EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; flavonoids + [absorbtion of UV radiation]; chloroplasts lacking pyrenoids; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
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 common ancestor of the group.
Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].
Plant woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; 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 +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; axillary buds +, (not associated with all leaves); prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development initially endosporic, lacking chlorophyll, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, 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], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine +, thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing 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, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, much larger than ovule at time of fertilization; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, 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; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].
[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]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; 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 [possible position]; pollen tube growth intra-gynoecial; 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; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), 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]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; whole nuclear genome duplication [palaeohexaploidy, gamma triplication], 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 , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / Sympetalae redux? / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; (nectary gynoecial); G , style single, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
[ASTERID I + ASTERID II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); style short[?]; duplication of the PI gene.
ASTERID II / CAMPANULIDAE: myricetin 0; vessel elements with scalariform perforation plates; endosperm copious, embryo short/very short.
[ASTERALES [ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]] / APIIDAE: iridoids +; C forming a distinct tube, tube initiation early; A epipetalous; ovary inferior, [2-3], style long[?].
[ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]: ?
[BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]: ?
[APIALES [PARACRYPHIALES + DIPSACALES]] / DIPSAPIIDAE: nodes 3:3.
Age. The age of this node is estimated at (105-)84(-58) m.y. (Lemaire et al. 2011b); K. Bremer et al. (2004) suggested an age of ca 113 m.y., Magallón and Castillo (2009: c.f. position of Paracryphiales) an age of ca 92 m.y., Naumann et al. (2013) an age of around 75.2 m.y., and Beaulieu et al. (2013a: 95% HPD) an age of (101-)91(-79) m.y..
Divergence & Distribution. Initial diversification of this clade probably occurred in the southern hemisphere, but diverse clades in it like Apiaceae "coincide" with more recent movements to the north (Beaulieu et al. 2013a).
APIALES Nakai Main Tree.
Woody; route II decarboxylated iridoids +; vessel elements with scalariform perforation plates, solitary; pits [both vessels and fibres] distinctly bordered; diffuse in aggregate axial parenchyma; ?stomata; lamina pinnatinerved, (margins toothed or lobed); inflorescence terminal, branched; plants dioecious; pedicels articulated; flowers small, [<1.5 cm across], K small, C apparently free; A free; G , abaxial carpel alone fertile [?Pennantia], placentation apical; ovules 1-2/carpel, apical, pendulous, apotropous, nucellus type?, funicular obturator +; fruit a drupe, single-seeded; endosperm nuclear; x = ?6; mitochondrial rpl2 gene lost. - 7 families, 494 genera, 5489 species.
Age. The age of crown Apiales is estimated to be (130-)117(-103.7) m.y. (Nicolas & Plunkett 2014).
For the fossil record of the order, see Martínez-Millán (2010) and Nicolas and Plunkett (2014).
Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many 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 is the not-so-trivial issue of how ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Apiales contain ca 2.4% eudicot diversity (Magallón et al. 1999). Although Magallón and Sanderson (2001) estimated that diversification in Apiales had increased, as Nicolas and Plunkett (2014) correctly point out, the bulk of the diversity in Apiales is in Apiaceae.
Nicolas and Plunkett (2014: conclusions not affected by the position of Pennantiaceae) suggest that Pennantiaceae, Torricelliaceae, Griseliniaceae, and a clade representing the rest of the order are ancient (Cretaceous) clades possibly of East Gondwanan origin, although East Asia is also involved. They thought that vicariance might be involved in some of the distributions, e.g. of the three genera of Torricelliaceae, Myodocarpaceae, etc..
Thinking about morphological evolution is particularly difficult here because of incomplete knowledge of and extensive variation in the characters of interest. The basal pectinations are genera that have transseptal bundles in common, as well as some rays over 10 cells wide and with square or upright cells (Noshiro & Baas 1998; Baas et al. 2000). Pennantia, with a superior ovary, may also be placed here (see below). Unfortunately, corolla initiation, pollen cell number, and many other characters are unknown for these taxa, although some information for the ex-Cornalean genera can be found in Patel (1973), Philipson (1967), and Philipson and Stone (1980). Pennantia has similar (plesiomorphic) wood anatomy, rather like Griseliniaceae but unlike that of other other Apiales (Lens et al 2008a); this suite of characters is scored as having two origins in Apiales... Griseliniaceae and Torricelliaceae both have the iridoid griselinoside, transseptal bundles in the ovary, and the abaxial carpel alone is fertile, the single ovule being apotropous. Pennantia has a superior ovary (and sometimes a thick, disciform, sessile stigma). In particular, how the gynoecium of Pennantia is interpreted (summarized in Kårehed 2003a) has many implications for character evolution. Here the gynoecium is interpreted as being tricarpellate, although it appears to be single ("pseudomonomerous"), and the carpel that is fertile is abaxial (see also Chandler & Plunkett 2004; Plunkett et al. 2004c for carpel number).
Erbar and Leins (1988a, 1996a, 2004) suggested that the nectary "disc" of Apiaceae and Araliaceae is a carpellary flank nectary displaced by intercalary growth, and that the axile placentation and inferior ovary of these two families is easily related to the parietal placentation and superior ovary of Pittosporaceae. The ovary of Pittosporaceae has a short basal zone with separate loculi, the ovules being borne above this zone - essentially the same position in which the ovules of Apiaceae and Araliaceae are found. However, gynoecial development, etc., in the whole Apiales badly needs reinvestigation, since apart from Pennantiaceae (perhaps sister to the rest of the order), nearly all Apiales have inferior ovaries. Furthermore, clades with with superior and inferior ovaries interdigitate in most campanulid orders.
Further complicating the issue, sister to the [Apiales [Paracryphiales + Dipsacales]] clade is Bruniales, a small but morphologically very heterogeneous clade, while within Apiales, Pittosporaceae are florally apparently very dissimilar to all other members (see below).
Yi et al. (2004) suggest that the basic chromosome number in Apiales is x = 6 (see also Raven 1975), although the order then would have all polyploid/dysploid members, with several independent origins of polyploidy.
Chemistry, Morphology, etc. Kårehed (2003, for which see for further details, also Chandler & Plunkett 2004) provides a good summary of what is known of the main clades in Apiales. For wood anatomy, see Lens et al. (2008a). Endress (2003c) summarizes the rather sparse literature on nucellus development in the clade. For nectary morphology, see Erbar and Leins (2010).
Phylogeny. In earlier studies a grouping [Griselinia [Aralidium + Torricellia]] was rather weakly supported (Backlund & Bremer 1997; see also Chandler & Plunkett 2002). Plunkett (2001) and Lundberg (2001c) both suggested that Torricelliaceae and Griseliniaceae were successive clades near the base of Apiales (Kårehed 2002a: four genes, all genera sampled, strong Bayesian support), and this topology is followed here (see also Soltis et al. 2011; Tank & Donoghue 2010); the relationship is reversed in Chandler and Plunkett (2004), but with a p.p. of 0.93.
The ex-icacinaceous Pennantia may be sister to all other Apiales, at least in chloroplast phylogenies (e.g. Kårehed 2003; Lens et al. 2008a: strong support), although nuclear markers place it elsewhere in the campanulids (e.g. Chandler & Plunkett 2004). Its position must be confirmed, but the monophyly of the rest of the order is not in doubt.
Pittosporaceae are sister to the rest of the clade, a clade made up of the old Apiaceae and Araliaceae (e.g. Kårehed 2002c; Andersson et al. 2006: strong support, Myodocarpaceae not included), a position that was strongly supported by Tank and Donoghue (2010). However, some earlier studies found Pittosporaceae to be embedded in the clade, some Bayesian analyses giving strong posterior probabilities for a relationship between Myodocarpaceae and Pittosporaceae (Chandler & Plunkett 2004), or they provided only weak support for a sister group position (Nicolas & Plunkett 2009). Overall, the relationships [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] seem most likely (Tank et al. 2007; Tank & Donoghue 2010; Soltis et al. 2011; Nicolas & Plunkett 2014).
There are some similarities between [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] and Asterales like Campanulaceae and Asteraceae (e.g. Erbar & Leins 2004; Leins & Erbar 2004b), thus 1-benzyltetrahydroisoquinoline alkaloids are found in both (Kubitzki et al. 2011). However, given the rather strongly supported set of relationships at the base of Apiales, the other clades that are in this part of the lamiids, and relationships within Asterales (Campanulaceae and Asteraceae are not immediately related), most of these similarities are likely to be parallelisms.
Includes Apiaceae, Araliaceae, Griseliniaceae, Myodocarpaceae, Pennantiaceae, Pittosporaceae, Torricelliaceae.
Synonymy: Apiineae Plunkett & Lowry, Aralidiinae Thorne & Reveal - Ammiales Small, Araliales Berchtold & J. Presl, Aralidiales Reveal, Griseliniales Reveal & Doweld, Hederales Link, Pennantiales Doweld, Pittosporales Link, Torricelliales Reveal & Doweld
PENNANTIACEAE J. Agardh Back to Apiales
Trees or shrubs; iridoids ?; vessel elements with scalariform oerforation plates, 1080-1500(-2250) µm long, fibers 1790-2270(-2900) µm long; nodes 3:3; petiole bundle annular (with a medullary bundle) and with solid annular wing bundles; stomata paracytic; hairs uniseriate; lamina margins also entire; K free, C valvate, connate, apex inflexed; nectary 0; staminate flowers: A (epipetalous), dorsifixed; pistillode +; carpellate flowers: staminodes +/0; G , also , styles short, stigmas punctate, or stigma sessile, broad; ovules at most thinly crassinucellate, integument vascularized; drupe with inner cells transversely elongated; seed coat thin; endosperm development?, embryo short/minute [to 1/3 the seed length]; n = 25.
1/4. N.E. Australia, Norfolk Island, New Zealand (map: from van Balgooy 1966; Fl. Austral. 4. 1984). [Photo - Habit.]
Chemistry, Morphology, etc. Collenchyma is only poorly developed, and a pericyclic sheath is present; pits in general are bordered. For the morphology of the stigma, see Kårehed (2002b). For information, which should be confirmed, on ovule morphology, see Mauritzon (1936c).
For other information, see Gardner and de Lange (2002: monograph), Sleumer (1942a: description), Bailey and Howard (1941a-d: anatomy), Heintzelmann and Howard (1948), van Staveren and Baas (1973: epidermis), Baas (1973: epidermis, 1974: stomata), Lobreau-Callen (1980: pollen), and Miers (1852: ovule orientation).
Previous Relationships. Pennantia is late of Icacinaceae and is the only genus that has wandered far from the three orders - - into which the other members of the family have been placed.
[Torricelliaceae [Griseliniaceae [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]]]]: polyacteylenes +; young stems with peripheral collechyma; pericyclic fibres 0 or few; nodes 5(+):5(+); leaf base broad [encircling 2/3 the stem or more]; C apparently free, imbricate; ovary inferior, style branches/stigmas recurved; nectary on top of ovary.
Age. A Santonian-Turonian age of some 90-85 m.y. for this node has been suggested; K. Bremer et al. (2004) dated it to ca 84 m.y.a., Wikström et al. (2001: note topology) to (74-)69, 63(-58) m.y., Janssens et al. (2009) to 87±14.1 m.y., Magallón and Castillo (2009) offered an estimate of ca 74.9 m.y., Bell et al. (2010) one of (63-)53, 49(-39) m.y., while Beaulieu et al. (2013a: 95% HPD) thought that it was (95-)84(-71) m.y.o.; (119.8-)106.9(-94) m.y.a. is the most recent estimate (Nicolas & Plunkett 2014).
Chemistry, Morphology, etc. Polyacetylenes, mainly aliphatic, including the C17 acetylenes, falcarinone, etc., are found in the [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] clade, while the polyacteylenes of Torricellia angulata, quite recently described, are C11 acids that are unique in having a chiral center (Pan et al. 2006); iridoids are found in the same species (Liang et al. 2009).
For the wood anatomy of this clade, see Noshiro and Baas (1998) and Lens et al. (2008a).
TORRICELLIACEAE H. H. Hu Back to Apiales
Trees; griselinoside [iridoid], (polyacetylenes, C11 and acidic +), ellagic acid +, tanniniferous [Torricellia]; vessel elements with simple perforation plates (scalariform - Aralidium), clustered, septate fibres with minutely bordered pits, exclusively scanty paratracheal parenchyma; petiole bundles scattered [Aralidium]; crystal sand +; mucilage cells +; stomata anomocytic (anisocytic); glandular hairs +; lamina margins lobed and toothed or toothed, (secondary veins ± palmate), petiole base with marginal flange, encircling stem or not, (small adaxial flange [ligule] +); K medium, imbricate or largely connate; staminate flowers: (C induplicate-valvate - Torricellia); pollen tectum reticulate; carpellate flowers: (C 0 - Torricellia); G [(2-4)], (nectary vascularized - Aralidium), transseptal bundles +, (stigmas ± bifid - Torricellia); ovules with massive integument [Aralidium]; fruit with two large empty loculi and one smaller fertile loculus [?Melanophylla], endocarp with sclereids; seed ± curved, (ruminate, coat vascularized - Aralidium), exotesta scalariform-thickened, unlignified [Melanophylla], testa slightly sclerified [Torricellia]; (embryo long, thin - Torricellia); n = 12, 20 ± 2.
3[list]/10. Madagascar, South East Asia and W. Malesia (map: fossils [blue] from Meller 2006). [Photo: Melanophylla Habit, Flower.]
Age. The age of this node is estimated at (81-)53(-27) m.y. (Lemaire et al. 2011b) or substantially older, (115.8-)103.1(-90.2) m.y.a. (Nicolas & Plunkett 2014).
Evolution. Divergence & Distribution. For the fossil history of the East Asian endemic Torricellia, see Meller (2006), Manchester et al. (2009) and Collinson et al. (2012); the genus was widespread in the northern hemisphere by the Eocene and can be dated to a minimum of 55.8 m.y. ago.
Chemistry, Morphology, etc. For fruit and seed of Melanophylla, see Trifonova (1998), for a revision, see Schatz et al. (1998). Other information is taken from from Philipson (1977), Lobreau-Callen (1977: pollen), Philipson and Stone (1980), and Takhtajan (2000).
Phylogeny. For the circumscription of this clade, see also Plunkett et al. (2004c); relationships are [Aralidium [Melanophylla + Torricellia]] (see also Soltis et al. 2011).
Previous Relationships. Melanophylla was included in Hydrangeales and Torricellia and Aralidium were placed in separate monogeneric orders, both in Cornidae-Cornanae, by Takhtajan (1997); all have been placed in Cornaceae s.l. in the past.
Synonymy: Aralidiaceae Philipson & B. C. Stone, Melanophyllaceae Airy Shaw
[Griseliniaceae [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]]]: petroselenic acid + [in seed: CH3-[CH2]10-CH=CH-[CH2]4-COOH, i.e. cis-6-octadecanoic acid], tannins 0; hairs rarely glandular; lamina vernation conduplicate; ovule with endothelium.
Age. Naumann et al. (2013) suggested an age of around a mere 33.9 m.y.a. for this node; (115.8-)103.1(-90.2) m.y.a., three times as old, is the estimate in Nicolas and Plunkett (2014).
GRISELINIACEAE A. Cunningham Back to Apiales
Trees or shrubs (climbing, epiphytic); griselinoside [iridoid] +, polyacteylenes?; vessel elements often >1,000 µm long; petiole bundles (incurved) arcuate; mucilage cells +; stomata cyclocytic; hairs unicellular; leaves often two-ranked, lamina margins with distant and strong spines to entire, petiole base encircling stem or not, adaxial flange +; K open; staminate flowers: A dorsifixed; pollen tectum striate; carpellate flowers: (C 0); nectary 0; G [(4)], transseptal bundles +, (2 carpels fertile); ovule?, funicular obturator +; fruit ± baccate; testa ?many layered, outer two (and esp. third) layers with thickened walls; n = 18.
1[list]/6. New Zealand and S. South America (map: from Dillon & Muñoz-Schick 1993). [Photo: Inflorescence, Leaves, Habit, Flower (scroll to end).]
Chemistry, Morphology, etc. The wood has solitary vessels and apotracheal parenchyma (Baas et al. 2000).For general information, see Philipson (1977) and Dillon and Muñoz-Schick (1993), for seed fatty acids, see Badami and Patil (1981), in part, for leaf insertion, c.f. Philipson (1967), and for leaf base, c.f. Takhtajan (1997); Takhtajan (2000) provides details of embryo and testa, for flowers, see Eyde (1964), and for the ovule, see Warming (1913).
Previous Relationships. Eyde (1964) suggested relationships of Griselinia to Garrya (Garryales) and Cornaceae (Cornales); the genus was placed in a monogeneric order in Cornidae-Cornanae by Takhtajan (1997).
[Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]]: plant often aromatic, ethereal oils, acetate-derived anthroquinones, coumarins +, C17 aliphatic acetylene falcarinone, iridoids 0, flavonols 0; lateral roots originating from either side of the xylem poles; vessel elements with simple perforation plates, clustered, septate fibres with minutely bordered pits, exclusively scanty paratracheal parenchyma; schizogenous secretory canals +, in cortex, pericycle, secondary phloem; secondary phloem with parenchyma surrounding the secretory canals and in groups with sieve tubes, fibres 0; (nodes 3:3); petiole bundles arcuate or annular; flowers perfect and imperfect, plant andromonoecious; C tube formation early; pollen grains tricellular; G , both fertile, stigma wet; x = 12; RPB2 duplication.
Age. Ages for this node are (52-)48, 46(-42) m.y. (Wikström et al. 2001), (55-)42, 41(-33) m.y. (Bell et al. 2010) and (110.2-)97.7(-85.1) m.y. (Nicolas & Plunkett 2014).
Evolution. Divergence & Distribution. For the evolution of the distinctive morphology of Pittosporaceae, see avove.
Plant-Animal Interactions. Ehrlich and Raven (1964) noted that some butterflies that do not seem to like Araliaceae, including Hydrocotyle, are found on Apiaceae (?including Saniculoideae); thus the Papilio machaon group is not found on Araliaceae because that family lacks the furanocoumarins that the caterpillars like (Berenbaum 1983).
Genes & Genomes. For the complex history of the RPB2 gene (DNA-dependent RNA polymerase) duplications, see Nicolas and Plunkett (2013).
Chemistry, Morphology, etc. There are a number of characters that may delimit clades of various sizes here. These include the presence of sesquiterpene lactones and benzylisoquinoline alkaloids; presence of crystal sand.
Triterpenoid ethereal oils produce the distinctive odour characteristic of many of these plants; see Jay (1969) for suggestions based on plant chemistry that members of this group are related. Kleiman and Spencer (1982) surveyed Apiaceae and Araliaceae for the occurrence of petroselenic acid. Triterpenoid saponins like oleanene are found throughout the group, and also elsewhere (Wang et al. 2012). Lateral roots originate from either side of the xylem poles because a resin canal runs down the stem at the apex of the pole (van Tieghem & Douliot 1888). The vessel:ray pits are bordered (Baas et al. 2000).
Members of both Araliaceae and Apiaceae in clades that are sister to the rest of these families have simple leaves, as have Myodocarpaceae (Plunkett 2001) and of course Pittosporaceae, so compound leaves may have evolved independently in Apiaceae and Araliaceae. Leaf teeth have a broad glandular apex with a main and two accessory veins, or one vein proceeds above the tooth; a survey of tooth morphology might be interesting.
Some Pittosporaceae and a few Araliaceae have basally connate petals (Plunkett 2001). For information on ventral carpel bundles, see Philipson (1970) and Eyde and Tseng (1971); when the united ventral bundles are opposite the carpels, the two bundles come from the same carpel, and when they are in the septal radii, the two bundles are derived from adjacent carpels. For ovule morphology, see Jurica (1922) and van Tieghem (1898). According to the latter, Apiaceae have a thick integument (e.g. ca 7 cells - Gupta 1970), that of Hedera is very thick, although Philipson (1977) described the integument of Araliaceae as being "thin". There is variation both in the kinds of calcium oxalate crystals that are found in the fruit wall, i.e., single rhomboidal crystals or druses, and also where they occur, e.g. in the endocarp or mesocarp, or all around the fruit or only in commissural area (Liu et al. 2006); I have only just begun to work out the phylogenetic significance of this variation (see also Rompel 1895; Burtt 1991a).
For similarities in woody anatomy between Apiaceae and Araliaceae, see Metcalfe and Chalk (1983); for the sequence of initiation of parts of the flower, see Erbar and Leins (1985: mostly Apiaceae, also Hydrocotyle); for chromosome numbers and evolution, see Yi et al. (2004); for fruit wings and fruit anatomy, see Liu et al. (2006); for nectaries, see Erbar and Leins (2010), and for bark anatomy, see Kotina et al. (2011: crystal types and distributions not integrated into the phylogeny).
Phylogeny. The old woody Araliaceae/herbaceous Apiaceae distinction is no longer tenable, and recent rearrangements have considerable implications for character evolution (c.f. Valcárcel et al. 2014 in part). Myodocarpaceae and Apiaceae-Mackinlayoideae as recognised here both include genera that used to be in Araliaceae, but the precise relationships of the former in particular have been uncertain - see Plunkett and Lowry (2001), Lowry et al. (2001), Plunkett (2001) and Chandler and Plunkett (2004) for more information. Since there are a number of morphological similarities between the Mackinlaya clade and Apiaceae s. str. (Chandler & Plunkett 2002, 2004), Mackinlayoideae are included in Apiaceae here. The old Apiaceae-Hydrocotyloideae, herbaceous and with simple leaves, are polyphyletic. The large genus Hydrocotyle is in Araliaceae, a position that makes morphological sense, and although sampling of Hydrocotyle and the related Trachymene must be improved, this is unlikely to affect their position. Arctopus is now in Apiaceae-Saniculoideae; Azorella and a group of genera form a well supported Apiaceae-Azorelloideae, and Centella, Micropleura, Actinotus, etc., are in Apiaceae-Mackinlayoideae (e.g. Downie et al. 1998, Downie et al. 2000; Chandler & Plunkett 2003, 2004; Plunkett et al. 2004; Andersson et al. 2006; esp. Nicolas & Plunkett 2009). Nodes along the backbone of this part of the tree have rather moderate support (e.g. Nicolas & Plunkett 2009), yet very few genera remain to be sequenced.
For other work on phylogenetic relationships in the Apiaceae-Araliaceae area, see e.g. Judd et al. (1994: Pittosporaceae not included), Oskolski et al. (1997), Oskolski & Lowry (2000), Plunkett (1998), Plunkett et al. (1996, 1997a, 1997b), and Kårehed (2002c).
PITTOSPORACEAE R. Brown, nom. cons. Back to Apiales
Trees, shrubs, or twining vines/lianes; furanocoumarins +, (hydroxycoumarins), non-hydrolysable tannins +, petroselenic acid 0, C20 and C22 fatty acids abundant; young stem with (± interrupted - Pittosporum) vascular cylinder; nodes 1:3, 3:3; petiole bundles arcuate; stomata paracytic; hairs uniseriate, terminal cells distinct, vertically or transversely [T-shaped hair] elongated or glandular; lamina vernation supervolute-curved, margins entire, secondary veins pinnate, leaf base narrow to sheathing; flowers medium-sized; K quite large, free (± connate), C often slightly basally connate, 3-5-veined; anthers ± basifixed, placentoid +; tapetal cells multinucleate; (pollen bicellular); nectary on flank of ovary; G superior, [(-5)], (placentation parietal), style undivided, straight, stigma capitate (lobed); ovules many/carpel, anacampylotropous (apotropous), integument 8-20 cells across, (incompletely tenuinucellate), endothelium 0, obturator hairs +, vascular bundle terminates in upper part of the funicle; fruit a loculicidal (+ septicidal) capsule or berry, K deciduous; seeds with sticky pulp; testa (multiplicative), 3 or more layers persisting, exotestal cells ± thickened, little differentiated, unlignified.
6-9[list]/200: Pittosporum (140). Old World, especially Australia, tropical and warm temperate, outside the immediate Australian region, mainly Pittosporum (map: from van Steenis & van Balgooy 1966; Good 1974; Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]
Age. The appproximate age for this node ([Sollya + Pittosporum]) is (17-)14, 13(-10) m.y. or (Wikström et al. 2001) or (20-)12, 11(-5) m.y. (Bell et al. 2010).
Evolution. Divergence & Distribution. Many of the apparently plesiomorphic characters of Pittosporaceae, e.g. superior ovary with several ovules, etc., are likely to be derived (see above).
Chemistry, Morphology, etc. Glucosinolates are reported from Bursaria spinosa, but this is probably a mistake (Fahey et al. 2001).
In Pittosporum, at least, the flowers are often functionally unisexual. There is a tendency, especially evident in taxa like Cheiranthera, for the flowers to be obliquely monosymmetric; asymmetry is largely because of the position of the stamens and gynoecium. In Pittosporum floribundum, ovules are epi- and apotropous within a single ovary (Narayana & Sundari 1983). Mauritzon (1939a) drew attention to the fact that the funicular bundle appears to expand and end in the upper part of the funicle, rather than in the chalazal region. This may be connected with how the embryo sac curves; I have not looked for this feature in other Apiales. Seedlings of Pittosporum have up to five cotyledons, and seedling leaves may be pinnatifid.
For embryology, see Narayana and Sundari (1983) and references, for endothelium in particular, see Batygina et al. (1985), for seed oils (undistinguished), Stuhlfauth et al. (1985), for vegetative anatomy, Wilkinson (1992, 1998), and for testa anatomy, see Takhtajan (2000: the ovules may be apotropous).
Phylogeny. Cayzer (references in Chandler et al. 2007) has carried out a number of morphological revisions and phylogenetic analyses of parts of Pittosporaceae; changes in taxon limits that she suggests are largely confirmed by a preliminary molecular study (Chandler et al., in Plunkett et al. 2004c). However, generic limits in the Billardiera-Sollya area are still unclear (Chandler et al. 2007). For relationships between species of Pittosporum found in the Pacific, see Gemmill et al. (2002).
Previous relationships. Pittosporaceae were included in Rosales by Cronquist (1981) and Mabberley (1997). However, evidence has been mounting for over 130 years that they were best associated with Apiaceae/Araliaceae (Hegnauer 1969b for a summary of some literature), van Tieghem (18) even placing Pittosporaceae, Aopiaceae and Araliaceae in his Ombellinées. Takhtajan (1997) included Pittosporaceae as a separate order in his Aralianae (but along with Byblidales).
[Araliaceae [Myodocarpaceae + Apiaceae]]: polyacetylenes + [mainly aliphatic, C18 tariric fatty acid in seed]; young stem with separate bundles; outer cortical collenchya +, forming a continuous layer; leaves compound, lamina margins toothed or otherwise incised; inflorescences terminal, ultimate units umbels; (pedicels articulated); K open; C valvate; nectary continuous with style [stylopodium], divided, ventral carpel bundles are fused bundles of adjacent placentae; ovules two/carpel, epitropous, one much reduced; fruit dry, schizocarpic, ± laterally flattened, (winged, wings with mesocarp and endocarp, vascular bundles at the margin of wing), endocarp sclerified; exotestal cells (tangentially elongated), tanniniferous [?level]; hemicellulosic seed reserves common; 92 bp deletion in rpl16 gene.
Age. The age of this node is estimated as (48-)38, 35(-25) m.y. (Bell et al. 2010), while Wikström et al. (2001) thought that this node was (49-)45, 41(-37) m.y. old and Xue et al. (2012) (43.6-)41.1(-40.4) m.y.; a much older estimate of (106.6-)94.6(-82.6) m.y. was given by Nicolas and Plunkett (2014).
Evolution. Pollination Biology & Seed Dispersal. For the evolution of andromonoecy in this clade, very rare elsewhere in flowering plants and perhaps connected with dichogamy, successively flowering umbels, and umbels as functional units in pollination, see Schlessman (2011).
Chemistry, Morphology, etc. For wood and stem anatomy, see Rodriguez C. (1957) and Oskolski (2001), for young stem and petiole anatomy, see Mittal (1961), for the anatomy of the fruit wing, see A. R. Magee et al. (2010a), and for the rpl16 deletion, see Downie et al. (2000a).
ARALIACEAE Jussieu, nom. cons. Back to Apiales
Hydroxycoumarins +, furanocoumarins 0; (vessel elements with scalariform perforation plates); fibres septate (not); axial parenchyma paratracheal; rays heterocellular; vascular bundles in pith, usu. inverted; stomata para- or aniso-(anomo-)cytic; stipules +; (plants andromonoecious); (A 3); stigma punctate (dry); ovules crassinucellate to tenuinucellate, integument "thin" [?level], (nucellar cap +), (endothelium +), funicle with short unicellular hairs as obturator; mesocarp thick-walled, lignified, with single rhomboidal crystals in cell layer immediately outside endocarp; (seeds ruminate); exotestal cell walls a little thickened.
43/1450. Largely tropical, few temperate (map: see Meusel et al. 1978; Hultén & Fries 1986; FloraBase 2006; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011). Two groups below.
Age. The age of crown Araliaceae is estimated to be (100-)80(-70) m.y. (Mitchell et al. 2012); Beaulieu et al. (2013a: 95% HPD) suggested an age of (48-)44(-41) m.y. while an age of (83.2-)65(-48.7) m.y. has also been mentioned (Nicolas & Plunkett 2014).
1. Hydrocotyloideae Link
± Herbaceous, perennial; nodes 3:3 [Hydrocotyle]; lamina orbicular-peltate (± palmately compound), margin crenate, stipules cauline or petiolar; (inflorescences axillary); (K 0 - Hydrocotyle); ovule with "short" funicle, integument ca 5 cells across, parietal tissue 0; (fruit with undivided carpophore); n = ³6.
4/175: Hydrocotyle (130), Trachymene (45). Tropical, including montane, also warm temperate.
Age. The age of crown Hydrocotyloideae has been estimated at ca 51.4 m.y. (Nicolas & Plunkett 2014).
Synonymy: Hydrocotylaceae Berchtold & J. Presl
[Harmsiopanax + Aralioideae]: ?
2. Harmsiopanax Harms (if here)
(Plant monocarpic); (spiny); ventral carpel bundles are fused bundles of the one placenta.
3. Aralioideae Eaton
(Herbaceous); (palisade mesophyll with arm cells); (prickles + - origin various); (hairs stellate, dendroid, lepidote); leaves usu. pinnately to palmately compound, (stipules 1, intrapetiolar, 2, cauline, 0); (inflorescences [sub]racemose); pedicels articulated or not; (C ± connate to calyptrate), (imbricate - Aralia, Panax, etc.); (A many), (filaments with two traces); tapetal cells 1-multinucleate, nectary [stylopodium] not divided; G [3<] [(1-5-200+)], when 5, opposite petals, when 3, median abaxial; integument 10-19 cells across, parietal tissue (0) 1-4 cells across, funicular obturator +/0, hypostase +/0; fruit a drupe (berry; dry, schizocarpic); testa multiplicative; (seed ruminate) ; n = ³11.
41 [list]/1275: Schefflera (1600: wildly polyphyletic), Polyscias (160), Oreopanax (80), Dendropanax (70), Aralia (68), Osmoxylon (50). Largely tropical, few temperate. [Photo - Flowers, Fruits.]
Age. For the clade [Gastonia + Hedera] an age of around 85 m.y. or more can be inferred from Valcárcel et al. (2014), while ages of (100-)84(-70) m.y. are suggested for the [Schefflera longipedicellata + The Rest] clade (Mitchell et al. 2012), while the clade [Harmsiopanax + The Rest] was estimated to be around 57.7 m.y.o. (Nicolas & Plunkett 2014) - but c.f. the ages above for the family.
Synonymy: Hederaceae Giseke, Botryodendraceae J. Agardh
Evolution. Divergence & Distribution. Major groupings within Aralioideae in particular show some geographical signal (see below), even if they do not map on to previous classifications. See Mitchell et al. (2012) for some dates in the Greater Raukaua clade, Valcárcel et al. (2014) for dates in the Asian Palmate clade, which depend on the marker used, and Nicolas and Plunkett (2014) for some dates from alomg the spine of the subfamily.
Genes & Genomes. For shifts in the rate of molecular evolution within Araliaceae that are correlated with changes in habit, see Smith and Donoghue (2008).
Chemistry, Morphology, etc. Hedera may have an interrupted fibrous pericyclic sheath; creeping forms have two-ranked leaves. As to stipules: Fatsia (no stipules) x Hedera (no stipules) = XFatshedera (stipules), but some species of Hedera do have a hollowed leaf base with a flanged margin that encloses the axillary bud.
Araliaceae show considerable floral variation, and this is reflected in their floral vasculature. The calyx may be entirely absent (e.g. Hydrocotyle: Tseng 1967), not even reduced vascular traces suggesting that it was ever there, the petals may have three traces and may be slightly to completely connate (Osmoxylon has basally connate petals), and the stamens sometimes have two traces (Nuraliev et al. 2010, 2011). Both Aralioideae and Hydrocotyle show early corolla tube initiation (Leins & Erbar 1997; Erbar & Leins 2004). Tetraplasandra gymnocarpa and T. kavaiensis have secondarily more or less completely superior ovaries (Costello & Motley 2000, 2001, 2004 - see photograph on the cover of American J. Bot. 91(6). 2004). Hydrocotyle, almost alone in the family, is highly polyploid (Yi et al. 2004).
Variation in meristicity is particularly striking in Aralioideae, and flowers are up to 12-merous or more there (Viguier 1906). Tupidanthus calyptratus (= Asian Schefflera) has up to 172 stamens and 132 carpels; the carpels are initiated in a single elongated and sometimes contorted whorl looking rather like a brain cactus (fasciation: Oskolski et al. 2005; Nuraliev et al. 2009, 2014; see also Eyde & Tseng 1971). Some species have about as many stamens as carpels, separate members of the calyx cannot be distinguished (the calyx forms a low, entire rim; Nuraliev et al. 2014), the petals may be connate and form a calyptra, and although the symplicate zone of the gynoecium develops first, the carpels are largely synascidiate; there is a large, flat remnant of the floral axis within the carpel whorl (Sokoloff et al. 2007b). Plerandra has up to 25 or more carpels and to 500 stamens, while other species there are up to five series of stamens initiated centripetally, the vasculature of members of each whorl being connected radially (very unusual for euasterids); carpel number is 14 or fewer (Philipson 1970; Oskolski et al. 2010c). For further discussion, see the [euasterid] clade.
For general information, see Philipson (1970), for general anatomy, see Viguier (1906), for that of the leaf, see de Villiers et al. (2010), for bark, see Kotina & Oskolski (2010), for wood, see Oskolski (1996), for gynoecial development in Seemannaralia, see Oskolski et al. (2010b), for embryology, see Ducamp (1902), Gopinath (1944) and Mohana Rao (1973b), and for fruit anatomy, see Konstaninova and Suchorukow (2010). Hydrocotyle: see Leins and Erbar (2010), flowers; Shu and She (2001), pollen of Chinese spp; Håkansson (1923), ovules.
Phylogeny. Basal Araliaceae may well be bicarpellate (see also Wen et al. 2001) and have simple leaves, as in the herbaceous Hydrocotyloideae (ex Apiaceae), which are sister to the rest of the family (Chandler & Plunkett 2004; Plunkett et al. 2004a; Nicolas & Plunkett 2009). The S.W. Australian genera Neosciadium and probably Homalosciadium also belong to Hydrocotyloideae (Andersson et al. 2006). Hydrocotyle has laterally flattened fruits with a sclerified (= woody) endocarp and stipules that are either cauline or are borne on the leaf base - and it also has trilacunar nodes (Sinnott & Bailey 1914). Trachymene, perhaps to include Uldinia, is also in Hydrocotyloideae; morphologically it is rather similar to them, and although there is a carpophore in the fruit, it is undivided. For a phyogeny of Trachymene, see Henwood et al. (2010).
Astrotricha and Osmoxylon may be part of a polytomy at the node immediately above Hydrocotyloideae (see also Lee et al. 2008), while the position of Harmisopanax, which has fruits that are schizocarpic like those of Hydrocotyloideae, is also uncertain (Nicolas & Plunkett 2009).
For more details on the phylogeny of Aralioideae in particular, see Henwood and Hart (2001) and especially Wen et al. (2001), Plunkett et al. (2004a, c), and Lowry et al. (2004). Schefflera, with perhaps 1,600 species under 2/5 of which have been described (Frodin et al. 2010), is highly polyphyletic, and five major clades have become apparent in it - of which Schefflera s. str. is perhaps the smallest. These are circumscribed geographically and some also have morphological support. African plus Madagascan taxa form a clade, as do the some 250-300 neotropical species, the Asian species (the last two clades are close on the tree), and two groups of species restricted to the Pacific, the small Schefflera s. str. and the much larger Melanesian clades (Plunkett et al. 2005 [general], 2009 [Melanesia], 2010 [Neotropics]; Gostel et al. 2009 [Africa-Madagascar]; Fiaschi & Plunkett 2011 [Neotropics]; Plunkett & Lowry 2012 [Melanesia]: Frodin et al. 2010 for a summary). In part these clades map on to earlier infrageneric groupings, although with the inclusion of segregate genera.
The Schefflera problem aside, there are four major clades in Aralioideae, the largely South East Asian Palmate and Aralia-Panax groups, and the Pacific and Indian Ocean basin Greater Raukaua (Mitchell et al. 2012) and the Polyscias-Psuedopanax groups (Wen et al. 2001; Mitchell & Wen 2004; Plunkett et al. 2004a; see Valcárcel et al. 2014 for a summary). Within the Palmate group, which includes Hedera, relationships are rather poorly resolved, and details depend on the markers used - polyploidy and ancient hybridization may be involved - and the position of Osmoxylon seems particularly uncertain (Yi et al. 2004; Mitchell & Wen 2004; Valcárcel et al. 2014). Lee et al. (2008) focused on relationships of Malesian Araliaceae; Osmoxylon was isolated. Most (?all) Dendropanax are likely to be monophyletic, with two large clades restricted to the Old and New Worlds (Li & Wen 2013).
Classification. For a now dated checklist of the family, see Frodin and Govaerts (2003), although this is already very dated. Generic limits in Aralioideae need much attention; see Plunkett et al. (2004a) for genera, but more changes will be needed. The Pacific clade of Schefflera is to be called Plerandra; Polyscias has been substantially enlarged (Lowry & Plunkett 2010).
[Myodocarpaceae + Apiaceae]: furanocoumarins +; A inflexed in bud.
Age. Ages for this node of (42-)32, 29(-20) m.y. (Bell et al. 2010), (42-)38, 33(-29) m.y. (Wikström et al. 2001), and much older, (103.2-)91.3(-78.6) m.y. (Nicolas & Plunkett 2014), have been suggested.
MYODOCARPACEAE Doweld Back to Apiales
(Sclereids in phelloderm); (vessel elements with scalariform perforation plates, numerous thin bars - Delarbrea); septate fibres 0; libriform fibres with very thick walls; axial parenchyma apotracheal (and paratracheal), diffuse-in-aggregates; rays homogeneous; leaves pinnately compound (simple), lamina margin entire (serrate), venation brochidodromous, base with adaxial or lateral flange; pedicels articulated; K valvate, C imbricate; nucellus?; fruits (terete, fleshy), endocarp thin, or dry, winged, carpophores free, secretory vesicles in mesocarp, endocarp with large oil ducts [different from vittae]; n = ?
2 (Myodocarpus, Delarbrea)/19. New Caledonia, E. Malesia, and Queensland, Australia (map: from van Balgooy 1993). [Photo - Habit.]
Age. Crown-group Myodocarpaceae are estimated to be (47.4-)25.4(-8) m.y.o. (Nicolas & Plunkett 2014).
Chemistry, Morphology, etc. In wood anatomy Myodocarpus is perhaps more like Cornaceae than any other members of the Apiaceae-Araliaceae complex, but in other features it is more like Apiaceae (Rodrigues C. 1957). Myodocarpus has a number of distinctive features of the flower and in particular its schizocarp. The mericarps are beautiful little laterally-flattened samaras that at first sight are similar to those of Serjania.
Some information is taken from Lowry (1986: Delarbrea), Raquet (2004: morphological phylogeny), Plunkett et al. (2004c: general) and Liu et al. (2010: apomorphies); for wood anatomy, see Oskolski (1996).
Previous Relationships. This group used to be included in Araliaceae as Myodocarpeae.
APIACEAE Lindley, nom. cons.//UMBELLIFERAE Jussieu, nom. cons. et nom. alt. Back to Apiales
Pyranocoumarins, myricetin, mannitol +, umbelliferose [raffinose (trisaccharide) isomer] the storage carbohydrate; hydroxycoumarins, flavones 0; vessel elements aggregated; axial parenchyma scanty, paratracheal; (vascular bundles in cortex); stomata various; lamina vernation also supervolute; K a ring of teeth, (obsolete), C clawed, free, petals usu. with inflexed tips, vein single, unbranched [?all]; stigma usu. capitate; ovule (with -2 lateral layers of nucellar tissue), funicle "short"; fruit (fleshy), ventral carpel bundles two, fused bundles of the same placenta, [opposite], mesocarp lignified, crystals single, rhombic, in small-celled inner layer, endocarp woody, 2(+) cell layers thick, sclereidal-fibrous; exotestal cells thin-walled.
434[approx. list]/3780 - 5 main groups below. World-wide, esp. N. temperate.
Age. Beaulieu et al. (2013a: 95% HPD) thought that crown-group diversification of Apiaceae began (66-)54(-43) m.y.a.; (98.9-)87.4(-76) m.y., much older, is the age in (Nicolas & Plunkett 2014).
Fruits from the late Cretaceous (Maastrichtian) of Wyoming and Montana, around 69 m.y.o., (Carpites) have been assigned to Apiaceae (Manchester & O'Leary 2010).
1. Mackinlayoideae Plunkett & Lowry
Herbs (annuals) to shrubs; (centellose [oligosaccharide] - Centella); (cork cambium subepidermal - Centella); (vessel elements with scalariform perforation plates); apotracheal (+ paratracheal) parenchyma; leaf ± pedately compound [Mackinlaya], ± palmate, to simple; (pedicel not articulated); (K petal-like); (nectary not divided; on style - Actinotus); nucellus?; crystals surrounding endocarp, carpophores 0; rib oil ducts + (not Diposis); n = 9, 10.
7-9/98: Centella (45), Xanthosia (25), Actinotus (18). Southern Hemisphere, scattered, Centella esp. the Cape, South Africa, C. asiatica pantropical (Map: from Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; Australia's Virtual Herbarium i.2013; GBIF i.2013; van Wyk et al. 2013; green = mostly Centella asiatica).
Age. The age of crown-group Mackinlayoideae is estimated to be (83.6-)66.3(-50.2) m.y. (Nicolas & Plunkett 2014).
Synonymy: Actinotaceae Konstantinova & Melikian, Mackinlayaceae Doweld
[Platysace [Azorelloideae [Hermas [Saniculoideae + Apioideae]]]]: plant herbaceous; vessel elements with simple perforation plates; umbels compound; fruits dorsally compressed, carpophore +, mericarps separating at maturity.
Age. The age of this node is estimated to be (94.8-)83.6(-72.9) m.y. (Nicolas & Plunkett 2014).
Herbs (annuals) to shrubs; leaves simple, blade entire (deeply trifid), base rather narrow; (oil ducts in ribs); K 0; ?carpophore; ?ventral carpel bundles; cotyledons rounded, toothed; n = 8.
1(-2)/26. Australia, most in the southwest (map: FloraBase viii.2009; Australia's Virtual Herbarium i.2013).
[Azorelloideae [Hermas [Saniculoideae + Apioideae]]]: mesocarp vittae irregular, anastomosing and/or branching.
Age. The age of this node may be (85.6-)75.8(-65.7) m.y. (Nicolas & Plunkett 2014).
3. Azorelloideae Plunkett & Lowry
Herbs to small shrubs; ?petroselinic acid; (cork cambium deep-seated - Mulinum); (hairs stellate); (leaves compound), stipules +; C flat; nucellus "large", relatively persistent; megaspore mother cells 2-4, embryo sac tetrasporic, 16-nucleate [more than one embryo sac "type"]; fruit with wings/ribs [made up of the entire fruit wall, including a vascular bundle], lateral ribs/wings largest, carpophore (0), entire (apically cleft, bifid), ventral bundles 0, 1, 2, lateral [commissural], (opposite), (druses in outer mesocarp - Azorella), companion cells [oil canals associated with the vascular bundles] +, inner layer of endocarp fibres running longitudinally [?distribution]; n = 8-10, x = ?8.
21/155: Azorella (?70). South American-Australian, Antarctic islands; Drusa glandulosa from the Canary Islands and Somalia, Dickinsia from China, probaly not native in North America (map: from Mathias & Constance 1965; Martinez 1993; Fl. China 14: 2005; Australia's Virtual Herbarium 1.2013). [Photo - Habit.]
Age. The age of this node - [Bowlesia et al. + The Rest] - is around 65.5 m.y. (Nicolas & Plunkett 2014).
[Hermas [Saniculoideae + Apioideae]]: stipules 0 [?here].
Age. The age of this node (assuming it exists) is estimated to be (80-)70.6(-62) m.y. (Nicolas & Plunkett 2014).
Woody perennials or shrublets; plant densely hairy; leaf blade simple, margin variable; umbels congested, bracts quite large; K large, persistent, C filiform; fruit dorsiventrally flattened, with 2 ventral bundles, lateral [commissural], (forming a cross), mesocarp with rhomboidal crystals, druses 0, rib oil ducts small, vittae irregular, anastomosing, not vallecular, carpophore single; n = 7.
1/8. South Africa (map: from van Wyk et al. 2013).
[Saniculoideae + Apioideae]: basal leaf with pinnate venation [?level]; ovules lacking parietal tissue [incompletely so], nucellar cap +, funicle "long"; fruit wings with mesocarp only, vascular bundles ar the base, (secondary [i.e. lateral] ribs +), rib oil ducts large, mesocarp cells lignified, endocarp single cell layer thick, parenchymatous, calcium oxalate as druses dispersed in mesocarp and around commissure, rhomboidal crystals 0; RPB2 duplication +.
Age. The age of this node has been estimated as (74.3-)65.8(-58.2) m.y. (Nicolas & Plunkett 2014).
4. Saniculoideae Burnett
Kaurene-type diterpenoids +; (cork cambium outer cortical); (nectary outside A); styles separated from disc by a narrow groove; ribs with oil ducts/cavities; cotyledons rounded.
Age. Crown-group Saniculoideae are estimated to be around 53.1 m.y.o. (Nicolas & Plunkett 2014).
[Steganotaenieae + Phlyctidocarpeae]: ?
4a. Steganotaenieae C. I. Calviño & S. R. Downie
Subshrubs to trees, (deciduous); phelloderm with chambered crystalliferous cells; dilation of secondary phloem by expansion of axial parenchyma [not ray cells]; leaves (simple) palmate to pinnate, basal leaves appearing well before flowering; fruits dorsi-ventrally flattened or not, heteromericarpic, 2-3 winged [wings exo- and mesocarp alone], rib oil ducts forming cavities, ventral bundles 2, lateral [commissural], carpophores free, bifid, (dispersed mesocarp druses 0); n = ?11, 12
2/5. Tropical, S.W. Africa (Map: van Wyk et al. 2013).
4b. Phlyctidocarpeae Magee, Calviño, Liu, et al.
Annual herb; stylopodium 0; fruits dorsi-ventrally flattened, with stipitate obconical processes, ribs bifurcate, with two vascular bundles, ventral bundles 2, lateral [commissural], carpophore 0, vittae +; n = ?
1/1: Phlyctidocarpa flava. Namibia (map: from van Wyk et al. 2013).
4c. Saniculeae Burnett
Plant ± herbaceous; (R)-3'-O-ß-D-glucopyranosylrosmarinic acid +, (cardenolides - Eryngium); leaves (compound), lamina often broad, teeth with hairy or spiny tips; umbels simple (a capitulum - Eryngium; pseudoracemose - Sanicula), with ± petal-like inflorescence bracts (green); pedicels ± 0; (flowers blue), carpellate flowers sessile; fruit barely flattened, scaly or spiny, (± smooth), (ribs with two vascular bundles), carpophore 0, or ventral bundles 2, opposite [carinal], (rib secretory ducts/cavities 0), (dispersed crystals throughout mesocarp 0), endocarp not lignified; n = 8 (9, 11, 12).
8/333: Eryngium (250). World-wide (map: see Meusel et al. 1978; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; Wörz 2011; Australia's Virtual Herbarium i.2013; van Wyk et al. 2013).
Synonymy: Eryngiaceae Berchtold & J. Presl, Saniculaceae Berchtold & J. Presl
5. Apioideae Seemann
Flavones, methylated flavonoids, furanocoumarins, phenylpropenes +; cortical collenchyma often interrupted; leaves palmately compound; (outer flowers of umbel monosymmetric); tapetum multinucleate; integument 6-8 cells across, hypostase +, (postament +); ventral bundles 2, opposite [carinal], intrajugal oil ducts small/0; seed reserves mannans [?right place]; x = 11; cotyledons (1), various.
Ca 380/3200. Worldwide, esp. N. Temperate.
Age. The age of crown-group Apioideae is some (71.6-)63.7(-56.1) m.y. (Nicolas & Plunkett 2014).
5A. Lichtensteinieae Magee, Calviño, Liu, et al.
Annual to pereniial herbs to compact shrublets; (basal leaves appearing well before flowering); K conspicuous or not; fruits dorsiventrally flattened or not, (heteromericarpic), (ventral bundles 0, 1), carpophore various [short, hygroscopic - Choritaenia] or 0, (endocarp woody, druses 0 - Choritaenia), two vascular strands in each rib, (huge oil ducts/cavities in wings), (surrounded by concentric rings of cells); n = 11.
3/9. South Africa, 1 sp. the Namib desert.
Age. The age of crown-group Lichtensteinieae is about 39.6 m.y. (Nicolas & Plunkett 2014).
[Annesorhizeae [Heteromorpheae + Euapoids]]: fruits with rib oil ducts small, carpophore free, bifid [mericarps attached at apex], vallecular vittae +.
Age. The age of this node is (65.3-)58.3(-52.2) m.y. (Nicolas & Plunkett 2014).
5B. Annesorhizeae Magee, Calviño, Liu, et al.
(Plant woody); (fruits heteromericarpic), carpophore bifid; vascular bundles highly lignified.
6/36. Most South Africa, also Southern Europe (1 sp.) and North Africa, Canary Islands and Madeira (1 sp.) (map: from van Wyck et al. 2013).
Age. Crown-group Annesorhizeae are around 37.4 m.y.o. (Nicolas & Plunkett 2014).
[Heteromorpheae + Euapoids]: tanniniferous exotestal cells 0.
Age. The age of this node is about 58.3 m.y. (Nicolas & Plunkett 2014).
5C. Heteromorpheae M. F. Watson & Downie
Plants often shrubby (scrambler); (chloroplasts in the phelloderm cells [het. pol.]), (periderm cortical - Anginon), vessel walls with helical thickenings; fibres septate; (leaves undivided); (involucral bracts dentate); (K well developed); fruits (heteromericarpic), not or slightly dorsiventrally or laterally compressed, carpophore bifid, (two vascular strands in each rib); n = 11, ?12.
12/27: Anginon (12). Africa (esp. the southwest) to the Yemen, Madagascar (Map: from Winter & van Wyk 1996; Allison & van Wyk 1997; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; van Wyk et al. 2013).
[Bupleureae + The Rest] / euapoids: druses in fruit wall absent.
Age. The age of this node is estimated to be (51.6-)44.5(-39.1) m.y. (Banasiak et al. 2013) or ca 51.5 m.y. (Nicolas & Plunkett 2014).
5D. Bupleureae Sprengel
(Plant shrubby); vessel walls with helical thickenings; fibres septate; leaves simple, margins entire, (venation parallel); umbels and umbellules (sessile), with well-developed leafy inflorescence/floral bracts [= "bracts" + "bracteoles"]; pollen usu. rhomboidal; fruit not flattened, ?carpophore; cotyledons linear, single veined, glabrous; n = 7, 8.
1/190. Europe and North Africa, to the Canary Islands and East Asia, also N.W. North America and South Africa, both one species (Map: from Meusel et al. 1978; GBIF iv.2010; van Wyk et al. 2013).
Synonymy: Bupleuraceae Berchtold & J. Presl
The Rest: (plant rarely shrub or little-branched small tree); (K present - e.g. Hohenackeria); fruit not or dorsiventrally flattened, carpophore bifid; (cotyledon 1).
360/3045: Ferula (175), Pimpinella (150), Angelica (110), Seseli (110), Peucedanum s.l. (110), Lomatium (74), Heracleum (65), Chaerophyllum (60), Arracacia (55), Ligusticum (50), Thapsia (45) (map: from Meusel et al. 1978; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; van Wyk et al. 2013).
Synonymy: Ammiaceae Berchtold & J. Presl, Angelicaceae Martynov, Caucaulidaceae Berchtold & J. Presl, Coriandraceae Burnett, Daucaceae Martynov, Ferulaceae Saccardo, Imperatoriaceae Martynov, Lagoeciaceae Berchtold & J. Presl, Pastinacaceae Martynov, Pimpinellaceae Berchtold & J. Presl, Scandicaceae Berchtold & J. Presl, Selinaceae Berchtold & J. Presl, Sileraceae Berchtold & J. Presl, Smyrniaceae Burnett
Evolution. Divergence & Distribution. As relationships get sorted out, evolutionary and biogeographic studies become possible. Nicolas and Plunkett (2014, q.v. for details) suggested an Australian origin for Apiaceae, with at least some scenarios suggesting a South American origin for Hydrocotyloideae and an African origin for Apioideae and Saniculoideae. Indeed, a glance at the maps of the clades from Hermas to core Apioids shows a concentration of taxa in southern Africa in particular. Spalik et al. (2010) looked at wide disjunctions in Apioideae, providing dates for various nodes. The three basal clades of Apioideae are small and made up very largely of southern African genera; this has considerable implications for synapomorphy positions (Calviño et al. 2006; Magee et al. 2010a for some details). Although Apioideae are likely to have evolved in Southern Africa (Banasiak et al. 2013), and a number of taxa from there are woody plants, the ancestral condition for this subfamily, at least, may be herbaceous (Calviño et al. 2006). The place of origin of Bupleurum may be in archipelagic early Tertiary Europe, with much subsequent diversification in eastern Asia, although anywhere from Europe and North Africa to Eastern Asia may have been involved (Banasiak et al. 2013, q.v. for much more detail).
Spalik et al. (2014) looked at biogeographic patterns in the largely aquatic Oenantheae; there has been much dispersal from Eurasia to North Americs. They found that the Hawaiian "Peucedanum sandwicense" (a split from stem Oenanthe) may have arrived on Hawaii around 17.2 m.y.a., so being another example of a clade older than the current islands. Lilaeopsis brasiliensis and L. mauritiana are very close, even though they are separated by the Atlantic Ocean and the African continent (Spalik et al. 2010).
Carpophores, chromosome numbers other than 8, and inflorescences that are not condensed (all in African taxa) could be plesiomorphic in Saniculoideae; simple umbels are apomorphic for Saniculeae, etc. (Magee et al. 2010a, q.v. for numerous character optimisations; see also Calviño et al. 2008a; Kadereit et al. 2008).
Plant-Animal Interactions. Caterpillars of Papilionidae-Papilionini butterflies are notably common (ca 13% of all records) on Apiaceae, perhaps shifting here from Aristolochiaceae (Fordyce 2010; see also Berenbaum & Feeny 2008; Simonsen et al. 2011; Condamine et al. 2011). Interestingly, they are not found on either Pittosporaceae or Araliaceae; thus they will not eat Hydrocotyle (here Araliaceae), many of the larvae of Papilio ajax tested absolutely refusing to eat it (see also Dethier 1941; Ehrlich & Raven 1967). Linear fumarocoumarins are often phototoxic but are tolerated by caterpillars that will not eat plants with the non-photoxic linear coumarins (Berenbaum & Feeney 1981). Microlepidopteran larvae of the Elachistidae-Depressariinae are common on Apiaceae, although they may have initially been associated with rosids and have also colonized some Asteraceae (Fetz 1994: host plants; Berenbaum & Zangerl 1998: chemistry of the [co]evolution of resistance; Berenbaum & Passoa 1999: phylogeny). There has been a diversification of agromyzid dipteran leaf miners in north temperate Apiaceae; they were previously on Ranunculaceae, also a group with noxious secondary metabolites (Winkler et al. 2009). For general insect-umbellifer relationships, see Berenbaum (1990) and Sperling and Feeny (1995).
Pollination Biology & Seed Dispersal. All the flowers in an umbel open more or less simultaneously. In a number of Saniculoideae and a few Hydrocotyloideae in particular the inflorescence bracts function as petals, the rest of the inflorescence being much reduced and the whole looking more or less like a simple flower (Froebe & Ulbrich 1978). In the umbels of a number of Apioideae, the marginal flowers are larger than the others, and their abaxial petals may be larger than the adaxial, so increasing the resemblance of the inflorescence to a polysymmetric flower. The dark flower in the centre of the umbel of taxa like Daucus carota may attract flies that pollinate the flowers (Westmoreland & Muntan 1996).
Although the flowers appear unspecialized, being potentially pollinated by a variety of pollinators, like other such systems, e.g. Asteraceae, oligolectic pollinators may play a major role in pollination - in the case examined, the bee Andrena ziziae as a pollinator of Thaspium and in particular Zizia in the southeast U.S.A. (Lindsey 1984; Lindsey & Bell 1985). However, as with other such systems, other bees (and a syrphid fly) were also effective pollinators, and pollinators varied with geography, too.
Platysace and some Mackinlayoideae have myrmecochorous fruits (Lengyel et al. 2010).
Vegetative Variation. Variation in leaf morphology, even within Apioideae, is considerable. Thus the small circum-Pacific genus Oreomyrrhis (= Anthriscus) includes species with ordinary-looking highly dissected leaves, leaves with a series of almost tooth-like leaflets on either side of the rachis, linear leaves, sometimes lobed at the apex, although the lobes are not articulated, and small, undivided leaves. In the last case the plant is tussock-forming and almost moss-like, and I have seen specimens identified as Centrolepidaceae (= Restionaceae), a monocot! Species with all these leaf morphologies are found on the mountains of New Guinea. Although Oreomyrrhis is probably monophyletic, it is well embedded in Chaerophyllum, a genus hitherto thought to be fairly well understood (Chung et al. 2005; Chung 2007). Lilaeopsis occidentalis and Oxyopolis greenmanii have linear, terete leaves that are marked by articulations at intervals. These leaves are comparable with the rhachis of compound leaves, hydathodes borne at the articulations representing much reduced and modified pinnae (Kaplan 1970b, c.f. esp. Figs 3E and 6A). Such leaves appear to have evolved several times (Feist & Downie 2008; Feist et al. 2012). Bupleurum has undivided leaves, those of B. rotundifolium being almost orbicular, entire, and perfoliate, hence its common name, thorow wax.
Seeds with relatively longer embryos may have evolved in open habitats and in plants with an annual life cycle (Vandelook et al. 2012b). There is considerable variation in seedling morphology. A number of taxa have cryptogeal germination during which the plumule ends up, planted, as it were, under ground; associated with this, monocotyly is also quite common (see Haccius 1952b; Cerceau-Larrival 1962; Haines & Lye 1979).
Chemistry, Morphology, etc. Gums and resins are scattered in the family. In Apiaceae the flavone apigenin is synthesized by an enzyme belonging to the oxoglutarate dependen dioxygenase family, not by a member of the cytochrome P450 family, as is usual in angiosperms (Pichersky & Lewinsohn 2011). For the distinctive rosmarinic acid glucoside found in Saniculoideae-Saniculeae, see Olivier et al. (2008). Oskolski et al. (2010a) describe wood and bark anatomy of Steganotaenieae in particular and Saniculoideae in general. Peripheral collenchyma in the stem is often especially well developed, and petiole anatomy is very variable and complex (e.g. Metcalfe 1950). Taxa such as Foeniculum have stipules of sorts.
The usually compact inflorescence units of Saniculoideae may be best interpreted as a group of reduced umbellules (Froebe 1964, 1971), although they are called simple umbels above. Centella (Mackinlayoideae) has a few branches from the petal bundle (Gustafsson 1995); petal vasculature may repay attention. Spichiger et al. (2002) show the two carpels as being collateral. According to Eyde and Tseng (1971), whether the ventral carpel bundles are fused bundles of adjacent placentae or are from the same placenta varies within Apiaceae without any particular systematic significance. Van Tieghem (1898) noted that in Apiaceae the ascending ovule aborts and the pendulous ovule persists, however, other reports suggest that both ovules are pendulous (Philipson 1970).
Fruit anatomy is currently being studied by M. Liu and co-workers, and there is a considerable amount of variation which shows at least some correlation with clades. For vittae, druses, etc. in the fruits, see Liu et al. (2007, 2012b), for fruit anatomy of Azorelloideae, see Liu et al. (2009), and for carpophores, see Liu et al. (2012a) - although Phlyctidocarpa (Saniculoideae) by one definition in this last paper would seem to lack a carpophore (group A), yet it is scored as having a bifid carpophore.
For chemistry, see Hegnauer (1971), Berenbaum (2001) and Olivier and van Wyk (2013: Saniculeae), for stomata, see Guyot 1971 and references - value slight?), for wood anatomy in Apioideae-Heteromorpheae and Mackinlayoideae, see Oskolski and van Wyk (2008, 2010) and in woody Saniculoideae, see Oskolski et al. (2010a), for inflorescences of Saniculoideae and Hydrocotyloideae in particular, see Froebe (1964, 1979), for those of Eryngium, see Harris (1999), for floral development, see Leins and Erbar (2004b), for pollen of Chinese Apiaceae, see Shu and She (2001), for the distribution of the hypostase, see Gupta (1970), for embryo sac morphology and fruit anatomy, esp. of genera in the old Hydrocotyloideae, see Tseng (1967), for ovules, etc., see Håkansson (1923), and for chromosome number and morphology, see Pimenov et al. (2003). There is much useful information in Chandler and Plunkett (2003, 2004) and also in all four numbers of Plant Divers. Evol. 128. 2010, inc. Stepanova & Oskolski (2010: Bupleurum); see also Burtt (1991a: southern African genera) and Van Wyk et al. (2013: African taxa) for information about Apiaceae in a biogeographically/phylogenetically critical area.
Phylogeny. The old Apiaceae-Hydrocotyloideae are hopelessly polyphyletic, and their members now occur in several quite separate clades of which most are in Apiaceae (Nicolas & Plunkett 2009).
Some genera of Mackinlayoideae used to be in Araliaceae-Mackinlayeae, others in Apiaceae-Hydrocotyloideae. Genera to be included here include Apiopetalum, Mackinlaya, Micropleura and Xanthosia. Melikian and Konstantinova (2006) thought that the gynoecial structure of Actinotus was so different from that of other Apiaceae that the genus deserved to be placed in its own family; it belongs here, although its position is unclear (Nicolas & Plunkett 2009).
The Australian Platysace - perhaps to include Homalosciadium - is not a member of Mackinlayoideae, where it had been placed (e.g. Chandler & Plunkett 2004). It is sister to Apioideae in some analyses (Henwood & Hart 2001; Andersson et al. 2006), but a position rather deep in the tree sister to [Azorelloideae [Saniculoideae + Apioideae]] is strongly supported (Nicolas & Plunkett 2009, 2014), although Soltis et al. (2011: but sampling) found that it was moderately supported as sister to Mackinlaya. The positions of Klotzschia ("distinctive fruits") and Hermas, both of which used to be in Hydrocotyloideae, are unclear (Andersson et al. 2006; Calviño et al. 2006, 2008). Klotzschia, herbs to subshrubs with peltate leaves from Brazil, may go with Azorelloideae, Apioideae, or join the back-bone immediately above Azorelloideae (Nicolas & Plunkett 2014). Hermas, a South African endemic, has some similarities with Saniculoideae, but it is unlikely to be placed within any currently recognized subfamily (Nicolas & Plunkett 2009); there is some support for a position as sister to [Saniculoideae + Apioideae] (e.g. Nicolas & Plunkett 2014), and I have tentatively placed it there.
For the phylogeny of Azorelloideae, which includes about half the genera that used to be in Hydrocotyloideae, see Downie et al. (1998, 2000a, 2001), Mitchell et al. (1999), Plunkett & Lowry (2001), Henwood and Hart (2001: the Bowlesia clade), Chandler and Plunkett (2004), Andersson et al. (2006) and Nicolas and Plunkett (2009: q.v. for details). Stilbocarpa used to be in Araliaceae, but it is probably sister to the Andean Huanaca. Klotzschia may also belong here, but its position is not stable (see above); this genus aside, Diposis is sister to other Azorelloideae (Nicolas & Plunkett 2009). Azorella is para/polyphyletic with respect to Laretia, Mulinum, and three other genera, in particular, the type of Azorella is rather distant from most of the rest of the genus (Nicolas & Plunkett 2012). Bowlesia lacks petroselenic acid, but it was apparently the only Azorelloideae studied (Kleiman & Spencer 1982).
The monophyly of Saniculoideae (except Lagoecia, now in Apioideae) is upheld in all molecular analyses, and details of relationships within it were suggested by Valiejo-Roman et al. (2002). In some analyses the African ex-hydrocotyloid Arctopus (see Magin 1980 for floral development) is sister to other Saniculoideae, and the woody Steganotaenia and Polemanniopsis, and perhaps Lichtensteinia, are part of the same clade (Downie et al. 2001; van Wyck 2001; M. Liu et al. 2003; Plunkett et al. 2004c; Magee et al. 2010a); at least some of the latter genera have a slightly lignified endocarp, apparently alone in both Saniculoideae and Apioideae (M. Liu et al. 2004). Calviño et al. (2006, esp. 2007: good general discussion of variation), however, expressed reservations about this expanded - and characterless - Eryngioideae, but Calviño and Downie (2007, c.f. Magee et al. 2010a) found that the clade could be circumscribed satisfactorily so long as Lichtensteinia moved to Apioideae; they recognised two tribes, both well supported and with unique indels. A clade including Lichtensteinia and Choritaenia were weakly supported as being sister to other Saniculoideae (Nicolas & Plunkett 2009); although this set of relationships has not been upheld, the monotypic African Phlyctidocarpa does seem to be a member of Saniculoideae, although its exact position there is unclear (Magee et al. 2010a, see also Nicolas & Plunkett 2014). The large genus Eryngium has separate New and Old World clades (Calviño et al. 2008b, 2010); a recent morphological analysis suggested that four unrelated species (in the system later used in the same paper) made up a series of basal pectinations, although there was no strong support for this topology (Wörz 2011).
Relationships at the base of Apioideae are very pectinate and are something like [Lichtensteinia [Annesorhiza clade [Heteromorpheae [Bupleurum + The Rest]]]] (Downie & Katz-Downie 1999; Plunkett et al. 2004; Calviño et al. 2006; Magee et al. 2008, also a revision of Ezosciadium; Magee et al. 2010a; Downie et al. 2010; Nicolas & Plunkett 2014). Apart from the position of Lichtensteinia, in some analyses sister to [Saniculoideae + Apioideae], relationships in Nicolas and Plunkett (2009) are similar; above Bupleurum on the tree was the Mexican Neogoezia. In some analyses the Annesorhiza clade appeared to be allied with Heteromorpheae (including Pseudocarum, which has branching/anastomosing vittae); Bupleurum also has branching vittae and is strongly supported as sister to the remainder of the subfamily (Calviño et al. 2005, 2006). For relationships within Bupleurum, in which the sole South African species is derived and a Mediterranean clade of sometimes shrubby, pinnately-veined taxa is sister to the rest of the genus, see Neves and Watson (2004) and H.-C. Wang et al. (2014). Woodiness in Bupleurum is derived and has evolved several times (H.-C. Wang et al. 2013); Myrrhidendron, from Central America and Colombia, is also woody.
Apioideae also include Lagoecia, with its quite well developed calyx and 1-seeded fruits, which was previously associated with Saniculoideae (Magion 1980). For other relationships within Apioideae, see e.g. Downie et al. (2000a, b, 2001, 2002), Plunkett and Downie (2000: junction of chloroplast inverted repeat/large single copy shifts, characterises clades in part of Apioideae), Spalik and Downie (2001a, b), Sun and Downie (2004, 2010a, b: perennial W. North American Apioideae, morphological and molecular analyses), Sun et al. (2004: Cymopterus and Lomatium about as polyphletic as you can get), Kurzyna-Mlynik et al. (2008: Ferula, somewhat paraphyletic, and relatives), Hardway et al. (2004), Downie et al. (2008) and Spalik et al. (2009: Sium, 2014), all Oenantheae, Zhou et al. (2008: China), Ajani et al. (2008: Iran), Winter et al. (2008: Africa), Sun et al. (2008: Ligusticum in China), Degtjareva et al. (2009: Bunium polyphyletic, monocotyledonous species separate), Magee et al. (2009: especially Cape genera), Magee et al. (2010b - Pimpinella), Logacheva et al. (2010: Tordylieae), Yu et al. (2011: Chinese Heracleum, genus polyphyletic), Valiejo-Roman et al. 2012: Pleurospermum - surprise, surprise, polyphyletic), Angelica and relatives (Liao et al. 2013), Feist et al. (2013: Tauschia), and Degtjareva et al. (2013: Asian geophilic genera).
Classification. The subfamilial classification of Plunkett et al. (2004c) is largely followed here, but some changes will be needed given the positions taken by some ex Hydrocotyloideae in the tree recovered by Nicolas and Plunkett (2009). Downie et al. (2010) build on this earlier classification, suggesting tribes and subtribes for Apioideae, and listing included genera; some groups of genera remain unnamed, and polyphyly is dealt with as satisfactorily as it can be. For tribes in Saniculoideae and in the basal pectinations in Apioideae, see Magee et al. (2010a); five of these latter tribes are new (and all are small) and I have combined Marlothielleae and Choritaenieae, both monospecific, with Lichtensteinieae above; even this expanded Lichtensteinieae can muster only some 10 species.
Classical generic and tribal limits in Apioideae are a notable disaster area. For genera, old style, see Pimenov and Leonov (1993). The traditional tribal and generic classification was based primarily on gross fruit morphology; convergence of fruit architecture as adaptations to modes of fruit dispersal has resulted in many non-monophyletic groupings. Just about all the papers dealing with phylogenetic relationships in Apioideae (see above) have implications for generic limits. For instance, 13/18 genera for which two or more sequences were included in a study by Downie et al. (2000b) were found not to be monophyletic, while Weitzel et al. (2014) include five genera in Thapsia, the deadly carrot, a genus of under 50 species. The problem is further compounded by the disproportionately large number of mono- or di-typic genera (see also Spalik et al. 2001; Valiejo-Roman et al. 2006; Spalik & Downie 2007). It is not that fruit characters never correlate with redrawn generic boundaries (c.f. Feist et al. 2012: rhachis-leaved North American taxa; Liu et al. 2012), but they often mislead when used by themselves and/or without detailed examination of fruit anatomy.
Thanks. I am particularly indebted to Mark Watson for comments on Apiaceae s.l.; mistakes remain mine.