EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, 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; blepharoplast +, 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, 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]; nuclear genome size [1C] <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.

Many of the bolded characters in the characterization above are apomorphies of subsets 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.


Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.

[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.


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


Vascular tissue + [tracheids, walls with bars of secondary thickening]; stomata involved in gas exchange.


Sporophyte with 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]; sporophyte with polar auxin transport, PIN [auxin efflux facilitator] involved; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, root hairs and root cap +; stem apex multicellular, 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 +; leaves/sporophylls 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; 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; 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]; root 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; plant 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], 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; origin of epidermis with no clear pattern [probably 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 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 +, ?insertion, members 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, pollenkitt +; nectary 0; carpels present, superior, free, several, 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 [no photosynthesis], 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 land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, 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 gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, 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 size [1C] <1.4 pg [mean 1C = 18.1 pg, 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 bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (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.

EUDICOTS: (Myricetin, delphinidin +), 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, PI-dB motif +; small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], (G [3, 4]), whorled, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC 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. However, the study by Moore et al. (2008, esp. 2010) using whole chloroplast genomes with moderately good sampling bids well to have cleared up this confusion. Nevertheless, the order of branching below the asterids is still somewhat unstable (e.g. Soltis et al. 2011). For further discussion, see the Rentapetalae node.

SANTALALES Berchtold & J. Presl  Main Tree.

Mycorrhizae absent; acetylenic fatty acids [e.g. santalbic 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, with adaxial hairs; A opposite C, anthers basifixed; pollen grains bipyramidal-spheroidal, surface smooth-perforate to reticulate; nectary [sometimes as "disc"] +; G [3], style +, stigma small; ovule 1/carpel, pendulous, apotropous, tenuinucellate, outer and inner integuments ca 4 cells across, (unitegmic), micropyle endostomal; embryo sac curved, with chalazal caecum [?here]; fruit a drupe, 1-seeded, K persistent; seed coat crushed; chalazal endosperm haustoria +, (endosperm with starch); embryo minute, green; germination hypogeal. - 13 families, 151 genera, 1,992 species.

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

Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. 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).

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. 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-Lycaeninae-Iolaini in particular are found on Santalales, and Loranthaceae (especially), Olacaceae, Ximeniaceae (all Lycaeninae in particular), Opiliaceae and Santalaceae-Santaleae, -Visceae, etc., are 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; there are no reports of pierine caterpillars on free-living Santalales (Braby 2005, 2006; Braby & Trueman 2006; Braby et al. 2006), although given rather few species of such plants, this is not very surprising. Some pieries have switched feeding 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 the 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), 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 which occurs in some taxa (see below), is probably connected with the adoption of the hemiparasitic habit.

Genes & Genomes.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 acid (octadeca-11-trans-en-9-ynoic acid) in this clade, see Aitzetmüller (2012); is found in most groups. For (poly)acetylenic and related fatty acids in the seeds, see Badami and Patil (1981).

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 the first seven families below. Vascular pits are notably variously bordered throughout the order (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 in the clade. First, there has been controversy over the nature of the perianth 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 and 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 bracteoles, 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. Finally, 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 a 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 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), as well as cotyledon number. 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). 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). Tthere 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 Santalaceae. The anther wall is monocotyledonous in development in Maburea (Erythropalaceae: see Maas et al. 1992).

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). For other information, see Roberston (1982), Barlow (1997), and Calder and Bernhardt (1983); for chromosome numbers see (Nickrent et al. 2010: supplement).

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. Malécot and Nickrent (2008) 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.

Mystropetalum, 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 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, perhaps monophyletic, but in a different position within the clade. Branch length of clade A are very long; clade B is made up of the three genera examined by Nickrent et al. (2005). 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 2002; Nickrent & Duff 1996; Barkman et al. 2007).

For additional information on relationships, see 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 Santalaes 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 and Icacinales.

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; 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, septate (not), 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.

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.

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); pollen tricolpate/tricolporoidate; G [3-6], (inferior), septate at base, style short to long; ovules (unitegmic, integument ca 6 cells across, micropyle long); (megaspore mother cells several), (embryo sac caecum 0); endosperm starchy, chalazal endosperm haustorium unicellular; 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 +); 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; embryo sac curved, with chalazal caecum, micropylar prolongation ± developed.

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; 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).

Ovule, embryo sac and embryo development of many plants in this clade are 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 and everything else (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, the integument(s) having become fused with the nucellus. Individual embryo sacs may elongate greatly, even approaching the stigma at the end of the long style. 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); nectary 0; G superior, style short to long; ovules (unitegmic), "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.

[Aptandraceae, Olacaceae [Octoknemaceae [[Loranthaceae [Misodendraceae + Schoepfiaceae]] [Opiliaceae + Santalaceae]]]]: pollen grains ± oblate; ovules unitegmic or ategmic.

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 a character to this node.

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 4-6-merous, (heterostylous); (K 0); (C 3 - Olax [?connate in pairs]); A 1-2 x C, staminodes +, (fertile A 3, staminodes 3-6, opp. C - Dulacia); 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] - Olax; K much accrescent/not; (chalazal haustorium growing into pedicel - Olax), endosperm starch slight, 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. Olacoideae are ategmic, and Olax has endosperm haustoria reaching into the pedicel.

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

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

OCTOKNEMACEAE van Tieghem nom. cons.   Back to Santalales


?Parasites; plants Al accumulators; essential oils 0; axial parenchyma strands ³7 cells wide; phloem with bundles of fibres; nodes 5:5; petiole bundle annular; 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 ?adaxial hairs; staminate flowers: pollen ± tricolporoidate; (disc +); pistillode; carpellate flowers: staminodes +; (glands alternating with staminodes); G 3 (5), inferior, style short, stigma flap-like, multi-lobed; integuments 2 or 1; seed longitudinally ruminate, 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); see also Kuijt (2015).

Phylogeny. 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.

[[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; testa 0; chalazal endosperm nucleus in caecum, haustorial.

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 "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) 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 two clades involved; see Johnson and 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.

[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; G [3].

Age. The age of this clade is perhaps ca 81 m.y. (Vidal-Russell & Nickrent 2008a); some 67.9 m.y.a. is the age 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; root hairs 0 [?level]; parenchyma apotracheal; cuticular epithelium developing [?]; flowers sessile, pedicels articulated [?level], medium-sized to large; K annular on initiation, lobes irregular, C ?adaxial hairs; A of different lengths; pollen grains oblate, trilobate-± triangular, apertures confluent; G inferior, placentation basal [= mamelon]; ovules 4-12, collenchymatous zone below the embryo sacs; megaspore mother cells many [archesporium multicellular], embryo sac growing up style (to tip); mesocarp with rubber outside vascular bundles; endosperm composite [derived from several ovules], suspensor long, biseriate [= biseriate proembryo], plane of first cleavage of zygote vertical; n = 12.


77[list]/950 - 2 groups below. ± Tropical.

Age. 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).

1. Nuytsieae van Tieghem

Ellagic acid +; successive cambia +; leaves spiral; plant monoecious; flowers in 3-flowered cymules; C 6-8, free, yellow; tapetal cells 3-4-nucleate; pollen trilobate; embryo sac with lateral caecum [near apex]; G fruit dry, 3-winged; ?endosperm reserve, embryo [immature] ca 1/3 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

2. The Rest.


Usu. stem parasites, forming burl at point of attachment and with epicortical roots running over the surface, often forming secondary burls, root hairs 0; indumentum quite often complex; leaves opposite (spiral); (plant dioecious); flowers (sessile), (slit-monosymmetric), (opening explosively), (3-)5-6(-9)-merous; (pedicel apex cupular), K usu. unvascularized (vascularized - Atkinsonia), (0), C (0, 4-7); A (dimorphic [one pair sterile]), (anthers septate); (tapetum plasmodial, microsporogenesis successive - Cladocolea), tapetal cells uni- or binucleate; pollen grains (spherical, 3-5-zonocolpate - Tupeia; demi - Dendropemon(syn - Oryctanthus)colpate), (heteropolar); G 3-12 [number sometimes estimated from "ovules"], (placentation axile - e.g. Lysiana), (style solid - Psittacanthinae), stigma bilobed and papillate, capitate; embryo sac bisporic [chalazal dyad], eight-celled [Allium-type]; fruit also a berry (nut), usually viscous; endosperm chlorophyllous, starchy, embryo chlorophyllous, ± plug-shaped, medium to long, cotyledons (connate), (unequal), (much reduced); (no radicle, primary haustorium +), (multicellular processes at radicular end of embryo); (germination cryptocotylar); n = (8-11).

67/950: Tapinanthus (250), Psittacanthus (120), Amyema (95), Agelanthus (60), Struthanthus (50), Phthirusa (40). ± Tropical (warm temperate) (map: from Meusel et al. 1965; Jäger 1970; Barlow 1983; Polhill & Weins 1998; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photo - Flower.]

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

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 (Grimmsson et al. 2017b). There are other records of the distinctive loranth pollen is from the early Eocene (Manchester et al. 2015). Note that the pollen form genus Aquilapollenites, bilaterally symmetrical and with four wing-like projections, which gives its name to the circumboreal Aquilapollenites pollen province, are similar to those of Loranthaceae, but they are also like those of a number of other families (Farabee 1991); they have not been associated with flowers (Friis et al. 2011 and references).

Loranthaceae are common in Australia and were, one might have thought, easily dispersed, however, they are unknown from Tasmania (but are found in New Zealand, etc.).

Kuijt (2009b) noted that floral variation in Neotropical Loranthaceae was far greater than in Palaeotropical members. Kuijt (2011) suggested that sessile, axillary, 4-merous flowers were primitive in the family - genera around Phthirusa were examples. 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 (Grímsson et al. 2017a).

Ecology & Physiology. The root parasitic habit, as in Nuytsia, is probably the basal condition in the family, since Nuytsia is sister to the rest of the family (Vidal-Russell & Nickrent 2005) and the most immediate out groups (but not Misodendraceae) are root parasites. Atkinsonia, from S.E. Australia (which has a vascularized "calyx" - see Johri & Bhatnagar 1972), and Gaiadendron, from Central and South America), are two other root parasitic genera that may also be near the base of the phylogeny (see Reid 1991 for the fruit types of Gaiadendron and Amylotheca; Grímsson et al. 2017a: 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). Hence be careful interpreting the characterisation of "the rest" above (Wilson & Calvin 2006a, b; c.f. Vidal-Russell & Nickrent 2008b: support not very strong).

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). The host-parasite junction may be much swollen, producing wood roses - vascular tissue in the form of variously channeled, split and branched cup-shaped structures - in the host. Morphological details of the association between stem parasite and hosts varies, and the epicortical roots, which may be plesiomorphous in the aerial parasites, form either sympodial or monopodial systems (e.g. Polhill & Weins 1998; Calvin & Wilson 2006; Wilson & Calvin 2006b). Wilson and Calvin (2006a, b) discuss the evolution of the various kinds of host attachments, although given the weak support for relationships at the base of the tree it is premature to worry too much about how many times aerial parasitism has evolved - perhaps only once in the family (Vidal-Russell & Nickrent 2008b). Loranthaceae are primarily xylem parasites, but their haustoria may sometimes tap the phloem (Barlow 1997). Some Loranthaceae 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 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 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 are pollinated by bees, etc. (Suaza-Gaviria et al. 2016). 44 species in two genera of Nectariniidae-Dicaeidae, flowerpeckers, are endemic to the Indo-Australian area, and they are involved in both pollination and seed dispersal of the family there (e.g. Docters van Leeuwen 1954; Reid 1983). In some taxa the flower opens only when pecked by the birds (hence their common name, "flower peckers"); opening is explosive, and the bird gets covered by pollen. Some Loranthaceae are generalists, while in others there is match brtween the shape of the bird's bill and that of the corolla tube (e.g. Feehan 1985). Other very common pollinators in the family are the closely related sunbirds (Nectariniidae-Nectariniini), also Old World, and they in Malesia they pollinate species whose flowers do not open explosively (Corlett 2004). Sunbirds are the main pollinators of most African Loranthaceae, and Kirkup (1998) provides a detailed study of the variety of floral morphologies involved. In tropical America humming birds are the major pollinators (Kuijt 2015). 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 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 the 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. 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). Caterpillars of the pierid Delias occur on Malesian Loranthaceae (Docters van Leeuwen 1954) and of Mylothris on African Loranthaceae (Braby 2005).

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. The apex of the pedicel 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), but it is calycine in origin and should be called simply the calyx (see above, also Eichler 1868; Suaza-Gaviria et al. 2016). Polysymmetric 6-merous flowers seem to be plesiomorphous in the family (Barlow 1983; Wilson & Calvin 2006; Suaza-Gaviria et al. 2016), but 7- (or 8-)merous flowers occur in Atkinsonia and Notanthera (see below), the stamens being inserted at two levels on the corolla (Kuijt 2010).

Cronquist (1981) and others describe the gynoecium as being 3-4-carpellate with 7-12 ovules. For literature about the nature of the mamelon, whether at least part placental or ovular, see e.g. Narayana (1959) and Suaza-Gaviria et al. (2016); it may be vascularized (Narayana 1959: as also in Dendrophthora - Santalaceae-Visceae). The embryo sac in Moquiniella is some 48 mm long, the longest in the angiosperms; it grows up the style and then may grow back downwards after reaching the stigma (this is sometimes called an embryo sac haustorium - see Mikesell 1990), and other members of the family have embryo sacs nearly as long (e.g. Johri & Bhatnagar 1972; Cocucci 1990). In general, after fertilization the embryo is "planted" back down at the base of the mamelon by the development of a long, biseriate suspensor. The embryo sac quite often has a caecum of some sort, e.g., there is a basal caecum in Lysiana and Lepeostegeres (Narayana 1958; Dixit 1959a). The embryos of Helicanthus, Lysiana, and some other genera have multicellular processes at the radicular end (Johri et al. 1957; Narayana 1959). Both Cronquist (1981) and Takhtajan (1997) describe the endosperm as being starchy (see also Dixit 1959a, b), but it is not so scored in Malécot (2002); the embryo sac may also be full of starch grains. In many Old World Loranthaceae the cotyledons are connate, but not basally; the plumule emerges through the basal slit (Kuijt 1969). González and Pabón Mora (2017) show that persistent reports of polycotyledony in Psittacanthus are incorrect - the "extra" cotyledons are lobes of green endosperm...

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), for growth habits, see Benzing (1990), for floral morphology and embryology, see Robles et al. (2016), for pollen, see Feuer and Kuijt (1985 and references) and especially Grímsson et al. (2017a), for embryology, etc., see Narayana (1958, 1959: Nuytsia), Dixit (1959a, b), Raj (1970), Bhatnagar and Johri (1983) and Subrehmanyam et al. (2015), and for seedlings of neotropical Loranthaceae, see Kuijt (1982).

Kuijt (2015) noted that neither embryology nor seedlings of Old Word genera were much known, nor the embryology of New World genera.

Phylogeny. Relationships within Loranthaceae are being clarified. Nuytsia may be sister to the rest of the family (Vidal-Russell & Nickrent 2005). The root parasitic Atkinsonia (S.E. Australia) and Gaiadendron (Central and South America) may also be near the base of the phylogeny (the fruits in the latter are not viscous), although there is rather weak support for the stem parasite Notanthera being sister to all Loranthaceae except Nuytsia (Wilson & Calvin 2006a, b; c.f. Vidal-Russell & Nickrent 2008b). Sun et al. (2015) also recovered Nuytsia and Atkinsonia as succesively sister taxa to the rest of the family, but only the position of first had strong support, and Gaiaodendron again seemed to be in this area. Grímsson et al. (2017a, b) found basal relationships in the family to be unclear, Grímsson et al. (2017a) noting that the position of the root-parasitic Gaidendron and Atkinsonia remained unclear. Indeed, 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).

Pollen variation correlates quite well with genera and generic groups, but relating it to a phylogeny awaits a better resolution of the latter (Grímsson et al. 2017a).

Classification. For a suprageneric classification of the whole family, see Nickrent et al. (2010); for some generic limits, see Kuijt (2011).

Previous Relationships. Loranthaceae and Viscaceae (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).

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: K 0, C 0; A 2-3, monothecal; pollen grains spheroidal, 4-19-pantoporate, pores operculate, surface spinuliferous; carpellate flowers: sessile; K 0, ?C 3, minute; staminodes alternate with K/C; style ± 0, stigma strongly 3-lobed; ovules straight; ?embryology; fruit dry, attached to 3 much accrescent long-plumose staminodes growing from slits in the ovary to one side of the attachment of the K/C; ovules and emnryology?; seed coat with some sclereids; endosperm 0-copious, chlorophyllous, embryo short to large, cotyledons connate; n = 6, 8.

1 [list]/8. Cool temperate South America (map: from Heywood 1978). [Photos - Misodendron Flower, Misodendron 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 evolved here well before that in Loranthaceae, which occurred some ca 40 m.y.a. (Vidal-Russell & Nickrent 2006, 2007).

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). According to Takhtajan (1997) the pollen is colpate.

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 seeds and seedlings, see Kuijt (1982: corrections to earlier work).

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

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, patch of hairs on C abaxial to A (0); pollen grains tetrahedral, heteropolar, apertures ± confluent, (zonasulculate), ektexine smooth; G (semi-)inferior, basally septate, stigma lobed to capitate; ovules ategmic; embryo sac U- or J- [Quinchamalium] or open heart-shaped [Schoepfia], chalazal haustoria branched [Quinchamalium], synergid haustorium +, very slender [Quinchamalium]; embryo short to long, first division vertical/obligue; 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 only.

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, (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; pollen usu. colporate, microechinate, spheroidal, triangular; (prominent nectaries alternating with A); G [2-5] (half inferior), placentation free central, style short or 0, stigma ± capitate; ovule 1, pendant (erect, basal - Agonandra), (1<, on mamelon - Anthobolus); (pedicel swollen, coloured - Anthobolus); chalazal endospermal cell haustorial, endosperm also oily, embryo narrow, long (rather short), radicle very short, cotyledons (2-)3-4; germination cryptocotylar; n = 10.

11 [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. Stauffer (1959) suggested that there might be viscin in the fruits of some Anthoboleae.

For embryology, see Swamy and Dayanand Rao (1956), 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. Other Anthoboleae are close to Santalum and relatives (Der & Nickrent 2008: support strong).

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

Synonymy: Anthobolaceae Dumortier, Cansjeraceae J. Agardh

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


Ellagic acid 0; axial parenchyma strands 0; cuticular epithelium common; (cuticle waxes as rodlets); guard cell thickenings unknown; epidermal cells sclerified, with druses; flowers small, (3-)4-5(-8)-merous; hypanthium + or 0; K 0, patch of hairs on C abaxial to A (0); large nectary glands often +, alternating with stamens; pollen various; G [2-5], inferior, odd member abaxial, (carpellary vascular supply recurrent), (placentation free central), stigma often capitate or lobed; ovules straight (anatropous), or not distinguishable; fruit [mesocarp stony] also baccate, (outer part exfoliating); endosperm (helobial), starchy or not, embryo short to long.

44 [list]/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). [Photos - Acanthosyris fruit.]

1. Comandra group

Plant herbaceous; (hypanthium +); pollen grains (3-colporoidate); stigma punctate to subcapitate; ovules anatropous, unitegmic; embryo sac with lateral caecum; secondary endosperm haustoria +, plane of first cleavage of zygote vertical; germination cryptocotylar; n = 13(14).

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

Synonymy: Comandraceae Nickrent & Der

[Thesieae + Cervantesia group]: ovules unitegmic.

2. Thesieae Meisner

?Santalbic acid; (thorns); (lamina terete); (plant dioecious); (K +, [strongly lobed]); (C connate); pollen grains (3-colporate), (heteropolar); ovules unitegmic; (embryo sac U-shaped); endosperm starchy; n = 6-9(-12).

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

Synonymy: Thesiaceae Vest

3. Cervantesia group

(Plant with axillary thorns); (gallic acid +); (lamina rhombic, with spines - Jodina); K 0; (pollen 3-colporate, surface striate - Buckleya), (heteropolar)n = ?

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

Synonymy: Cervantesiaceae Nickrent & Der

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

4. Nanodea group

?Santalbic acid; (flowers 4 merous); (K +); heteropolar, etc., Mida]; (G semi-inferior); embryo sac with micropylar end protruding; secondary endosperm haustoria + [Mida]; n = ?

2/2. New Zealand, south South America.

Synonymy: Nanodeaceae Nickrent & Der

[Santaleae [Amphorogyneae + Visceae]]: (stem parasites +); (cuticular epithelium +); (ovules 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).

5. Santaleae Dumortier

(Stem parasites, epicortical roots +/0); cuticular epithelium + [?all]; (leaves spiral), (scale-like); flowers (unisexual), (sessile); (K +), (C 0); pollen grains (3-colporate), (surface spinuliferous); (large nectaries alternating with A - Osyris); (G inferior); embryo sac with micropylar end long-protruding, (U-shaped), (bisporic, 8-nucleate [Allium type]); (pedicel swollen, fleshy in fruit); (seed with a complete viscous covering); (chalazal endosperm haustorium multicellular - Exocarpus), (endosperm composite [derived from several ovules]), (green), (suspensor long), (primary [radicular] haustorium +); n = 10, 11, 13, 15.

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.

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; anthers loculi above one another in pairs, opening separately; (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; (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 opposite A 0; staminate flowers: anthers opening by pores°, (longitudinally), (polythecate), (connate, forming a synandrium, opening circumferentially); (endothecium 0); pollen 3-colporate, (pseudocolpi +), spherical°, surface echinate; carpellate flowers: nectary ± 0; G with mamelon (0), style short, (solid); 2 "ovules"°; embryo sac bisporic, 8-nucleate [Allium type], tetrasporic [Adoxa type], monosporic, 8-nucleate [Polygonum type - Viscum minimum], (elongated), straight to U-shaped, micropylar [egg cel] end outside mamelon [Phoradendron, etc.], starch copious; ("berry" explosive - Arceuthobium), viscous covering +, incomplete, inside the vascular bundles°, consisting of polysaccharide threads and mucilage°, thin endocarp +° (always?); endosperm chlorophyllous°, starchy, (plane of first cleavage of zygote vertical - Korthalsella, Arceuthobium), suspensor short or 0, embryo chlorophyllous, with 1 cotyledon [= 2 connate]; 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; Fl. Austral. 22. 1984; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010 - note that Barlow shows the group throughout much of the northern Sudano-Sahelian-Zambezian zone).

Synonymy: Arceuthobiaceae 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 perhaps been two migrations from Australia to Hawaii and also two migrations out of Hawaii to the south Pacific (Harbaugh & Baldwin 2007).

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). 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 (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; 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, polleination here seems particularly unclear/variable; wind may sometimes be involved, and the female flowers can have large blobs of ?nectar on the stigma (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); 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.

Genes & Genomes. Molecular evolution has greatly speeded up in the Viscum clade (Vidal-Russell & Nickrent 2008). A very large genome with a 2C value of some 205.8 pg or more is found 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 (Skippington et al. 2015).

Economic Importance. Mathiasen et al. (2008) provide a list of Santalaceae that harm crops and timber trees. Thus 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 cuticle in Visceae becomes progressively thicker, 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, this layer may be thicker than the cork on tree stems of equivalent thickness (Damm 1901; 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). The orientation of cataphylls and their relation to prophylls in genera like Phoradendron as described by Kuit (1996) are unclear. Similarly, the structures called prophylls by Kuijt (2013) and found on vegetative shoots, as in Arceuthobium azoricum, are probably colleters or something similar, since the axillary branches have their first pair of leaves lateral in position (= true prophylls?) in the same plane as these putative prophylls (see also Kuijt 2015: pp. 10-11, esp. Fig. 1d for a discussion).

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 also 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). York (1913) even described the chalazal ends of the two embryo sacs of Dendrophthora as fusing. 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, Norverto (2004, 2011) for wood anatomy, Wilson and Calvin (2003) for some aspects of anatomy, Feuer and Kuijt (1978) and Feuer et al. (1982) and references for pollen, Steindl (1935), Rutishauser (1937), Ram (1957: Comandra), Bhandari and Vohra (1983) and Zaki and Kuijt (1995) and references for embryology, about which there is quite a bit of information, especially for Viscoideae, Leins (2000) for floral morphology of Viscum, Ronse de Craene and Brockington (2013) for flowers of Colpoon and Wiens and Barlow (1971) for cytology. For a monograph of Phoradendron, see Kuijt (2003).

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.

Genera of 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 Nickrent et al. (2004b: ?rooting) for a relationships in Arceuthobium, Nickrent et al. (2008), Moore et al. (2010) and Nickrent and García (2015) for those within the large genus Thesium, and Harbaugh and Baldwin (2007) for the phylogeny of Santalum, the sandalwood genus. Ashworth (2016) examined relationships in Phoradendreae.

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

Classification. 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. For the circumscription of Thesium see Moore et al. (2010) and Nickrent and García (2015).

Botanical Trivia. Viscum crassulae is 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, with underground tuber-like structures either parasite or parasite-host mixed, these rupture and leave a collar-like structure at ground level; shoot endogenous, apex develops inside schizogenous cavity [Balanophora]; santalbic acid?, plant tanniniferous; roots 0; cork ?; vessel elements with simple perforation plates; cuticle wax crystalloids 0; stems endogenous; 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 [2, 3(-5)], (inferior), [2 transverse - Rhophalocnemis], or acarpellate, styluli +, impressed, or style single, stigma punctate or ± expanded; "ovules" 1/carpel, 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. 2017). 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. 2017: plants of different sexes of Thonningia sanguinea over 2 km apart on average; and references).

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 a pseudoendothelium developed 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, 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.

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).

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

Classification. Sun et al. 2015) recognised a clade that includes Mystropetalum, 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