clade, with five genera, includes taxa with a more or less extra-staminal nectary, valvate anthers, pollen with concave meso- and apocolpium, and a calyx that is accrescent in fruit, while the Anacalosa clade, with three genera, has lignified guard cells, anthers dehiscing by pores and with prolonged connectives, diploporate pollen, and the disc or extradiscal area is accrescent in fruit (Malécot et al. 2004; Nickrent et al. 2010). Taxa in both clades have petals with apical thickenings.

Synonymy: Cathedraceae van Tieghem, Chaunochitonaceae van Tieghem, Harmandiaceae van Tieghem

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

SiO₂ bodies in ray cells; (nodes 3:3 - Dulacia); leaves distichous; (flowers heterostylous); (K 0); (C 3 - Olax); A 1-2 x C, [fertile A 3, staminodes 3-6, opp. C (Dulacia)]; pollen breviaxial, (trinucleate); G ridged or not; ovules ategmic, (unitegmic, integument 5-6 cells across), (nucellar cap + - Olax); embryo sac bisporic, 8-nucleate [Allium-type] - Olax; K much accrescent/not; (chalazal haustorium growing into pedicel), starch slight, cotyledons 0-1; n = 12.

3/57: Olax (40). Pantropical (also S.E. China, Formosa) (map: from Sleumer 1984a, b; George 1984; Malécot 2002).

Evolution. Ecology. 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. Dulacia is heterostylous. 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.

Some information is taken from Sleumer (1984a, b: general); for embryology, see Agarwal (1963a).

[Octonemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]: ?

OCTONEMACEAE van Tieghem nom. cons.   Back to Santalales

Axial parenchyma strands ³7 cells wide; nodes pentalacunar; petiole bundle annular; no silicification of foliar cells; stomata cyclocytic, anomocytic, etc., cork warts on leaf [from hair bases]; hairs stellate-peltate; inflorescence fasciculate, from endogeneous buds; plant dioecious; pistillate flowers: staminodes +; G 3, stigma multi-lobed; integuments 2 or 1; fruit drupaceous; seed longitudinally ruminate, radicle relatively very long, cotyledons 6.

1/7. Tropical Africa (map: from ).

Chemistry, Morphology, etc.

Phylogeny Molecular data place Octonema rather differently than do morphological observations, which put the genus with the free-living members of Santalales (e.g. Malécot et al. 2004); if confirmed, this may suggest that there have been a number of reversals in this clade.

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

Chemistry, Morphology, etc. ?Cristarque cells.

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

LORANTHACEAE Jussieu, nom. cons.   Back to Santalales

Ellagic acid +; parenchyma apotracheal; cuticular epithelium developing; (stomatal orientation transverse); flowers medium-sized to large (small), (K 0); C 7; A biseriate; pollen usu. flattened, triradiate to triangular, apertures confluent or not; G 3-12 [number sometimes estimated from "ovules"], inferior, placentation basal; ovules 4-12, ategmic; megaspore mother cells many [archesporium "massive"], embryo sac growing up style (to tip); "hypostase" [= collenchymatous zone below the embryo sacs] +, mesocarp viscous, with rubber outside vascular bundles; endosperm composite [derived from several ovules], suspensor long, first cleavage of zygote vertical.

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

1. Nuytsieae van Tieghem

Stomata tranverse to long axis of leaf; leaves spiral; plant monoecious; C 6-8, free, yellow; fruit dry, 3-winged; embryo size?, cotyledons 3-4, foliaceous; n = 12.

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

Synonymy: Nuytsiaceae van Tieghem

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; calys usu. unvascularized (vascularized- Atkinsonia); C (0) 6; (A not biseriate; dimorphic [one pair sterile]; anthers septate); (pollen spherical); (placentation axile - e.g. Lysiana); embryo sac bisporic, 8-nucleate [Allium-type]; 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]

Synonymy: Bifariaceae Nakai, Elytranthaceae van Tieghem, Gaiadendraceae Nakai, Psittacanthaceae Nakai

• 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. Divergence & Distribution. 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).

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). Press and Phoenix (2005) discuss interactions of Loranthaceae with their hosts (see also below).

Kuijt (2009b) notes that floral variation in Neotropical Loranthaceae is far greater than in Palaeotropical members. Kuijt (2011) suggested that sessile, axillary, 4-merous flowers were primitive in the famnily - genera around Phthirusa were examples.

Floral Biology & Seed Dispersal. 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). The flowers often open explosively, scattering pollen on the pollinator.

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. Dicaeidae are also involved in seed 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 defaecates, swinging its body parallel to the branch so the seed lands on the branch and germinates there (Docters van Leeuwen 1954 in particular; Godschalk 1983; 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, and sometimes the seeds are in long, dangling strings, "rosaries" (Restrepo 1987), held together by the viscin. 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). However, the efficacy of mistletoe specialists in dispersing seed to uninfected trees has been questioned, more generalist fruit-eaters perhaps being more efficient in doing this (Watson & Rawsthorne 2011).

Plant-Animal Interactions. 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).

Ecology & Physiology. 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) and the toor-paraitic habit is found in the out groups. It is also known from Atkinsonia, from S.E. Australia (which has a vascularized "calyx" - see Johri & Bhatnagar 1972), and Gaiadendron, from Central and South America), two other genera that may also be near the base of the phylogeny. Hence the characterisation of "the rest" above is incorrect; it is really "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. Morphological details of the association between 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).

Genes & Genomes. 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 - but this is perhaps unlikely (see above). Polysymmetrical 6-merous flowers seem to be plesiomorphous in the family (Barlow 1983; Wilson & Calvin 2006), but 7- (or 8)merous flowers occur in Atkinsonia, Gaiadendron and Notanthera (see below), and the stamens are inserted at two levels on the corolla of these species (Kuijt 2010). 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. Johri & Bhatnagar 1972; 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 much information about all aspects of the family, see Johri and Bhatnagar (1972), for embryology, etc., see Raj (1970) and Bhatnagar and Johri (1983), 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 an account of Nuytsia, see Hopper (2010); for a monograph of Psittacanthus, see Kuijt (2009a), and for a suprageneric classification of the whole family, see Nickrent et al. (2010); for some generic limits, see Kuijt (2011).

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.

[Misodendraceae + Schoepfiaceae]: ?

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

Stem parasites; stem apex aborting; bundle fibres +; sieve tube plastids lacking starch and protein inclusions; plant dioecious; inflorescence (compound) raceme or spike; pedicels pubescent; staminate flowers: K/C 0; A 2-3, monothecal; pollen 4-12-colporate, spinuliferous; carpellate flowers: C 3; staminodes alternate with P; ovules straight, ategmic; 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. Ecology. 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 occurred 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 +; epidermal cells not lignified, (stomata anomo-/cyclocytic); hairs unicellular/0; bract and bracteoles immediately below and surrounding G; (flowers distylous), medium-sized; (K asymmetrical [Quinchmalium]), C tubular, with adaxial hairs; pollen tetrahedral, heteropolar, 4-colporate, apertures ± confluent, ektexine psilate; G (semi-)inferior, basally septate, stigma lobed to capitate; ovules ategmic/?unitegmic; embryo sac with with synergid haustoria [Quinchamalium]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. Sleumer (1984) noted that the wood had aliform-confluent parenchyma, unlike other "Olacaceae". 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. That Schoepfia is rather different from "Olacaceae" has often been remarked (e.g. Metcalfe & Chalk 1950; Sleumer 1984). 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

Opiliaceae + Santalaceae: ?

Chemistry, Morphology, etc. The single perianth whorl - very common in this clade - 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; K very small, C free to ± connate, (in carpellate flower of Gjellerupia 0); A adnate to C or not; pollen usu. colporate, microechinate, triangular; (prominent nectaries alternating with A); G [2-5] (half inferior), placentation free central, style short or 0, stigma ± capitate; ovules undifferentiated, 1(-few) embryo sacs only, (ovules erect, basal - Agonandra); (pedicel swollen, coloured - Anthoboleae); secondary endosperm haustoria +; endosperm also oily, embryo narrow, as long as seed, (rather short), radicle very short, cotyledons (2-)3-4; germination epigeal; n = 10.

11[list]/36. Pantropical (map: from Stauffer 1959; Hiepko 1984, 2000, M. Gustafsson pers. comm. ii.2010 - Africa). [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), and for general information, see Stauffer (1959) and Hiepko (1984).

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: Anthobolaceae Dumortier, Cansjeraceae J. Agardh

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

Ellagic acid 0; axial parenchyma strands 0; cuticular epithelium common; (cuticle waxes as rodlets); guard cell thickenings unknown; epidermal cells sclerified, with druses; stem stomata transversely oriented; flowers small, (3-)4-5(-8)-merous; hypanthium + or 0; K 0, usually a patch of hairs on C where A are inserted; nectary on inside of C, pollen various; G [2-5], inferior, odd member abaxial, (placentation free central), stigma often capitate or lobed; ovules straight (anatropous), or not distinguishable; fruit [mesocarp stony] also baccate, (outer part exfoliating); endosperm (helobial; green), starchy or not, embryo short to long; n = 5-7.

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

1. Comandra group

Plant herbaceous; (hypanthium +); large nectary glands alternating with stamens; stigma punctate to subcapitate; ovules anatropous, unitegmic; embryo sac with lateral caecum; secondary endosperm haustoria + [and Mida], first cleavage of zygote vertical.

2/2. North America, Europe, ± temperate.

Synonymy: Comandraceae Nickrent & Der

[Thesieae + Cervantesieae]: ovules unitegmic.

2. Thesieae Meisner

(K +, [strongly lobed]); (C connate); ovules unitegmic.

5/345: Thesium (345). More or less world-wide, not Arctic; Thesium esp. Africa.

Synonymy: Thesiaceae Vest

3. Cervantesia group

(Plant with axillary thorns); (lamina rhombic, with spines - Jodina); nectary glands alternating with stamens.

8/21. Tropical, warm temperate, esp. America.

Synonymy: Cervantesiaceae Nickrent & Der

4. Nanodea group

(Flowers 4 merous); (K +); large nectary glands alternating with stamens; (G semi-inferior).

2/2. South Temperate.

Synonymy: Nanodeaceae Nickrent & Der

[Santaleae + Amphorogyneae + Visceae]: (ovules reduced to embryo sac, otherwise indistinguishable).

5. Santaleae Dumortier

(Stem parasites); (K +); (large nectaries alternating with A - Osyris); (G half inferior); embryo sac with micropylar end long-protruding; (chalazal endosperm haustorium multicellular - Exocarpus).

11/51: Exocarpus (26). Widely scattered, not N. temperate.

Synonymy: Canopodaceae C. Presl, Eremolepidaceae Nakai, Exocarpaceae J. Agardh, Lepidocerataceae Nakai, Osyridaceae Rafinesque,

6. Amphorogyneae Stearn

(Stem parasites); pyrrolizine alkaloids +; flowers 4-6-merous, (C connate); A with short filaments, anthers with loculi above one another in pairs, opening separately.

9/68: Dendromyza (21), Leptomeria (17). Southeast Asia, Malesia, Australia and New Caledonia.

Synonymy: Amphorogynaceae Nickrent & Der

7. Visceae Horaninow

Stem parasites, often with haustoria ramifying through the host, no roots running over the surface°; toxic polpypeptides +; cuticular epithelium developing; stems brittle and jointed°, stomata transverse; cuticle waxes usu. platelets with irregular margins; leaves opposite, lamina with 2ndary veins usu. ± palmate, petiole obscure; plant monoecious° (dioecious - Viscum), no bract and bracteole immediately under the ovary°; flower 3-4-merous°, short°; A with short/0 filaments, anthers (polythecate), opening by pores°, (connate, forming a synandrium); pollen spherical°; G with 2 "ovules"°, usu. mamelon +; embryo sac bisporic [Allium type], (often straight); "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, (first cleavage of zygote vertical - Korthalsella, Arceuthobium), embryo green, apparently with 1 cotyledon [= 2 connate]; n = 10-14(-17).

7/520: Phoradendron (235), Viscum (65-150), Dendrophthora (70). Worldwide (Map: from Barlow 1983).

Synonymy: Arceuthobiaceae Nakai, Dendrophthoraceae van Tieghem, Ginalloaceae van Tieghem, Phoradendraceae H. Karsten, Viscaceae Batsch

Evolution. Divergence & Distribution. 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 large genus Thesium may be of South African origin, with a stem age of ca 60 million years and a crown age of (56.5-)42.7-35.9(-24.4) million years (Moore et al. 2010, ages from a variety of analyses). 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 to the south Pacific (Harbaugh & Baldwin 2007).

Ecology & Physiology. 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 Santaleae and Amphorogyneae respectively. Phacellaria is an obligate hyperparasite on a few other Santalaceae (Dendrophthoe) and especially Loranthaceae, Taxillus in particular (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. Expanded wood roses may be produced by the host at places where the parasite attaches. For root parasitism in Santalum album, see Tennakoon and Cameron (2006). Press and Phoenix (2005) discussed host-parasite interactions of Visceae (see also below).

Floral Biology & Seed Dispersal. In Santalum, filament hairs are involved in secondary pollen presentation (Howell et al. 1993), while some ex-Viscaceae are wind pollinated.

Many mistletoes and their relatives and other stem parasitic Santalaceae have fleshy fruits and are dispersed by birds in a fashion rather similar to the fleshy fruits of Loranthaceae; again, strings of seeds, "rosaries", may dangle from the branch (Godschalk 1983; 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.

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

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 on the stem and 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). For information on genes expressed during ovule/embryo sac development, see Brown et al. (2010); in taxa with higly reduced ovules genes normally expressed in integuments are expressed immediately in tissues surrounding the embryo sac and in the carpel wall surrounding the loculus. 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, Norverto (2004, 2011) for wood anatomy, Wilson and Calvin (2003) for some aspects of anatomy, Bhandari and Vohra (1983) for embryology, Leins (2000) for floral morphology of Viscum.

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).

Within Santaleae, Eremolepis n = 10, Lepidoceras is sister to Eubrachion, Antidapne n = 13 is perhaps a member of a separate clade. 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) and Moore et al. (2010). For the phylogeny of Santalum, the sandalwood genus, see Harbaugh and Baldwin (2007).

Two groups, both stem parasites, are morphologically rather distinctive:

• 1. Visceae. Note that characters with ° after them in the characterization of Visceae above differentiate them from Loranthaceae - the two are neither close nor morphologically very similar beyond superficialities! The development of the ovule and embryo of Visceae is also noteworthy, e.g., there is no suspensor (Ross & Sumner 2005; Friedman & Sumner 2009 and references).

• 2. Ex-Eremolepidaceae. Like Visceae they develop a cuticular epithelium, and their stem stomata are transversely arranged and their leaves are spiral. The inflorescence is catkin-like, the pollen is spherical, the ovules are borne at the base of the ovary loculus and there is no obvious placenta, and the embryo sac is bisporic; the seeds have a viscous covering that is more or less complete, and some have green endosperm (cf. Visceae). In growth these stem parasites are rather like Notanthera (Loranthaceae).

BALANOPHORACEAE Richard, nom. cons.   Back to Santalales

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; cork ?; vessel elements with simple perforation plates; 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 (imbricate), (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, styles separate or style single, stigma punctate or ± expanded; "ovules" 1/carpel, ategmic, basically reduced to an embryo sac; embryo sac usu. bisporic [chalazal spores], 8-celled [Allium type], hooked or not, (antipodal cells 0); fruits minute, drupes or nut-like; endosperm +, (helobial), chalazal haustorium single-celled, first cleavage of zygote vertical, embryo short to undifferentiated, suspensor 0; 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.

Evolution. Infection of the host seems to vary greatly. Arekal and Shivamurthy (1976) described Balanophora abbreviata at attaching to the host by sticky endosperm tubules, tubular embryonal primary haustorium processes then infecting the host; the whole process is reminiscent of infection by a T4 phage. Holzapfel (2001) recorded a radicle in Dactlanthus taylori that attached to the host by epidermal hairs.

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). For the anatomy of the vegetative body, see Gonzalez and Mauseth (2010).

It is very difficult to understand the morphology of the flower, the number of stamens, whether the ovary is superior or inferior, etc., in Balanophoraceae, although there are a fair number of detailed early studies on individual species of the family. Since development of the gynoecium of Balanophora, for example, is perhaps best compared with that of the nucellus, the morphology of the "fruit", too, becomes unclear. Eberwein et al. (2009) note that the naked female flowers of Balanophora can to be adnate to clavate bodies, perhaps modified bracts, that are 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. Thus Fagerlind (e.g. 1945c) notes that the apical cell of the megaspore tetrad in Lansdorffia develops into the embryo sac, but that will depend on orientation...; interestingly, the plane of the first division in the embryo is vertical. Mystropetalon has a clearly inferior ovary and cuboid pollen with pores at the eight corners and other variously angled pollen is known from other Santalales. Embryo sac development varies, and in Balanophora there is a chalazal caecum, as in many other Santalales, but such a caecum is weakly developed in Dactylanthus and absent in Corynaea (Johri et al. 1992; Holzapfel 2001). Holzapfel (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), Fagerlind (1938a, 1945b, c, d: all embryogeny), 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