EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia +, jacketed*, surficial; mblepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte +*, multicellular, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.

Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.

All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group, [] contains explanatory material, () features common in clade, exact status unclear.


Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].


Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].


Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome size [1C] = 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.


Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].


Growth of plant bipolar [roots with positive geotropic response]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].


Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ - zeta - duplication], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.


Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating from inner layer of root cap, trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P = T, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [2C] (0.57-)1.45(-3.71) [1 pg = 109 base pairs], ??whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.

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

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0 [or next node up]; fruit dry [very labile].

EUDICOTS: (Myricetin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

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

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

[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], x = 21, 2C genome size (0.79-)1.05(-1.41) pg, PI-dB motif +; small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = K + C, K enclosing the flower in bud, with three or more traces, C with single trace; A = 2x K/C, in two whorls, internal/adaxial to C, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], whorled, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression.



Age. Moore et al. (2010: 95% highest posterior density) suggested ages of (107-)103(-98) m.y. for this clade, Sun et al. (2013) and age of 115-109 m.y., Z. Wu et al. (2014) an age of about 163 m.y.a., and Naumann et al. (2013) an age of around 109.7 m.y. (but note position of Berberidopsidales - 112.6 m.y.).

Although Soltis et al. (2008) give the ages of divergence of a number of branches below asterids, they are based on a topology [Berberidopsidales [[Caryophyllales + Dilleniales], Santalales, asterids]], and the ages of (131-)120, 117(-112) m.y. in Bell et al. (2010) are based on a similar topology.

Phylogeny. Prior to the seventh version of this site asterids were part of a major polytomy that included rosids, Berberidopsidales, Santalales, and Caryophyllales, and the order of branching below the asterids is still somewhat unstable. For further discussion, see the Pentapetalae node.

SANTALALES Berchtold & J. Presl - Main Tree.

Mycorrhizae absent; acetylenic fatty acids [e.g. santalbic/ximenyic acid; triglycerides with C18 acteylenic acids], triterpenic sapogenins + [Loranthaceae?], essential oils; 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; flowers quite small [10> mm across], K small, open, cupular, teeth ± inconspicuous, C valvate, large and protecting bud, (apex inflexed ["hooded"]), with adaxial hairs; A opposite C, anthers basifixed; pollen grains bipyramidal-spheroidal, surface smooth-perforate to reticulate; nectary [sometimes as "disc"] +; G [3], ovary septate below, placentation free central above, style +, stigma small; ovule 1/carpel, pendulous, apotropous, tenuinucellate, outer and inner integuments ca 4 cells across, micropyle endostomal; embryo sac curved, with chalazal caecum; fruit a drupe, 1-seeded, K persistent; seed coat crushed/o; chalazal endosperm haustoria +, (endosperm with starch); embryo small/minute, green; germination hypogeal. - 13 families, 151 genera, 1,992 species.

Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).

Age. Anderson et al. (2005) date crown-group Santalales at 108-101 m.y. old.

Evolution: Divergence & Distribution. Where a number of 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, the characterization above will need to be adjusted accordingly. Grímsson et al. (2017a) summarized pollen variation in the clade.

Plant-Animal Interactions. Santalales are the food plants of caterpillars of some Pieridae-Pierinae-Aporiina, including the large genus Delias, with 165-to 250+ species (all told, ca 440 species recorded, but on only 9+ genera; 2/5 of all host-plant records) and Lycaenidae, Loranthaceae (especially), Olacaceae, Ximeniaceae (all Lycaeninae in particular), Opiliaceae and Santalaceae-Santaleae, -Visceae, etc., all being recorded as hosts (Ehrlich & Raven 1964; Fiedler 1991, 1995, 1996; Congdon & Bampton 2000; Braby 2005, 2006; Burns & Watson 2013). The ancestors of the butterflies seem to have eaten mostly species of Brassicales and their initial santalalean hosts may have been Loranthaceae (Braby 2005, 2006; Braby & Trueman 2006; Braby et al. 2006); there are no reports of pierine caterpillars on free-living Santalales, although given that there are rather few species of such plants, this is not very surprising. The misteltoe-eating aporiine butterflies have been dated to 42 m.y. (Braby et al. 2007). Some pierids have switched food plants from the mistletoe to its host (Braby & Trueman 2006). The origin of mistletoe feeding is dated to (57-)50, 42(-38) m.y.a., but Delias itself diversified only (29-)25(-23) m.y.a., i.e. butterfly diversification would have had to occur well after the diversification of that of their hosts (Braby 2006 for information). There ia a record of the monogeneric Pieridae-Pseudopontiinae on Opiliaceae (Robinson et al. consulted vii.2015). Interestingly, a number of the adults of these pierines have warning colouration on the undersides of their wings, and some caterpillars also have warning colourations. However, it is unclear what particular compounds the insects might pick up from their santalalean hosts that would discomfit potential predators (Braby & Trueman 2006), although there is movement of alkaloids from host to parasite in both Santalaceae and Loranthaceae (Cabezas et al. 2009).

Bacterial/Fungal Associations. Little is known about mycorrhizae in Santalales, but the few taxa studied largely lack them (Landis et al. 2002; see also Brundrett 2017b), exceptions being Ongokea, Coula and Strombosia (Malécot 2002 for references); the second two genera are not hemiparasitic. The absence of mycorrhizae, as well as that of root hairs in some taxa, is probably connected with the adoption of the hemiparasitic habit. The absence of root hairs is perhaps unlikely to be a synapomorphy for the whole clade (c.f. Judd & Olmstead 2004), and although there is little information on this feature in Kuijt et al. (2015), they are quite widely present in Santalaceae, at least (Fineran 1963), but I know nothing about root hairs in the first seven families below.

Genes & Genomes. Nickrent et al. (2010: supplement) summarize information about chromosome numbers.

The mitochondrial coxII.i3 intron is absent in Comandra, the only member of the order to have been sampled. The rate of change in the nuclear 18s rDNA gene has been greatly accelerated, but that in other nuclear protein-coding genes much less so (Su & Hu 2012).

Chemistry, Morphology, etc. For the general chemistry of the group, see Kubitzki (2015). For the distribution of the acetyleneic santalbic (= ximenyic) acid (E-11-octadecen-9-ynoic/octadeca-11-trans-en-9-ynoic acid) in this clade, see Aitzetmüller (2012); it is found in most groups, and Aitzetmüller (2012) suggests that there are similar compounds with quite wide distributions in the order. For (poly)acetylenic and related fatty acids in the seeds, see also Badami and Patil (1981).

Vascular pits are notably variously bordered throughout Santalales (Herendeen et al. 1999b); Carlquist (2006) suggests that non-bordered perforation plates are a possible similarity with Caryophyllales. The foliar vascular bundles may lack fibers (but c.f. Olacaceae, Loranthaceae, ?some Opiliaceae). Terminal veinlet tracheids and cristarque cells are scattered through the whole group (Baas et al. 1982; Kuijt & Lye 2005). Wax tubules with palmitone as the main wax occur in several members (Ditsch & Barthlott 1997).

The are a number of morphological issues surrounding the flower. First, there has been controversy over the nature of the various whorls encircling the flower. What appears to be the outer perianth whorl - often a minute, rim-like structure - has been interpreted as being a "caylculus" of paired, connate structures of prophyllar/bracteolar origin in a number of Santalales (Wanntorp & Ronse De Craene 2009; Ronse de Craene 2010; Ronse de Craene & Brockington 2013). However, if bracteolar, their shift on to the top of an inferior ovary needs explanation, as does their presence in the terminal flower of a cymule since these would not normally be expected to have any prophylls at all associated directly with them. Oddly, in Loranthaceae, a "calyculus" is described in flowers which are also shown as having a prophyll (Wanntorp & Ronse De Craene 2009). This "calyculus" is a calyx that, initiated as a ring, may become irregularly lobed as it develops (Suaza Gaviria et al. 2016 and references). 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) note that this structure is not regularly lobed and usually lacks any vascular supply, although it is vascularized in Nuytsia, at least. Finally, in Santalaceae like Comandra there is no evidence of any calyx, at least from gross morphology. It seems best to call any "calyculus", a calyx (see also Kuijt 2013, 2015), and the single perianth whorl of some Santalales represents the corolla of other members (Wanntorp & Ronse De Craene 2009; Ronse de Craene & Brockington 2013; Kuijt 2015), however, at least sometimes its members are reported to have three vascular traces, two coming from commissural bundles (F. H. 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 (F. H. Smith & Smith 1942, 1943; Eyde 1975).

The second issue is the complex embryology in the order, which is first evident in the loss of the integuments and the disappearance of an organized ovule and placental tissue; the number of integuments in "Olacaceae" is unclear (e.g. Johri & Bhatnagar 1960; Maas et al. 1992; Breteler et al. 1996; Malécot 2002; summary in Brown et al. 2010 and references). Tracheids in the "nucellus" have been reported from some species, as has vascular tissue directly reaching the embryo sac (Werker 1997). Some taxa may have both micropylar endosperm and embryo sac haustoria (Mickesell 1990), and variation in embryo and endosperm development and embryo sac morphology is very considerable (see e.g. Johri & Bhatnagar 1960; Kuijt 2015), and the remarkable embryo sacs growing up the style of Loranthaceae are without parallel elsewhere (see Bachelier & Friedman 2011 for literature). There may sometimes be two ovules per carpel (see Maas et al. 1992). Further developmental studies are much needed.

Corolla hairs commonly occur in small tufts immediately abaxial to where the stamens are inserted on the petals, as in Strombosia and most Santalaceae. The anther wall is monocotyledonous in development in Maburea (Erythropalaceae: see Maas et al. 1992). It is difficult to estimate the thickness of the single integument - even when you think there is one - because it is often more or less digested by the endosperm quite soon after fertilization (e.g. Bhatnagar & Agarwal 1961).

For general information, see van Tieghem (1896), Kuijt (2015), the Parasitic Plants website (Nickrent 1998 onwards), and Heide-Jørgensen (2008), for the first six families in particular, the old Olacaceae, see Reed (1955) and Malécot et al. (2004), both general, Baas et al. (1982: leaf anatomy), Sleumer (1984a: New World taxa, pollen, anatomy, etc., 1984b: Malesian taxa, general), Lobreau-Callen (1980, 1982: pollen) and Johri (1962: embryo sac). For other information, see Roberston (1982; Olac).

Phylogeny. Malécot (2002) analyzed the variation in four genes emphasizing members of the old Olacaceae; he discussed variation of morphological characters in the context of molecular and combined morphological-molecular phylogenies. A number of clades appear to be fairly well supported. Erythropalaceae s.l., including Strombosiaceae and Coulaceae (Coulaceae were not included in all analyses, and their position was rather labile) are perhaps sister to all other Santalales and are free-living (Malécot 2002). These clades tend to differ in most probably plesiomorphic features (e.g. life style) from other Santalales (data from Michaud 1966; Malécot 2002; Malécot et al. 2004: a morphological analysis). However, exactly where they should be placed on the tree still waits for a strongly-supported resolution of relationships within Santalales, indeed, Coulaceae were not immediately associated with Erythropalaceae and Strombosiaceae in any analyses (Sun et al. 2015). 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. Molecular data place Octoknema rather differently than do morphological observations, which put the genus with the free-living members of Santalales (e.g. Malécot et al. 2004); if the latter position is confirmed, this may suggest that there have been a number of reversals in habit in this clade. Malécot and Nickrent (2008) have since found that the old Olacaceae formed about eight clades basal to other Santalales, but relationships between these clades were unclear (Nickrent et al. 2010: see the tree below) and remain so in the recent analyses of Sun et al. (2015). Few members of these basal clades were included in Z.-D. Chen et al. (2016), and there was some support for a paraphyletic Santalaceae that included Opiliaceae.

However, the big picture of relationships between the other hemi-parasitic taxa seems to be stabilizing (see Sun et al. 2015). 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; Sun et al. 2015: both plastid and non-plastid genes); this topology is followed here. Opiliaceae (one genus) were strongly supported as being sister to a clade [Santalaceae + Viscaceae] in Soltis et al. (2007a; see also Nickrent et al. 2010). Der and Nickrent (2008) found that Santalaceae were polyphyletic, a few genera being placed in Opiliaceae and Schoepfiaceae, while within Santalaceae there are eight well supported clades; for further details of the latter, see that family.

Mystropetalon, Dactylanthus, and Hachettia, three members of Balanophoraceae, formed a clade (100% p.p.) 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). Although Nickrent et al. (2005) suggested that Balanophoraceae were to be placed within Santalales, not sister to them, the former position had very little support. 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 Balanophora, but not in other Santalales. Su and Hu (2012) looked at several mostly nuclear genes; relationships were still not clear, but Balanophoraceae certainly seemed to be outside Santalaceae. Balanophoraceae are the only holoparasitic Santalales, and being holoparasitic, they lack most or all of the distinctive vegetative and even floral features of the other members, but they do usually have a bisporic embryo sac and a curved embryo sac (e.g. Fagerlind 1945c, d); the first feature might suggest relationships to Loranthaceae in particular. Sun et al. (2015) attempt to clarify the situation in their analyses, which included 11 species of Balanophoraceae and 186 other Santalales. Balanophoraceae formed two clades in maximum likelihood analyses, one (A) sister to [Loranthaceae [Shoepfiaceae + Misodendraceae]] [Opiliaceae + Santalaceae]], and the other (B) within the first of the subclades, while in strict maximum parsimony analyses both were in the first subclade, and were perhaps monophyletic and in a different position. Branch lengths of clade A are very long; clade B is made up of the three genera examined by Nickrent et al. (2005: see above). Interestingly, Balanophoraceae have granule-containing tracheidal tissue, known also from Loranthaceae, Opiliaceae, and throughout Santalaceae (and also Orobanchaceae) (Weber 1986). Balanophoraceae are included in Santalales below, but with no particular position (see also Nickrent & Duff 1996; Nickrent 2002; Barkman et al. 2007).

For additional information on relationships, see Kuijt (1968: olacacean complex central), Nickrent and Duff (1996) and Nickrent et al. (1998).

Classification. For a classification of all Santalales except Balanophoraceae, see Nickrent et al. (2010). The seven small families for the seven clades of the poorly-supported basal pectinations are recognised pending resolution of relationships there; if any are sister taxa, they will almost certainly be combined; furthermore, if these families were not recognised, the whole order would have to be placed in a single family (c.f. Sun et al. 2015: p. 500). Families within the old Santalaceae are not recognised, despite the inclusion of highly autapomorphic ex-Viscaceae there. Note that the classification of Santalales in Kuijt (2015) tends to follow morpology in part. Erythropalaceae are not included there at all, although three of the four genera mentioned below are placed in a broadly circumscribed Olacaceae.

Previous Relationships. Santalales have often been compared with Icacinaceae (now known to be polyphyletic). Both have a single-seeded fruits, often small calyx, valvate corolla, etc. (e.g. Takhtajan 1997). However, there is little other evidence for such a relationship; for Icacinaceae, see especially Aquifoliales, Icacinales and Metteniusales.

Thanks. I thank M. F. Braby for information on pierine host-plant preferences.

Includes Aptandraceae, Balanophoraceae, Coulaceae, Erythropalaceae, Loranthaceae, Misodendraceae, Octoknemaceae, 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 - Balanophoranae Reveal, Santalanae Reveal - Loranthopsida Bartling, Santalopsida Brongniart

ERYTHROPALACEAE Miquel, nom. cons.  - Back to Santalales


Trees, shrubs, or lianes with branch tendrils; (gallic acid +); 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), (4-6-merous); K ± free/connate basally; C connate to free, (adaxial hairs 0); stamens = and opposite K or C (with two lateral scales), 2X C; (pollen tricolporoidate); (disc 0); G 10-ridged, ± inferior [Erythopalum], opposite sepals (opposite petals) or odd member adaxial, (not septate), style short, stigma ± lobed or not; ovules with micropyle exostomal, (unitegmic); fruit 5-valved [Erythropalum], K much accrescent, fleshy, spreading, lobed or not [Heisteria]/not; endosperm with starch or oil, (cotyledons orbicular, foliaceous); n = 16.

4/40 [list]: 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; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photo - Flower, Fruit.]

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

The stamens differ quite considerably in size, and the smallest stamens are opposite the petals, the largest stamens opposite the sepals (Michaud 1966). For some information on pollen, see Lobreau-Callen (1982). The gynoecium is often 10-ridged. A nectary is sometimes present, being described as adnate to the ovary (Sleumer 1984a) or on top of the ovary (Sleumer 1984b; c.f. Nickrent et al. 2010).

Baas et al. (1982: they examined Brachynema ramiflorum) recorded only infrequent and thin-walled sclereids. However, in the material examined here (see below) 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, q.v. for stamen position, etc.) described the inflorescence as being an ebracteate corymb. The seed coat is almost obliterated, and it is difficult to make out details of cell walls. 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 below.

See Kuijt (2015) for some general information (esp. under Olacaceae) and Maas et al. (1992) for information on Maburea.

The embryology of this clade is unknown.

Phylogeny. 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.; Nickrent et al. 2016; not mentioned by Nickrent et al. 2010). Nodal anatomy and stomatal morphology, at least, are in agreement with this position. Maas et al. (1992) noted the similarity of Maburea and Brachynema in leaf anatomy.

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 [Octoknemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]]]: C ± connate; A adnate to C; ovules pendulous, apotropous; embryo sac elongated, often curved, with a chalazal caecum, micropylar caecum +, ± developed.

STROMBOSIACEAE van Tieghem  - Back to Santalales


(Mycorrhizae +); ?santalbic acid; (vessel elements with simple perforation plates); ground tissue of libriform fibres; (nodes 1:1, 5:5); (petiole bundle with adaxial bundles); (groups of minute unlignified fibres associated with foliar vascular bundles); epidermal cells crystalliferous, with silica sand, stomata aniso-, cylco-, (helico)cytic; leaves spiral to 2-ranked, (lamina venation palmate); inflorescence fasciculate; flowers 4-5 merous, (hypanthium +); C (fleshy), (adaxial hairs 0); (nectary extrastaminal - Engogemona); A & adnate to C, = and opposite, (10, adnate on either side of C - Scorodocarpus), (filaments short, connective massive, anthers transversely multiseptate - Tetrastylidium), (loculi dehiscing separately - Engomegoma); tapetal cells bi/multinucleate; pollen tricolpate/tricolporoidate; G [3-6], (inferior), style short to long; ovules (5), (unitegmic, integument ca 6 cells across); (megaspore mother cells several), (embryo sac caecum 0); endosperm starchy, chalazal endosperm haustorium unicellular, growing into the funicle, embryo tiny; n = 20.

6 [list]/18. Scattered Pantropical (map: Sleumer 1984a, b; Malécot 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). Photo - Fruit.]

Evolution: Ecology & Physiology. Strombosia pustulata is one of the 18 species in the Congo Ituri rainforest that together made up 50% of the above-ground biomass (at 1.8%: Bastin et al. 2015).

Chemistry, Morphology, etc. For general information, see Sleumer (1984a, b) and Kuijt (2015: as Olacaceae, no Diogoa), Agarwal (1963b) for Strombosia, and Breteler et al. (1996) for Engomegoma.

Synonymy: Scorodocarpaceae van Tieghem, Tetrastylidiaceae van Tieghem

[Coulaceae [Ximeniaceae [Aptandraceae, Olacaceae [Octoknemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]]: stomata paracytic.

Age. The age of this clade is about 103.6 m.y. (Magallón et al. 2015).

COULACEAE van Tieghem  - Back to Santalales


(Mycorrhizae +); ?santalbic acid; laticifers +; mesophyll ?lignified; epidermis lignified, with druses, epidermis with cork-warts [from stomatal complexes]; hairs dendritic; lamina venation scalariform; inflorescence (branched), with 3-flowered cymes along axis; flowers sessile; C basally connate, (adaxial hairs 0); A 10-20; pollen grains tricolporoidate, large verrucae along colpi and in polar regions; nectary 0?; G [(3-)4(-5)], style 0-short, stigma ± lobed; ovules with outer integument 5-6 cells across, inner integument 5-6 cells across; endosperm with starch; n = ?

3 [list]/3. Interrupted pantropical (map: Sleumer 1984a, b; Malécot 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

Evolution: Ecology & Physiology. In the Congo Ituri rainforest, Coula edulis is described as a hyperdominant species (Bastin et al. 2015: one of the 18 trees that made up 50% of the above-ground biomass - it makes up 2.7%).

Chemistry, Morphology, etc. The arrangement of the androecium is complex (Kuijt 2015).

For general information, see Sleumer (1984a, b) and Kuijt (2015).

[Ximeniaceae [Aptandraceae, Olacaceae [Octoknemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]: root hemiparasites [contact with host by xylem]; 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; silicification of mesophyll cells +, cuticular thickening +, guard cell chamber small.

Age. Moore et al. (2010: 95% highest posterior density) suggested ages of (99-)96(-91) m.y. for this clade, 98-75 m.y. is the age in Sun et al. (2013), while around 128 m.y. is the age in Z. Wu et al. (2014).

Evolution: Divergence & Distribution. Santalales are unusual in that this parasitic clade is much more diverse than its free-living sister group, the reverse of the size relationship normal in parasitic:non-parasitic clades, however, most Santalales are only hemiparasitic (Hardy & Cook 2012); Orobanchaceae, slightly larger, are another example of the same pattern.

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 the families above have a superior ovary, and so do, for example, [Exocarpos + Omphalomeria], a "basal clade" in Santalaceae (Der & Nickrent 2005), Loranthaceae are inferior, Schoepfiaceae are half inferior, and more or less superior ovaries are also found in the clade. Either there are independent origins for the character of inferior ovary, or reversals, or both.

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) suggested that this may represent competition between female gametes given that their normal spatial constraints (i.e., being enclosed in an organised ovule, see below) are absent.

Ecology & Physiology. The plesiomorphic life style in Santalales 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); for hemiparasitism, see also Fineran (1991). Aerial hemiparasitism has been derived some five times (Nickrent 2002), intermediate taxa 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; Mathiasen et al. 2008: good survey of stem parasites). Some Santalales are largely endophytic, although the part of the plant that is visible is chlorophyllous (Santalaceae, e.g. some species of Viscum and Arceuthobium), while Balanophoraceae are holoparasitic (Nickrent et al. 2005; see also Tesitel 2016). A few Santalaceae in particular are hyperparasites, often parasitizing Loranthaceae, and some species of Phoradendron (Santalaceae) are even obligate parasites on other members of the same genus (Calvin & Wilson 2009; C. A. Wilson & Calvin 2016: "epiparasites"). For general information on parasitiism, see Kuijt (2015), for physiological details of parasitism, see Stewart and Press (1990).

Chemistry, Morphology, etc. Gran(ul)iferous 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). The haustoria may differ considerably in morphology (Kuijt 1968), but I have not followed this up.

Ovule, embryo sac and embryo development of many plants in this clade are all more or less remarkable. Distinct integuments, or even distinct ovules, may not be recognizable, the embryo sacs being borne in a spherical body, the mamelon; this may consist of a basal placenta containing embryo sacs (see e.g. Paliwal 1956; Ross & Sumner 2005; Brown et al. 2010 for discussion as to what this structure might actually be). Brown et al. (2010) surveyed the distribution of integument number across the order, and looked at the expression of two genes, one expressed in the integuments in Arabidopsis, at least, and the other in the chalaza; they found that both genes were expressed in the outer layer of ovules in Santalaceae-Santaleae and -Visceae that apparently lacked integuments, suggesting that the integument(s) had become fused with the nucellus. Individual embryo sacs are often much elongated, even approaching the stigma at the end of the long style, as in several Loranthaceae. In some taxa the endosperm surrounding the single developing embryo is a composite affair, representing the products of more than one embryo sac (Fagerlind 1947a, 1948; Maheshwari 1950; Bhatnagar & Johri 1960; Ram 1970; Bhatnagar 1970; Bhandari & Vohra 1983; Johri et al. 1992; Shamrov et al. 2001; Subrahmanyam et al. 2015; Kuijt 2015 and references). Cocucci (1983) outlined 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 sac. However, more work on embryology and gynoecial morphology is needed.

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

XIMENIACEAE Horaninow  - Back to Santalales


(Axillary thorns - Ximenia); rhombic crystals (and silica bodies) in ray cells; ground tissue of fibre tracheids; (stomata anomocytic); (lamina venation palmate); inflorescence ± umbellate; C 4, 5, 8, 10, free; A (= and opposite C), 2 (3) x C, (adnate to C), (filaments very long - Curupira); anther wall with only one middle layer, tapetal cells uninucleate; nectary 0; G superior, style short to long; ovules (unitegmic/ategmic), "strikingly linear"; cotyledons connate or not; n = 12 (13); germination hypogeal.

4 [list]/13. Pantropical, warm temperate (map: from van Balgooy 1993; Fl. Austral. 8. 1984; Sleumer 1984a, b; Malécot 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

Chemistry, Morphology, etc. Ximenia americana is crassinucellate. Some information is taken from Sleumer (1984a, b) and Kuijt (2015), all general, see also Sankara Rao and Shivaramiah (1978: embryology).

[Aptandraceae, Olacaceae [Octoknemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]: pollen grains ± oblate; ovules anatropous, apotropous, unitegmic or ategmic; endosperm digesting inner part of fruit wall [?Apt.}.

Age. An approximate age of this clade is 96.6 m.y. (Magallón et al. 2015: no Aptandraceae).

Phylogeny. There is no strong evidence that this is a clade; I have simply optimized some characters here.

APTANDRACEAE Miers  - Back to Santalales


Branches plagiotropic [?many]; (arbuscular mycorrhizae + - Ongokea); laticifers +; rhombic crystals in ray cells; nodes 1:1, 5; (petiole bundle fibres +); (epidermis with cork-warts [from stomatal complexes] - some Aptandra); twigs somewhat zig-zag; leaves 2-ranked; (plant dioecious); flowers 4-6 merous, bracteoles ± connate; C ± free, (with apical thickenings), (adaxially glabrous); A connate around style, epipetalous, (free), (extrorse), (valvate - 3-valvate in Hondurodendron); (filaments short); pollen grains mostly oblate, (heteropolar), (4-porate, quadrangular in polar view), (6-aperturate, tri-diporate); (nectary 0; outside A [Aptandra]; alternating with A); G [2(-3)]; ovules often bitegmic; fruit surrounded by fleshy, ± unlobed, accrescent disc, K, or adjacent structures, (nut-like); (endosperm with starch), cotyledons 0-2, connate or not; n = ?

8 [list]/34: Anacalosa (18). Pantropical (also SE China, Formosa) (map: from Michaud 1966; van Balgooy 1993; Sleumer 1984a, b; Malécot 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photo - Flower.]

Age. For records of the distinctive breviaxial tri-diporate fossil pollen Anacalosidites, very similar to pollen of Anacalosa, Cathedra, and Phanerodiscus, from the Upper Cretaceous (Europe, Australia: Maastrichtian, 75-65.5 m.y.a.) and Palaeocene and particularly Eocene (worldwide) onwards, see Krutzsch (1988), Malécot (2002), Malécot and Lobreau-Callen (2005), and Carpenter et al. (2015).

Chemistry, Morphology, etc. In the anthers of Chaunochiton (Aptandra clade) each loculus opens by a separate slit. Androecial variation in Aptandraceae is considerable, as is palynological variation; pollen grains that have four apertures tend to be quadrangular in polar view (Grímsson et al. 2017a). The fruits of Phanerodiscus have what appear to be five, small, backwardly-pointing green perianth lobes, and opposite these are five large, strongly lobed fleshy structures that loosely surround the fruit.

Some information is taken from Sleumer (1984a, b) and Kuijt (2015), all general; see also Ulloa Ulloa et al. (2010) for the remarkable Hondurodendron.

Phylogeny. There are two easily-characterizable clades within Aptandraceae. 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, unique in Santalales, 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). Some 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 1:3); leaves 2-ranked; flowers 3-6-merous, (heterostylous); (K 0); (C 3 - Olax [?connate in pairs]); A 2-3 x C, staminodes +/0, (paired), opposite K, thecae long; tapetal cells 2-4-nucleate; pollen grains (tricellular), 3-porate, (tri-diporate); G ridged or not; ovules ategmic, (unitegmic, integument 5-6 cells across), (nucellar cap + - Olax); embryo sac (bisporic [chalazal dyad], eight-celled [Allium-type]), elongated, (growing to the base of the style); K much accrescent/not; endosperm (chalazal haustorium 4-nucleate), (growing into pedicel), starch slight, embryo tiny, cotyledons 0-1; n = 12.

3 [list]/57: Olax (40). Pantropical (also S.E. China, Formosa) (map: from Sleumer 1984a, b; Fl. Austral. 8. 1984; Malécot 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

Evolution. Ecology & Physiology. For the hemiparasitism of Olax phyllanthi, see Tennakoon et al. (1997 and references); the haustoria tap the xylem. 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. The embryology of Olax is known, and it is quite variable.

Information is taken from Sleumer (1984a, b) and Kuijt (2015), all general; for embryology, see Shamanna (1954) and Agarwal (1963a).

[Octoknemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]: style short.

OCTOKNEMACEAE van Tieghem nom. cons.  - Back to Santalales


?Parasites; ?santalbic acid; essential oils 0; axial parenchyma slight, strands ³4 cells wide; phloem with bundles of fibres; nodes 5:5; sclereids/cristarque cells +; petiole bundle annular (with medullary bundles); silicification of mesophyll cells 0; hairs stellate or dendritic; stomata cyclocytic, anomocytic, etc., cork warts on leaf [from hair bases]; plant dioecious; inflorescences branched or not, in fascicles; (flowers 3-merous); C adaxially glabrous/papillate; staminate flowers: pollen ± tricolporoidate; (disc +); pistillode; carpellate flowers: staminodes +; (glands alternating with staminodes); G [3 (5)], inferior, stigma 3-lobed, lobes bifid/flap-like, multi-lobed; integuments 2 or 1; seed longitudinally ruminate [(6) 9-11 lamellae], radicle relatively very long, cotyledons 6; n = ?

1 [list]/14. Tropical Africa (map: from Gosline & Malécot 2012; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

Chemistry, Morphology, etc. For a summary of what is known about this genus, see Gosline and Malécot (2012), also Kuijt (2015).

[[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]: stem and/or leaves often with transversely-oriented stomata; inflorescence axis indeterminate; (bracteoles 0); G not septate, style hollow; ovules undifferentiated, ategmic; embryo sac protruding at the microyle-growing up stylar canal; endosperm digesting inner part of fruit wall, testa 0; chalazal endosperm haustorium with single nucleus.

Age. This node was dated to (102-)97, 85(-80) m.y. by Wikström et al. (2001); Bell et al. (2010) suggested an age of (115-)99, 91(-76) m.y. and Magallón and Castillo (2009) suggest ages of ca 90.6 m.y., while Plectranthus L'Héritier - N ann et al. (2013) estimated that its age was around 67.1 m. years.

Ecology & Physiology. In ecological literature in particular "mistletoes" usually implicitly or explicitly include members of Loranthaceae, Santalaceae-Visceae and -Santaleae, and Misodendraceae, an ecological grouping like "mangroves" (see references in Watson 2001; Aukema 2003; Ndagurwa et al. 2016). Loranthaceae and Santalaceae in particular can have considerable effects on the communities in which they are found, far beyond any immediate effects they might have on their hosts. Their fruits may be valuable food resources for specialised frugivores, flowers of the Loranthaceae in particular are important nectar sources, their leaves decay rapidly and affect nutrient cycling in the community, and they may also provide valuable real estate for nesting birds and a variety of other animals.

The photosynthetic potential of "mistletoes" (here Loranthaceae and Santalaceae-Visceae, also Misodendraceae) may be low relative to that of their hosts (as little as 10% in some Arceuthobium - Hawksworth & Wiens 1996), or about the same, and if low on a per unit chlorophyll basis, that may be compensated for by high chlorophyll concentrations. Transpiration rates and timing of stomatal opening may also be of interest, however, records need to be sorted out and assigned to the various clades involved (Johnson & Choinski 1993 for literature).

Plant/Animal Interactions. These are still not well understood, but Burns and Watson (2013) emphasized their distinctive nature when they called them "islands in a sea of foliage"; herbivorous arthropods in particular are associated with particular species of mistletoe, and witches brooms are great habitats for many kinds of animals (see also Hawksworth & Wiens 1996).

Chemistry, Morphology, etc. Stems have tranversely orientated stomata in Visceae and Loranthaceae, at least (Kuijt 1959), indeed, such stomata on stem and/or leaf are scattered throughout all the named clades below, although there has been no exhaustive survey of their distribution.

For inflorescence morphology - which can be hideously complex - of this group of families, see Suaza-Gaviria et al. (2017); the main axis seems to be indeterminate, the lateral branches more or less modified cymes with a fair amount of "fusion"/recaulescence, etc.. Suaza-Gaviria et al. (2017) rightly note that inflorescences here are not racemes.

For general information, see Calder and Bernhardt (1983).

[Loranthaceae [Misodendraceae + Schoepfiaceae]]: acetylenic fatty acids 0, essential oils 0; cambium storied; petiole astrosclereids 0; guard cell thickenings?; epidermal cells sclerified, with druses; K minute.

Age. The age of this clade is perhaps ca 81 m.y. (Vidal-Russell & Nickrent 2008a); some (74.8-)71.1(69.5) m.y. is the age in B. Liu et al. (2018), 67.9 m.y.a. in Magallón et al. (2015), and a mere 36.2/40.1 m.y. in Tank et al. (2015: Table S1, S2).

LORANTHACEAE Jussieu, nom. cons.  - Back to Santalales

Inositol as storage carbohydrate; parenchyma apotracheal; cuticular epithelium developing [?]; flowers in triads, peduncle +, articulated, flowers sessile, subtended by recaulescent bract + bracteoles, medium-sized to large; K [= "calyculus"] annular on initiation, lobes irregular, C hairs behind anthers 0; A of different lengths [= heteranthy], adnate to base of C, anthers dorsifixed, versatile; pollen grains oblate, trilobate-± triangular, apertures confluent [trisyncolpate]; G inferior, placentation basal, mamelon extended up style [?all], style long; collenchymatous zone below the embryo sacs; megaspore mother cells many [= multicellular archesporium], embryo sac growing up style (to tip); primary endosperm nucleus moving down the embryo sac, endosperm composite [derived from several ovules], aggressive, variously vertically channelled or angled, embryonic suspensor massive, long, biseriate [= biseriate proembryo], plane of first cleavage of zygote vertical, embryo chlorophyllous [?level]; n = 12; germination phanerocotylar.


77[list]/950 - 6 groups below. ± Tropical.

Age. It has been suggested that the family started diversifying only 28-40 m.y.a. (Vidal-Russell & Nickrent 2008a), however, pollen identified as Nuytsia from rocks ca 48-41 m.y.o. in Tennessee suggest crown ages of (56.1-)50.8, 41.6(-34.2) m.y.a - ages in general may need to be re-evaluated (Grimmsson et al. 2017b, q.v. for details). Another age is (65.6-)59.4(-52.6) m.y. (B. Liu et al. 2018).

1. Nuytsieae van Tieghem

Tree to shrub; ellagic acid +; successive cambia +; plant with mucilage ducts; leaves spiral; plant monoecious; inflorescence racemose; C 6-8, free, yellow; A 6-8, sporangia open separately; tapetal cells 3-4-nucleate; pollen trilobate; G (-4); ovules -4/carpel; embryo sac with lateral caecum near apex; fruit dry, 3-winged; endosperm copious, ?chlorophyll, embryo ca 1/2 the length of the seed, cotyledons 3(-6), foliaceous, ?chlorophyll.

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

Synonymy: Nuytsiaceae van Tieghem

Other Loranthaceae[Atkinsonia [Gaiadendreae [Elytrantheae [Psittacantheae + Lorantheae]]]]: leaves opposite; fruit viscid, rubber outside vascular bundles.

Map: from Meusel et al. 1965; Jäger 1970; Barlow 1983; Polhill & Weins 1998; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010. [Photo - Flower.]

Age. The age of this node may be (57.4-)51.3(-45.7) m.y. (B. Liu et al. 2018).

2. Atkinsonia van Tieghem

Shrub; flowers single, 6-7-merous; K with isolated tracheids, pollen grains spherical; fruit drupaceous; embryo sac remaining in mamelon, with lateral caecum near apex; endosperm longitudinally furrowed, ?chlorophyllous; germination cryptocotylar.

1/1: Atkinsonia ligustrina. S.E. Australia.

[Gaiadendreae [Elytrantheae [Psittacantheae + Lorantheae]]]: ?

Age. The age of this node is around (57.4-)51.3, 50.0(-44.6) m.y. (B. Liu et al. 2018: tribe paraphyletic).

3. Gaiadendreae van Tieghem

Shrub to tree (epiphytic), stoloniferous; flowers 6-7-merous; K (0); fruit drupaceous, viscin 0; endosperm white, longitudinally furrowed; germination ?.

1/1: Gaiadendron punctatum. Montane tropical America.

Synonymy: Gaiadendraceae Nakai,

[Elytrantheae [Psittacantheae + Lorantheae]]: stem parasites, shrubs, forming burl at point of attachment and with epicortical roots running over the surface (0), often forming secondary burls, (shoots developing from roots), root hairs 0; (plant dioecious, flowers then small); (pedicel apex cupular); K not vascularized; C 4-6; anthers often "long", (locellate); G [(3-)4(-5)], (style short), canal + [?distribution]; tapetal cells (uni-/bi-/multinucleate/polyploid); (G [5]); fruit baccate; endosperm chlorophyllous [?level], embryo ± plug-shaped, medium to long, (multicellular processes (also uniseriate hairs) at radicular end - ?Psittacantheae), radicle 0;

Age. The age of this node, and hence of the branch-parasitic habit, is estimated to be (53.2-)48.0(-42.4) m.y. (B. Liu et al. 2018).

4. Elytrantheae Danser

(Endothecium 0 - Lepeostegeres); (G 4-locular, placentation axile; endosperm chlorophyllous - Lysiana).

98/95: Macrosolen (30). South East Asia to the Antipodes, W. Pacific.

Age. The age of crown-group Elytrantheae is some (42.1-)39.3(-36.5) m.y. (B. Liu et al. 2018).

Synonymy: Elytranthaceae van Tieghem

[Psittacantheae + Lorantheae]: n = other than 12.

Age. The age of this node is around (52-)46.9(-41.4) m.y. (B. Liu et al. 2018).

5. Psittacantheae Horaninow

(Stem phyllodinous); C (with basal ligule), (fenestrate, opening explosive - stylar pressure: Tristerix); (1 series of A sterile); (tapetum plasmodial, microsporogenesis successive - Cladocolea); pollen grains (spheroidal, 3-5-zonocolpate - Tupeia), (demicolpate - Dendropemon = Oryctanthus); (style solid); endosperm (0), (white - Struthanthus), embryo (undifferentiated), (cotyledons unequal); (germination cryptocotylar); n = 8 (10, 11 (Tupeia), 12).

19/335: Psittacanthus (120), Struthanthus (50), Passovia (40). New World, Baja California southwards, the Caribbean (New Zealand: Tupeia - doubtfull).

Age. Crown-group Psittacantheae are estimated to be (51.1-)44.3(-36.8) m.y.o. (B. Liu et al. 2018: Tupeia sister to the other genera).

Synonymy: Psittacanthaceae Nakai

6. Lorantheae Reichenbach

(Hairs dendritic/stellate); (inflorescence in involucre/surrounded by coloured bracts); C (basally connate), often fenestrate, opening explosive - staminal pressure; pollen grains (heteropolar); (heterocotyly), (tips of cotyledons fused, germination cryptocotylar); n = 9 (11).

36/400: Amyema (95), Agelanthus (60). Europe, Africa-Madagascar to China, Japan, the S.W. Pacific and the Antipodes.

Age. Crown-group Lorantheae are around (46.3-)42(-37.5) m.y.o. (B. Liu et al. 2018).

Evolution: Divergence & Distribution. The discovery of pollen identified as Nuytsia in Tennessee, as well as other less dramatic pollen finds from elsewhere in the N. hemisphere (Grímmsson et al. 2017b; see also Manchester et al. 2015 for early pollen records) makes one wonder about the biogeography of the family (see below). Pollen grains of the pollen form genus Aquilapollenites, bilaterally symmetrical and with four wing-like projections, are somewhat similar to those of Loranthaceae, but they are also like those of a number of other families (Farabee 1991). There is a Cretaceous circumboreal Aquilapollenites pollen province, however, the pollen has not been found associated with flowers (Friis et al. 2011 and references).

Despite this palynological connection with the northern hemisphere, it is the Australian region in particular that seems to have been important in the origin and early diversification of the family (B. Liu et al. 2018, q.v. for details): There have been at least two major radiations in West Malesia-Southeast Asia, one (?via Asia) in Africa, and one in South America. Loranthaceae are important nectar and even more important fruit sources for birds, and Liu et al. (2018) thought that their evolution might be tied up with thar of songbirds, describing a generalized coevolutionary relationship between the two. Timing is, as one might expect, tricky here. Thus meliphagids, basal oscines, are common on Old World loranths (see below), and Selvatti et al. (2015) suggest that they diverged from other oscines ca 35 m.y.a. and speciated/radiated ca 27 m.y.a. (Early and Late Oligocene respectively), but in Moyle et al. (2016) the crown-group age of the group is a mere 11 m.y. or so. Passerida initially diversified 26-20 m.y.a., Zosteropidae and [Nectarinidae + Dicaeidae], the latter in particular long known for their close association with Loranthaceae, are all less than (31-)27.6, 27.1(-23.1) m.y.o. (Selvatti et al. 2015). Surprisingly, although Loranthaceae are common and widespread in Australia today (see map above) and were, one might have thought, easily dispersed, they are unknown from Tasmania (but are found in New Zealand, New Caledonia, etc.).

Kuijt (2009b) noted that floral variation in Neotropical Loranthaceae was far greater than in Palaeotropical members. It has been suggested that sessile, axillary, 4-merous flowers were primitive in the family - genera around Phthirusa were examples (Kuijt 2011), but c.f. the character hierarchy above... Indeed, much of the discussion about inflorescence and floral morpholology was carried out when there was no real understanding of the evolution of the family. It may well be that a way to understand inflorescence morphology in the family is to think of the main axis of the inflorescence as being indeterminate and bearing triads, pedunculate units each bearing three often sessile flowers with a recaulescent bract and two bracteoles, and these triads are variously reduced and aggregated. Much of the major variation in pollen morphology is to be found in the old Psittacantheae, but resolution in this part of the tree is poor. Although pollen variation correlates quite well with genera and generic groups, relating it to a phylogeny awaits a better resolution of the latter, but Grímmsson et al. (2017a) attempt this task.

Ecology & Physiology. The root parasitic habit, as in Nuytsia, is the basal condition in the family (e.g. Vidal-Russell & Nickrent 2005); the most immediate outgroups (but not Misodendraceae) are also root parasites, as are Atkinsonia and Gaiadendron that appear to be near the base of the family phylogeny (see below for relationships). Roots of Phrygilanthus acutifolius are described as growing down from the host into the soil, and thence to trees many metres away, which the plant then parasitizes (Benzing 1990).

It is estimated that the stem/branch parasitic habit evolved ca 28-40 m.y.a. (Vidal-Russell & Nickrent 2006, 2008a), about when the family started diversifying (rather older estimates in Grímsson et al. 2017b, (53.2-)48(-42.4) m.y. in B. Liu et al. 2018), perhaps later than in Misodendraceae (ca 75 m.y.a., e.g. Vidal-Russell & Nickrent 2007), although exactly when stem parasitism evolved in the Misodendraceae clade is unclear. The host-parasite junction may be much swollen, the host producing wood roses - vascular tissue in the form of variously channeled, split and branched cup-shaped structures. Morphological details of the association between stem parasite and hosts varies, and epicortical roots, which may be plesiomorphous in aerial parasites, form either sympodial or monopodial systems (e.g. Thoday 1961 and references; Polhill & Weins 1998; Calvin & Wilson 2006; C. A. Wilson & Calvin 2006b). Wilson and Calvin (2006a, b) discuss the evolution of the various kinds of host attachments; it is becoming increasingly likely that stem parasitism evolved only once in the family (c.f. Vidal-Russel & Nickrent 2008a) given the topology used here (e.g. Vidal-Russell & Nickrent 2008b; B. Liu et al. 2018). Loranthaceae are primarily xylem parasites, but their haustoria may sometimes tap the phloem (Barlow 1997). Some members of the family are hyperparasites, parasitizing other Loranthaceae, while the endophytic Tristerix aphyllus is almost holoparasitic, only the inflorescence appearing on the surface of the cacti it inhabits (e.g. Mauseth 1990; Amico et al. 2007; Fisher et al. 2013; Mauseth et al. 2015). Host specificity is often very low (Grímsson et al. 2017b and references). See also Kuijt (2015) for further details of parasitism.

Loranthaceae can be keystone resources - and not simply because they provide tasty snacks for elephants (see below). They are a reliable source of both fruit and nectar for vertebrates, birds in particular, and the dense clumps of stems they form on branches are valued as nest sites by many birds (Watson 2001; Watson & Hering 2012). Fallen leaves, and excreta of organisms associated with the parasite, may enrich soil nutrients in nutrient-poor communities, and increase total biomass, diversity, etc. (Watson 2009; Watson & Hering 2012; Ndagurwa et al. 2016). In Australia, at least, mistletoe diversity in a community is unconnected with its productivity, but host ranges are narrower in less productive (= less diverse) communities (Kavanaugh & Burns 2012). In South Africa it has been suggested that a high nitrogen content of the host, perhaps along with efficent water conductance (which will also facilitate nitrogen acquisition) may positively influence parasitism by mistletoes, which is most frequent on species in mesic savanna communities (Dean et al. 1994). Cryptic species of mistletoe have higher concentrations of nitrogen than do non-cryptic species (Fiedler 1996; Canyon & Hill 1997). Press and Phoenix (2005) discuss interactions of Loranthaceae with their hosts (see also under Santalaceae-Visceae).

In Australia, the shapes of loranth leaves and of the eucalyptus host on which they grow are often similar (Barlow & Wiens 1977), although Loranthaceae tend not to be very specific as regards their hosts (see above). Explanations for this phenomenon, at most uncommon elsewhere, vary. Canyon and Hill (1997: p. 395) examined this phenomenon in detail, concluding "[Our] results contradict, in some crucial aspect, all of the mimicry hypotheses currently on offer", indeed, recent work suggests that mimicry is not involved (Blick et al. 2012). For possible host—parasite mimicry, see also Alseuosmiaceae and Lardizabalaceae.

Pollination Biology & Seed Dispersal. Loranthaceae are a major source of both nectar and fruit for birds throughout the tropics. There are about 200 species of bird-pollinated Loranthaceae in Africa (Polhill & Wiens 1998), about 70 species in Australia (Barlow 1984), 36 in China (Qiu & Gilbert 2003), 165 in Malesia (Barlow 1998), and 125 in the New World. Most species with large flowers are pollinated by birds, those with small flowers - often dioecious - are pollinated by bees, etc. (Suaza-Gaviria et al. 2016). 44 species in two genera of Nectariniidae-Dicaeidae, flowerpeckers, endemic to the Indo-Australian area are involved in both pollination and seed dispersal of the family there (e.g. Docters van Leeuwen 1954; Reid 1983). In some Loranthaceae from both the Old and New World the flower opens only when the bud is squeezed or pecked at by the birds (hence the common name of Dicaeidae, flower peckers), opening being by rapid elongation of the initial slits (fenestrae) apparent in the flower buds. This opening can be explosive, the bird being showered by pollen from the anthers which have already opened in bud. Some Loranthaceae are generalists, while in others the shape of the bird's bill and that of the corolla tube match and pollination is more conventional (e.g. Feehan 1985). Other very common pollinators in the family are sunbirds (Nectariniidae-Nectariniini), closely related to Dicaeidae and also Old World, and in Malesia they pollinate species whose flowers do not open explosively (Corlett 2004). Sunbirds are the main pollinators of most African Loranthaceae, and explosive pollination occurs there; Kirkup (1998) provides a detailed study of the variety of floral morphologies involved. In tropical America humming birds are the major pollinators (Kuijt 2015). There is also explosive opening of the flowers in the New World Tristerix (see Abrahamczyk et al. 2017 for pollination of Chilean species), and there the initial slits in the corolla tube are caused by pressure exserted by the style, while in Old World taxa pressure from the stamens causes the slits to appear (literature in González & Pabón-Mora 2017c). For bird-pollination of New Zealand Loranthaceae, see Ladley et al. (1997). Vidal-Russell and Nickrent (2008b) discussed the evolution of bird-pollinated flowers in the family, which, they thought, had occurred several times.

The birds that disperse loranthaceous/mistletoe seeds may specialize almost entirely on fruits of this clade, being part of an association that has evolved six or more times (e.g. McKey 1975; Reid 1991; Restrepo et al. 2002). Defaecation, regurgitation or simply leaving the sticky seed on the branch having removed the flesh are the three common mechanisms of dispersal (Reid 1991: Table 1). The behaviour of the disperser is often very distinctive. Flower peckers, for example, swing their bodies parallel to the branch so the seeds in their excreta land on the branch - or can be wiped off on the branch (Docters van Leeuwen 1954 in particular), and in Africa tinkerbirds (barbets) are common mistletoe eaters, and wipe the seeds on their bills off onto a branch, the seeds being linked in long, dangling strings, "rosaries" (Restrepo 1987), held together by viscin (see also Reid 1983; Godschalk 1983; Polhill & Wiens 1998). In South America friar birds (Euphoniinae, near Fringillidae) commonly eat mistletoe fruits, and they also eat similar fruits from other epiphytic taxa such as Cactaceae (Rhipsalis), Araceae (e.g. Anthurium) and Bromeliaceae-Bromelioideae (Snow 1981; Restrepo 1987; Reid 1991). The seeds may pass through a bird's gut in a mere 20 minutes - some of these birds lack much in the way of a stomach at all (e.g. Reid 1991) - and when they are deposited on a branch, germination is almost immediate. Overall, about 90 species of birds from 10 families are mistletoe specialists, eating fruit of Loranthaceae and some Santalaceae (see Mathiasen et al. 2008). However, how effective mistletoe specialists are in dispersing seed to uninfected trees has been questioned, more generalist fruit-eaters perhaps being better at this (Watson & Rawsthorne 2011).

Plant-Animal Interactions. Loranthaceae are the major hosts for caterpillars of pierid and lycaenid butterflies (see introduction to Santalales for literature), some other hemiparasitic Santalales also being involved. Caterpillars of the pierid Delias occur on Malesian Loranthaceae (Docters van Leeuwen 1954) and of Mylothris on African Loranthaceae (Braby 2005). Lycaenidae-Iolaini caterpillar preferences show fair 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).

Elephants like to eat Loranthus, and will knock over Acacia (= Senegalia) trees to get at the plant (White 1983: see also Santalaceae-Visceae); as noted above, the parasites may be quite rich in nitrogen (see also goats and Santalaceae-Visceae).

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 Davis et al. (2005b) suggested, the absence of root-parasitic Loranthaceae from that area is notable.

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

Chemistry, Morphology, etc. González and Pabón-Mora (2017c) describe the flower of Tristerix as if its orientation were inverted, i.e. the odd petal is adaxial. The apex of the "pedicel" - but see above for inflorescence morphology - is quite often swollen and forms a cupular structure that may be accrescent in fruit (Suaza-Gaviria et al. 2016). The irregularly lobed and rim-like structure on top of the flower, sometimes - but confusingly - called the calyculus, is thought to be of prophyllar origin in Struthanthus and Phthirusa, at least, by Wanntorp and Ronse De Craene (2009). However, evidence suggests that it is calycine in origin and it should be called a calyx (see also Eichler 1868; Kuijt 2015; Suaza-Gaviria et al. 2016), even if it is not vascularized (Schaeppi & Steindl 1942). Polysymmetric 6-merous flowers seem to be plesiomorphous in the family (Barlow 1983; C. A. Wilson & Calvin 2006a; Suaza-Gaviria et al. 2016), but 7-(or 8-)merous flowers occur in Atkinsonia. Stamen dimorphism - even although there are only as many stamens and petals - is supposed to be almost exclusively a New World phenomenon (Kuijt 2010), but the androecium of e.g. Australian taxa like Nuytsia and Atkinsonia are described as being in two series. Anther loculi dehisce independently in Peraxilla (Prakash 1960).

The imbalance of embryological work carried out on Old Word and New World Loranthaceae is extreme. As an example of possible surprises in the latter, Venturelli (1981) found that Struthanthus produced only a single embryo sac and so compound endosperm could not form there, apparently unique in the family (it was formed in Tripodanthus - Venturelli 1983). For literature about the nature of the mamelon, whether at least part placental or ovular (the former is surely likely: see e.g. Narayana (1959) and Suaza-Gaviria et al. (2016); it may be vascularized or not (Narayana 1959: as also in Dendrophthora - Santalaceae-Visceae). Cronquist (1981) and others describe the gynoecium as being 3-4-carpellate with 7-12 ovules. 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 a little 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; Johri et al. 1991). In general, after fertilization the embryo is "planted" back down at the base of the mamelon by the development of a long, biseriate suspensor. Polar and primary endosperm nuclei can also be peripatetic. Thus Venturelli (1981) described how one polar nucleus migrated up the embryo sac in Struthanthus, and after double fertilisation there was apparently an uniseriate strand of endosperm cells in the style, endosperm developing back down in the ovary - however, Johri et al. (1991) in their summary of the literature suggested that the primary endosperm nucleus migrated to the base of the embryo sac, and this migration is indeed mentioned in a number of accounts. The embryo sac quite often has a caecum of some sort, e.g., there is a basal caecum in Lysiana and Lepeostegeres, the antipodal cells being lateral, and the endosperm develops in the caecum (Narayana 1958; Dixit 1959a; Prakash 1960). Both Cronquist (1981) and Takhtajan (1997) - and many primary sources - describe the endosperm as being starchy (e.g. Dixit 1959a, b), but it is not so scored in Malécot (2002); the embryo sac may also be full of starch grains. The endosperm is aggressive, and adjacent tissues become obliterated. However, the vascular bundles are resistant, the result being a mature endosperm that is almost a variant of ruminate endosperm - it is longitudinally furrowed, the furrows marking the position of the vascular bundles. The endosperm may be merely angled in transverse section, as in Amyema (Dixit 1959a). Kuijt (1982) was perplexed by the cotyledons of Psittacanthus ramiflorus which, he thought, showed infraspecific variation - there were either two flat cotyledons, or 7-10 prismatic cotyledons. However, González and Pabón-Mora (2017a) suggested that the persistent reports of polycotyledony in Psittacanthus were incorrect, the "extra" cotyledons being lobes of green endosperm formed in the way just described, and although Kuijt (2017) thought that González and Pabón-Mora had misinterpreted morphology in the context of misidentified seedlings, González and Pabón-Mora (2017d) defended their interpretation, which is followed here. In many Old World Loranthaceae the cotyledons are connate, but not basally; the plumule emerges through the basal slit (Kuijt 1969). The embryos of Helicanthus, Lysiana, and some other genera have multicellular processes and uniseriate hairs at the radicular end (e.g. Johri et al. 1958; Narayana 1958), and a true radicle may not be present (Prakash 1960).

For much information about all aspects of the family, see Johri and Bhatnagar (1972) and Kuijt (2015), for Nuytsia, see Hopper (2010), for a monograph of Psittacanthus, see Kuijt (2009a), for foliar anatomy, see Kuijt and Lye (2005: terminal tracheids of veinlets), for growth habits, see Benzing (1990), for floral morphology and embryology, see Schaeppi and Steindl (1942) and Robles et al. (2016), for pollen, see Feuer and Kuijt (1985 and references) and especially Grímsson et al. (2017a), and for embryology, etc., see Treub (1882: Loranthus), Singh (1951: Dendrophthoe), Maheshwari and Singh (1952), Narayana (1959: Nuytsia), Dixit (1959a, b, 1962), Prakash (1962: Atkinsonia, 1963), Raj (1970), Bhatnagar and Johri (1983) and Subrahmanyam et al. (2015).

Kuijt (2015) noted that the seedlings of genera from the Old Word were not much known, nor the embryology of those of the New World.

Phylogeny. Relationships within Loranthaceae are slowly being clarified. Nuytsia is sister to the rest of the family (Vidal-Russell & Nickrent 2005; Sun et al. 2015; B. Liu et al. 2018). The root parasitic Atkinsonia (S.E. Australia) and Gaiadendron (Central and South America) are also near the base of the phylogeny (Liu et al. 2018: ML bootstrap support low). However, there was rather weak support for the stem parasite Notanthera being sister to all Loranthaceae except Nuytsia (C. A. Wilson & Calvin 2006a, b), both Vidal-Russell and Nickrent (2008b) and Liu et al. (2018) placed this in Psittacantheae. Sun et al. (2015) also recovered Nuytsia and Atkinsonia as succesively sister taxa to the rest of the family (support for the latter position weak), and Gaiadendron again seemed to be in this area. Grímsson et al. (2017a, b) thought that basal relationships in the family were unclear, Grímsson et al. (2017a) noting that the positions of the root-parasitic Gaiadendron and Atkinsonia were uncertain, and they thought that Tupeia might be sister to the rest of the family - but see Liu et al. (2018).

Relationships in Psittacantheae (?basal, ?paraphyletic) were unclear, but Elytrantheae included two well supported clades and the bulk of the family was included in a well supported Lorantheae within which there was a moderate amount of structure (Grímsson et al. 2017a). Indeed, although support for relationships along the spine ranged from strong (PP) to rather poor to strong (ML bootstrap) in B. Liu et al. (2018), support values for both monophyly and basal relationships in Elytrantheae and Psittacantheae and for basal relationships in Lorantheae were low, and the monophyly of a number of genera remains to be established.

Classification. For a suprageneric classification of the whole family, see Nickrent et al. (2010); for some generic limits, see Kuijt (2011). It will be clear from the above discussion that support for elements of the classification above, basically that of Nickrent et al. (2010), are weak.

Previous Relationships. Loranthaceae and Viscaceae (see Santalaceae below, as Visceae) 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. Thus the viscous covering of the seeds of Loranthaceae is mesocarpial in origin, being outside the vascular bundles and, the fruits of Loranthaceae contain rubber (and are sometimes used as bird lime). Although some Loranthaceae such as Phthirusa have very small flowers and congested inflorescences, they are easily separated from Visceae which also have these features; plants of the latter are often lighter green in color, they lack roots running over the surface of the host, their flowers are often three merous, and they have green endosperm, etc..

[Misodendraceae + Schoepfiaceae]: style ?hollow.

Age. The age of this node is ca 75 m.y. (Vidal-Russell & Nickrent 2006, 2007) or ca 58 m.y.a. (Magallón et al. 2015).

Phylogeny. Kuijt (1968) rejected the ides of a close relationship between Misodendraceae and Scopfiaceae (Quinchamalium) obecause of differences he saw between their female gametophytes and endosperm haustoria.

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

Stem parasites; successive cambia + [cambia develop centripetally]; sieve tube plastids lacking starch and protein inclusions; wood rayless [?all]; bundle fibres +; ?stomatal orientation; leaf mesophyll undifferentiated; hairs 0/unicellular; stem apex aborting; plant dioecious; staminate flowers: pedicel +; K 0, C 0; A 2-3, monothecal, dehiscing by apical slit; pollen grains spheroidal, 4-19-pantoporate, pores operculate, surface spinuliferous; pistillode inconspicuous; carpellate flowers: sessile; K 0, ?C 3, minute; staminodes alternate with C; style ± 0, stigma strongly 3-lobed; ovules straight; fruit dry, achenial, attached to 3 much accrescent long-plumose staminodes growing from slits in the ovary; endosperm chlorophyllous, with a single nucleate haustorium that branches in the receptacle, "hypocotylar" zone very broad, cotyledons ± connate, radicle replaced by sticky sheath; n = 6, 8; germination ± cryptocotylar.

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

Evolution: Divergence & Distribution. Pollen of Misodendraceae has been found in Patagonia in deposits ca 45 m.y.o. (Del Carmen Zamaloa & Fernández 2016).

Ecology & Physiology. Stem parasitism may have evolved here ca 75 m.y.a. (e.g. Vidal-Russell & Nickrent 2007) well before that in Loranthaceae or other mistletoes, its origin in the former being dated to some ca 40 m.y.a. (Vidal-Russell & Nickrent 2006, 2007) or - less of a difference - (53.2-)48(-42.4) m.y. (B. Liu et al. 2018). However, exactly when stem parasitism evolved after the separation of this clade is unclear.

Seed Dispersal. Seeds are dispersed by wind, unlike those of other mistletoes, or they stick to passing animals (Reid 1991 and references).

Chemistry, Morphology, etc. The inflorescence may look like a (compound) raceme or spike, but there are clearly cymose units in some species (Suaza Gaviria et al. 2017). The most prominent stucture in the staminate flower is the pedicel. According to Takhtajan (1997) the pollen is colpate. There are reports that the chalazal endosperm haustorium is multicellular ().

For general information, see Kuijt (1969; 2015: in the latter the ovary is described as being superior), for details of wood anatomy, which is rather distinctive, see Carlquist (1985c), for pollen, see Del Carmen Zamaloa and Fernández (2016 and references), and for floral morphology, embryology, etc., see Skottsberg (1914).

Phylogeny. For a phylogeny of Misodendrum, see Vidal-Russell and Nickrent (2007). Misodendron quadriflorum is sister to the rest of the genus, thus making subgenus Angelopogon paraphyletic - c.f. earlier classifications, including that in Zavaro et al. (1997: morphological cladistic analysis).

SCHOEPFIACEAE Blume  - Back to Santalales


(Perennial herbs); aliform confluent parenchyma +; epidermal cells not lignified, (stomata anomo-/cyclocytic); hairs unicellular/0; bract and bracteoles usuaully immediately below and surrounding G, fused; (flowers distylous), medium-sized; (K +, shallowly lobed]), C tubular, ± connate, hairs on C abaxial to A (0); pollen grains tetrahedral, heteropolar, apertures ± confluent, (zonasulculate), ektexine smooth; G (semi-)inferior, style?, stigma lobed to capitate; ovules ategmic; embryo sac U- or J- [Quinchamalium] or open heart-shaped [Schoepfia], chalazal haustoria branched [Quinchamalium], (synergid haustoria +, very slender, growing up style - Quinchamalium); embryo short to long, first division vertical/obligue; chalazal endosperm haustorium +; embryo long [Q.]; n = 12, 14.

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

Chemistry, Morphology, etc. Sleumer (1984) noted that the wood had aliform-confluent parenchyma, unlike other "Olacaceae".

There are prominent bracteoles immediately below the 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) - other genera? Agarwal (1962) described the integument as being "massive", but there is neither micropyle nor obvious integument (Johri & Agarwal (1965).

For additional information, see Dawson (1947 and Kuijt (2015), both general, also F. H. Smith and Smith (1943: floral morphology), Jarzen (1977: pollen of Arjona), Grímsson et al. (2017a: pollen, extensive variation), and Watanabe (1943) and Agarwal (1961), embryology, Schoepfia and Quinchamalium respectively.

Schoepfiaceae are very poorly known.

Phylogeny. That Schoepfia is rather different from "Olacaceae" had often been remarked (e.g. Metcalfe & Chalk 1950; Sleumer 1984). Arjona, ex Santalaceae, was found to be sister to Schoepfia (Malécot 2002), and Quinchamalium, another ex Santalaceae, is also to be included here. Support for the relationships [Schoepfia [Arjona + Quinchamalium]] is strong (Vidal-Russell & Nickrent 2006; Der & Nickrent 2008); Smith and Smith (1943) had noted relationships between Quinchamalium and Schoepfia.

Synonymy: Arjonaceae van Tieghem

[Opiliaceae + Santalaceae]: single perianth whorl [= C].

Age. Bell et al. (2010) dated this node to (106-)89, 82(-64) m.y.a., Wikström et al. (2001) suggested an age of (85-)80, 69(-64) m.y., and Tank et al. (2015: Table S2) an age of a mere 45/44 m.y.a., by far the youngest.

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), 1:3, 1:5; silicification of mesophyll cells 0; cystoliths + (0); stem stomata transversely oriented [Anthoboleae]; leaves two-ranked to spiral; inflorescences axillary, (racemose/spicate/catkin-like, with relatively large bracts), (plant dioecious); bracteoles 0; flowers small, (3-)4-6(-8)-merous; hypanthium + or 0; C free (± connate), (0 in carpellate flowers); A = C, adnate to C or not; tapetal cells 4-nucleate; pollen usu. colporate, microechinate, spheroidal, triangular; (prominent nectaries alternating with A); G [2-5], ovary on elongated receptacle, style (0), hollow, stigma ± capitate; ovule 1(2), pendant, erect, basal [Agonandra], 1<, on mamelon [Anthobolus], with micropyle [Cansjera]; micropylar caecum almost breaks through the "integument"; (pedicel swollen, coloured - Anthobolus); (endosperm haustorium with dendritic branches developing), (additional unicellular secondary endosperm haustoria with dendritic branches - Cansjera), endosperm also oily, embryo narrow, long, (rather short), radicle very short, cotyledons (2-)3-4; germination cryptocotylar; n = 10.

12 [list]/36. Pantropical (map: from Stauffer 1959; Hiepko 1984, 2000, M. Gustafsson pers. comm. ii.2010 - Africa; FloraBase x.2012; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photo - Flower]

Chemistry, Morphology, etc. Metcalfe and Chalk (1950) describe a branching system of lignified cells connecting veins in Olacaceae s. str., i.e. not including Anthobolus. Agonandra and Anthobolus have amphistomatic leaves and green twigs.

Cansjera has a basal ovule (Swamy 1961), and this can also be interpreted as an ovule on a much reduced mamelon. The basal part of the gynoecium elongates greatly before anthesis, leaving the ovary + stigma-style perched on the end of quite a long podium (Swamy 1961). Stauffer (1959) suggested that there might be viscin in the fruits of some Anthoboleae.

For embryology, see also Swamy and Dayanand Rao (1956), Swamy (1961) and Ram (1970), and for general information, see Stauffer (1959), Hiepko (1984) and Kuijt (2015).

Phylogeny. The Australian Anthobolus, ex Santalaceae, is to be included here, relationships being [Lepionurus (support strong) [Anthobolus + The Rest (support weak)]] (Der & Nickrent 2005, esp. 2008); it, like other Opiliaceae, has a superior ovary. Le et al. (2019) in a study that included all but one genus of the family found that Agonandra, probably also with Gjellerupia, was sister to the rest of the family, and in one clade Anthobolus was sister to Champereia etc., but in neither case was support strong. They examine the distributions of a number of morphological characters on their tree (Strombosia is a rather distant outgroup).

Classification. Le et al. (2018) propose a tribal classification for the family - 3 tribes, 12 genera, 36 species - but given the poor support in the basal nodes I do not follow it.

Previous Relationships. Stauffer (1959), who monographed Anthoboleae, considered that they were closer to Santalaceae than to Opiliaceae; Anthoboleae ex Anthobolus are indeed close to Santalum and relatives (Der & Nickrent 2008: support strong).

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; flowers small, (3-)4-5(-8)-merous; hypanthium + or 0; K 0, hairs on C behind A, unicellular, base swollen (0); large nectary glands often +, alternating with stamens; pollen various; G [2-5], inferior, odd member abaxial, (carpellary vascular supply recurrent), stigma often capitate or lobed; ovules straight (anatropous), or not distinguishable, micropylar end ± protruding; fruit drupaceous [mesocarp stony], also baccate, (outer part exfoliating); endosperm (helobial), starchy or not, embryo short to long.

44 [list, tribal assignments]/990 - seven groups below. World-wide, esp. tropics (map: see Meusel et al. 1965; Hawksworth & Wiens 1972; Fl. Austral. 8. 1984; Jalas & Suominen 1976; Polhill & Weins 1998; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

1. Comandra group

Plant herbaceous; (hypanthium +); endothecial thickenings poorly developed; (pollen grains (3-colporoidate); nectary lobes between C; placental column long, twisted, stigma punctate to subcapitate; ovules anatropous, unitegmic; (epicarp dry); secondary endosperm haustoria +, zygote with first division vertical; germination cryptocotylar; n = 13 (14).

2/2. North America, Europe and the Mediterranean, ± temperate.

Synonymy: Comandraceae Nickrent & Der

[Thesieae + Cervantesia group]: placental column long, twisted; ovules unitegmic.

2. Thesieae Meisner

?Santalbic acid; (axillary thorns +); (lamina terete); (plant dioecious); flowers 4-5-merous; (K +, strongly lobed); (C connate); pollen grains (3-colporate), (heteropolar); ovules +, unitegmic; embryo sac not extending beyond ovule; fruit drupaceous [stony layer mesocarp]; endosperm composite, massive, starchy, chalazal haustorium 1-several-celled, branched deep in receptacle, (zygote with first division longitudinal), embryo (suspensor 0), of medium length; n = 6-9(-12).

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

Synonymy: Thesiaceae Vest

3. Cervantesia group

(Axillary thorns +); (gallic acid +); (lamina rhombic, with spines - Jodina); (pollen 3-colporate, surface striate - Buckleya), (heteropolar); nectary lobes between C; G superior to inferior; ovules +; ?embryology; n = ?

8/21. Tropical, warm temperate, esp. America. [Photos - Acanthosyris fruit.]

Synonymy: Cervantesiaceae Nickrent & Der

[Nanodea group [Santaleae [Amphorogyneae + Visceae]]]: ?

4. Nanodea group

?Santalbic acid; (flowers 4 merous); (K +); pollen heteropolar, etc. [Mida]; tapetal cells mulyinucleate; nectary lobes between C; G (semi-)inferior; micropylar endosperm +, cells with dendritic haustoria, 1-celled secondary chalazal endosperm cells parallel to caecum; embryo small, suspensor massive, multicellular; n = ?

2/2. New Zealand, south South America.

Synonymy: Nanodeaceae Nickrent & Der

[Santaleae [Amphorogyneae + Visceae]]: (stem parasites +); (cuticular epithelium +); (ovule reduced to embryo sac).

Age. The age of this node is some (71-)67, 65(-61) or (57-)53(-49) m.y. (Wikström et al. 2001).

Evolution. Genes & Genomes. A genome duplication event (EXCUα) ca 44.8 m.y.o. has been associated with this node (Landis et al. 20180.

5. Santaleae Dumortier

(Stem parasites, epicortical roots +/0); cuticular epithelium + [?all]; (leaves spiral), (scale-like); flowers (unisexual), (sessile); flowers 3-6-merous; (K +), (C 0); pollen grains (3-colporate), (3 porate, surface spinuliferous); (large nectaries alternating with A - Osyris); G ± inferior, mamelon beaked or not; (ovary 1-locular, embryo sacs 2, basal), (ovules epitropous); embryo sac (not extending beyond ovule), (bisporic, 8-nucleate [Allium type]); (pedicel swollen, fleshy in fruit); (seed with a complete viscous covering); endosperm (helobial), (0), (composite [derived from several ovules] - Santalum), (chalazal haustorium multicellular - Exocarpus), (chlorophyllous), embryo (large), (undifferentiated - Lepidoceras), suspensor long/0, (primary [radicular] haustorium +); n = 10, 11, 13, 15, chromoosomes "very small" {Eremo.].

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

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

[Amphorogyneae + Visceae]: (plants hyperparasitic); (C basally connate); stamens with short/0 filaments; pollen grains 3-colporate; G inferior.

Age. Stem Visceae, i.e. the age of this node, are some 72 m.y. old (Vidal-Russell & Nickrent 2008).

6. Amphorogyneae Stearn

(Stem parasites); pyrrolizine alkaloids +; (leaves opposite), lamina with ± palmate (pinnate) venation, (linear), (much reduced); (plant dioecious); flowers 4-6-merous; anther loculi above one another in pairs, all four sporangia form common chamber [Leptomeria]; tapetal cells binculeate; (nectary lobed); G [5], mamelon not beaked, style short; endosperm not starchy; (embryo very small); n = ?

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

Synonymy: Amphorogynaceae Nickrent & Der

7. Visceae Horaninow


Stem parasites, often ± endophytic°, epicortical roots 0°; inositol storage carbohydrates, methylated cyclitols, myricetin, caffeic acid esters, toxic polypeptides +, essential oils 0, ?santalbic acid; (sclereids +); cuticular epithelium +; stems brittle and jointed°; cuticle waxes usu. platelets with irregular margins; leaves opposite, lamina with secondary veins usu. ± palmate, petiole obscure; plant monoecious° (dioecious - Viscum), (flowers perfect - Phacellaria); no bract and bracteole immediately under the ovary°; flower (2-)3-4(-5)-merous°, usu. sessile, small° [<4 mm long]; C hairs abaxial to A 0; staminate flowers: C often 4, hairs 0 [?all]; A sessile, anthers opening by pores°/slits, (3-1-locular), (polythecate, dehiscence transverse), (connate [= a synandrium], opening circumferentially); (endothecium 0); pollen 3-colporate, (pseudocolpi +), spherical°, surface echinate; carpellate flowers: C often 3, (reduced to apiculae); nectary ± 0; style (solid); ovary with mamelon (0), tracheids 0, 2 "ovules"°; embryo sac bisporic, 8-nucleate [Allium type]/tetrasporic [Adoxa type]/monosporic, 8-nucleate [Polygonum type - Viscum minimum], (elongated), straight [Viscum] to U-shaped, starch copious; ("berry" explosive - Arceuthobium, Korthalsella), viscous covering +, incomplete, inside the vascular bundles°, consisting of polysaccharide threads and mucilage°, endocarp +, thin°; endosperm chlorophyllous°, starchy, (plane of first cleavage of zygote vertical - Korthalsella, Arceuthobium), suspensor short or 0, embryo small to large, chlorophyllous, with 1 cotyledon [= 2 connate], lateral in seed; n = 10-14(-17), nuclear genome size [1C] to 100.6 Gb.

7/520: Phoradendron (235), Viscum (65-150), Dendrophthora (70). Worldwide (Map: from Barlow 1983: throughout much of the northern Sudano-Sahelian-Zambezian zone; Fl. Austral. 22. 1984; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

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

Evolution: Divergence & Distribution. Visceae have perhaps been branch parasites for much of the 72 m.y. the clade may have existed (Vidal-Russell & Nickrent 2008). Arceuthobium is well represented (six species, leaves quite well developed) in Eocene Baltic amber 47-34 m.y.o. (Sadowski et al. 2017a).

The large genus Thesium may be of South African origin and with a stem age of ca 60 m.y. and a crown age of (56.5-)42.7-35.9(-24.4) m.y. (T. E. Moore et al. 2010: a variety of analyses). Santalum, the sandalwood genus, is centred on Australia and the Pacific, and there have been perhaps two migrations from Australia to Hawaii and also two migrations out of Hawaii to the south Pacific (Harbaugh & Baldwin 2007); polyploidy seems often to have occurred before these long distance dispersal events (Harbaugh 2008).

The leaves of Viscum crassulae are supposed to mimic those of its preferred host, Portulacaria afra (Didieraceae: ?reference).

Ecology & Physiology. For root parasitism in Santalum album, see Tennakoon and Cameron (2006). The branch-parasitic habit seems to have evolved three times in Santalaceae, in Visceae, Eremolepis (Santaleae) and Dendromyza (Amphorogyneae) (Der & Nickrent 2008; Vidal-Russell & Nickrent 2008). Some ex-Eremolepidaceae have a decided preference for Myrtaceae as hosts (Kuijt 1988). Expanded wood roses may be produced by the host at places where the parasite attaches.

Press and Phoenix (2005) and Ndagurwa et al. (2016) and references discussed the general ecological effects of the host-parasite interactions of Visceae. Most species of the dwarf mistletoe Arceuthobium parasitize Pinaceae (over 2/3 the records are from Pinus alone), with a few species growing on Cupressaceae (Hawksworth & Wiens 1996; Farjon 2008). Phacellaria (Visceae) is an obligate hyperparasite on a few other Santalaceae (Dendrophthoë) and especially Loranthaceae, Taxillus in particular (Li & Ding 2006; see also Mathiasen et al. 2008), while Phoradendron durangense and P. falcatum parasitize only other species of Phoradendron (Calvin & Wilson 2009). Other hyperparasites are known from Amphorogyneae, notably Phacellaria (C. A. Wilson & Calvin 2016).

Some species of Arceuthobium and Viscum are almost holoparasites, being largely endophytic (Nickrent & García 2009; Mauseth & Rezaei 2013). The mistletoe V. minimum, from the eastern Cape, has aerial stems about 3 mm long and with but a single internode (Don Kirkup, pers. comm.); these arise from the endophytic portion of the plant (for its growth, see Mauseth & Rezaei 2013). It is also an indicator of elephant grazing, the animals preferentially eating branches on which it is growing since it is succulent and nutrient-rich (Germishuizen et al. 2007, and references: see also Loranthaceae). Indeed, from the Mediterranean eastwards, A. oxycedri-infested stems are preferred forage for sheep and goats, sometimes to the decided detriment of the vegetation in which the parasite grows (Hawksworth & Wiens 1996; see references in Delibes et al. 2017 for the arboreal habit of goats...).

Parasites like Arceuthobium depend on their hosts for water and also much photosynthesate, since although they have chlorophyll, it may be as little as 10% of normal amounts; when witches brooms develop, the host becomes particularly severely stressed (Hawksworth & Wiens 1996). Indeed, initial development in Arceuthobium in particular is within the host (there are no cotyledons, etc.) and in some species an extensive endophytic system develops. In largely endophytic Visceae there is both a phloic and xylary connection between host and parasite, in the others, the connection is only through the xylem (Aukema 2003; Tesitel 2016); in Arceuthobium the flow of nutrients from host to parasite is commonly apoplastic (Calvin & Wilson 1996; C. A. Wilson & Calvin 1996).

Pollination Biology & Seed Dispersal. In Santalum, filament hairs are involved in secondary pollen presentation (Howell et al. 1993), while some Visceae are wind pollinated. Three species of Arceuthobium from the Rocky Mountains were visited by 200+ species of insects, although their flowering times were only somewhat overlapping and their major pollinators (up to six) were also only partly overlapping; pollen was also dispersed by the wind up to 150 m (Penfield et al. 1976). Indeed, pollination here seems particularly unclear/variable; wind may sometimes be involved, and the female flowers can have large blobs of ?nectar on the stigma - c.f. pollination droplets in gymnosperms (Hawksworth & Wiens 1996).

Many Visceae, and some Amphorogyneae and Santaleae, stem parasites, have fleshy fruits and are dispersed by birds in a fashion rather similar to the fleshy fruits of Loranthaceae, indeed, information about these (and other Santalalean) families is often to be found under the general name, "mistletoes" (Watson 2001; Aukema 2003). Strings of seeds, "rosaries", from the bird faeces may dangle from the branch (Godschalk 1983; Restrepo 1987: South American species; Reid 1991; see also Loranthaceae). In Arceuthobium seed discharge is explosive, the seed leaving the fruit at about 1370 cm/second and travelling up to 20 meters (66 feet) (Hinds et al. 1963; Hinds & Hawksworth 1965). Although immediately prior to seed discharge fruit temperature increases substantially because of uncoupled respiration, how that increase might effect seed discharge is unclear (deBruyn et al. 2015). For the dispersal of seeds of some Visceae and Santaleae by birds, see Restrepo et al. (2002).

Fertilization may be considerably delayed after pollination (Hawksworth & Wiens 1996; Ross & Sumner 2005). In Arceuthobium the seeds can take two years to mature and the embryo lacks a plumule but has a well developed radicle (Ross Friedman & Sumner 2009). Photosynthesis in the green endosperm of Visceae is described as facilitating germination by providing energy for the establishment of the seedling (Tesitel 2016); green endosperm in also known in the very different Crinum (Amaryllidaceae-Amaryllidoideae).

Vegetative Variation. Leaf morphology in the old Eremolepidaceae (Santaleae) is very diverse. Thus Eubrachion has peltate scale leaves, while in some taxa what were initially scale leaves resume growth and the expanded leaf is then tipped by the apex of the scale leaf.

The orientation of cataphylls and their relation to prophylls in genera like Phoradendron (Visceae) as described by Kuit (1996) are unclear. Similarly, the structures called prophylls by Kuijt (2013) and found on vegetative shoots, as in Arceuthobium azoricum, may well be colleters or something similar, since the axillary branches have their first pair of leaves lateral in position with respect to the axis (= true prophylls?) in the same plane as these putative prophylls (see also Kuijt 2015: pp. 10-11, esp. Fig. 1d for a discussion). Along the same lines, Ashworth (2000) noted that in Phoradendron, if the first leaves were cataphylls they were in the ad/abaxial plane, while the next pair of leaves, expanded, were lateral whether or not there were cataphylls - but she also noted that there was infraspecific variation in such features. Anatomical/developmental work is needed here.

Genes & Genomes. See Wiens and Barlow (1971) for cytology. Molecular evolution has greatly speeded up in the Viscum clade (Vidal-Russell & Nickrent 2008). There is a very large genome with a 2C value of some 205.8 pg or more in Viscum, alone of Santalales examined, Viscum album having the largest (Leich et al. 2005; c.f. Zonneveld 2010), and the amount of DNA per chromosome is perhaps the highest in all eudicots (Jordan et al. 2014; Hidalgo et al. 2017c).

Viscum scurruloideum, not a notably reduced species, has a tiny mitochondrial genome (ca 66 kb) with high substitution rates that has lost its respiratory complex I, pratically unique in eukaryotes, yet at the same time it has remarkably large repeat pairs that are practically identical; V. album, on the other hand, has a far larger mitogenome of ca 565 kb (Skippington et al. 2015). It and at least some other species of Viscum lack nad genes, genes that code for the first enzyme in the mitochondrial electron transport chain that is involved in respiration - a few unicells are the only other organisms that lack this complex. Oxidative phosphorylation is much reduced, although the rest of the mitochondrial genome is rearranged and some respiration does occur (see also Skippington et al. 2017), however, Viscum is slow-growing and the plant may have little need for much much mitochondrial ATP (Senker et al 2018; Maclean et al. 2018). Substituution rates are high in other species of Viscum like V. album, and here there has been lateral gene transfer from a host in Ericales (matR: the Diapensiaceae-Ericaceae area) and in other Santalales (ccmB: Loranthacaeae, perhaps close to Amyema), the latter gene probably moving during a hyperparasitism event (Skippington et al. 2017).

Economic Importance. Mathiasen et al. (2008) provide a list of Santalaceae that harm crops and timber trees. Species of Arceuthobium (e.g. A. americanum) are major pests on conifers in west North America in particular, causing extensive witches' brooms and the ultimate death of the host; the amount of timber lost is substantial, some 15.1 million m3 per year in the U.S.A. and Canada alone (e.g. Unger 1992; Hawksworth & Wiens 1996; Sadowski et al. 2017).

Chemistry, Morphology, etc. The pith of twigs of Viscum album is like an eight-pointed star (IAWA J. 23(1) - Cover). The cuticle in Visceae becomes progressively thicker and epidermal cells may die and get incorporated into this cuticular layer (it may be close to 600 μm across - Damm 1901), some subepidermal cells may divide, but there is no cork cambium/cork - indeed, the cuticular layer may be thicker than the cork on tree stems of equivalent thickness (Damm 1901; C. A. Wilson & Calvin 2003). This is the cuticular epithelium, and it lacks both suberin (c.f. cork) and lenticels (Wilson & Calvin 2003); it is present in Eremolepidaceae (Santaleae), some other Santaleae, and Visceae, but its distribution needs clarification. Stomata on the stem and leaf are very commonly tranversely oriented in Santalaceae (Kuijt 1959: stem; Butterfass 1987).


For inflorescence morphology in Viscoideae, see e.g. Kuijt (1959) and Suaza Gaviria et al. (2017) and references. To say that inflorescence vasculature can be difficult to interpret is an understatement, as the illustration of that of Dendrophthora flagelliflorus by Kuijt (1959) suggests, although little work seems to have been done in this area (but see York 1913). A number of Santalaceae have three traces in their perianth members, the two lateral traces coming from commissural bundles (F. H. Smith & Smith 1943), but Viscoideae, for example, have but a single trace, and the stamens may even lack traces (Kuijt 1959).

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. 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 in the tissues immediately surrounding the embryo sac and in the wall surrounding the loculus. Ross and Sumner (2005: Arceuthobium) and York (1913: Dendrophthora) describe the antipodal end of the embryo sac as being apical on the mamelon, while Zaki and Kuijt (1994: Viscum) show it as being basal; there seems to be variation here (see also Rutishauser 1935), while York (1913) even described the chalazal ends of the two embryo sacs of Dendrophthora as fusing. Bhatnagar and Agrawal (1961) draw an embryo sac of Thesium in the apical prolongation of the nucellus; might it be the prolongation of a normally-positioned embryo sac? Luna et al. (2017) suggest that the large nectary lobes alternating with the corolla in Jodina and the corolla lobes themselves develop into the fleshy part of the fruit, the latter eventually falling off and the former persisting and forming the flesh of the drupaceous fruit, the stone is mesocarpial in origin; the endosperm haustorium demolishes first the placenta and integument and finally the endocarp. Furthermore, the endosperm has nests of tracheary cells in it (Luna et al. 2017: Fig. 5C, D). Antidaphne seems to have three vascular traces in its cotyledons.

See Stauffer (1969) for Amphorogyneae, Solms-Laubach (1867) and Benzing (1990) for haustorial anatomy, growth, etc., of stem parasitic Santalaceae, Hawksworth and Weins (1972, 1996) for Arceuthobium, Kuijt (1988: Eremolepidaceae, 2003: Phoradendron), Norverto (2004, 2011) for wood anatomy, C. A. Wilson and Calvin (2003) for some aspects of anatomy, Leins (2000) for floral morphology of Viscum, Ronse de Craene and Brockington (2013) for flowers of Colpoon, Feuer and Kuijt (1978) and Feuer et al. (1982) and references for pollen, van Tieghem (1869: Viscum), Treub (1882: Viscum}, Steindl (1935), Rutishauser (1937), Ram (1957: Comandra, 1959: Exocarpos), Paliwal (1956), Joshi (1960: Osyris), Manasi Ram (1960: Leptomeria), Bhatnagar (1968: Mida), Bhatnagar and Agarwal (1961: Thesium), Bhandari and Vohra (1983), Zaki and Kuijt (1995) and Ross and Sumner (2004, 2005) and references for embryology, and Kuijt (1982) for embryos of Eremolepidaceae.

Phylogeny. Der and Nickrent (2005, esp. 2008; see also Nickrent et al. 1998) found seven well supported clades in Santalaceae (see the groups above), 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. There is very slight support for a [Cervantesieae + Thesieae] clade, and some support for a [Amphorogyneae + Visceae] clade, etc.; the last clade appeared in both plastid and non-plastid analyses in Sun et al. (2015), but again, other relationships were unclear.

Thesieae. Nickrent et al. (2008), Moore et al. (2010) and Nickrent and García (2015) examined relationships within the large genus Thesium.

Santaleae. Genera of the old Eremolepidaceae have very often been kept separate before, but they are well embedded in the Santalum clade (Der & Nickrent 2008), their strongly supported relationships being [Antidapne [Lepidoceras + Eubrachion]]. See Harbaugh and Baldwin (2007) for a discussion of the phylogeny of Santalum, the sandalwood genus.

Visceae. See Nickrent et al. (2004b: ?rooting) for relationships in Arceuthobium. Ashworth (2000, 2017) examined relationships around Phoradendron, which is probably not monophyletic (Dendrophthora is muddled up with it).

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

Classification. Eremolepidaceae, now in Santaleae, gave Kuijt (1968) some trouble; he thought that they were perhaps close to Misodendraceae, not to Viscaceae (= Visceae), while he toyed with the idea that Lepidoceras was better placed in Loranthaceae. Der and Nickrent (2005) proposed that all major clades in Santalaceae should be recognized as families; the seven families listed there are the necessary result if Viscaceae are kept separate (see especially Nickrent et al. 2010; also Sun et al. 2015); apart from Visceae and Amphorogyneae, distinctive features for the clades are elusive. Much of the character hierarchy above is rather notional, given the uncertainty of relationships within the family.

Previous Relationships. Both Cronquist (1981) and Takhtajan (1997) recognized Eremolepidaceae, Viscaceae and a quite broadly delimited Santalaceae, the latter also including some Schoepfiaceae in his Santalaceae.

Botanical Trivia. Viscum crassulae is apparently a pleasing horticultural subject with its bright red fruits; it must be about the only stem parasite so grown.

BALANOPHORACEAE Richard, nom. cons.  - Back to Santalales


Root parasites, echlorophyllous; santalbic acid?, lignans +, plant tanniniferous; roots 0; underground tuber-like structures either parasite or parasite-host mixed, these rupture and leave a collar-like structure at ground level; stems endogenous, apex develops inside schizogenous cavity [Balanophora]; cork ?; vessel elements with simple perforation plates; cuticle wax crystalloids 0; leaves spiral, two-ranked, whorled, or 0; stomata 0; plant monoecious or dioecious; inflorescence ± capitate or spicate, terminal, axis racemose, inflorescence bracts peltate or clavate, subtending fascicles of flowers; flowers small, (monosymmetric); staminate flowers: bracts peltste-clavate or 0; 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), (endothecium biseriate); tapetal cells uninucleate [Lophophytum]; pollen grains (tricellular), (syn)tricolpate or tri- or pantoporate; pistillode 0 (+); carpellate flowers: P 0 or minute; staminodes 0; G 1, [2, 3(-5)], (inferior), [2 transverse - Rhophalocnemis], or acarpellate, styluli +, impressed, or style single, stigma punctate or ± expanded; ovary solid [mamelon visible early], "ovules" 1-2, ategmic, reduced to an embryo sac, vascular supply 0; embryo sac polarity sometimes reversed, development also bisporic [chalazal spores], 8-celled [Allium type], or tetrasporic, 8-celled [Adoxa type], (chalazal caecum 0), (antipodal cells 0), polar cells divide, or central cell coenocytic; fruits minute, (nut-like); endosperm persistent, (diploid), chalazal haustorium single-celled, plane of first cleavage of zygote vertical, embryo usually undifferentiated, suspensor 0; n = 14, ?16, 18; germination via germ tube.

16 [list]/42: Balanophora (15). Mostly tropical (map: from Hansen 1972, 1980, 1986; van Balgooy 1975; Heide-Jørgensen 2008; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photo - Flower]

Age. Naumann et al. (2013) estimated the age of a clade [Balanophoraceae [Loranthaceae + Schoepfiaceae]], the only Santalales in the study, at ca 92.5 m.y. (the ages in Table 2 are for a different node); given the findings of Su et al. (2015), this clade, or something similar, may hold. The node [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]] has been dated to (102-)97, 85(-80) m.y. by Wikström et al. (2001), (115-)99, 91(-76) m.y. by Bell et al. (2010) and ca 90.6 m.y. by Magallón and Castillo (2009).

Evolution. Ecology & Physiology. Families of plants parasitized by Thonningia sanguinea are all laticiferous (references in Quintero et al. 2016). How the host is infected varies. Balanophora abbreviata attaches to the host by sticky endosperm tubules, tubular embryonal primary haustorium processes then infecting the host (Arekal & Shivamurthy 1976); the process looks like infection by a T4 phage. Holzapfel (2001) recorded a radicle in Dactylanthus taylori that attached to the host by epidermal hairs.

Pollination Biology & Seed Dispersal. Birds, including flightless parrots on New Zealand, small mammals and insects have been recorded visiting the flowers, and the nectar can be quite copious (Santos et al. 2016); Quintero et al. (2016) observed that plants of different sexes of Thonningia sanguinea over 2 km apart on average.

Genes & Genomes. The mitochondrial genes cox1, atp1 and matR of Ombrophytum showed massive divergence (Barkman et al. 2007). Recently it has been found that there has been very extensive movement of host (Fabaceae-the mimosoid clade) mitochondrial genes into Lophophytum mirabile, the mimosoid genes replacing the parasite genes and apparently remaining functional (Sanchez-Puerta et al. 2017). There was also some chloroplast and nuclear DNA in the mitochondria, nearly all from mimosoids.

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 development of the shoot, see Shivamurthy et al. (1981), and for anatomy of the vegetative body, see Gonzalez and Mauseth (2010).

It can be difficult to understand the morphology of the flower, the number of stamens, whether the ovary is superior or inferior, the curvature of the embryo sac, etc., although there are a fair number of detailed early studies on individual species of the family. Eberwein et al. (2009) note that the carpellate flowers of Balanophora may entirely lack any appendages and be adnate to clavate bodies, perhaps modified bracts, that are borne in no particular order in the inflorecence. Indeed, because of the extreme reduction of the flower, the basic morphology of the ovule, fruit, etc., become unclear. For cautionary comments on attempts to determine ovule type and orientation in the family, see Holzappel (2001). Thus Fagerlind (e.g. 1945c) notes that the "apical" cell of the megaspore tetrad in Langsdorffia develops into the embryo sac, but determination of what is apex and base is impossible. Embryo sac development varies, and in Balanophora, Lophophytum and Langsdorffia, at least, 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; Sato & Gonzalez 2016). Holzapfel (2001) noted that a pseudoendothelium was quite common in the family. Endosperm development is sometimes categorized as "helobial". The basal cell produced by the first division of the endosperm nucleus is massive and the nucleus usually remains undivided (if it does divide, cell walls do not form - Ernst 1914); it is perhaps to be compared with the chalazal haustorium in other Santalales. Dahlgren (1923) called the endosperm cellular. Division of the smaller upper cell and its descendants always involves the formation of cell walls (see also Ekambaram & Panje 1935). There may be reversed polarity of the embryo sac in Balanopora amd Lophophytum, at least (Arekal & Shivamurthy 1978; Sato & Gonzalez 2016). But this all seems simple compared with some reports. Thus Sato and Gonzalez (2017) suggest that there is parthenogenesis in Lophophytum. In the formation of endosperm, a coenocytic structure with 2-11 nuclei first forms, the cells coming from the antipodal region, there is also incorporation of nuclear and cytoplasmic material from the nucellus, then all the nuclei, including some from the nucellus, fuse to form a single meganucleus, and then that nucleus divides, and when there are ca 12 nuclei, cell walls form...

The florally relatively unspecialized Mystropetalon has a clearly inferior ovary and triangular to pentagonal pollen grains with pores at the corners, and pollen variation in the clade is quite extensive (Grímsson et al. 2017a). In Helosis the inner layer of cells of the seed coat is massively thickened on the inner and anticlinal walls, very unlike other Santalales, while in Balanophora it is the outer layer that is thickened; taxa like Hachettia are more complex. Dactylanthus and apparently Lophophytum lack any seed coat.

For additional information, see Hooker (1859), Kuijt (1969), Takhtajan (1988, 1997), the Parasitic Plants website (Nickrent 1998 onwards), Heide-Jørgensen (2008) and Hansen (2015), all general; see also Solms-Laubach (1867) for haustorial anatomy, Grímsson et al. (2017a, also as Mystropetalaceae) for a summary of pollen variation - very extensive, and Zweifel (1939), Harms (1935b), Fagerlind (1938a, 1945b, c, d) and Sato and Gonzalez (2013), all embryogeny.

Phylogeny. A family phylogeny (Nickrent 1998: accessed 16.5.2009) based on nuclear SSU rDNA data suggest that [Mystropetalon [Dactylanthus + Hachettea]] are sister to a clade containing the rest of the family examined; see also Su et al. (2012: unrooted tree) and Sun et al. (2015).

Previous Relationships. Cronquist (1968) thought that Balanophoraceae and Santalales were related, and later (Cronquist 1981) he placed them all in Santalales. However, Kuijt (1968: p. 138) thought that any connection between Balanophoraceae and Santalales s. str was "an historical accident and taxonomic artefact". In the past Balanophoraceae have often been much more widely circumscribed since parasitic plants show common adaptations to the parasitic habitat and their flowers are often very much reduced. Thus Takhtajan (1997) linked Balanophoraceae with Cynomoriaceae (Saxifragales), Rafflesiales (here Malpighiales) and Hydnoraceae (here Piperales), relationships rejected by Kuijt (1968), including them all in his Magnoliidae; within Balanophorales he included all the families in synonymy below (apart from Hachetteaceae) as separate families.

Classification. Sun et al. (2015) recognised a clade that includes Mystropetalon, Dactylanthus, and Hachettia as Mystropetalaceae, the other genera remained in Balanophoraceae s. str., and whether families or not, the two groups need to be split out.

Botanical Trivia. Balanophora has the smallest flowers of any angiosperm; female flowers may have a mere 50 cells in total.

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