EMBRYOPSIDA Pirani & Prado (crown group)
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; 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, sporangium +, single, with polar transport of auxin, 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]; spores trilete; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the crown embryophytes.
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; 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.
[Hornworts + 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 +); 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, sporangia derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; 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 with xylem and phloem originating on alternate radii, vascular tissue not medullated, 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 first endo- then exosporic, 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 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, becoming 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; embryogenesis cellular; 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.]; (vessels 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 I / LAMIIDAE: loss of introns 18-23 in d copy of RPB2 gene.
[GARRYALES [GENTIANALES [[VAHLIACEAE + SOLANALES] [BORAGINALES + LAMIALES]]]]: G , superposed; loss of introns 18-23 in RPB2 d copy.
[GENTIANALES [[VAHLIACEAE + SOLANALES] [BORAGINALES + LAMIALES]]]: (8-ring deoxyflavonols +); vessel elements with simple perforation plates; nodes 1:1; C forming a distinct tube, initiation late [sampling!]; A epipetalous; (vascularized) nectary at base of G; style long; several ovules/carpel; fruit a septicidal capsule, K persistent.
[[VAHLIACEAE + SOLANALES] [BORAGINALES + LAMIALES]]: chalazal endosperm haustorium +.
[BORAGINALES + LAMIALES]]: iridoids 0; inflorescence cymose; placentation parietal.
LAMIALES Bromhead Main Tree.
Cornoside, verbascosides [caffeoyl phenylethanoid glucosides (CPGs), caffeic acid esters, = acteosides], methyl- and oxygenated flavones +; eglandular hairs multicellular; leaves opposite; K connate; anther sacs with placentoids; cotyledons incumbent; protein bodies in nuclei; mitochondrial coxII.i3 intron 0. - 24 families, 1059 genera, 23810 species.
Age. Estimates of the age of crown-group Lamiales are about 97 m.y. (Bremer et al. 2004).
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. Lamiales contain ca 12.3% eudicot diversity. Most of this diversity is concentrated in families whose members are herbaceous to shrubby and have rather large, monosymmetric flowers, and about half have fruits with many rather small seeds (Sims 2013), and although about half the species have eight or fewer seeds per fruit, they are not very big.
For a useful general discussion, including suggestions of apomorphies for some clades, see Soltis et al. (2005b); Kadereit (2004) provided a summary of the order and its evolution. Endress (2011a) suggested that a key innovation somewhere in Lamiales was tenuinucellate ovules. Monosymmetry is unlikely to be plesiomorphic in the order (c.f. Ronse de Craene 2010 and references). The four clades that are successively sister to other Lamiales either lack iridoids or have iridoids distinctively different (Oleaceae) from those in the other members of the clade, so iridoid (re)aquisition is pegged well within Lamiales; whether or not Carlemanniaceae have iridoids is unknown.
Taxa with 4-merous or predominantly 4-merous flowers are common in the basal pectinations of the Lamiales tree (see also Mayr & Weber 2006). Carlemanniaceae have both 4- and 5-merous flowers, while Calceolariaceae, on the other hand, have 4-merous flowers, each lip representing two completely connate petals, although some have interpreted their flowers as being 5-merous (Mayr & Weber 2006 and references). Floral evolution in basal Lamiales is not simple, and where changes in floral meristicity and floral symmetry are to be placed on the tree is unclear.It has been suggested that families such as Orobanchaceae, Lamiaceae and Acanthaceae form a clade with strongly monosymmetric flowers that mostly lack a staminode (Endress 2001b), but such a grouping is not obviously consistent with the relationships being recovered.
Confirmation of the phylogenetic positions of Carlemanniaceae, placed sister to Oleaceae, and of Plocospermataceae, as well as studies of their anatomy, chemistry, floral development, etc., and also resolution of relationships within Oleaceae, are important for understanding the evolution of the chemistry and floral morphology in particular of Lamiales as a whole (c.f. Endress 2001). Thus, given their position, one might expect Carlemanniaceae to lack iridoids - at least, to lack route II decarboxylated iridoids - and to have only a single (micropylar) endosperm haustorium. As might be anticipated, there is little morphological support for internal nodes in much of Lamiales and also for several of the families, and this is likely to be true whatever the relationships in the order.
For the complex pattern of variation in a number of other characters in this part of the tree, see the Gentianales page.
Bacterial/Fungal Associations. Both parasitic and insectivorous members of Lamiales are largely non-mycorrhizal (Brundrett 2004 and references).
Genes & Genomes. The pattern of duplication of the FLO=LFY and DEF=AP3 genes within Lamiales is largely congruent with the relationships discussed above; duplication occurred in the representatives of Phrymaceae, Verbenaceae, Paulowniaceae and Orobanchaceae examined, but not in those of Plantaginaceae or Oleaceae (Aagard et al. 2005).
Chemistry, Morphology, etc. For other characters that may clarify the relationships of Lamiales, see Gentianales.
A great deal of work on characterising iridoids and understanding their distribution in Lamiales has been carried out by S. R. Jensen and collaborators. The presence of cornosides and iridoids in Lamiales is largely mutually exclusive, except in Martynia louisiana (Jensen 1992, 2000a, 2000b). Verbascoside, a disaccharide derivative of the hydroxycinnamic acid, caffeic acid (= caffeoyl phenylethanoid glycoside), is common. It and trisaccharide derivatives (over 325 structures altogether - S. R. Jensen, pers. comm.) are phenylpropanoid glycosides, a class of compounds usually with a central glucose, a C6C2 unit, commonly dihydroxyphenyl-ß-ethanol, and a C6C3 unit, hydroxycinnamic acid (Mølgaard & Ravn 1988). Such compounds are very rarely found elsewhere; an exception is Cassinopsis (Cometa et al. 1993), which is sister to Icacinaceae s.str. (Byng et al. 2014; Stull et al.).
Nodal anatomy needs study. Neubauer (e.g. 1977, 1978) suggested that the single trace often divided immediately into three or more, and this nodal type is indeed common in the order. Bailey (1956) recorded 2:2 nodes in Lamiaceae, and other nodal morphologies occur, e.g. in Gesneriaceae, Bignoniaceae, etc. Intermediary cells with distinctive plasmodesmata associated with the ultimate leaf veins may be plesiomorphic in Lamiales; their presence is linked with the transport of raffinose and stachyose, oligosaccharides commonly found in phloem exudate in the order (Turgeon et al. 2001; Turgeon 2010a). Leaf teeth have a glandular apex, with one accessory vein proceeding into the tooth, the other going above it.
Taxa with tricellular pollen grains are scattered throughout the order. For integument thickness, for which I have no generally comparable information but which may be of systematic importance, see also Hjertsen (1997) and Fischer (2004b). A chalazal hypostase is common - e.g. Buddleja, some "scrophs" - but the level of this feature is unknown. Oleaceae seem to have a rather diferent embryo development from that of other Lamiales studied (Yamazaki 1974). A long, narrow suspensor may be common in Lamiales (di Fulvio 1979; Maldonado de Magnano 1987), but I do not know the general distribution of this character - it is certainly not found in Loganiaceae. Details of endosperm development and of endosperm haustoria are variable, but there is little obvious phylogenetic signal in the former. Thus endosperm development in Orobanchaceae is overall rather similar - four cells or nuclei at the micropylar end, two at the chalazal - but in Bignoniaceae, Incarvillea differs greatly from the rest, as does Gratiola (PLantaginaceae) from other ex-Scrophulariaceae s.l. (see e.g. Mauritzon 1935; Krishna Iyengar 1940a, 1942 and references). The seed is ruminate in various ways (Hartl 1959, 1965-1974). Seed pedestals, developed from the funicle and/or placenta, are scattered, being known from e.g. Tetrachondraceae, Calceolariaceae, Orobanchaceae and Paulowniaceae (Rebernig & Weber 2007).
For chemistry, see Harborne and Williams (1971: scutellarein, etc.), Zindler-Frank (1978: oxalate accumulation), Young and Siegler (1981: anthraquinones), Mølgaard and Ravn (1988: caffeoyl esters), Tomás Barberán et al. (1988: flavone glycosides), Scogin (1992: acteoside), Jensen (1992), and Grayer et al. (1999: general). For proteinaceous nuclear inclusions, see Bigazzi (1984, 1989a, 1989b, 1993, 1995) and Speta (1977, 1979). Information on a number of families recognised here is to be found under Scrophulariaceae in the old sense - see e.g. Schmid (1906: ovules), Hartl (1956: placentation), and Hartl (1965-1974), Fischer (2004b), and Rahn (1996), all general. For a sumary of inflorescence morphology, see Weber (2013).
Phylogeny. For the relationships of Lamiales, see Refulio-Rodriguez and Olmstead (2014), and discussion under Gentianales.
Oxelman et al. (1999a), Mueller et al. (2001) and Hilu et al. (2001) among others suggested that Plocospermataceae are sister to other Lamiales. Savolainen et al. (2000b, rbcL data alone; see also H.-L. Lee et al. 2007, Plocospermataceae not included) placed Carlemannia as sister to Oleaceae (only 1 species in analysis) with moderate support, and Bremer et al. (2001) found that the two genera formed a sister group that was part of a trichotomy at the base of Lamiales; Oleaceae (Ligustrum only included) and [all other Lamiales] completed the trichotomy, while Plocospermataceae again were not studied. A sister relationship [Carlemanniaceae + Oleaceae] is also supported by Yang et al. (2007: 1.0 p.p., Plocosperma included, but sampling still very poor; Refulio-Rodriguez & Olmstead 2014), and that seems the best place to put the family. The peltate, glandular hairs with unicellular stalks and flowers with two stamens (their position is not entirely certain) also suggest Lamiales, and anatomical features (see below) are consistent with this relationship.
S. Andersson (2006, two genes, sampling poor) found 75% jacknife support for the clade [Calceolariaceae + Gesneriaceae], and 100% support for that clade as sister to remaining Lamiales, even though Mayr and Weber (2006) did not think that the two families were particularly near each other. However, chemistry and morphology also suggest a close relationship between the two, and their position as sister to the remaining Lamiales. Qiu et al. (2010), Soltis et al. (2011) and Refulio-Rodriguez and Olmstead (2014) suggest that Peltanthera may fall outide the [Calceolariaceae + Gesneriaceae] clade (see below, but c.f. Perret et al. 2012).
Relationships in the "Scrophulariaceae" - Acanthaceae - Bignoniaceae - Lamiaceae area have been uncertain for some time, see e.g. Wagstaff and Olmstead (1997), Olmstead et al. (2001), and Xia et al. (2009). B. Bremer et al. (2002) analysed variation in three coding and three non-coding regions of the chloroplast genome; their sampling was sketchy, so the support for some family groupings is difficult to evaluate; Freeman and Scogin (1999) focussed on the old Scrophulariaceae, but the pattern of relationships they found was unclear. A tree in Müller et al. (2004) suggested that at least a partial resolution of relationships was in sight, although sampling was again poor (this study focused on Lentibulariaceae); the three families then known or suspected to be carnivorous (Byblidaceae, Lentibulariaceae and Martyniaceae) were not immediately related. Rahmanzadeh et al. (2004), Albach et al. (2005) and Oxelman et al. (2005) began to clarify the contents of the separate clades that used to be subsumed in Scrophulariceae s. l. (see also Tank et al. 2006 for a summary). Thomandersia, from tropical Africa, previously usually included in Acanthaceae, appeared to go near Schlegeliaceae, however, support for this association was weak (Wortley et al. 2005a and especially 2007a). Thomandersia may also go somewhere near Schlegeliaceae, from tropical America. Characters like the vasculature of the floral nectary and petiole, also the nectaries on the outside of the calyx, might link it with that family, however, support for any Thomandersiaceae-Schlegeliaceae association is weak (Wortley et al. 2007a).
Lamiaceae and Verbenaceae were initially separated on the distinctions more or less herbaceous vs. more or less woordy and style (often) gynobasic vs style terminal. However, gynoecial morphology had long suggested (Junell 1934) a separation along the lines of those followed today: inflorescence branches cymose vs inflorescence racemose and stigma bifid vs. more or less capitate. Many Lamiaceae have a single layer of sclerenchymatous, bone-shaped cells on the inside of the mesocarp, others have thicker pericarp walls, and the cells are often crystalliferous, while the pericarp anatomy of Verbenaceae is more complex (Ryding 1995). There may be differences in seed coat anatomy: the testa of at least some Verbenaceae has the hypodermal layer(s) thickened, while in Lamiaceae it is the exotestal cells that are thickened, particularly on their inner periclinal and anticlinal walls (Rohwer 1994a). The molecular relationships of Verbenaceae s. str. and Lamiaceae were for a time unclear (e.g. Olmstead et al. 2001, only one member of each sampled); see Wagstaff & Olmstead (1997) for more information. Petraea (Verbenaceae) was sister to Bignoniaceae in some early molecular phylogenies (Wagstaff & Olmstead 1997), similarly, Nie et al. (2006) linked Verbenaceae with Bignoniaceae, and Phrymaceae went with Paulowniaceae. Phrymaceae are cladistically closest to Paulowniaceae (see below , although they were included in Verbenaceae by Cronquist (1981) and others in the past, in part because they have a similar racemose inflorescence and gynoecium (see Cantino 2004). Indeed, the gynobasic style and four nutlets that were supposed to characterize Lamiaceae may have evolved more than once (Cantino 1992a), and a considerable number of ex-Verbenaceae are now included in Lamiaceae (Cantino et al. 1992a, b).
Amyloid is found in both Pedaliaceae and Acanthaceae, a family that has sometimes been weakly associated with Pedaliaceae in molecular analyses (Soltis et al. 2005b and references), and both Martyniaceae and Pedaliaceae, perhaps not immediately related, have 10-hydroxylated carboxylic iridoids. However, Refulio-Rodriguez and Olmstead (2014) link all three families, although support is weak. Byblidaceae may be sister to Lentibulariaceae (e.g. Albert et al. 1992), although Müller et al. (2004) found no association between the two, nor of either with any Lamiales with viscid indumentum like that of Martyniaceae and Pedaliaceae, a feature which could perhaps be considered to be "precursory" to insectivory. On the other hand, Müller et al. (2004) found a weak association of Lentibulariaceae and Bignoniaceae. Soltis et al. (2007a) found few strongly supported relationships in the bulk of the order; Wortley et al. (2005b), who had sequenced over 4600 bp, estimated that at least 10000 bp more would need to be added to resolve relationships within the clade.
Although focusing on Triaenophora (ex "scroph", now Orobanchaceae s.l.), the relationships that Albach et al. (2009) found are broadly consistent with those suggested by others and the phylogeny of Schäferhoff et al. (2010), in part followed here, The bulk of the free-living Scrophulariaceae are paraphyletic at the base of the iridoid-containing clade of Lamiales, Lamiaceae and Verbenaceae not sister taxa, the insectivorous and putatively insectivorous clades in Lamiales are all unrelated, etc. (Schäferhoff et al. 2010). The recent discoveries of Pereira et al. (2012) have added another phylogenetically isolated carnivorous clade (in Plantaginaceae). Albach et al. (2009) cast doubt on the monophyly of Phrymaceae (see also Schäferhoff et al. 2010); taxon limits in this area have had to be narrowly drawn, the result of keeping Orobanchaceae separate. The tree still lacked resolution, especially around the Bignoniaceae-Verbenaceae area.
Recent findings by McDade et al. (2012: focus on Acanthaceae) apparently contradict part of the tree found by Schäferhoff et al. (2010). In particular, Byblidaceae, Stilbaceae and, surprisingly, Thomandersiaceae all occur on the tree between Plantaginaceae and Scrophulariaceae (support is strong), and Linderniaceae are sister to Scrophulariaceae (support is weak). Although Bell et al. (2010) recovered a clade [Oleaceae [Byblidaceae, Plantaginaceae, The Rest (including Gesneriaceae)]], support along the spine was rather weak for the most part. On the other hand, Perret et al. (2012: focus on Gesneriaceae) found relationships more similar to those in Schäferhoff et al. (2010), although the two carnivorous clades Byblidaceae and Lentibulariaceae were sister taxa.
Refulio-Rodriguez and Olmstead (2008: summary) suggested that substantial progress in disentangling relationships around Lamiacae-Verbenaceae and Scrophulariaceae s.l. might be on the horizon (see also Xia et al. 2009). Details of their findings (Refulio-Rodriguez & Olmstead 2014) largely agree with those of Schäferhoff et al. (2010), although more genes were analyzed and support values are usually higher. In particular, nodes along the back-bone of the tree up to [Stilbaceae + The rest] all have very strong support. Resolution along much of the rest of the backbone remains weak, and family groupings also have little support. The family groupings in the part of the tree [Byblidaceae + The Rest] are those of Refulio-Rodriguez and Olmstead (2014), but for the most part they await confirmation.
A clade including Lamiaceae, Orobanchaceae, etc., was retrieved by McDade et al. (2012), although many of the internal support values were low. It had moderate-good support in Refulio-Rodriguez and Olmstead (2014), and with rather higher internal support values. Genera are still being added to this clade, and relationships within it are not entirely clear; for further discussion, see below.
Two other genera have sometimes been associated with Lamiales. Lens et al. (2008a) and Weigend et al. (2013b) suggested that Vahlia was sister to all other Lamiales, although support was weak and Plocosperma was not included. However, Vahlia is more likely to be sister to Solanales (Refulio-Rodriguez & Olmstead 2014), and that is where it is provisionally placed. The position of Hydrostachys within the asterids has also not been easy to determine. Here it is included in Cornales, and there is a discussion of its relationships there; Burleigh et al. (2009) suggested that it is a member of Lamiales, and indeed its morphology is in general agreement with such a position. If it should end up in Lamiales, it is likely to be towards the basal part of the tree.
Classification. R. Olmstead (pers. comm.) has been compiling a synoptical classification of Lamiales from which some of the numbers of taxa included in the families below are taken. The limits of families like Scrophulariaceae have long been problematic (Thieret 1967 for a summary), and Olmstead (2002) provided a readable account of some of the changes in our ideas of relationships in the Scrophulariaceae s.l. in particular.
Despite the lack of morphological support for some of the families, little is to be gained and more lost if their limits are much expanded.
Includes Acanthaceae, Bignoniaceae, Byblidaceae, Calceolariaceae, Carlemanniaceae, Gesneriaceae, Lamiaceae, Lentibulariaceae, Linderniaceae, Martyniaceae, Mazaceae, Oleaceae, Orobanchaceae, Paulowniaceae, Pedaliaceae, Peltanthera, Phrymaceae, Plantaginaceae, Plocospermataceae, Schlegeliaceae, Scrophulariaceae, Stilbaceae, Tetrachondraceae, Thomandersiaceae, Verbenaceae.
Synonymy: Acanthales Berchtold & J. Presl, Antirrhinales Döll, Aragoales D. Don [?status], Bignoniales Berchtold & J. Presl, Byblidales Reveal, Callitrichales Link, Carlemanniales Doweld, Fraxinales Berchtold & J. Presl, Gesneriales Berchtold & J. Presl, Globulariales Dumortier, Hippuridales Link, Jasminales Berchtold & J. Presl, Lentibulariales Berchtold & J. Presl, Ligustrales Bischof, Myoporales Berchtold & J. Presl, Oleales Berchtold & J. Presl, Orobanchales Berchtold & J. Presl, Pedaliales Berchtold & J. Presl, Pinguiculales Dumortier, Plantaginales Berchtold & J. Presl, Rhinanthales Dumortier, Scrophulariales Lindley, Selaginales Martius, Stilbales Martius, Utriculariales Döll, Verbascales Döll, Verbenales Berchtold & J. Presl, Viticales Link (?status]
PLOCOSPERMATACEAE Hutchinson Back to Lamiales
Shrubs or trees; cork?; vessels in radial multiples; large groups of fibres in outer cortex at nodal region; petiole bundle annular; styloids +; hairs unicellular, calcified and/or with cystoliths, also bicellular, club-shaped, glandular; cuticle wax crystalloids 0; petiole articulated near base; plant cryptically dioecious; inflorescences axillary; bracteoles 0; flowers 5-6-merous; staminate flowers: anthers extrorse, versatile, with largely separate thecae; nectary 0; pistillode +; carpellate flower: staminodes +; nectary +; stylar fusion postgenital, style divided twice, stigmas not expanded; ovules 2/carpel; seeds with tuft of hairs at chalazal end, hairs multicellular; coat ?; endosperm ?development, slight; n = ?; protein bodies in nucleus?
1[list]/1: Plocosperma buxifolia. Central America (map: from Leeuwenberg 1967).
Chemistry, Morphology, etc. Plocospermataceae are poorly known. Jensen (1992) recorded verbascosides and cornoside from Plocosperma, but not iridoids.
Struwe and Jensen (2004) described the inflorescence as being a congested raceme or dichasium, and this, and the apparent absence of nectaries in the staminate flowers, should be confirmed. For ovule position, see (Leeuwenberg 1967).
See also D'Arcy and Keating (1973: as Lithophytum, esp. anatomy), Jensen (1992: chemistry), M. Endress et al. (1996), and Struwe and Jensen (2004), both general, for information.
Previous Relationships. Plocospermataceae were included in Gentianales by Takhtajan (1997), probably because Plocosperma had long been associated with Loganiaceae. Cronquist (1981) included the genus in his Apocynaceae, probably because of the hairs on its seeds.
[[Carlemanniaceae + Oleaceae] [Tetrachondraceae [[Peltanthera [Calceolariaceae + Gesneriaceae]] [Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]]]]: cells in heads of glandular hairs with vertical walls only; flowers 4-merous [?: reverses to 5-merous....]; placentation axile.
Age. Bell et al. (2010) estimated the age of this node to be (78-)74, 69(-61) m.y., Janssens et al. (2009) give a date of 95±11.9 m.y., while Magallón and Castillo (2009) offer estimates of ca 62.8 m.y.; at around 53.9 m.y.a., the estimate by Naumann et al. (2013) is the youngest.
Chemistry, Morphology, etc. Note that the arrangement of the sepals (and petals) is orthogonal in Oleaceae and Calceolariaceae, while that of Tetrachondraceae (and of 4-merous Veronica) is diagonal (Mayr & Weber 2006).
[Carlemanniaceae + Oleaceae]: C valvate; A 2; pollen tricolpate; stigma ± clavate; exotestal cells ± palisade, endothelium persistent.
CARLEMANNIACEAE Airy Shaw Back to Lamiales
Perennial herbs or shrubs; chemistry?; vessel elements with simple perforations; pericyclic fibers few; nodes?; cuticle waxes 0; lamina margins toothed; inflorescences terminal and axillary; flowers weakly obliquely monosymmetric, 4- or 5-merous, (heterostylous - Silvianthus); K members unequal or not, ± linear, aestivation open?, C aestivation induplicate-valvate; anthers connivent around the style, latrorse, ?attachment; ovary inferior, nectary on top, style clavate; many ovules/carpel; fruit fleshy-capsular, loculicidal or 5-valved [valves correspond to calyx segments, opening widely, exposing the placenta - Silvianthus], K persistent; exotestal cells with radial walls thickened, interior cells unthickened, or polygonal, all walls thickened [Carlemannia], (endothelium persistent - Silvianthus); endosperm +, ruminate [Silvianthus], embryo small; n = 15, 19; protein bodies in nucleus?
2[list]/5. E. Nepal eastwards to Myanmar, Thailand, Laos, Vietnam, S.W. China, Sumatra (map: Fl. China 19. 2011).
Chemistry, Morphology, etc. Carlemanniaceae are very largely unknown. Even fruit dehiscence does not really make sense - 5 valves from a two-carpellate gynoecium?
Some information is taken from Tange (1999); Thiv (2004) provides a general account, and Yang et al. (2007) information on chromosome numbers, etc.
Previous Relationships. Carlemanniaceae have usually been associated with Caprifoliaceae or Rubiaceae in the past. However, characters such as superficial cork, two stamens with connivent anthers and two carpels each with many ovules would remove Carlemanniaceae from Caprifoliaceae, and the toothed, exstipulate leaves, 2 stamens, anomocytic stomata, and absence of raphides from Rubiaceae (Solereder 1893; Airy Shaw 1965). Carlemanniaceae were included in Caprifoliaceae by Cronquist (1981) and in Rubiales by Takhtajan (1997).
OLEACEAE Hoffmannsegg & Link, nom. cons. Back to Lamiales
Woody; route I iridoids [deoxyloganic acid, loganin, etc. precursors], verbascoside or variants, myricetin, orobanchin, mannitol +; wood with minute calcium oxalate crystals; (vessel elements with scalariform perforation plates); fibre tracheids +; libriform fibres 0; foliar crystals of various types, inc. styloids and raphides (0; druses); petiole bundle arcuate; sclereids + (0); cuticle deeply furrowed (waxes ribbons, platelets); (serial [superposed] axillary buds +); branching from previous innovation; leaf margins entire to toothed, (secondary veins palmate); flowers 4-merous; K valvate, initiation orthogonal; anther thecae ± back-to-back; pollen (grains tricellular); (style short), stigma dry; ovules apical, (hemitropous), epitropous or apotropous, integument ca 7 cells across, (postament +); testa often vascularized, exotesta moderately and evenly thickened, (endotesta fibrous; endothelium ?not persistent); endosperm +/0; protein bodies in nuclear crystalline-globular; 9 bp deletion in ndhF.
24[list]/615 - five tribes below. More or less worldwide, especially East Asia (map: from Meusel et al. 1975; Australia's Flora Online xii.2012).
1. Myxopyreae Boerlage
Myxopyroside iridoids [carbocyclic]; inverted cortical bundles in corners of angled stem (Dimetra not); petiole bundles three, arcuate; (K initiation diagonal, C contorted, early tube formation - Nyctanthes); (G collateral); placentation ± basal; ovules 1(-3)/carpel, integument to 20 cells across [Nyctanthes]; (megaspore mother cells several, embryo sac bisporic, 8-nucleate [Allium type]); fruit a berry or schizocarp; n = 11, 12.
3 (Myxopyrum, Dimetra, Nyctanthes)/7. Indo-Malesia.
Synonymy: Nyctanthaceae J. Agardh
2. Fontanesieae L. Johnson
Route 1b iridoids [carbocyclic and seco-iridoids]; pits ± vestured; petiole bundle annular; C free, imbricate; ovule 1/carpel; fruit a samara; n = 13.
1/2. Sicily, W. Asia, China.
3. Forsythieae L. Johnson
Cornosides, (route 1b iridoids - forsythide (carbocyclic)) +; pith chambered; ovules 1-several/carpel; fruit a samara or capsule; n = 14.
2/8. S.E. Europe, East Asia.
[Jasmineae + Oleeae]: route 1b/1c irioidoids [secoiridoids - oleoside]; leaves odd-pinnate to simple; ovules 2(-4)/carpel; fruit fleshy.
Age. The age of this node may be (52-)48, 39(-35) m.y. or (Wikström et al. 2001) or (62-)45, 41(-24) m.y. (Bell et al. 2010).
4. Jasmineae Lamarck & Candolle
(K, C to 14 or more), first 4 K initiation diagonal, C quincuncial-imbricate, tube formation early; endothelium 0; (megaspore mother cells several, several elongated embryo sacs developing); fruit bilobed, berry or circumscissile capsule; seed coat multilayered, mesotesta with wholly thickened or band-thickened anticlinal walls; n = 11-13; 21kb chloroplast inversion.
1/225-450 (Jasminum: inc. Menodora). Tropical to warm temperate Old World, some in America. [Photo - Flower]
Synonymy: Bolivaraceae Grisebach, Jasminaceae Jussieu
5. Oleeae Dumortier
Flavone glycosides +; vessel elements in multiples; (pits vestured); libriform fibres + (0); fibre tracheids 0 (+); marginal parenchyma +/0; (indumentum of peltate scales); lamina (with flat abaxial glands - Ligustrum), vernation conduplicate [Chionanthus]; (plant dioecious); K (diagonal), (open), C valvate, (imbricate; free; 0), tube formation late (early - Ligustrinae); (A 4 - e.g. Nestegis); (fruit a samara); n = (20) 23.
17/415: Noronhia (105), Chionanthus (60-120), Fraxinus (45-65), Ligustrum (50), Olea (33). Tropical and subtropical, inc. New Zealand and Hawaii.
Synonymy: Forestieraceae Meisner, Fraxinaceae Vest, Ligustraceae G. Meyer, Schreberaceae Schnizlein, Syringaceae Horaninow
Evolution. Divergence & Distribution. Samaras of Fraxinus have been reported from Eocene deposits some 44 m.y.o. (Call & Dilcher 1992).
Much diversification within Oleaceae occured during the Tertiary (Besnard et al. 2009a).
Pollination Biology & Seed Dispersal. For the evolution of wind pollination, dioecy, etc., in Fraxinus, see Wallander (2013).
Plant-Animal Interactions. Caterpillars of some Sphinginae are quite common on Oleaceae (and the same genera may also be on Solanaceae: Forbes 1958).
Genes & Genomes. For the reorganization of the platid genome in Jasminum s.l., see H.-L. Lee et al. 2007). The chloroplast gene accD (= ORF512, zpfA) has been lost (Doyle et al. 1995 and references) in at least some Oleaceae.
Chemistry, Morphology, etc. The route I secoiridoids are unlike other route I secoiridoids, e.g. those in Gentianaceae (Jensen 1992; Jensen et al. 2002). Damtoft et al. (1995) noted that the secoiridoids of Fontanesia (loganic acid, etc., and 5-hydroxylated derivates like swertiamarin) were produced by a somewhat different biosynthetic pathway than the oleoside-type secoiridoids common elsewhere in the family. Abeliophyllum, in a clade possibly sister to rest of Oleaceae, has cornosides and verbascosides, and some lack iridoids; these features may be plesiomorphies (but certainly not if Myxopyreae are sister to the rest of the family - see below), but absence (= loss) or iridoids occurs elewhere in the family (Jensen et al. 2002). There is a single report of cornosides from the [Jasmineae + Oleeae] clade (Jensen et al. 2002).
At least some species of Osmanthus have a lignified, torus-bearing, pit membrane (Coleman et al. 2004: Dute et al. 2010b). Govil (1973) showed how the lateral bundles of the petiole in Nyctanthes were derived from the cortical vascular system. The diversity of crystal types in the vegetative plant (other than the wood) is very great, but druses, the common crystal form in which calcium oxalate occurs, are uncommon (Lersten & Horner 2008a, 2009a, esp. b). Crystals are often clustered in epidermal cells at the bases of trichomes, an unusual distribution pattern (Lersten & Horner 2009b). Groups of few-celled secretory hairs may form extrafloral nectaries (Zimmermann 1932).
The calyx is sometimes diagonally oriented (Sehr & Weber 2009). There is variation in corolla tube initiation, both early and late initiation being known in the family (Sehr & Weber 2009). Nectar is reported to be secreted from the ovary in Syringa and Ligustrum (Weberling 1989). Osmophores are common and their absence from the anthers may be of systematic interest (Nilson 2000: sampling?); orbicules may be absent (Vinckier & Smets 2002a). There is infrageneric variation in the orientation of the two carpels; however, the two stamens are always borne in the plane of the ovary septum (Eichler 1874). Baillon (1891) illustrated both epitropous and apotropous ovules.
For more information, see Green (2004: general), Jensen et al. (2002 and references: iridoids), Baas et al. (1988: wood anatomy), Song and Hog (2012: some petiole anatomy, Naghiloo et al. (2013: inflorescence morphology), Sehr and Weber (2009) and Dadpour et al. (2011), both floral ontogeny, the latter also some inflorescence morphology. Bigazzi (1989a: protein nuclear inclusions), Kiew and Baas (1984) and Rohwer (1994b: both Nyctanthes), Andersson (1931), Kapil and Vani (1966) and Maheswari Devi (1975), all embryology, and Rohwer (1993b, 1996: fruit and seed).
Phylogeny. Wallander and Albert (2000: some morphology also) found that the tribes above had strong support, but that there was a basal polytomy. H.-L. Lee et al. (2007), however, found Myxopyreae to be sister to the rest of the family (100% bootstrap support), with Fontanesieae, Forsythieae and [Jasmineae + Oleeae] forming a tritomy; they emphasized the complex pattern of chloroplast inversions in Jasmineae. Kim and Kim (2011) suggested a quite well supported set of groupings [[Fontanesieae + Jasmineae] [Oleeae + Forsythieae]]; unfortunately, they did not sample other members of the family.
Franzyk et al. (2001) noted that Myxopyrum and Nyctanthes, both in Myxopyreae, had similar iridoids. Besnard et al. (2009a) and Guo et al. (2011) examined relationships in some Oleeae, while Hong-Wa and Besnard (2013, see also 2014) found considerable geographical signal in the clades they obtained in a study of relationships around Noronhia and other Oleinae - although polyploidy presented a problem in their analysis. For the phylogeny of Fraxinus, see Wallander (2013 and references).
Classification. The tribes recognised above are those of Wallander and Albert (2000). Generic limits in Oleeae in particular need much attention; Olea itself, Osmanthus, and Chionanthus are all polyphyletic (Besnard et al. 2009a; Guo et al. 2011). Thus Chionanthus had included Linociera, but this is questionable; Hong-Wa and Besnard (2013) have begun the necessary process of generic realignment.
Previous Relationships. The position of Nyctanthes has been uncertain, and it was often included in Verbenaceae in the old sense; Filonenko et al. (2010) considered the genus to be separate from both families.
[Tetrachondraceae [[Peltanthera [Calceolariaceae + Gesneriaceae]] [Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]]]: plants ± herbaceous; C and A initiated simultaneously, or A before the C; seeds <4 mm long; endosperm also with chalazal haustoria; deletion in the matK gene.
Age. The age of this node is around 87 m.y. (Bremer et al. 2004).
Chemistry, Morphology, etc. For information on the matK deletion, see Hilu et al. (2000); the sampling needs to be improved.
TETRACHONDRACEAE Wettstein Back to Lamiales
Creeping to erect herb; sorbitol +; cork?; nodes split laterals; hairs moniliform [Polypremum], leaves amphistomatic; leaf bases connate or connected by membranaceous stipules; (inflorescence of 1-2 axillary flowers - Tetrachondra), bracteoles two or more pairs; flowers rather small [<5 mm across], 4-merous; K initiation diagonal [Polypremum], C with very short tube; stamens free, ?thecae; pollen in tetrads, 6-sulcate, psilate; nectary 0; G transverse [when 2 pairs bracteoles], (ovary 4 partite, slightly inferior, placentae peltate - Polypremum), style (gynobasic - Tetrachondra), (0 - Polypremum), stigma small, subglobose; ovules (2/carpel, basal - Tetrachondra), or many, integument 3-4 cells across [Polypremum]; fruit with persistent green K, either a schizocarp, or a loculicidal (+ septicidal) capsule, seed pedestals +; testa thin, endothelial cells with persistent thickened inner walls; endosperm copious; n = 10, 11, protein bodies in nucleus?
2[list]/3. Patagonia, New Zealand (Tetrachondra), S. U.S.A. to South America (Polypremum procumbens) (map: from Fl. Neotrop v. 81. 2000). [Photo - Polypremum Flower.]
Age. Crown-group Tetrachondraceae are ca 46 m.y.o. (Bremer et al. 2004).
Evolution. Divergence & Distribution. Wagstaff et al. (2000) found that the sequences of the two species of Tetrachondra, from the Antipodes and S. South America, were almost identical - the distribution is probably recent.
Chemistry, Morphology, etc. Polypremum has both micropylar and chalazal endosperm haustoria; this should be checked in Tetrachondra, a very poorly known genus. The embryo sac of Polypremum protrudes through the nucellar epidermis (Moore 1948).
For general information, see Wagstaff (2004a), some additional information is taken from Mayr & Weber (2006), and Sehr and Weber (2009), also chemistry (Harborne & Williams 1971 - scutellarein +, c.f. Gelsemium!; Jensen 2000a), endothelium presence (absent in Loganiaceae), endosperm type, etc., of Polypremum are right for position in Lamiales.
Phylogeny. The [Polypremum + Tetrachondra] clade is strongly supported (Oxelman et al. 1999a); see also Wagstaff et al. (2000).
Previous Relationships. Tetrachondra was placed in Boraginales by Takhtajan (1997: two ovules/carpel, gynobasic style in common) and in Lamiaceae by Cronquist (1981: ditto). Polypremum has always been associated with Loganiaceae s.l.; Takhtajan (1997) included it in his Buddlejaceae.
[[Peltanthera [Calceolariaceae + Gesneriaceae]]] [Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]] / Core Lamiales: shikimic-acid derived anthraquinones, 6- and/or 8- hydroxylated flavone glycosides + [? Tetrachondraceae], storage substances stachyose and other oligosaccarides; flowers vertically monosymmetric; K ± asymmetric, C usu. ± bilabiate, 2-lobed upper lip, 3-lobed lower lip [= 2:3], adaxial lobes outside the others in bud [ascending cochleate], tube formation late; A 4, didynamous, placentoids +; pollen tubes lacking callose [?level]; ovules many/carpel; second division of the endosperm longitudinal, suspensor large.
Age. Bell et al. (2010: note topology) estimated an age of (72-)64, 61(-56) m.y. for this node; the age in Bremer et al. (2004) is around 78 m.y. and in Wikström et al. (2001: note topology) it is (60-)56, 45(-41) m.y. old.
Evolution. Divergence & Distribution. Martínez-Millán (2010), using a rather scanty fossil record, suggested an Oligocene age for diversification within Lamiales - this would be this node, since fossil Oleaceae are known from the Eocene.
This clade includes the bulk of the diversity within Lamiales. Many of its members are herbaceous or shrubby and have often quite large monosymmetric, bilabiate flowers, and about equal numbers of species have fruits with many small seeds or with about eight or fewer (but still not very big) seeds. A didynamous androecium, with stamens in two pairs of unequal lengths, is common; the fusion, or at least close attachment, of the paired anthers may improve pollen removal from the flower (Ren & Tang 2010). The evolution of monosymmetric flowers may be a key innovation in Lamiales (Endress 2011) and would be pegged to this level, but this monosymmetry is not a simple character. Furthermore, if the position of Peltantha, with five stamens and a more or less polysymmetric flower, is confirmed (see below), optimisation becomes interesting.
Genes & Genomes. It appears that CYC genes have duplicated independently within the clade and become separately involved in the development of the strongly monosymmetric flowers of Antirrhinum, Mimulus and Gesneriaceae (e.g. Damerval & Manuel 2003; Gübitz et al. 2003; Preston et al. 2011b).
Chemistry, Morphology, etc. For callose, see Prospéri and Cocucci (1979: Oleaceae, etc., not sampled, ?Gesneriaceae). For the distribution of various flavone glycosides, see Tomás-Barberán et al. (1988): Mimulus and Orobanche lack the glycosides of Lamiaceae, Verbenaceae, Scrophulariaceae and Plantaginaceae, while those of Lentibulariaceae are somewhat different, variation broadly consistent with phylogenetic relationships here.
Westerkamp and Claßen-Bockhoff (2007) outline the morphological variation in the corolla. Monosymmetry of the 2:3 type is common and there are four stamens which are often didynamous and sometimes with connivent anthers; for staminodes and stamen reduction in general, see Endress (1998) and Song et al. (2009: molecular mechanisms). Nectary vascularization varies. Nectaries may be vascularized by branches from the main carpellary vascular traces, as in Schlegeliaceae, some Pedaliaceae, Verbenaceae, or separately from the gynoecium, as in Bignoniaceae, Acanthaceae, other Pedaliaceae. This variation suggests that either the distinction between gynoecial and receptacular nectaries (Smets 1988; Smets et al. 2003) is overly simplistic and/or there is homoplasy in this feature. There are septal vascular bundles, the gynoecial vascular system forming a sort of figure of 8 in transverse section, in Bignoniaceae and Schlegeliaceae, while in taxa like Acanthaceae there are no septal bundles, the gynoecial vasculature being almost in a circle (there are of course placental bundles: see Wortley et al. 2005a for details). Knowledge of the distribution of this character needs to be extended. The level at which to peg the character "embryo suspensor large" is unclear. There is much about ovules, seeds, etc. on various taxa, esp. Scrophulariaceae sensu latissimo and Lentibulariaceae, in Takhtajan (2013).
[Peltanthera [Calceolariaceae + Gesneriaceae]]: ?
Age. The age for this node is ca 71 m.y. (Bremer et al. 2004).
Phylogeny. Peltanthera has been placed with Gesneriaceae (e.g. Oxelman et al. 1999a; see also Clark et al. 2010), and is perhaps to be included in Gesneriaceae, but c.f. Soltis et al. (2011). More recently Perret et al. (2012), in a study focusing on Gesnerioideae, found the well supported clade [Peltanthera [Sanango + Gesneriaceae s. str.]]. However, Refulio-Rodriguez and Olmstead (2014) found strong support for the position of Peltanthera as sister to the whole group, a relationship that is followed here.
Chemistry, Morphology, etc. See Weber (2013) for inflorescence morphology; the ultimate units of the inflorescence of Peltanthera are not so very different from the pair-flowered cymes that characterize the rest of the clade.
Peltanthera Bentham Back to Lamiales
Small tree; verbascosides, cornoside derivatives +; nodes 3:3; petiole bundle ± flattened-annular, with (medullary and) wing bundles; lamina bundle sclerenchyma slight; hairs branched-moniliform; leaves not joined at the base; lamina vernation involute; inflorescence axillary, much branched; flower ± polysymmetric, "small" [<5 mm long], bracteoles 0; K ± free, C valvate; A 5, anther thecae confluent, appearing to be peltate; nectary small; stigma capitate; capsule loculicidal; seeds dust-like, cells in longitudinal rows, longitudinally ridged [from cell walls]; n = ?
1/1: Peltanthera costaricensis. Costa Rica to Bolivia (Map: from Fl. Neotrop. v. 81. 2000; TROPICOS ii.2013).
Chemistry, Morphology, etc. See Hunziker and di Fulvio (1957) and Norman (2000) for general information, Carlquist (1997c) for wood anatomy, and Jensen (2000a) for chemistry. A poorly known species.
[Calceolariaceae + Gesneriaceae]: leaves rather soft, leaf bases joined by a slight ridge, lamina margin serrate; inflorescence branches pair-flowerered cymes; endothelial cells in longitudinal rows; endosperm longitudinally furrowed [aulacospermous].
Age. The age for this node is (108.6-)87.7, 46.7(-26.2) m.y. (Nylinder et al. 2012).
Chemistry, Morphology, etc. In paired-flower cymes the two flowers of the flower-pair have the same orientation. It has been suggested that the flower in front of the terminal flower is sometimes subtended by a "bracteole", and this may represent the bract of that flower, the flower opposite it being totally suppressed; what appears to be a rather strange dichasial cyme is then a modified "panicle" (Weber 1973; Haston & Ronse De Craene 2007). Both Calceolariaceae and Gesneriaceae have at least some taxa with septicidal capsule dehiscence, but how the distribution of this character might appear on a combined tree of the two is unclear.
CALCEOLARIACEAE Olmstead Back to Lamiales
Herbs to shrubs; cork?; nodes 1:1; pericyclic fibres 0; petiole bundle(s) arcuate; (lamina margins entire); flowers 4-merous, strongly monosymmetric; K orthogonal, valvate, C bilabiate, abaxial lobe saccate, (adaxial "lip" strongly bilobed - Calceolaria triandra), elaiophores on inside of abaxial lip [pads of hairs] (0); A 2 [lateral pair] (3 [inc. abaxial member - C. triandra]), thecae (parallel) divergent, confluent on dehiscence or not, (theca 1), staminodes 0; nectary 0; (G semi-inferior), stigma small or capitate or obscurely bilobed; ovules with integument 3-4 cells across; capsule both septicidal and loculicidal; seed pedestals +; testa with anticlinal walls sinuous (straight); endosperm +; n = (8) 9.
2[list]/260: Calceolaria (240-270). Upland tropical and W. temperate South America, Brasil, also New Zealand (some Jovellana) (map: from Sérsic 2004). [Photo - Habit, Flower.]
Age. Crown group diversification began (27-)15(-4) m.y.a. (Renner & Schaefer 2010) or (51.3-)30.8, 12.9(-5.1) m.y. (Nylinder et al. (2012).
Evolution. Divergence & Distribution. The bulk of the diversity in the family is included in Calceolaria, and Calceolaria crown group age may be as little as (6-)5(-1) m.y. (Renner & Schaefer 2010), while within Jovellana mean ages for the split between the South American and New Zealand clades range from 9.3-5.3 m.y. - probably long distance dispersal was involved (Nylinder et al. 2012).
Pollination Biology & Seed Dispersal. Pollination in Calceolaria has been studied in detail by Rasmussen and Olesen (2000) and Sérsic (2004). Sternotribic flowers pollinated by Centris bees seem to be plesiomorphous in Calceolaria; species with this and some other morphological features are diploid and have a geographic range that is basically Chilean (Cosacov et al. 2009). Smaller Chalepogenus bees are the other main pollinators (both are anthophorids). Flowers with a closed mouth are visited by larger bees, those with an open mouth by smaller bees; Bombus and Xylocopa visit flowers that lack oil. Visitors remove either oil from oil glands or from specialised hairs, or pollen if there are no oil glands; specialised food bodies on the lower lip are the reward for species that are pollinated by non-nectarivorous birds like the fruit- and seed-eating charadriform Thinocorus rumicivorous (Vogel 1974; Sérsic & Cocucci 1996; Rasmussen & Olesen 2000). All told, about 4/5 of the genus have oil flowers (Sérsic 2004), and the ability to produce oil has been lost several times (Renner & Schaefer 2010). Oil glands may have been acquired any time after the split of Calceolaria from Jovellana, which lacks oil glands, i.e., after the crown group age for the whole family (see above: Renner & Schaefer 2010), and it has been suggested that the development of nototribe pollination mechanisms was a key innovation (Cosacov et al. 2009).
Chemistry, Morphology, etc. There has been much discussion over the basic floral meristicity, but flowers in the family seem to be best interpreted as being 4- rather than modified 5-merous (Mayr & Weber 2006: superb micrographs; c.f. e.g. Sérsic 2004). From vasculature, etc., each lip of the flower seems to be formed from two petals; these primordium pairs may become connate only rather late in floral development (Mayr & Weber 2006). For floral development, see also Endress (1999).
Some information is taken from Weber (1973: inflorescence) and Molau (1988), Ehrhart (2000), and Fischer (2004b), all general, in Scrophulariaceae; see also Tank et al. (2006).
Phylogeny. For a phylogeny of the family, see S. Andersson (2006).
Classification. Porodittia, with three stamens, is a synonym of Stemotria, but neither name is needed as Stemotria is clearly derived from within Calceolaria, thus P. triandra = C. triandra (S. Andersson 2006). The limits of the sections need adjusting.
Thanks. I am grateful to Pamela Puppo for comments.
GESNERIACEAE Richard & Jussieu, nom. cons. Back to Lamiales
Distinctive verbascosides [e.g. sanangoside]; nodes trilacunar or thereabouts; petiole bundle annular; stomata anisocytic; A 4 + staminode.
147(+)[list]/ca 3460 - three main groups below. Largely tropical.
Age. The age for this node is (68.1-)57.5(-45.1) m.y. (Perret et al. 2012).
1. Sanangoideae A. Weber, J. L. Clark & Mich. Möller
Shrub or small tree; nodes 7:7 + split lateral; stem with cortical bundles; petiole bundle with inverted adaxial bundles; lamina bundle with sheathing sclerenchyma; stomata in groups; lamina quite coriaceous; flower weakly monosymmetric; K ± free; A thecae confluent; G semi-inferior, placentation axile, style short, stigma capitate-lobed; capsule loculicidal + septicidal; n = 8.
1/1: Sanango racemosum. Ecuador to Bolivia, Venezuela (Map: from Norman 1994; TROPICOS ii.2013).
[Gesnerioideae + Didymocarpoideae]
Usu. herbs or weak-stemmed trees (trees), often epiphytes [ca. 1/5 spp.]; hairs often dense, soft, of stalked glands, or with thickened terminal cells; (cambium storied); (vessel elements with scalariform perforation plates); nodes 1:1 (+ split laterals), 3 or more:3 or more + split laterals); petiole bundle(s) also arcuate; lamina bundle lacking sheathing sclerenchyma; (stomata in groups); leaves (anisophyllous; two-ranked; spiral), lamina vernation involute, (margins entire); inflorescence axillary (terminal); flowers strongly monosymmetric (polysymmetric); K connate, C with abaxial lobe(s) outside others in bud< [= descending cochleate] or quincuncial, (C spurred); A (5, 2, staminode 0, 3), anthers connivent, (thecae apically confluent); nectary vascularized; placentation intrusive parietal, placentae ± bilobed, triangular, usu. covered by ovules, stigma broadly bilobed to trumpet-shaped, wet or dry; integument 3-5 cells across; fruit a septicidal capsule; exotestal cells variously elongated and thickened, endotestal cells at most simply persisting; GCyc duplication.
147/3460. Largely tropical.
Age. Crown-group core Gesneriaceae may be a mere (47-)44, 34(-31) m.y. (Wikström et al. 2001); Perret et al. (2012) thought that at (60.5-)44.7(-37.1) m.y. they were rather older; Bell et al. (2010: note relationships) give an age of (66-)56, 52(-44) m.y. for this node.
2. Gesnerioideae Link
3-desoxyanthocyanins +, chalcones, aurones 0; seeds without surface ornamentation, cells much elongated, spirally arranged (ornamented; shorter; not spirally arranged); endosperm conspicuous; GCyc2 gene lost.
75/960. Predominantly Neotropical, a few S.W. Pacific, East Asia. [Photo - Flower.]
Age. Crown-group Gesnerioideae can be dated to (48.7-)36.2(-32.3) m.y.a. (Perret et al. 2012).
2a. Coronanthereae Fritsch
Trees to ± shrubby-herbaceous, (rooting from the nodes); stomata anomocytic (paracytic); (inflorescence racemose - Pagothyra); (flowers polysymmetric); (C fringed); (A 2 [adaxial pair]; 5); nectary embedded in G wall, vascularized from A traces; capsules septicidal (and loculicidal), (placentae fleshy), (fruit a berry); n = 37(-45); gcyc duplication.
9/23: Coronanthera (11). Solomon Islands, Antilles, New Caledonia, S. South America (map: red, from Burtt 1998).
Age. Crown-group Coronanthereae are (32.2-)9.5(-7.6) m.y.o. (Perret et al. 2012).
2b. Titanotricheae W. T. Wang
Scaly rhizomes +; (stomata anomocytic); ± anisophyllous; inflorescence racemose, branched, with bulbils; testa striate-reticulate; n = 20.
1/1: Titanotrichum oldhamii. China, Japan, Taiwan (map: green above, from Fl. China v. 18. 1998).
2c. Gesnerieae Dumortier
(Plant with scaly rhizomes); (raphides, styloids +); (nodes 3:3; split-laterals - Episcieae); (petiole bundles deeply arcuate to annular); (stomata on raised mounds, usually single [widespread]); (leaves spiral); (flowers resupinate); (K ± free), (C margins fimbriate); ovary superior to inferior, nectary vascularized from numerous vascular bundles in wall; fruit various, berry, loculicidal or septicidal + loculicidal capsule, with fleshy placentae or funicles ["display capsule"] or not; n = (8) 9 (10) 11 (12) 13-14 (16), polyploidy rare.
53/1500: Besleria (150), Drymonia (140+), Alloplectus (75+), Nautilocalyx (70+), Paradrymonia (70+), Gesneria (60), Sinningia (60), Columnea (s.l. = 270+, s. str., 75+, + 4 genera, inc. Dalbergaria , Tricantha [75+]), Gesneria (50). New World (map: from Brummitt 2007, in part). [Photo - Leaves, Flower.]
Age. The age of the clade [Episcieae + Gesnerieae + Gloxinieae + Sinningieae + Sphaerorrhizae] is (36.9-)31.7(-24.8) m.y. (Perret et al. 2012).
Synonymy: Belloniaceae Martynov, Besleriaceae Rafinesque
3. Didymocarpoideae Arnott
(Plant body of leaf + inflorescence unit[s]); 3-desoxyanthocyanins 0, chalcones, aurones +; ?stomata; ovary wall not richly vascularized, nectary vascularized from A traces; testa cells little elongated; endosperm slight, cotyledons unequal, one accrescent.
71: ca 2510. Predominantly Old World, esp. South East Asia-Malesia and the Pacific (map: from van Steenis & van Balgooy 1966 [Malesia and Pacific]; Hilliard & Burtt 1971 [Africa].)
3a. Epithemateae C. B. Clarke
Dihydroxyphenolics [e.g. acteoside] 0; secretory canals; (medullary bundles + - Rhynchoglossum); cymes lacking bracteoles; (abaxial C lobe inside others in bud); (A 2 [adaxial pair]); (nectary variously vascularized); (placentation axile), ovary short, abruptly narrowed into the style; integument 2-3 cells across [Platystemma]; endosperm ?0; n = (8-)10(-12); (seedling primary root not developed).
6/80: Monophyllaea (35+). Predominantly Indo-Malesia, 1 sp. West Africa, 1 sp. (Rhynchoglossum azureum) S. southern Mexico to Peru.
3b. Trichosporeae Nees
(Plant woody); (nodes 1:1 with split laterals; 3:3 with split laterals; 5:5); (sclereids +); (A not coherent), (2 [abaxial pair]); placentae lamelliform-recurved, ovules restricted to distal end, ovary gradually narrowed into the style; (ovules hemitropous); (fruit with septicidal and loculicidal dehiscence; ± elongated, twisted; circumscissile; a berry); (testa cells with [extremely long] hairs); n = (4, 8) 9-11 (12, 13) 14-17, etc., polyploidy not uncommon.
82/2275: Cyrtandra (652-818), Aeschynanthus (185), Streptocarpus (155), Primulina (150), Paraboea (130), Codonoboea (120), Agalmyla (100), Didymocarpus (100), Oreocharis (85), Henckelia (56). S. Europe (scattered), Old World, mostly Sri Lanka to Malesia (especially southern China) and the Pacific to Hawaii.
Synonymy: Cyrtandraceae Jack, Didymocarpaceae D. Don, Ramondaceae Godron
Evolution. Divergence & Distribution. Möller and Cronk (2002) discussed biogeographic relationships within the large African genus Streptocarpus. Cyrtandra, with its baccate fruits, is a very diverse genus found throughout Malesia, being particularly speciose in places like New Guinea. Diversification may have begun ca 48 m.y.a. in Malesia (Clark et al. 2009). Cyrtandra is also widely distributed in the Pacific - the species there form a single clade - and it has been called a "supertramp" genus (Cronk et al. 2005), although surprisingly, perhaps, it is absent from the New Caledonian mainland (c.f. Psychotria s.l.). Fiji may have been the first area in the Pacific to be colonized (from the west) somewhat over 20 m.y.a.; the Hawaiian colonization, also from the west, was independent of that of the other Pacific islands and happened very soon afterwards; there are now ca 60 endemic species on the islands.
Perret et al. (2012) give dates for tribal divergences in Gesnerioideae. Within Coronanthereae there seems to have been one (Smith et al. 2006) or two (Woo et al. 2011) E to W dispersal events across the Pacific. Diversification in the New World Gloxinieae occurred some 30-20 m.y.a. (Roalson et al. 2008b: see also biogeographic relationships; estimate in Perret et al. 2012 somewhat younger at (25.0-)21.7(-14.8) m.y.). There is extensive diversification in both flower and fruit in the speciose Episcieae (Clark et al. (2011, 2012).
Ecology & Physiology. Although many taxa are rather succulent or sometimes quite delicate herbs, a surprising number grow on exposed rocks (Haberlea rhodopensis and Boea hygrometrica are examples) and are resurrection plants (Burtt 1998; Bogacheva et al. 2013 for literature); along with sucrose, galactose oligosaccharides are quite abundant in the dried leaf (Marinone Albini et al. 1999; see also Navari et al. 1995). Hardly surprisingly, epiphytes are common, with well over 400 epiphytic species in neotropical Episcieae alone (Madison 1977; Weber 1978; Gentry & Dodson 1987), although Zotz (2013) estimated that there were only 570 epiphytic species in the whole family, of which ca 275 species were found in the Old World Aeschynanthus and Agalmyla. The evolution of epiphytism within Coronanthereae is described by Salinas et al. (2010).
Pollination Biology & Seed Dispersal. Birds and bees are the major pollinators of Gesneriaceae. Harrrison et al. (1999) discuss floral diversification in Streptocarpus, which includes species with strongly monosymmetric flowers as well as Saintpaulia, with almost polysymmetric flowers, so encompassing very different flower morphologies and pollinators; for instance, Saintpaulia-type flowers have the buzz pollination syndrome (Clark et al. 2011). Wiehler (1978) estimated that perhaps 60% of neotropical Gesnerioideae - some 600 species - were humming-bird pollinated, and he divided the floral morphologies involved into three common and one less common "types" - rather narrowly tubular; strongly and broadly bilabiate; with a narrow mouth and an asymmetrically swollen tube; and tubular, with the limb more or less rotate. The centers of diversity of both neotropical Gesneriaceae and of hummingbirds are in the Colombia-Ecuador region (Weber 2011; see also Ericaceae). Perret et al. (2007) found that humming birds pollinated perhaps 2/3 of the ca 80 species of Sinningieae (= Ligeriinae), a group centred in the Atlantic forest of Brazil. Wiehler (1978) thought that another ca 30% of Gesnerioideae (ca 300 spp.) were pollinated by euglossine bees of both sexes (c.f. Orchidaceae where only male bees seeking scents are involved), and in these flowers the spreading corolla lobes sometimes have long-fimbriate margins; divergence of euglossine bees occurred 42-27 m.y.a. (Ramírez et al. 2010). Martén-Rodriguez et al. (2010) discuss the variety of pollinators of Caribbean Gesnerieae. Bird pollination is relatively less common in Old World Gesneriaceae, but is likely to predominate in Aeschynanthus, which has some 185 species.
More or less polysymmetric flowers - the corolla may be radial and rotate, although the androecium is often technically monosymmetric - have arisen independently several times in the family, the ten or so genera involved not being immediately related (e.g. Burtt 1970; Smith et al. 2004a), indeed, polysymmetric flowers are notably abundant here compared with some other core lamialean families (Endress 1997a). Relatively little is known about the pollination of such flowers, although as might be expected buzz-pollination has sometimes been recorded (Clark et al. 2011 and references).
Flowers with inverted orientation are known from some Episcieae (Clark & Zimmer 2003); they seem to have evolved ca 3 times. This inverted orientation is evident from the very earliest stages of the ontogeny of the flower, and since there is no twisting of the pedicel (Clark et al. 2006), they are not resupinate by some definitions.
Many Gesneriaceae have capsular fruits with wind dispersed seeds. Splash-cup dispersal is quite common, occurring in around 190 or more species from the New World alone. The species involved grow in damp, forest floor/stream side type conditions; a persistent calyx may form the cup (Ertelt 2013). In the New World birds and perhaps other animals may disperse Gesneriaceae, either eating fleshy fruits in their entirety or black, glistening seeds exposed on a fleshy placenta or swollen funicles, in turn displayed against the coloured inside of the capsule wall (and sometimes surrounded by a coloured calyx). Other variants of fleshy capsule/drupe fruit type are quite common (Weber 2004b; Clark et al. 2006, 2012). In the Old World, the speciose Cyrtandra has fleshy fruits.
Plant-Animal Interactions. Gesneriaceae are not often eaten by lepidopteran caterpilars (Ehrlich & Raven 1964).
Vegetative Variation. Variation in growth patterns in this family is considerable (see Weber 2004 for a useful survey). The architecture of some Didymocarpoideae and Epithematoideae is particularly diverse and distinctive. For anisocotyly in general - more accurately, one cotyledon is accrescent - and its development in [Didymocarpoideae + Epithematoideae], see Burtt (1970) and Saueregger and Weber (2004). Streptocarpus (Didymocarpoideae) shows much variation in growth patterns, some species having only a single, huge, ever-growing cotyledon (e.g. Hilliard & Burtt 1971; Jong & Burtt 1975). The evolution of growth form here has many parallelisms and reversals, as well as being linked with other life history variables, such as age to flowering and flowering periodicity (Möller & Cronk 2001). Jong & Burtt 1975) thought that these ever-growing cotyledons, which they called phyllomorphs, were an example of the evolution of morphological novelty. However, Kaplan (1997, 1: ch. 6) suggested that they were an extreme example of the dominance of the leaf in development, the apical meristem effectively having been evicted. Harrison et al. (2005a) found that genes involved in shoot development were expressed on the petiole in rosulate species of the genus, plants producing leaves, etc., from the petiole, but these genes were not expressed in strictly unifolioliate species. Mantegazza et al. (2009) also suggested that the developmental pathways controlling meristem development appear to have become relocalised. The petiole (= petiolode) itself of Streptocarpus, at least, is unifacial, although not at the seedling stage, when it is bifacial (Tononi et al. 2010). Imaichi et al. (2007) also discuss growth patterns and the evolution of monophylly in Streptocarpus, and Jong et al. (2012) discussed the morphology of two woody Madagascan species.
Within Epithematoideae, too, anisophylly is common. The plant body of many species of Monophyllaea is rather like that of Streptocarpus, consisting of a single, ever-growing structure that is derived from a single cotyledon. A meristem develops at the base of the cotyledon, and inflorescences also develop at the base of the lamina; in some species the flowers even arise along the midrib of the blade rather than from separate inflorescences (Imaichi et al. 2001; see also Tsukaya 2005). The cotyledon that keeps on growing is the one that is exposed to more light (Saueregger & Weber 2005). In some species of Monophyllaea the plant body becomes more complex by repetition of the cotyledonary unit. The radicle of the seedling may not develop, although this has also been noted in other Epithematoideae (Imaichi et al. 2001). Taxa like Rhynchoglossum have two-ranked leaves with very aymmetrical blades; vegetatively they look like Begonia or Pentaphragma, which grow in the same general area.
Monophylly in general and some forms of heterophylly seem to be an adaptation for life on rocks and/or shady conditions. The plant grows in cracks of the rock and the single leaf hangs down and covers the rock surface quite efficiently; that the better lighted cotyledon of Monophyllaea is the one that develops make sense in this context. Plants whose stems consist of sprays of alternating leaves - if they are opposite, then there is often strong anisophylly, as in Pilea (Urticaceae) - are also common in such situations; again, a photosynthetic surface covering the rock is deployed.
Chemistry, Morphology, etc. Secondary metabolites (lack of iridoids, presence of the caffeoyl phenylethanoid glycoside, sanangoside) seem to suggest an association between Sanango and Gesnerioideae in particular (Jensen 1996). Peltanthera in particular is very similar in wood anatomy to Buddleja (but both genera are woody!), Sanango has vessel elements with scalariform perforation plates like a few other Gesneriaceae such as Kohleria (Carlquist 1997c).
There is quite a lot of anatomical variation which I have not integrated with the clades above. Thus sclereids are common in the stem; Aeschynanthus has strongly U-thickened sclereids in the pericycle, other taxa lack fibres or sclereids in the pericyclic position; some taxa have lignified hairs; Gesneria has a U-shaped petiole bundle cradling a unmedullated circle of vascular tissue, and there are also two wing bundles; in other taxa the petiole bundle may be annular, with adaxial bundles, etc. Nodal anatomy is quite variable (see also Howard 1970; Jong et al. 2012), and a fuller survey would repay being placed in the systematic context that is developing for the family. In addition to its distinctive anatomy, Gesneria also has spirally-inserted serrate leaves with an almost coriaceous texture - it looks quite ungesneriaceous.
Song et al. (2009) found that CYC2 genes were involved in repression of the growth of both the single adaxial stamen and the abaxial stamen pair in Opithandra, so resulting in a flower with but two functional stamens, the adaxial stamen pair - c.f. Lentibulariaceae, where it is the abaxial stamen pair that remains fertile.
For more information, see Burtt and Wiehler (1995), Wiehler (1983), Weber (2004a: excellent account, 2004b: history of classification), all general, Wiehler (1970: vegetative anatomy, esp. Gesnerioideae), Weber (1973: inflorescence), Trapp (1956b: androecium), Wilson (1974a, b: nectary vascularization), Skog (1976: Gesnerieae s. str.; 1984: chromosomes), Beaufort-Murphy (1983: seed morphology under the S.E.M., 1984: response to growth hormones, etc.; Cyrtandroideae much more responsive than Gesnerioideae), Kvist and Pedersen (1986: phenolics), Citerne et al. (2000), Smith et al. (2004a), and Zhou et al. (2008: all molecular details of floral development), Möller and Kiehn (2004) and Christie et al. (2012), both cytology, considerable infra-generic variation. Pan et al. (2002) discussed the floral development of Titanotrichum (see below for phylogeny). Pollen variation is either uninformative or suggests problems in everything from species delimitation on up (Schlag-Edler & Kien 2001).
Dickison (1994), Jensen (1994, 1996), Norman (1994), and Wiehler (1994) all deal with Sanango.
Phylogeny. For an extensive summary, see Möller and Clark (2013). The relationships of Peltanthera are dealt with above; it has support as sister to [Calceolariaceae + Gesneriaceae]. Sanango is sister to the rest of the family (e.g. Perret et al. 2012; Refulio-Rodriguez & Olmstead 2014); Epithematoideae are sister to Didymocarpoideae (= Cyrtandroideae), and the monophyly of these clades is well established - see Smith (1996), Smith et al. (1997a, b), Wang et al. (2010), etc., and especially Mayer at al. (2003).
Within Didymocarpeae, Haberlea and Ramonda, temperate, European, and with polysymmetric flowers and five stamens, may be sister to the rest (e.g. Mayer et al. 2003), or more likely near the base of the clade (Wei et al. 2010; Wang et al. 2010); they have dihydrocaffeoyl ester found nowhere else in flowering plants (Jensen 1996). Indeed, Möller et al. (2009) placed a number of small Asian and European clades all with four or five, rarely two, stamens "basal" in Didymocarpoideae. Of these, the odd Jerdonia, from the Western Ghats, India, has pollen in tetrads, four parietal placentae, large seeds with alveolate endosperm, and n = 14 (Burtt 1977b); it may be sister to the rest of the subfamily (Möller et al. 2009). Wang et al. (2010: Jerdonia not included) found that Corallodiscus, the Ramonda clade, and Streptocarpus are successive branches in the phylogeny; taxa with radially symmetric flowers are scattered through the tree. For Didymocarpoideae phylogeny, see also Möller et al. (2011a).
Didymocarpus itself has been dismembered (Weber & Burtt 1998) and many species placed in Henckelia, but the circumscription and relationships of the latter remain unclear (Möller et al. 2009). Within the diverse Cyrtandra, particularly speciose in places like New Guinea, all Pacific species studied are members of a single clade with a long branch, and within this clade Hawaiian species are monophyletic and possibly sister to the rest (Cronk et al. 2005; J. R. Clark et al. 2009; Atkins et al. 2013). The long branch of the Pacific species has been broken up by a clade of species from the Solomon Islands, and other clades of Solomon Islands species are in both the Pacific and Malesian parts of the tree (J. R. Clark et al. 2013). For relationships in Streptocarpus, which includes Saintpaulia, see Möller and Cronk (2001), for a study of Aeschynanthus linking seed morphology and geography, see Denduangboripant et al. (2001), for a phylogeny of Chirita and relatives, see Wang et al. (2011) and in particular Weber et al. (2011), and for relationships in an expanded Oreocharis, see Möller et al. (2011b).
Epithemateae are perhaps to include Cyrtandromoea (molecular data), but that genus is also sometimes placed in "Scrophulariaceae" - and it does have iridoids and is otherwise chemically similar to the latter; it also has endosperm, an exotesta with laminated, U-shaped thickenings in transverse section, the seeds are isocotylous, and the gynoecium is bilocular (Burtt 1965: q.v. for a revision); Burtt placed the genus in Scrophulariaceae and linked it with Leucocarpus (now in Phrymaceae). Branch lengths are long. Chemistry - Napeanthus (Gesnerioideae) is also similar! More work is needed on these taxa.
Kotarski et al. (2007) found 80% bootstrap support for the position of Coronanthereae as sister to the other Gesnerioideae, and Titanotrichum was sister to the remainder. For a phylogeny of Coronanthereae, see Smith et al. (2006) and Woo et al. (2011). Other studies also place the Old World but more or less isocotylar Titanotrichum basal in Gesnerioideae (C.-N. Wang et al. 2004: substantial amount of molecular data; c.f. D. Soltis et al. 2000; Albach et al. 2001), although that genus has also sometimes been placed in "Scrophulariaceae". Besleria and Napeanthus (n = 16) may also be near the base of the Gesnerioideae. Shuaria, a woody plant superficially similar to Sanango that sometimes also has "alternate" leaves, was placed firmly in Beslerieae (Clark et al. 2010). In general agreement with earlier studies, Perret et al. (2012) found basal relationships in Gesnerioideae to be [[Napeantheae + Beslerieae] [Coronathereae [Sinningieae + the rest]]]; Titanotrichum was sister to Napeanthus, and although neither Shuaria nor Cyrtandromoea were included in their study, there is little doubt about the placement of the former genus.
Relationships along the rest of the spine of Gesnerieae remain only weakly supported (e.g. Woo et al. 2011; Perret et al. 2012). However, there seem to be five well supported clades, Ligeriinae (= the old Sinningieae), Sphaerorrhizinae, Gesneriinae, Gloxiniinae, and Columneinae (= the old Episcieae) (Perret et al. 2012). For other relationships in Gesnerieae, see Smith (2001), Zimmer et al. (2002) and Smith et al. (2004a, b); see Skog (1976) for a revision of Gesneria and relationships in Gesneriinae. For relationships around Alloplectus, see Clark and Zimmer (2003). For the phylogeny and biogeographic relationships of Gloxiinae, see Roalson et al. (2005 a, b; 2008b: relationships in Central America and the Antilles). For diversification in Beslerieae, see Roalson and Clark (2006) and in Ligeriinae, see Perret et al. (2003, 2006: the limits of Sinningia need adjusting). For relationships within Columneinae, see Clark and Smith (2009) and in Columnea itself, see Smith et al. (2013) and Schulte et al. (2014). For a preliminary study of relationships in the complex Episcieae, see Clark et al. (2012).
Classification. Perret et al. (2012) were undecided as to the circumscription of the family, sometimes suggesting that it be broadened to include Peltanthera and Sanango, sometimes suggesting that those genera might be excluded. However, Peltanthera seems not to be immediately associated with Gesneriaceae (Refulio-Rodriguez & Olmstead 2014), while Sanango is. Weber et al. (2013) include it in the family, for which they provide a formal classification down to the subtribal level, which is being followed here (I will stop at tribes).
As might be expected of a family in which there are conspicuous flowers and much obvious adaptation to pollinators, many recently-followed generic limits, based as they were on floral characters, have turned out to be unsatisfactory. Thus Clark et al. (2012) found that six of fifteen genera of Episcieae for which they sampled two or more species were para- or polyphyletic. However, much-needed changes are underway, and some in New World Gesneriaceae are clearly explained in a series of articles in Gesneriads 56(3). 2006. See the World Checklist and Bibliography of Gesneriaceae (Skog & Boggan 2005 a, b) and The Genera of Gesneriaceae (Weber & Skog 2007).
In general the old tribes of Didymocarpoideae were decidedly unsatisfactory (Möller et al. 2009), and some genera, perhaps most notably Chirita, are polyphyletic. Primulina, originally monotypic, has been greatly expanded in the course of understanding the limits of Chirita (Weber et al. 2011). Indeed, Möller et al. (2011a) found that only 12/29 genera with more than one species they sampled were monophyletic, and there are also many monotypic genera - thus Oreocharis has been expanded to include eleven mostly very small Chinese genera (Möller et al. 2011b). The huge Didymocarpus itself has been dismembered (Weber & Burtt 1998), species that had been included there being assigned to 27 genera (including two in Plantaginaceae); many species were placed in Henckelia, although this was not monophyletic, and it is now considerably restricted (see Middleton et al. 2013). The large genus Cyrtandra has been broken up into some 40 sections, although the form any final classification here will take is unclear (Atkins 2013); the limits of Paraboea have been adjusted (Puglisi et al. 2011), and on it goes.
Previous Relationships. The limits of Gesneriaceae have by and large been quite stable, although Sanango has previously been placed in Loganiaceae or Buddlejaceae and it is still unclear if a few genera belong here or elsewhere in Lamiales (see above).
[Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]: route II decarboxylated iridoids as glucosides [aucubin, catalpol widespread], 6- or 8-hydroxyflavones or 6 methoxyflavones +, cornosides 0; inflorescence racemose [lateral and main axes of inflorescence indeterminate]; (embryo sac haustoria +).
Age. Bremer et al. (2004) suggested an age of ca 76 m.y. for this node, the age, (51.7-)31.5(-12.8) m.y., suggested by Naumann et al. (2013) is substantially younger.
Evolution. Plant-Animal Interactions. Caterpillars of Nymphalinae-Melitaeini and -"Kallimini" butterflies are quite common on plants in this group (see Plantaginaceae, Acanthaceae and Orobanchaceae below). They probably moved on to these families from the Urticaceae group of families (Rosales) around about the K/T boundary, a shift that may have been followed by an increased diversification rate (Fordyce 2010). Some Melitaeini in turn adopted members of Asteraceae as food plants (Nylin & Wahlberg 2008).
Chemistry, Morphology, etc. For the synthetic pathway of route II iridoids, see Jensen et al. (2002); 8-epi-irodial, 8-epi-iridotrial and 8-epi-deoxyloganic acid are the precursors. Iridioid acquisition seems best placed here, with an independent origin in Oleaceae (modified route I iridoids - Jensen et al. 2002). Flavonoid 7-O-glucosides and glucuroides are scattered here (Lamiaceae, Pedaliaceae, Plantaginaceae: Noguchi et al. 2009).>/p>
Extrafloral nectaries in this clade commonly consist of scattered multicellular trichomes (Zimmermann 1932).
PLANTAGINACEAE Jussieu, nom. cons. Back to Lamiales
Herbs (shrubs; rooted aquatics); (cardenolides [Digitalis], mannitol, sorbitol, iridoids 0), little oxalate accumulation; cork various; (leaf endodermis +); hairs with gland head not often vertically divided, (with cystolith); leaves also spiral, simple to compound; (inflorescence branches pair-flowered cymes), (bracteoles 0 - Antirrhineae); (corolla spurred; 0), (descending cochleate); stamens (2 [adaxial pair] + 2 staminodes [Trapella]; 2; 5-8), thecae parallel, end-to-end, sagittate, or on connective arms, confluent [Penstemon] or not, connective well developed, placentoids usu. 0, (staminode + - esp. Cheloneae, Antirrhineae); pollen exine tectate and reticulate; (placentation intrusive parietal); ovules (>1/carpel), (campylotropous?), integument 3-22 cells across [3-6 cells in Gratioleae], stigma (slightly) capitate or bilobed, dry (wet); fruit a septicidal capsule (loculicidal [Veronica]; poricidal [Antirrhineae]; circumscissile); seeds (1-)many, (pedestals +), exotestal cells with inner walls ± thickened, when winged, cells with reticulate thickenings; endosperm +/0, mannose-rich polysaccharides + [?distribution], (embryo green; short; curved; suspensor long); n = 6-10 +; protein bodies in nucleus amorphous [not Angelonieae and Gratioleae].
Ca 90[list]/1900: Veronica (ca 450, inc. Hebe, Parahebe, Synthyris, etc.), Penstemon (275), Plantago (275), Linaria (150: tubular protein bodies), Bacopa (55), Stemodia (55), Russelia (50). Mostly temperate (map: from van Steenis & van Balgooy 1966; Hultén 1971; Meusel et al. 1978; Frankenberg & Klaus 1980; Hong 1983; Heide-Jørgensen 2008). [Photos - Callitriche Habit, Hippuris Habit, Veronica Flower.]
Age. Bell et al. (2010: note sampling) suggested an age of (57-)46, 42(-34) m.y. for crown Plantaginaceae; an age of ca 66 m.y. was suggested by Bremer et al. (2004).
Ecology & Physiology. Philcoxia, a recently described white sand endemic from Brasil, was suspected of being carnivorous (Fritsch et al. 2007). This has been confirmed by Pereira et al. (2012): Nematodes stick to the glandular secretions covering the leaves, which are underground, and are then digested by the plant; phosphatase activity has been detected in the hairs. The plants lack mycorrhizae, as is common when there is carnivory.
Pollination Biology & Seed Dispersal. Floral morphology is very variable (see Reeves & Olmstead 1998), but Plantaginaceae are predominantly pollinated by large insects and birds; Kampny (1995: as Scrophulariaceae) discussed pollination in the family as a whole. The speciose North American Penstemon is noted for is prominent bearded staminode, and Wilson et al. (2006, 2007) discussed the estimated 21 shifts from bee to bird pollination in the Penstemon clade (over 40 species are pollinated by humming birds); there were no switches in the opposite direction (see also Barrett 2013). The South American Monttea and Angelonia have weakly bisaccate oil-producing corollas; in the latter genus the visiting bees have either their front (Centris) or middle (Tapinotaspis) legs elongated (Sérsic & Cocucci 1999; Machado et al. 2002; Martins et al. 2013). At least 30 species in Angelonieae produce oil, although the bees may sometimes also pick up nectar or pollen (Martins & Alves-dos-Santos 2013). Collinsia has remarkable papilionoid flowers. The distinctively bicolored and erect standard is formed from the two adaxial petals, while the three other petals are flat-coloured, the median abaxial petal forming a keel that encloses the stamens. Indeed, the overall colour scheme and functional floral morphology is very like that of some species of Lupinus (Kampny 1995; see Baldwin et al. 2011 for floral evolution in Collinsia). Sibthorpia has 5-8-merous, polysymmetric flowers; polysymmetric flowers have been derived from monosymmetric flowers several times in this family.
Muñoz-Centeno et al. (2006) discuss seed morphology in the context of the phylogeny of Plantago; the seeds are mucilaginous, which may have facilitated the three dispersals of this genus from Australia to New Zealand (Tay et al. 2010).
Plant-Animal Interactions. For feeding preferences of a variety of insect groups that might suggest that the erstwhile Plantaginaceae s. str. and Scrophulariaceae s. l. are close, see Airy Shaw (1958), Allen (1960, 1961) and Tempère (1969). Allen (1960) found different insects eating Plantaginaceae s. str. and Scrophulariaceae s. str. (see also below). Larvae of Nymphalinae-Melitaeini butterflies are commonly found here and on Orobanchaceae, but not on Scrophulariaceae s. str. (Wahlberg 2001). Agromyzid dipteran leaf miners have diversified on Plantaginaceae (Winkler et al. 2009).
Genes & Genomes. Bakker et al. (2006a) found major increases in the rate of evolution of the mitochondrial gene nad1 in Plantago and Littorella; Plantago has substitution rates at synonymous sites in the mitochondrial genome (but not in the chloroplast genome) that are 3,000-4,000 times those of nearly all other angiosperm clades (Cho et al. 2004; Mower et al. 2007). In an interesting development, at least three mitochondrial genes have recently been transferred from Cuscuta to species of the Plantago coronopus group, although they do not seem to be functional there (Mower et al. 2010).
In Veronica s.l. no correlation was found between speciation rates and rate of molecular evolution (Müller & Albach 2010).
Economic Importance. For Digitalis, the source of important drugs, see Luckner and Wichtl (2000).
Chemistry, Morphology, etc. Details of characters like the distribution of hair morpholgies and timing of androecium initiation remain to be clarified, and morphological/developmental synapomorphies for Plantaginaceae may yet be found.
Both Digitalis and Isoplexis have cornosides. Iridoids with an 8,9 double bond - rather uncommon - are scattered in a number of genera (Jensen et al. 2007); at what level this character might be an apomorphy is unclear, although they are to be found in both Veronica and Plantago (Rønsted et al. 2000), and the two genera are close phylogenetically (Bello et al. 2002, 2004). Veronica has mannitol (Taskova et al. 2012), while Plantago has sorbitol.
Penstemon is reported () to have a storied cambium. Veronica lyallii has successive subhypodermal phellogens (Gray 1937), while Besseya and Plantago have a foliar endodermis. Hair morphology may be of interest. The cell walls in the heads of the glandular hairs are variously oriented. Lindernieae were until very recently included in Plantaginaceae but the heads of their glandular hairs are divided by vertical partitions. However, taxa like Russelia and even some Penstemon, still in Plantaginaceae, also have similar hairs (Raman 1991 and references).
Penstemon and a few other genera have paired-flower cymes (Weber 2013). The development of the petaloid calyx of Rhodochiton is not connected with the expression of B-class genes (Landis et al. 2012).
There has been much work on floral development in this clade. Linaria has flowers with a single well-developed abaxial spur, but its well-known Peloria mutant has all five perianth members with spurs, a feature under simple genetic control. Antirrhinum majus is a model organism used for understanding the development of monosymmetric flowers and the involvement of the CYC gene in this (e.g. Rosin & Kramer 2009; Preston et al. 2011 for references); duplication of the gene is evident in Antirrhineae, but not in Digitalis (Gübitz et al. 2003). Floral evolution in the Veronica/Plantago clade is becoming better understood. Veronica has an open, 4-lobed corolla, but only two stamens; some species have two main veins in the adaxial corolla lobe, perhaps suggesting that it is formed by the fusion of the two adaxial lobes of other members of the family. Wulfenia, sister to Veronica, has tubular and rather weakly lipped (2 + 3) flowers. Aragoa has 4-merous, polysymmetric flowers (c.f. Oleaceae and Tetrachondraceae!), but with five sepals. The flowers of Plantago, sister to Aragoa, are small, polysymmetric, and in dense spikes; they have four sepals, petals and stamens, and are wind pollinated. Their evolution is connected with the degeneration of some floral symmetry genes (Preston et al. 2011a). Bello et al. (2004: see Bello et al. 2002 for a phylogeny) discuss floral evolution in the Plantago area, also emphasizing the evolution of polysymmetry.
In a number of taxa in Plantaginaceae the androecium is initiated before the corolla, but other patterns also occur, so the timing of androecium initiation is perhaps unlikely to be a synapomorphy for the family (Bello et al. 2004, c.f. Judd et al. 2002). Veronica/Plantago, as well as Digitalis, are members of a clade that has descending-cochleate aestivation (Bello et al. 2004), i.e. in bud the abaxial corolla lobes are outide the others. Petals have sometimes been lost in Synthyris (Hufford 1992b). Illustrations in Chatin (1874) suggest that the ovules of Veronica may be crassinucellate. The large, transversely elongated endothelial cells in vertical rows in Gratiolaceae cause their seeds to have longitudinal ridges, and the extotestal cells have hook-like thickenings.
For general references, see Rahn (1996: Plantaginaceae), Leins and Erbar (2004a: Hippuridaceae), Erbar and Leins (2004b: Callitrichaceae), Schwarzbach (2004: Plantaginaceae), Ihlenfeldt (2004) and Takhtajan (2013), both Trapellaceae, Fischer (2004b: Scrophulariaceae p. pte) and Wagenitz (2004: Globulariaceae). For chemistry, see Jensen (2005), Taskova et al. (2006), and Jensen et al. (2009c), for Trapella, see Oliver (1888), and for a general survey, see Thieret (1967). Additional information is provided by Schmid (1906: ovules, Scrophulariaceae s.l.), Junell (1961: gynoecium), Elisens and Tomb (1983: considerable seed variation even in Antirrhineae), and Schrock and Palser (1967), Leins and Erbar (1988, 2010), and Endress (1999), all floral development.
Phylogeny. For the circumscription of Plantaginaceae, which initially had only rather weak support, see Olmstead et al. (2001, as Veronicaceae: inclusion of Cheloneae and Hemimerideae may be the problem; for the latter, see Scrophulariaceae below), Oxelman et al. (2005: support stronger), and Tank et al. (2006, summary, as Veronicaceae), also Olmstead and Reeves (1995) and Reeves and Olmstead (1998).
Gratiolaceae were recognised as a distinct family by Rahmanzadeh et al. (2004), although only three species were examined; Rahmanzadeh et al. (2004) thought that Angelonieae might also be included and Limosella, here Scrophulariaceae, was included without comment. Albach et al. (2005a) found that Antirrhinum was not associated with the rest Plantaginaceae, where relationships were [[Cheloneae + Gratioleae] [Angelonieae [Antirrhineae + The Rest (incuding Antirrhineae)]]]. However, Estes and Small (2008) placed Antirrhinum, along with members of Cheloneae and other tribes, in a clade sister to [Angelonieae + Gratioleae]; Limnophila was part of Gratioleae (1.0 p.p.), Limosella was not sampled. Kornhall and Bremer (2004) placed Limosella in Scrophulariaceae, but they did not look at other members of Gratiolaceae.
For the phylogeny of Antirrhineae, see Ghebrehiwit et al. (2003) and Vargas et al. (2004); Fernândez-Mazuecos et al. (2013) discuss relatonships within Linaria. Bräuchler et al. (2004) discussed the phylogeny of the cardenolide-rich Digitalis (to include the bird-pollinated Isoplexis). For a phylogeny of Veroniceae, see Albach et al. (2004a, c, 2005c), Taskova et al. (2004, 2006), and Albach and Meudt (2010); the "new" molecular relationships are at least sometimes supported by other data such as chromosome number and iridoid type (Albach et al. 2004b, 2005c; Albach & Meudt 2010). Pedersen et al. (2007 and references), Jensen et al. (2008a) and Maggi et al. (2009) report on some chemistry of ex-Hebe or Hebe s.l.; of the ca 125 species of this complex, all except for a few from New Guinea are found in New Zealand (Albach et al. 2005b) and the genus is polyphyletic. Albach (2008) discussed the limits of Veronica s.l., which includes Hebe, and Wolfe et al. (2006) outline phylogenetic relationships in Penstemon (see also P. Wilson et al. 2007). For the phylogeny of Collinsia and the related Tonella, see Baldwin et al. (2011).
Classification. The circumscription of Plantaginaceae adopted here is broad on the one hand (it incorporates several highly divergent but small clades previously recognized as families) but narrow on the other (it is but a part of the old Scrophulariaceae). Molecular studies suggest that these small but florally very distinctive families are derived members of a clade that also includes numerous species with relatively large but undistinguished monosymmetric flowers. Maintaining them as distinct would entail the recognition of a number of other families that would be poorly characterised.
Rahmanzadeh et al. (2004) did not characterise their Gratiolaceae; they included the widespread Limosella (here Scrophulariaceae) and, somewhat hesitantly, Lindenbergia (here Orobanchaceae) along with 30 other genera. Souza and Lorenzi (2012) included ca 20 genera and 250 species in the family, among them the carnivore Philcoxia. Rahmanzadeh et al. (2004) thought that Angelonieae might also be part of their Gratiolaceae, but Souza and Lorenzi (2012) recognized an Angeloniaceae, often oil flowers with a spurred corolla (5 genera, with 30 species, were mentioned); Ourisia seems not to have been accounted for. Oxelman et al. (2005) located the majority of Gratiolaceae in Plantaginaceae; Limosella remained in Scrophulariaceae (see also Schäferhoff et al. 2010). Sampling of Plantaginaceae s.l. is still very poor, and little is gained by segregating at most poorly distinguishable clades as families.
Sutton (1988) monographed Antirrhineae.
Previous Relationships. Both Cronquist (1891) and Takhtajan (1997) recognise several of the smaller families just mentioned, but they are in the same general part of their sequences; Cronquist had a notably broad circumscription of Globulariaceae and included a number of genera here placed in Scrophulariaceae. Trapella has been included in Pedaliaceae (e.g. Cronquist 1981), in part because its stoutly-spiny fruits appear to be so similar to those of Pedaliaceae.
Botanical Trivia. Linnaeus was initially so impressed with the distinctive morphology of the Peloria mutant, since it differed strikingly in floral (= generic) characters from Antirrhinum, that he proposed to place it in a genus of its own, but Smith sourly observed.
Thanks. I thank Dirk Albach for comments.
Synonymy: Angeloniaceae V. C. Souza, P. Dias & Udulutsch, Antirrhinaceae Persoon, Aragoaceae D. Don, Callitrichaceae Link, nom. cons., Chelonaceae Martynov, Digitalidaceae Martynov, Ellisophyllaceae Honda, Erinaceae Pfeiffer, Globulariaceae Candolle, nom. cons., Gratiolaceae Martynov, Hippuridaceae Vest, nom. cons., Linariaceae Berchtold & J. Presl, Littorellaceae Gray, Oxycladaceae Schnizlein, Psylliaceae Horaninow, Scopariaceae Trinius, Sibthorpiaceae D. Don, Trapellaceae Honda & Sakisaka, Veronicaceae Cassel
[Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]: cornosides at most uncommon.
Age. Bremer et al. (2004) suggested an age of ca 75 m.y. for this node.
SCROPHULARIACEAE Jussieu, nom. cons. Back to Lamiales
Herbs to shrubs; harpagide, harpagioside [8ß-8α-methyl substituted iridoids] +, little oxalate accumulation; (cork inner cortical/pericyclic - Buddleja); nodes also 1:3 + girdling bundle; (secretory cavities +); (indumentum stellate); (stomata anisocytic); leaves opposite, (basally connate), or spiral, lamina (punctate), vernation flat, (± foliaceous, stipuliform structures +); inflorescence branches cymose; (bracts recaulescent); (flowers polysymmetric; 4-merous); K unequal or not; (A 5 - Verbascum, Capraria; 2), anther thecae head to head and confluent, ± clavate, or parallel; tapetal cells binucleate; (colpi diorate); staminodia +/0; nectary small or 0; stigma capitate (lingulate), dry or wet; ovules ³1 /carpel, apo/epi/pleurotropous, integument 5-11(-12) cells thick, (hypostase +); capsule septicidal (and apically loculicidal - Buddleja), (berry; drupe; schizocarp); seeds many, pedestals/cushion-shaped scars on the placentae widespread; exotestal and endotestal cells with thickened inner walls, (testa multiplicative, exotestal cells ± longitudinally elongated, inner walls thickened - Buddleja); endosperm (alveolate because of inpushings of individual entotestal cells [bothrospermous]), copious to 0; n = 6-9, 12+ [18 - Myoporaceae s. str.], (protein crystal stacks in nucleus).
65[list]/1800: Verbascum (360), Eremophila (215), Scrophularia (200), Selago (190), Buddleja (125), Jamesbrittenia (85), Manulea (75), Diascia (70), Nemesia (65), Zaluzianskya (55), Chaenostoma (46). World wide (map: from Hultén 1958, 1971; van Steenis & van Balgooy 1966; Meusel et al. 1978; Leeuwenberg 1979; Hong 1983; Hilliard 1994; Norman 2000; Lebrun 1977, 1979 [Sahara]) [Photo - Flower, Myoporaceae s. str. flower, also Myoporaceae s. str.].
Age. Bell et al. (2010) estimated an age of (58-)53, 51(-45) m.y. for the clade [Myoporum, Scrophularia, Verbascum]; note that Buddleja was widely separated and sister to Paulowniaceae. Bremer et al. (2004: Buddleja placed here) suggested an age of ca 68 m.y..
Evolution. Pollination Biology & Seed Dispersal. Scrophulariaceae include quite a few taxa that have oil-flowers with oil-secreting hairs (Vogel 1974; Vogel & Cocucci 1995 for a list; Renner & Schaefer 2010; Martins et al. 2013). Details of the pollination of the remarkable two-spurred oil-flowers of Diascia are well known. The bee Redivia collects oil from the oil-secreting hairs in the spurs using its sometimes remarkably elongated front pair of legs (Vogel 1984; Steiner 1990; Rasmussen & Olesen 2000; Steiner & Whitehead 1991); flowers of some Orchidaceae from the same area are rather similar. Flowers of Scrophularia are sometimes pollinated by wasps (see Kampny 1995: also pollination elsewhere in the family), and evolution of pollinator preferences has been studied in detail there (Navarro-Pérez et al. 2013).
Plant-Animal Interactions. Mohrbutter (1937) noted both fungi and leaf miners that attacked members of the old Buddlejaceae and Scrophulariaceae s. str.. For example, the dipteran agromyzid miner Amauromyza verbasci has been found on Verbascum, Scrophularia and Buddleja (Spencer 1990). Some other insect herbivores seem to be able to distinguish between Plantaginaceae and Scrophulariaceae (e.g. Allen 1960; Tempère 1969).
Chemistry, Morphology, etc. The iridoids harpagide and harpagioside, found quite commonly here, are also scattered elsewhere in Lamiales, in Lamiaceae (inc. Caryopteris) and Pedaliaceae (Hegnauer & Kooiman 1978; Nicoletti et al. 1988; Georgiev et al. 2013); Soltis et al. (2005b) suggest that such acylated rhamnosyl iridoids characterise Scrophulariaceae. The chemistry of Buddlejaceae (see Jensen 2000b) and Scrophulariaceae s. str. is in general similar (Houghton et al. 2003); for the chemistry of Myoporaceae s. str., see Ghisalberti (1994), and for that of Verbascum, see Georgiev et al. (2011). Nicodemia (= Buddleja) is reported to have tannin (Bate-Smith & Metcalfe 1957).
The wood anatomy of Buddleja is similar to that of Nuxia, Peltanthera, Androya, etc. (Carlquist 1997c), i.e. with taxa that are not immediately related to it. Some Scrophulariaceae have opposite leaves, an angled stem, and 1:3 nodes, however, I have not seen the little bundles of fibres that run along the ridges of otherwise similar stems in Linderniaceae. There are glands in the leaves of Leucophyllum and Capraria, c.f. those of Myoporaceae (Lersten & Beaman 1998; Lersten & Curtis 2001). Scrophularia and Verbascum also have distinctive cells (idioblasts) in their leaves (Lersten & Curtis 1997) perhaps similar to the glands of Myoporaceae s. str.
Taxa with more or less polysymmetric flowers - sometimes rather like those of Silene, which some South African species may mimic - are common in almost all tribes, although the corolla tube of such flowers may be more or less bent and the two pairs of anthers are borne at different heights in the tube. There are also taxa with five rotate corolla lobes and five stamens (Capraria) and four lobes and stamens (some species of Buddleja), and in both cases the flowers are fully polysymmetric. Flowers of Verbascum s. str. have five stamens, but those of Celsia, embedded in Verbascum, have only four. Hemimeris may have inverted (and inversostylous!) flowers, but the adaxial lobe of the corolla is patterned, i.e. it is not functionally different from the normal condition with patterning on the abaxial lobe and adjacent lateral abaxial lobes. Stamens with two apically-confluent thecae are common; the anthers may be straight or U-shaped, but not sagittate. Both Buddleja and Verbascum lack orbicules in their anthers (Vinckier and Smets 2002a).
A number of taxa have cushion-shaped scars on the placenta, often with a central umbo or pedestal; these mark the place where the seeds fell off. Other taxa, e.g. the single-ovuled members of Manuleeae, have much thickened funicles.
Additional general information is taken from Rogers (1986) and Norman (2000), both Loganiaceae, Oxelman et al. (2004a: Buddlejaceae s. str., 2005), Theisen and Fischer (2004: Myoporaceae), Fischer (2004b: Scrophulariaceae p. pte); see also Jansen (1999) and Harborne and Williams (1971), both chemistry, Carlquist (1997c: wood anatomy), Hartl (1959: seed coat/rumination), and Bendre (1975), Maheshwari Devi and Lakshminarayana (1980) and Maldonado de Magnano (1986b, 1987: embryology); for floral development, see Armstrong and Douglas (1989) and Endress (1999).
Phylogeny. For phylogenetic relationships, see B. Bremer et al. (1994) and Nickrent et al. (1998). The main issues are relationships with the old Selaginaceae, Buddlejaceae and Myoporaceae.
The old Selaginaceae/Selagineae with a single apical ovule per loculus link with Scrophulariaceae-Manuleeae, although the latter have more ovules, these are very variable in both number and orientation (see also Hilliard & Burtt 1977; Hilliard 1994). A number of these taxa have bracts that are adnate to the calyx, a deeply lobed calyx, nectary to one side of the ovary, lingulate stigma, etc. (Kornhall et al. 2001, which see for phylogeny and optimisation of characters). Also included here are Scrophulariaceae-Hemimerideae (see also Oxelman et al. 1999b); the cosmopolitan aquatic Limosella is to be placed with these southern African taxa (Kornhall & Bremer 2004).
Buddleja, ex Loganiaceae, is very much paraphyletic and includes Nicodemia, Emorya, and Gomphostigma; several lines of evidence place it in Scrophulariaceae (e.g. Maldonado de Magnano 1986b). Teedia and Oftia have strong support as the sister group to Buddleja s.l. (Wallick et al. 2001, 2002), while Kornhall et al. (2001) found that most other Scrophulariaceae were in a clade sister to Buddleja and immediate relatives.
The old Myoporaceae are usually shrubby plants with more or less sessile and isobilateral leaves that have pellucid gland dots, and sympetalous and often strongly monosymmetric flowers. Core Myoporaceae have only a few epitropous ovules per loculus, the seeds have only slight endosperm, and the fruit is a drupe or schizocarp. Leucophyllum has only a single pellucid gland at the apex of the lamina and Eremogeton has none. The association of Leucophyllum with Myoporaceae is well established (e.g. Schwarzbach & McDade 2002; Gándara & Sosa 2013), and both have distinctive pollen - tricolpate, with each colpus diorate (Niezgoda & Tomb 1975; Argue 1980). Within Leucophylleae, Leucophyllum is strongly paraphyletic, including Eremogeton, etc. (Gándara & Sosa 2013: support poor to strong). Capraria has glands in its leaves and pollen like that of other Myoporaceae; again, it fits nicely here (for leaf glands of these two genera, see Lersten & Beaman 1998; c.f. also Henrickson & Flyr 1985; Lersten & Curtis 2001). Oftia has intraxylary phloem; this is not known for Teedia, its close relative. Oftia, with a racemose inflorescence, only four ovules/carpel, and a drupaceous fruit, the seeds having a very hard testa and copious endosperm, is also Myoporaceae (see Takhtajan 1997: some information from Dahlgren & Rao 1971). Androya (used to be Buddlejaceae) and Aptosimum may be around here; the former, however, has pollen that has been compared with that of Nicodemia (Loganiaceae s. str.). Androya is sister to Myopyrum (Kornhall et al. 2001). Kornhall and Bremer (2004) found relationships that can be represented as [Myoporum, etc. [Buddleja, etc. [Limosella, Manueleae, etc.]]]. The position of Myoporum, etc., vary: sister to Scrophulariaceae s.l., inc. Buddleja (Kornhall et al. 2001), or sister to Leucophylleae, in turn sister to Androya, the whole lot embedded in Scrophulariaceae (Oxelman et al. 2005), and all with tricolpate diorate pollen.
For relationships in the South African Nemesia, see Datson et al. (2008: unreversed woody -> herbs), and for those in Scrophularia, see Scheneurt and Heubl (2014 and references).
Classification. Olmstead et al. (2001) suggested that recognition of Myoporaceae might make Scrophulariaceae paraphyletic; Chinnock (2007), monographing Myoporaceae s. str., suggested that they could well be included in Scrophulariaceae.
Generic limits in Leucophylleae will need to be redrawn; a single genus for the tribe would work, but Gándara and Sosa (2013) propose the recognition of five.
Previous Relationships. The limits of Scrophulariaceae have long been problematic (Thieret 1967 for a summary; Olmstead 2002 for a readable account of the implications of the findings of molecular data). Albach et al. (2005a) and Oxelman et al. (2005) are clarifying the contents of the separate clades that used to be subsumed in Scrophulariaceae s. l. (see also B. Bremer et al. 2002; Tank et al. 2006); for further details see the introduction to Lamiales above.
Members of the classical Scrophulariaceae are now to be found in Plantaginaceae and Orobanchaceae (these have most of the taxa that have moved), as well as in Stilbaceae, Phrymaceae, Mazaceae, and Linderniaceae. Other genera previously associated with Scrophulariaceae and thought to be links with other families include Nelsonia and its relatives (see Acanthaceae) and Paulownia (see Paulowniaceae). Buddleja (et al.) was included in Loganiaceae or placed in its own family.
Thanks. To F. Zapata, for useful comments on the family.
Synonymy: Bontiaceae Horaninow, Buddlejaceae K. Wilhelm, nom. cons., Caprariaceae Martynov, Hebenstretiaceae Horaninow, Hemimeridaceae Doweld, Limosellaceae J. Agardh, Myoporaceae R. Brown, nom. cons., Oftiaceae Takhtajan & Reveal, Selaginaceae Choisy, nom. cons., Verbascaceae Berchtold & J. Presl
[Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]: ?
Age. This clade was estimated to be (70-)61, 54(-51) m.y.o. by Bell et al. (2010).
STILBACEAE Kunth, nom. cons. Back to Lamiales
Ericoid shrubs, ordinary shrubs, or herbs; (iridoids from deoxyloganic acid - C-8 iridoid glucosides), (cornosides +); cork just outside pericycle; vessel elements also with scalariform perforation plates; nodes ?; petiole bundle?; stomata?, cuticle waxes as rods or threads; lamina vernation revolute or not, (margins minutely toothed); inflorescence branches cymose, (plant cauliflorous), (flowers axillary); bracteoles as long as K; flowers often radial, (4) 5(-7)-merous; K bilobed or not (free), C lobes equal to unequal; stamens = sepals, (one fewer; staminode +), anther thecae confluent apically, or parallel and with separate slits; ovary apically unilocular, or unilocular, [1 G infertile, or septum 0], or bilocular, stigma slightly bifid or punctate; ovules 1-2/carpel, ascending and/or descending, apo/epitropous, or many; fruit a loculicidal (and septicidal) capsule, (indehiscent), K and C persistent; (seeds with pedestals - Charadrophila); embryo cylindrical [always?], endosperm +; n = 10, 12, 19; protein bodies in nucleus crystalline [Halleria].
11[list]/39: Nuxia (15). Most South Africa, the Cape Province, also to tropical Africa, Madagascar, the Mascarenes and Arabia (map: from Leeuwenberg 1975). [Photo - Nuxia Inflorescence, Halleria Flower.]
Evolution. Pollination Biology. Oil flowers are quite common in the family (Renner & Schaefer 2010).
Chemistry, Morphology, etc. The C-8 iridoid glucosides common in Stilbaceae are extremely uncommon elsewhere (Frederiksen et al. 1999); for unedoside, present in at least some genera of Stilbaceae, see Oxelman et al. (2004a). Indeed, some iridoids in Stilbaceae are like those of Loasaceae and Hydrangeaceae; all three have unedoside (Jensen et al. 1998). By and large, the gynoecium is reminiscent of that of Scrophulariaceae-Manueleae. Thesmophora appears to have two collateral carpels, each with one descending ovule (Rourke 1993) - perhaps an abaxial carpel divided by a false septum.
For general information, see Linder (2004: narrow circumscription), Fischer (2004b: some genera in Scrophulariaceae), for anatomy and morphology, see Carlquist (1986) and Dahgren et al. (1979), for embryology, see Junell (1934) and Engell (1987), and for the morphology of Charadrophila, see Weber (1989).
Phylogeny. Retziaceae and Stilbaceae come out together in rbcL trees (Wagstaff & Olmstead 1997); for another early study, see B. Bremer et al. (1994). Nuxia (ex Loganiaceae) is also placed here in molecular phylogenies (Backlund et al. 2000; Wallick et al. 2002), and this makes phytochemical sense (Frederiksen et al. 1999). The cauliflorous Halleria is also to be included in Stilbaceae (Olmstead et al. 2001). Genera like the gesneriad-like Charadrophila (the common name for this plant is "Cape gloxinia") and Scrophulariaceae-Bowkerieae (Bowkeria, Anastrebe and Ixianthes) are now members of the family; Charadrophila and Halleria may form a clde - but little support yet - that is sister to the rest of the family (good support: Oxelman et al. 2005). Thesmophora has not been included in these studies.
Classification. Rourke (2000) recognised two subfamilies, Retzioideae and Stilboideae, in Retziaceae, Kornhall (2004) recognized three tribes. However, the circumscription of the family has greatly changed from what it was ten years ago (see also Tank et al. 2006).
Synonymy: Halleriaceae Trinius, Retziaceae Choisy
[[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]: ?Evolution. Divergence & Distribution. Sensitive stigmatic lobes occur sporadically in this part of the tree (see also Endress 1994b).
[Byblidaceae + Linderniaceae]: bracteoles 0; x = 8, 9.
Chemistry, Morphology, etc. Flowers are either axillary or the inflorescence is racemose in this clade - not too much difference between the two!
BYBLIDACEAE Domin, nom. cons. Back to Lamiales
Rhizomatous and woody to ephemeral herbs; cork?; young stem with separate bundles; nodes 1:1 or 1:3; stomata paracytic; leaves spiral, lamina linear, abaxially curved or straight, veins parallel; flowers single, axillary; flowers subpolysymmetric; K connate only basally, C contorted, connate only basally, margins fimbriate; A ± monosymmetric, stamens 5, shortly epipetalous, anthers dehiscing by short slits or pores, epidermal cells ephemeral; nectary 0; stigma punctate to capitate (slightly bilobed); ovules 2-several/carpel, ± apical; exotestal cells tangentially somewhat elongated, anticlinal walls not uniformly thickened, mesotesta sclerenchymatous; endosperm starchy, with aleurone, copious; proteinaceous inclusions in the nucleus?
1[list]/6. W. and N. Australia, S. New Guinea (map: from van Steenis 1971; FloraBase 2004). [Photos - Collection.]
Age. A single seed, now destroyed, from the Middle Eocene of South Australia may be assignable to this family (Conran & Christophel 2004).
Evolution. Ecology & Physiology. Although there is no evidence that the plant absorbs nutrients from the insects that often stick to it (Hartmeyer 1997, 1998; Mueller et al. 2001), Conran and Carolin (2004) note that mirid bugs are associated with the genus, and so there may be a relationship similar to that in Roridula (Ericales) where the plant absorbs nutrients from the excreta of the bug.
Pollination Biology & Seed Dispersal. Although the flowers are basically polysymmetric, the stamens are held to one side of the flower. Buzz pollination is likely.
Chemistry, Morphology, etc. Byblis linifolia has leaves that are sometimes abaxially curled in bud and so are like those of Drosophyllum (Drosophyllaceae, Caryophyllales). However, the glandular hairs of Byblidaceae have the typical structure of those of core Lamiales and look like little parasols; those of Drosophyllum are vascularized and have irregularly arranged cells in the head.
Diels (1930b) drew the flower of Byblis with the odd sepal abaxial. Byblidaceae are often described as being bitegmic, but c.f. Diels (1930b) and Vani-Hardev (1972).
See Conran and Carolin (2004), McPherson (2008, 2010), and the Carnivorous Plants Database for more information, also Conran (1996: embryology), Cutler and Gregory (1998: anatomy), Conran et al. (2002: chromosome numbers), and Lloyd (1942) and Juniper et al. (1989) for plant morphology.
Previous Relationships. Roridula (see Roridulaceae - Ericales) has hitherto often been placed in the same family as Byblis as Byblidaceae and then included in Rosales, as by Cronquist (1981), or the two kept separate, but both placed in Byblidales, in Aralianae, as by Takhtajan (1997).
LINDERNIACEAE Borsch, K. Müller, & Eb. Fischer Back to Lamiales
Ephemerals to suffruticose perennials; iridoids 0; cork?; nodes 1:3; stems angled; leaves (basally connate), lamina venation also pamate, margins entire or serrate; (flowers single, axillary); (K free); C with glandular hairs on the inside; A curved, 4, staminode +/0, or A 2, the adaxial pair, also 2 large abaxial Z-shaped staminodes with an appendage, or staminodes much reduced, anther thecae parallel to ± head to head; pollen 3(-5)-colpate; stigma bilobed, sensitive; ovule with spathulate embryo sac, embryo sac protrudes through the micropyle, integument 3-4 cells across; capsule septicidal or -fragal; seeds with ruminate endosperm [surface alveolate - bothrospermous - or furrowed - aulacospermous] (smooth); n also = 12-14, etc. [x = 7-9?].
17[list]/255: Vandella (55), Torenia (51), Crepidorhopalon (30), Lindernia (30). Pantropical to warm temperate (map: based on Fischer 1992; Lewis 2000).
Evolution. Ecology & Physiology. Although many Linderniaceae seem to be rather delicate little herbs, a number are dessication tolerant (poikilohydric). These include the remarkable Chamaegigas intrepidus, which grows in transient pools - it is an aquatic resurrection plant - on inselbergs and probably uses glycine and serine as nitrogen sources (Heilmeier & Hartung 2011). Fresh leaves of Craterostigma plantagineum store large amounts of the unusual sugar, 2-octulose, which is converted into sucrose as the leaf dries (Bianchi et al. 1993; Farrant 2000). For more information on dessication tolerance in the family, see Dinakar and Bartels (2012 and references).
Pollination Biology & Seed Dispersal. In some species the anthers of the abaxial stamens are yellow and lie against the abaxial lip; they appear to contribute to the attractive aspect of the lip. In other species the long, curved abaxial filaments are joined by the connate anthers and form a sort of balustrade across the mouth of the corolla. Various hairs develop on the abaxial anther knees, and also inside the corolla, and the latter may have projections, flanges, etc.; all in all, a complex little flower (see e.g. Magin et al. 1989; Rahmanzadeh et al. 2004 for photographs). It would be interesting to know details of pollination mechanisms for such flowers, although small bees have been recorded as visitors (Magin et al. 1989). In Torenia fournieri, which has a less obviously distinctive floral morphology, the adaxial stamen pair elongate quickly and then more ot less protrude from the mounth of the corolla; the abaxial pair has anthers which, when touched on lever-like lateral flanges, open and forcibly extrude their pollen (Armstrong 1992).
Chemistry, Morphology, etc. The nodes appear to be 1:3, rather than 3:3 as I originally thought. Small strands of lignified tissue are associated with the sharp ridges of the stems in the couple of species that I have seen. The glandular heads of the hairs on the corolla and the vegetative plant have vertical partitions, as is common in Lamiales.
For the floral development of Torenia, see Armstrong (1988). Lewis (2002) suggests that the anthers are extrorse and the ovules are straight; Fischer (1992), however, gives a floral diagram showing introrse anthers and describes the ovules as being anatropous to hemitropous. The embryo sac protrudes beyond the micropyle in some species of both Torenia and Lindernia, at least (Wardlaw 1955; Yamazaki 1955); the synergids can then be ablated easily in studies of fertilization (Higashiyama et al. 2006). The rumination of the endosperm is caused by inpushings of endothelial cells (alveoli); these can become confluent and the seeds then have longitudinal ridges.
For more information, see Fischer (1989, 1992, 2004b - the latter Scrophulariaceae pro parte: general), and Takhtajan (2013: ovule and seed).
Phylogeny. Rahmanzadeh et al. (2004: Micranthemum not included) recovered this clade with 100% bootstrap support. Albach et al. (2005a) analysed four genes, separate analyses of three of which suggested this clade was distinct from Plantaginaceae; the joint analysis also supported separation. Micranthemum, with only two stamens, was sister to Lindernieae, whose members made up the rest of this clade (Albach et al. 2005a). Oxelman et al. (2005) found that Micranthemum was sister to Torenia, the two in turn were sister to Stemodiopsis, the only three Linderniaceae they examined. In a more extensive analysis, Fischer et al. (2013) found that the African Stemodiopsis was sister to the rest of the family, which was made up of the [Lindernia, etc.] and [Torenia, Craterostigma, Vandella, etc.] clades, all with strong support. See also Tank et al. (2006) for a summary of our ideas of relationships within this clade, and for the inclusion of Cubitanthus, ex-Gesneriaceae, see Perret et al. (2012; not included by Fischer et al. 2013) - it is sister to Stemodiopsis.
Classification. See Rahmanzadeh et al. (2004) and Tank et al. (2006) for the composition of Linderniaceae; the generic list here is rather notional. If Micranthemum belongs in this clade, some other Scrophulariaceae-Microcarpeae may also have to be included; they include aquatic herbs whose flowers usually have only the abaxial stamen pair fertile; the filaments have "clavate geniculations at base" (Fischer 2004b: p. ).
[[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]: ?
[Pedaliaceae [Martyniaceae + Acanthaceae]]: ?
PEDALIACEAE R. Brown, nom. cons. Back to Lamiales
Annual to perennial herbs (stems ± succulent), (roots swollen) to deciduous trees; 10-hydroxylated carboxylic iridoids [harpagoside], orobanchin, amyloid +; (cambium storied); pericycle also with sclereids (fibers few); petiole bundle interrupted-annular; hairs broadly capitate-stellate, mucilaginous; leaf (spiral - Sesamum), lamina (venation palmate), margins toothed, lobed or entire; flowers usu. axillary, (inflorescence branches cymose); paired nectaries (modified flowers) at base of pedicel (not - Uncarinia); (C with spur); A (5), thecae ± confluent, at right angles to filaments, staminode + (0); pollen 5-13 stephanocolpate; G [2-4], with false septae, (8 loculi - Josephinia), stigma with 2 broad lobes, often sensitive, wet; ovules 2-many/carpel, (1 ovule/"loculus" - Josephinia), integument 7-20 cells across, hypostase +; fruit with hooks or glochidiate spines, etc., (schizocarp; nut; wind-dispersed); seeds winged or not, surface often sculpted, testa multiplicative, exotestal cells palisade or otherwise thickened, (mesotesta with crystals); endosperm slight, cotyledons with fat and amyloid [xyloglucans]; n = 8 (13); protein bodies in nucleus?
14[list]/70: Sesamum (19), Pterodiscus (13). Mostly Old World tropical, in coastal or arid habitats (map: from Ihlenfeldt & Grabow-Seidensticker 1979; FloraBase 2005; Australia's Virtual Herbarium xii.2012; Ihlenfeldt 1994b, 2010).
Evolution. Pollination Biology & Seed Dispersal. The diversity of fruit morphology and dispersal "strategies" in this small family is remarkable, as is their variation in growth form (Ihlenfeldt 2010).
Chemistry, Morphology, etc. The iridoid glycoside harpagoside, known from Harpagophytum and Rogeria, is scattered in other Lamiales such as Lamiaceae, Plantaginaceae, and quite commonly in Scrophulariaceae (Georgiev et al. 2013). The mucilage glands that are often so conspicuous normally have four apical cells.
The apparently single axillary flowers of some taxa appear to represent reduced cymes, the paired nectaries at the base of the pedicel representing modified flowers (Manning 1991). Josephinia may have four carpels, each loculus being divided - an unusual combination for a euasterid. Although Rogeria is reported to occur in Brasil, this seems to be a mistake (Volker Bittrich, pers. comm.).
Some information is taken from Stapf (1895), Carlquist (1987b: wood anatomy), S. D. Manning (1991: U.S.A., general), and Ihlenfeldt (1967, 2004, 2010: general), also Jordaan (2011: seed coat of Harpagophytum - complex).
Synonymy: Sesamaceae Berchtold & J. Presl
[Martyniaceae + Acanthaceae]: ?
MARTYNIACEAE Horaninow, nom. cons. Back to Lamiales
Annual herbs, roots often tuberous (perennials; woody); petiole bundle deeply arcuate, also adaxial cortical and medullary bundles; plant long sticky-hairy; leaves also spiral, lamina margins toothed; (K free); A (2 + 2 staminodes - Martynia), connective with apical gland, staminode(s) +; pollen grain tricellular, inaperturate, exine dissected into 20-40 platelets, adjacent or somewhat separate, with reticulate sculpture (smooth raised rings, surface inside smooth - Craniolaria); G with parietal placentation, placentae T-shaped, ovules at the end, stigma bilobed, sensitive; 2-many ovules/carpel; capsule with paired apical spurs or hooks [developing from sterile upper part of ovary], (± smooth), outer mesocarp ± fleshy, caducous, inner mesocarp woody, with crests and spines; seeds large [>10 mm long], (ca 3 mm long); testa ca 5 layers thick, exotesta subgelatinous, or inner and radial walls with cellulosic bands, inner layers lignified [Proboscidea], or single outer layer, hair-like structures below [?bands of thickening - Martynia, no other cellular details], or lignified exotesta only persistent; endosperm at most thin; n = 15 (16, 18).
5[list]/16: Proboscidea (10). Tropical and subtropical America, rather scattered (for map, see Gutierrez 2011).
Evolution. Divergence & Distribution. The primary division in the family is between North American and South American taxa (Gutierrez 2011).
Ecology & Physiology. Insects may stick to the very viscid indumentum of Martyniaceae, although there is no evidence that the plants are carnivorous (see Rice 2008; Plachno et al. 2009; c.f. Stylidiaceae [Asterales], which also have sticky hairs and for which there are recent suggestions that there may be carnivory). Martyniaceae are not immediately related to Lentibulariaceae and Byblidaceae, which are both directly or indirectly carnivorous (Müller et al. 2004).
Seed Dispersal. The outer part of the pericarp rots away to expose the distinctive spiny/thorny fruits that are quintessential trample burrs; the anatomy of the fruit wall is complex (Horbens et al. 2014). The seeds of several Martyniaceae are very large compared with those of other core Lamiales.
Chemistry, Morphology, etc. General information is taken from Stapf (1895), Ihlenfeldt (2004) and McPherson (2010, vol. 2, esp. photographs) and especially Gutierrez (2011); see also S. Singh (1970: embryology, etc.), Carlquist (1987b: wood anatomy) and Bretting and Nilsson (1988: pollen morphology). For the seed coat, see Ricketson & Schmidt 4981 (Proboscidea areania), Gentry & Zardini 48864 (Martynia annua).
Phylogeny. For relationships within Martyniaceae, see Gutierrez (2008, esp. 2011); the northern Proboscidea and Martynia form a clade sister to the rest of the family.
Previous Relationships. Martyniaceae and Pedaliaceae have often been combined (as Pedaliaceae, e.g. Cronquist 1981), but there is currently little evidence that they form a monophyletic group. Differences in pollen (inaperturate and with platelets vs several colpi) and placentation (parietal vs axile) clearly separate the two morphologically. In addition, the remarkable branched spines, etc., of Pedaliaceae develop as such while those of Martyniaceae become exposed as the outer layer of the fruit rots away.
ACANTHACEAE Jussieu, nom. cons. Back to Lamiales
Quaternary methylammonium compounds, amyloid +; (cork cambium deep seated); stomata diacytic; nodes swollen [?level]; lamina margins entire to toothed; (inflorescence branches cymose), bracts large, conspicuous; K free or connate, often sharply pointed, adaxial lobes of C outside others in bud [= descending cochleate aestivation], (C lobes narrow); A (2; 2 + 2 staminodes; 5), staminode +/0; G lacking septal bundles; ovule with "thin" integument; embryo sac long, curved, (apex of 4-nucleate sac growing out of the micropyle and eventually into the placenta); (zygote pushed back into the ovule by a long suspensor); capsule dehiscence explosive, walls cartilaginous, K persistent; endosperm development highly asymmetric, the two haustoria lying close to each other, second division of the endosperm transverse, embryo often ± curved.
220[list]/4,000 - eleven groups below. Mostly tropical.
Age. Crown-group Acanthaceae may be slightly over 90 m.y.o. (Tripp et al. 2013b), around 57 m.y. (Tripp & McDade 2014a), or (92.3-)81.9(-71.7) m.y. (Tripp & McDade 2014b).
1. Nelsonioideae Sreemadhavan
Herbs; gland-headed hairs with 2-celled heads; (leaves spiral); bracts spiral, (bracteoles 0 - Nelsonia); (A 2), anthers variable (e.g. thecae ± separate); ovary (with parietal placentation - Elytraria); stigma broadly (unequally) lobed, (sensitive - Elytraria); ovules many(-4)/carpel, campylotropous, endothelium +; antipodal cells persistent; funicular obturator +; jaculators rudimentary[?]; seeds 2-many, ruminate, testa ± disorganised (± visible - Nelsonia); endosperm +, oily; n = 9.
6-7/170: Staurogyne (140). Tropical.
Age. Crown-group Nelsonioideae are estimated to be (81.5-)67.7(-53.8) m.y.o. (Tripp & McDade 2014b).
Synonymy: Nelsoniaceae Sreemadhavan
[Acanthoideae [Thunbergioideae + Avicennioideae]]: (inverted vascular bundles in the pith); acicular fibres +; pollen usu. other than tricolpate or -colporate; ovules 2/carpel; collateral, endothelium 0, funicular obturator 0; (amyloid [xyloglucans] in cotyledons +), endosperm 0.
Age. Estimates of the age for this node are (50-)41, 38(-29) m.y. (Bell et al. 2010), (38-)35, 27(-24) m.y. (Wikström et al. 2001), ca 54 m.y. (Bremer et al. 2004) and (80.7-)70.9(-61.4) m.y. (Tripp & McDade 2014b).
2. Acanthoideae Eaton
Herbs (to shrubs); (benzoxazinones +); cystoliths + (0); petiole bundles arcuate, arranged in a circle, (annular); (leaf margins spiny); C often with abaxial lobe outside others in bud [= ascending cochleate aestivation], (slit-monosymmetric - rare); anthers sagittate, or thecae displaced and not opposite, (one theca ± reduced); pollen hideously variable, often porate; stigma dry, usu. bifid; ?funicular obturator; capsules obovoid; seeds flattened, 2-few, (hairy), borne on hook-like hardened funicles [jaculators, retinacula]; exotesta palisade, (mucilaginous), (hypodermal cells thickened); cytologically very variable.
217/3,220: Asystasia (70). World-wide; the bulk of the family (map: from Brummit 2007). [Photo - Habit, Flower.]
Age. The age of this node was estimated at (102-)79(-65) m.y.a. (Tripp et al. 2013b) or (80.1-)71.1(-61.9) m.y.a. (Tripp & McDade 1014b).
Nodes not swollen; A 4, anthers monothecous; pollen tricolpate.
21/500: Aphelandra (170), Blepharis (130).
[[Ruellieae + Justicieae] [BAWN clade]]: cystoliths +; pollen porate.
[Ruellieae + Justicieae]: pollen with false apertures.
(Filament curtain +); C left-contorted; pollen often reticulate, with compound apertures; adaxial stigmatic lobe shorter than the abaxial lobe, to 0; (ovules 3+/carpel); seeds with hygroscopic trichomes; n = 6 and just about everything else in the family, 15 and 16 common, x = 8?
38/1185: Ruellia (355), Strobilanthes (350), Hygrophila (100), Dyschoriste (80), Hemigraphis (60), Sanchezia (60).
(Flowers resupinate - Diclipterinae); parallel ridges on upper lip of corolla [rugula] holding style (0); A (2), thecae displaced, not opposite, connective expanded, etc.; pollen tricolporate, hexapseudocolpate.
Justicia (600), Ptysiglottis (60).
Synonymy: Justiciaceae Rafinesque
[Barlerieae + Andrographidae + Whitfieldieae + Nemacanthus] / BAWN clade: ?
C quincuncial; seed with hygroscopic trichomes.
/420: Barleria (300). Pantropical.
Pollen colporate, ornamented and thickened exine surrounding or over apertures; (ovules 3+/carpel).
(C left-contorted); pollen biporate, lenticular, granular around apertures; stigma capitate; seeds with concentric rings of ridges, (also hygroscopic trichomes + - Lankesteria).
K united, 3 + 2; pollen tricolporate, intercolpal regions psilate/foveolate; seed with hygroscopic trichomes.
1/30. Africa, Madagascar, Arabia to Vietnam.
[Thunbergioideae + Avicennioideae]: C left-contorted; filament bases thickened; ovules collateral; embryo sac ± on surface of nucellus; cotyledons folded.
Age. The age of this node was estimated to be ca 86 m.y. (Tripp et al. 2013b) or (80.7-)70.9(-61.4) m.y. (Tripp & McDade 2014b).
3. Thunbergioideae Kosteletzky
Twining vines (erect); (iridoids from deoxyloganic acid - C-8 iridoid glucosides, unedoside); rays 0 [Thunbergia], (intraxylary phloem/bicollateral vascular bundles +); petiole bundles arcuate or annular; lamina vernation strongly curved; inflorescence with 2 or more axillary flowers in the median plane of the leaf/inflorescence bract, adaxial flowers opening first; bracts 0, bracteoles very large, connate; K a rim, (up to 16 lobes), C (not contorted); anthers with lignified unicellular hairs (multicellular awns), sagittate, (thecae slightly displaced), dehiscing by (elongated) pores/slits, connective elongated, endothecium 0; pollen 8-colpate or spiraperturate; (adaxial carpel aborting - Mendoncia), stigma wet, small and sub-bilobed to trumpet-shaped, with broad and often unequal papillate lobes; capsule also septifragal, (fruit a 1-2-seeded drupe - Mendoncia); chalazal endosperm haustorium 0, (cotyledons twice folded - Mendoncia, etc.); n = 9, 28.
Ca 5/150: Thunbergia (90), Mendoncia (60: M. belizensis has rather boraginaceous hair bases). Tropical America, Africa and Madagascar, fewer in South East Asia - Malesia. [Photo - Flowers.]
Age. Crown-group Thunbergioideae are estimated to be (59.5-)47.2(-34.5) m.y.o. (Tripp & McDade 2014b).
Synonymy: Mendonciaceae Bremekamp, Meyeniaceae Sreemadhavan, Thunbergiaceae Lilja
4. Avicennioideae Miers
Trees; betaines +, tanniniferous; wood with successive cambia, phloem islands occurring in bands of conjunctive tissue; vessels in radial multiples; nodes 3:3; petiole bundle annular; sclereids +; lamina thick, with salt glands on both sides, colleters +; inflorescence in dense thyrsoid spicate units[!]; flowers (polysymmetric), 4(-6)-merous; K ± free, C with nectar glands on tube; stamens = and alternating with C; pollen 3-colporate; (G with false septae), loculi apically confluent, stigma with 2 blunt lobes; ovules apical on partitions, ± straight, apex of nucellus exposed; fruit an achene, K persistent, green; embryo green, cotyledons induplicate-reduplicate; n = 18, 32; embryo breaking the seed coat before the seed falls from the tree.
1/8 (species limits need attention). Mangroves in tropics, but also warm temperate (map: from Moldenke 1960; Tomlinson 1986). [Photo - Flower]
Age. Ricklefs et al. (2006) dated ?crown-group Avicennia to ca 42 m.y.; (39.3-)38.7(-38.4) m.y. is the estimate in Tripp and McDade (2014b).
Synonymy: Avicenniaceae Miquel, nom. cons.
Evolution. Divergence & Distribution. For a careful discussion of dating in the family, and also dates for nodes other than those given above, see Tripp and McDade (2014b). Depending on the calibration, dates varied by a factor of about two; the dates here are those preferred by Tripp and McDade (2014b); the analysis included several fossil calibrations, but no calibrations far from the in-group, no secondary calibrations, and so on. Tripp and McDade (2014b) validated the identity of a surprisingly large number of fossils that had been attributed to the family.
There are more species of Acanthoideae in the New World, more genera in the Old World, but that is probably an artefact of taxonomists' minds (Tripp et al. 2013a) - and of course genera don't mean very much anyhow. However, nearly all intercontinental (11/13) movements seem to have been from the Old to the New World; they have occurred in Acanthoideae, probably by long distance dispersal, and within the last 20 m.y. or so (Tripp & McDade 2014b).
Physacanthus is apparently the product of an ancient hybridization event between Acantheae and Ruellieae and has characters of both; it lacks cystoliths, as do the former, but it has pollen with compound germinal apertures, as do the latter (Tripp et al. 2013b).
Borg and Schönenberger (2011) mention possible floral/developmental apomorphies of Thunbergioideae and Avicennioideae. The features characterizing Nelsonioideae mentioned by Scotland and Vollesen (2000) - no retinacula or cystoliths, descending cochleate aestivation (i.e. the adaxial petals overlapping the abaxial petals in bud) - are likely to be plesiomorphies (see Eichler 1875; c.f. McDade et al. 2012), as is their sometimes rather undistinguished tricolpate or tricolporate pollen.
Ecology & Physiology. Many of the distinctive morphological features of Avicennia are common in other plants found in the mangrove habitat in which it grows. These include the large, green, more or less viviparous embryos that are the units of dispersal, pneumatophores, and salt glands on both surfaces of the fleshy leaf (Tomlinson 1986: for the evolution of the mangrove habitat, see Rhizophoraceae). These salt glands have largely radially-arranged cells in their heads (Fahn 1979), and appear to be variants of the common glandular hair type in Lamiales. Robert et al. (2009, 2011) discuss the hydraulic architecture of the wood of Avicennia in which both xylem and phloem are organized in a three-dimensional network.
C4 photosynthesis has been detected in a number of species of Blepharis section Acanthodium (Sage 2004). Blepharis includes mostly plants of dry habitats, some very small, very spiny, and with remarkable growth forms.
Pollination Biology & Seed Dispersal. Tripp and Manos (2008) studied the pollination systems in the speciose Ruellia. They found that although flowers specialised for bird or bee pollination may reverse pollinators (bee to bird transitions are usually decidedly uncommon - Barrett 2013), sphingid-adapted flowers do not reverse, perhaps because they had entirely lost their floral pigments. For bird pollination in Aphelandra, see McDade (1992). All told, 500-600 species of Acanthaceae are humming-bird pollinated (E. A. Tripp and L. McDade, pers. comm.: also Tripp & Manos 2008). Tripp et al. (2013c) noted that in two New World groups, justicioids and Ruellia, diversification of the acanths was after diversification of the birds, suggesting that diffuse co-evolution was unlikely. In a study focusing on Ruellia, of which around 130 species may be bird pollinated, Tripp and McDade (2014a) found that hummingbirds diversified considerably in the mid to late Miocene, diversification of Ruellia itself beginning (13.5-)9.0(-8.3) m.y.a., i.e. most of this spread is decidedly younger.
Full (180o) or partial resupination has evolved several times in Acanthoideae, and this is sometimes caused by the twisting of the corolla tube rather late in development (Daniel & McDade 2005), a rather unusual mechanism. Elytraria (Nelsonioideae) may also have inverted flowers. The filament curtain, formed from decurrent filament ridges in the corolla tube and more or less connate filaments immediately above the adnate portion of the filaments, is probably involved in pollination in Ruellieae and perhaps other taxa, too. The curtain divides the corolla tube vertically into compartments; transverse ridges may develop near the base of the corolla tube, and the nectar becomes enclosed in a separate chamber (Mantkelow 2000; see also Moylan et al. 2004b).
Capsules open explosively in all taxa except Avicennioideae and some Thunbergioideae, and Witztum and Schulgasser (1995) discuss in detail capsule dehiscence in Acanthoideae with their distinctive retinacula. There is some dispute as to whether Nelsonioideae have jaculators, but even if present, they are not functional; thus "rudimentary" retinacula are reported from the subfamily (Johri & Singh 1959; Roham Ram & Masand 1963). In a number of taxa the testa is mucilaginous.
In some species of Strobilanthes all the individuals flower and fruit in synchrony and then die; this happens in a regular cycle every few years and can occur over very large areas (Janzen 1976). Both pollinators and seed dispersers (the seed are rich in oils) are attracted to the plants in large numbers.
Plant-Animal Interactions. Gall-forming fruit flies of the Tephretidae-Tephrellini are found here (and on Verbenaceae and Lamiaceae: Korneyev 2005). Larvae of Nymphalinae-Melitaeini butterflies commonly feed on Acanthaceae (Wahlberg 2001; Nylin & Wahlberg 2008). Mass defoliation of Avicennia by lepidopteran larvae seems to be not uncommon (Fernandes et al. 2009).
Genes & Genomes. Physacanthus appears to represent the descendents of an ancient hybridization between Acantheae and Ruellieae and with back-crossing to the latter, remarkably, it has remained heteroplasmic (Tripp et al. 2011, esp. 2013b). Plants may be variegated, perhaps because of incompatibilies developing between organelles from plants with different genomes (Tripp et al. 2013b).
Chemistry, Morphology, etc. Mendoncia lacks iridoids. Inverted vascular bundles in the pith, or anomalous secondary thickening where an internal and inverted cambium develops, are scattered in the family, but neither have yet been found in Nelsonioideae or Avicennioideae (Schwarzbach & McDade 2002 for literature).
Thunbergia has extrafloral nectaries on the calyx as well as nectaries inside the corolla tube, while in Avicennia nectar is secreted from glands on the corolla tube (for details, see Tomlinson 1986). In Avicennia there may be fewer corolla than sepal lobes ("connation" of a pair of the former?). Bravaisia (Acanthoideae) is distinctive in that it has small bracteoles and rounded calyx and corolla lobes (the former are more or less scarious); the anthers have short basal appendages. There is discussion as to the nature of corolla tube initiation, which is probably usually more or less late, rarely early (c.f. Leins & Erbar 1997; Schönenberger & Endress 1998; see also Endress 1999 for floral development). Anther morphology is particularly variable in neotropical Justicia (Kiel et al. 2013). Pollen variation is extensive, but also shows extensive homoplasy (e.g. Kiel et al. 2006). Indeed, the variation in pollen morphology in the family is spectacular: for variation within Strobilanthes s.l., see Carine and Scotland (2000) and Wang and Blackmore (2003), for that within Acanthoideae as a whole, see Daniel (1998), Scotland and Vollesen (2000) and references, and Daniel (2010). Many Isoglossinae (Justicieae) have distinctive "Gürtelpollen" (Kiel et al. 2006) - lenticular biporate pollen with a prominent circumferential band. Although Acanthaceae (minus Nelsonioideae) are extremely heterogeneous palynologically, any functional significance of this variation is unclear. The [Acanthoideae [Thunbergioideae + Avicennioideae]] clade appears to lack a funicular obturator, but I am uncertain as to the polarity of this feature. The fruit of Avicennia is a capsule, according to Takhtajan (1997) and Schatz (2001), but it may split only as the seed germinates. In Mendoncia and relatives only one carpel is functional and the fruit is a drupe, while in Thunbergia and relatives the stigma is more or less trumpet-shaped and the fruit is a capsule, usually with four seeds. For cotyledon folding, see Schwarzbach and McDade (2002).
Embryo sac development in some/most Acanthaceae is very distinctive. The tip of the embryo sac grows through the micropyle and eventually may lodge in the placenta, and this where the egg apparatus is formed (the movements of the polar nuclei are unclear). As the embryo develops, a very long suspensor forms and the embryo is pushed back into the endosperm - and so into the ovule and the developing seed (e.g. Mohan Ram & Masand 1963 and references). This is rather similar to comparable, but more extreme, behavious in Loranthaceae. The ovule of Avicennia is reported to be straight; the embryo sac is extra-ovular, and the micropylar endosperm haustorium at least is also extra-ovular, being very much branched and reaching the placenta (Junell 1934; Padmanabhan 1964, 1970).
In Acanthoideae other than Acantheae, details of endosperm development show considerable variablity. There is often a central area in which divisions are free nuclear, walls being laid down subsequently, but in some taxa there is what is known as a "basal apparatus", an area in which walls are not laid down; this pattern of endosperm development occurs in no other angiosperms (Mohan Ram & Wadhi 1964; Johri et al. 1992 and references). In Nelsonioideae the central area is entirely cellular, but other details of endosperm and embryo sac development are like those just described (Johri & Singh 1959; Moham Ram & Masand 1963). This distinctive asymmetric endosperm development is also to be found in Lamiaceae-Nepetoideae (a parallelism).
For general anatomy, capsule dehiscence, etc., see van Tieghem (1908), for embryology, etc., see Mauritzon (1934a), and Wadhi (1970), and for stomata, see Rohweder et al. (1971). Some information on Nelsonioideae is taken from Bremekamp (1955), and on Thunbergia, etc., from Schönenberger (1999). For embryology, etc., of Avicennia, see Padmanabhan (1970, as Verbenaceae) and also Borg and Schönenberger (2011) and for wood anatomy, see Carlquist (1990b), for general information, see Tomlinson (1986) and Sanders (1997). Within Acanthoideae, for information on acicular fibres, see Bremekamp (1965: "raphidines"), for chemistry, see H. F. W. Jensen et al. (1988) and Sicker et el. (2000: benzoxazinones), for corolla aestivation, which shows interesting variation, see Scotland et al. (1994), and for floral morphology, see Endress (1994b).
Phylogeny. The erstwhile Nelsoniaceae were placed sister to rest of Acanthaceae in Hedren et al. (1995), and this position seems quite firm (see esp. McDade et al. 2012). The position of Avicennia (Avicenniaceae) within Acanthaceae s.l. is fairly well established (they all have the same distinctive endosperm development, swollen nodes, etc.); it shows a rather weakly supported sister group relationship with Thunbergioideae (Schwarzbach & McDade 2002; Hilu et al. 2003). Support for the [Thunbergioideae + Avicennioideae] clade has remained rather weak and comes mostly from the chloroplast genes (McDade et al. 2008). Relationships in Tripp and McDade (2014a) were [Nelsonioideae [Thunbergioideae [Avicennioideae + Acanthoideae]]], although again the position of Avicennioideae was not well supported.
Within Nelsonioideae, Nelsonia and Elytraria are probably successively sister to the rest of the subfamily, within which there is quite a lot more structure (McDade et al. 2012, see also 2009; Wenk & Daniel 2009: position of Nelsonia uncertain).
For the phylogeny of Acanthoideae, see McDade et al. (2008: see also McDade & Moody 1999; McDade et al. 2000a; McDade et al. 2006; Tripp & McDade 2014a): Acantheae are sister to the rest. In Acantheae, McDade et al. (2005) found that taxa with one- and two-lipped corollas form separate clades, Old World and largely New World respectively. For Justicieae, mostly New World, see McDade et al. (2000b), Kiel et al. (2009), and in particular the very useful treatment by Tripp et al. (2013a). For relationships in the Tetramerium group, see Daniel et al. (2008). Ruellia is defined by pollen morphology, and it includes genera like Blechum, etc.; many taxa are cleistogamous (Tripp & Manos 2006; Tripp 2007). Ruellieae and Acantheae appear to have hybridized in the past (Tripp et al. 2013b). For more on phylogenetic relationships, see Scotland et al. (1995).
TBorg et al. (2006) provide a phylogeny for Thunbergioideae and discuss their biogeography and the evolution of some characters.
Classification. The tribal classification of Acanthoideae follows that in McDade et al. (2008). Generic limits are difficult, as in other groups where the genera are often based on variation in corolla morphology that represent adaptations to particular pollinators (e.g. Daniel et al. 2008 and references); Bremekamp (1944) dismembered Strobilanthes into some 54 genera most of which have been returned to whence they came. Floral variation may be less reliable in marking genera than variation in e.g. seed and pollen[!] (Kiel & McDade 2014). Genera in Justicieae are being recircumscribed and have been assigned to subtribes (Tripp et al. 2013a).
Species numbers seem particularly uncertain here, as Tripp et al. (2013a) suggest.
Previous Relationships. Nelsonioideae have often been placed in Scrophulariaceae s.l. or considered "intermediate" between Scrophulariaceae and Acanthaceae. Avicennia was often included in Verbenaceae, largely because it is woody, has a more or less cymose inflorescence, and a gynoecium with two ovules per carpel, but the similarity is only superficial. For Thomandersia, the seeds of which have a structure described as a retinaculum (c.f. Acanthoideae), although they do not dehisce explosively, see Thomandersiaceae.
[Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]: ?
BIGNONIACEAE Jussieu Back to Lamiales
Woody, trees or shrubs; C-4 carboxyl and ecarboxylated iridoids +; cork also cortical; scanty paratracheal axial parenchyma; nodes 1:1-9; petiole bundles annular (also rib or adaxial bundles); stomata helicocytic [?level]; leaves bicompound, lamina vernation conduplicate (involute - Pyrostegia), margins entire (toothed); inflorescence branches cymose; flowers large; K often with nectaries, A (5, 2), thecae sagittate or head-to-head, usu. not confluent, tapetum amoeboid; pollen tricolpate, psilate, nonperforate; bundles in the ovary wall and also opposite septum, ovules in two groups in each loculus, (placentae lobed), stigma lobes broad, sensitive, wet; integument 5-7 cells across, nucellar endothelium +; fruit often with epidermal extrafloral nectaries; seeds many, winged, relatively large; cells in wings with helical or annular (none; reticulate) thickenings; endosperm 0, micropylar haustoria 0; n = 20; germination epigeal, phanerocotylar (cryptocotylar), cotyledons obcordate, lobed, persistent.
110[list]/800 - eight groups and unassigned below. Mainly tropical, esp. South America (map: from van Steenis 1977). [Photos - Amphitechna Flower, Distictella Flower.]
Age. Fossil seeds and fruit of Bignoniaceae are known from the Eocene of Washington State, being dated to ca 49.4 m.y. (Pigg & Wehr 2002).
1. Jacarandeae Seeman
Aliform parenchyma +; K ± free, staminode large, bearded; G with parietal placentation; fruit orbicular, angustiseptate; n = 18.
1(?2)/55: Jacaranda (50). Tropical America.
[Tourrettieae [Tecomeae [Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleae]]]]]: (vessel elements with reticulate and/or foraminate perforation plates).
2. Tourrettieae G. Don
Vines, climbing by tendrils; (leaves pedate);inflorescence racemose, bracteate; staminode 0.
2/6. Andes in South America and N. to Mexico. [Photo - Eccremocarpus Flower.]
[Tecomeae [Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleae]]]]: leaves once compound; (staminodes +, simple).
3. Tecomeae Endlicher
Distinctive C-4 formyl iridoids; (perforated ray cells).
12/55. Worldwide, not Arctic.
[Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleae]]]: ?
Age. An estimate of the age for the clade [Campsis, Catalpa] is (32-)25(-17) m.y. (Bell et al. 2010).
4. Bignonieae Dumortier
Lianes, climbing by tendrils; (monofluoracetates +); (cambium storied); anomalous secondary thickening + [phloem discontinuous, the basal condition is for the xylem cylinder to be 4-lobed]; rays tall [usu. >1 mm tall], ray cells perforated; leaves usu. ternate; fruit usu. septifragal, with persistent septum and separate whip-like strands of woody tissue [= vascular bundles opposite septum].
21/380: Adenocalymma (78), Arrabidea (69), Anemopaegma (42), Amphilophium (41). America, largely tropical.
Age. Crown-group Bignonieae have been dated to (54.2-)49.8(-45.7) m.y., the crown clade that includes the tribe minus the monotypic Perianthomega being (52.2-)48.0(-43.9) m.y. old (Lohmann et al. 2012).
[[Catalpeae + Oroxyleae] [Crescentieae + Coleae]]: (vasicentic or aliform parenchyma +).
[Catalpeae + Oroxyleae]: ?
5. Catalpeae Meisner
Leaves simple; (A 2).
2-3/11. North America, the Greater Antilles, East Asia.
6. Oroxyleae A. H. Gentry
(Flowers polysymmetric); (A 5); fruits septicidal.
[Crescentieae + Coleae]: ?
7. Crescentieae G. Don
Cambium storied; leaves palmate, (unifoliolate; spiral, simple, phyllodinous); (flowers bat-pollinated, ± cauliflorous); (fruits ± indehiscent; seeds not or barely winged).
12/147: Tabebuia (70). Central and South America and the Greater Antilles.
Synonymy: Crescentiaceae Dumortier
8. Coleae Bojer
(Leaves phyllodinous, articulated); flowers bat-pollinated, ± cauliflorous; fruits ± indehiscent; seeds ?not winged.
4/60. Madagascar and surrounding islands.
Evolution. Divergence & Distribution. The family is probably New World in origin, with five or six shifts to the Old World and one back to the New World (Olmstead et al. 2009; Olmstead 2013). Lohmann et al. (2012, q.v. for many dates in the tribe, etc.) suggested that the ancestors of Central and North American (Panama, Washington State) fossils assignable to Bignonieae, as well as North American Bignonia itself, might have arrived there by long distance dispersal. Interestingly, members of three clades which are surmised to have been involved in long distance dispersal are currently dispersed by animals; Olmstead (2013) thought that adaptation to animal dispersal had occurred after wind-assisted dispersal events.
Ecology & Physiology. Bignoniaceae-Bignonieae are, along with Sapindaceae, the most ecologically important neotropical group of lianes; Sousa-Baena et al. (2014) discuss the evolution of their tendrils. Bignoniaceae as a whole are the second most speciose family in drier tropical forest types in America (Gentry 1988, 1991).
Extrafloral nectaries are extremely common; these may be on reduced prophylls, on the tips of young leaflets, at the nodes, on the outer surface of the calyx and on the ovary; ants are attrcted (e.g. Gonzalez 2011). Domatia are also common.
Pollination Biology & Seed Dispersal. The large flowers of Bignoniaceae are animal pollinated, and the considerable variation in floral morphology and flowering phenology can be associated with the behaviour and type of visitor (Gentry 1974a, b, 1990; Alcantara & Lohmann 2010a, b). One of the commonest flower types in the New World is the Anemopaegma type, visited by euglossine bees (along with anthophorids); this may be ancestral in Bignonieae, and has an infundibular, straight corolla tube, nectar, and is magenta, yellow or white in colour (Alcantara & Lohmann 2010a). The nectarless Cydista type, otherwise rather similar florally, is also visited by euglossines. (Note that euglossine bees began diversifying some 42-27 m.y.a. - Ramírez et al. 2010.) Oroxylon is bat pollinated, and its flowers are almost polysymmetric and have five stamens; Fleming et al. (2009) list species in the family that are known to be pollinated by bats. Alcantara and Lohmann (2010a, b) found that, in general, flower size in the lianescent Bignonieae was larger in the past than it is is in extant species.
Dispersal syndromes are also quite diverse (Gentry 1983; 1990) but they are not particularly correlated with pollination syndromes. Thus Kigelia africana is bat-pollinated and has massive, sausage-shaped, indehiscent fruits that are eaten by everything from monkeys to elephants. Oroxylon is also pollinated by bats, but it has capsules and wind-dispersed seeds. Wind dispersal is common, and the seeds often have broad, papery wings. A number of taxa have seeds dispersed by water, including Dolichandrone, a mangrove plant; here the modified seed wing is corky and serves as a flotation device. In Crescentieae, Amphitecna and Crescentia (calabash) have spherical indehiscent fruits, Parmentiera has elongated fleshy fruits, although its seeds still have a small wing, and Spirotecoma and Tabebuia and relatives have elongated, dehiscent fruits and winged seeds.
Vegetative Variation. Bignonieae are nearly all lianes with branched tendrils and distinctively rayed xylem (Lohmann 2006 for a phylogeny). Perianthomega has biternate leaves, it also has robust unbranched tendrils that represent petioles, the three small scars at their ends represent leaflets. Within Bignonieae, variation in the detail of the ray-like fluting of the xylem can be interpreted as complexity increasing by terminal addition and is mirrored by ontogenetic increases within an individual; the simple pattern in shrubby Bignonieae (polyphyletic) results from a heterochronic reversal (Pace et al. 2009). Pace et al. (2011) note that the variant phloem that causes the fluting of the vascular cylinder has large-diameter sieve tubes and numerous fibres, hence contributing substantially both to translocation and to stem support; regular phloem has sieve tubes with much smaller diameters.
Palmate leaves have arisen more than once within Bignoniaceae, but are known only in New World taxa. The New World Tabebuia s.l., which has opposite, palmate leaves, is polyphyletic (Grose & Olmstead 2007b); a number of taxa - some apparently very different vegetatively - are derived from it. These include Amphitecna, with spiral, simple leaves like those of Crescentia. The petioles are short and the lamina has distinctive, widely spreading venation; they are phyllodinous, and in some species of Crescentia palmate leaflets are borne on the end of a lamina-like petiole confirming the morphological nature of the latter. Parmentiera and Spirotecoma, both with more ordinary opposite palmately-compound leaves, are also close; all four genera have bat-pollinated flowers. They are part of a clade of palmately-leaved taxa (Grose & Olmstead 2002, 2007a; see expanded Crescentieae above).
The simple and clearly petiolate leaves of Catalpa (opposite or whorled) and Chilopsis (spiral: the two genera hybridise), have a very different morphology from those of Crescentia, etc.; they appear to be more conventionally simple.
Chemistry, Morphology, etc. Variation in wood anatomy in the family is discussed in detail by Pace and Angyalossy et al. (2013) and optimised on a phylogentic tree for the family.
There are four main carpel bundles, but only two in "Scrophulariaceae" (Armstrong 1985), Gesneriaceae, etc. In Tourrettieae, Tourrettia has sub four-locular ovaries each with a single rank of ovules, while Eccremocarpus has parietal placentation. Ovule shape varies considerably, some species having a long chalazal beak; there is also variation in endosperm development, thus Incarvillea has a huge micropylar endospermal cell (Mauritzon 1935). A number of Bignonieae with septifragal dehiscence also have cracks in the loculicidal position along the backs of the valves.
For general information, see Manning (2000) and Fischer et al. (2004a: the classification is very "classical", c.f. e.g. Lohmann 2006 and esp. Lohmann & Taylor 2014). Also, for toxic monofluoracetates, see Lee et al. (2012) and for iridoids, von Poser et al. (2000), for wood anatomy, see Gasson and Dobbins (1991: lianes and the rest compared) and for nodal anatomy, see Trivedi et al. (1976), for information on pollen, which is very variable, see Gentry and Tomb (1979) and Burelo-Ramos et al. (2009: Pithecocteniinae), for tapetum, Huysmans et al. (1998), for some embryology, see Bittencourt and Mariath (2002), for seed anatomy, including that of Schlegliaceae and Paulowniaceae, see Lersten et al. (2002), and for protein bodies in the nucleus, see Bigazzi (1995).
Phylogeny. The basic phylogenetic structure within the family is [[[Jacarandeae [Tourrettieae [Bignonieae + the rest]]] (Olmstead et al. 2002). This has been further amplified by Olmstead et al. (2009: ca 3/4 of the genera sampled, three genes), although a number of relationships between major groups, e.g. those of Tecomeae, remain poorly supported.
For a comprehensive (2-gene + morphology) phylogeny of Bignonieae, see Lohmann (2006a, 2012); [Perianthomega [[Adenocalymma + Neojobertia + The Rest]] is the basic phylogenetic structure. Major clades there are supported by a mixture of floral and vegetative characters, and generic limits have been reorganized accordingly (Lohmann 2002, esp. 2006). Bignonieae may be close to Oroxylum and relatives - which have bicompound leaves and septicidal capsules - and Catalpa - which has only two stamens (Olmstead et al. 2002). Coleae as narrowly delimited here are restricted to Madagascar, and their phylogeny and fruit evolution has been examined by Zjhra et al. (2004); they are part of a larger and well supported clade that includes Kigelia, Spathodea, etc.. Coleae and Crescentieae, both have taxa with similar flowers and fruits and "simple" leaves, but latter are of different morphologies. Relationships between the New World Tabebuia, with opposite, palmately-compound leaves and its relatives have recently been clarified. Amphitecna and Crescentia, both with spiral, simple leaves, are probably derived (Grose & Olmstead 2007a, b).
Classification. The tribes above are those recognised by Olmstead et al. (2009). Note, however, that their tribal classification is not exhaustive in that not all genera are assigned to tribes, partly because their phylogenetic position is still ambiguous (e.g. Argylia, Delostoma) or simply because extension of the circumscription of some tribes and the addition of new ones will be needed in a classification such as that used here. Crescentieae have been expanded to include Tabebuia, etc. (the Tabebeuia alliance of Grose & Olmstead 2007a, b), the expanded clade being characterized by palmate leaves. Coleae, too, could well be expanded to include genera like Kigelia, Spathodea, etc.
Over-reliance on characters associated with pollination and dispersal syndromes as markers of generic distinctness has caused serious problems with generic limits (see Lohmann 2003, 2006), however, generic limits in Bignonieae have now been extensively reworked (Lohmann & Taylor 2014).
There is a species level checklist for the family (Lohmann & Ulloa 2007).
Thanks. I am grateful to L. Lohmann for comments.
[[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]: ?
[[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]]: ?
[Schlegeliaceae + Lentibulariaceae]: ?
Phylogeny. For sampling, and support for this odd couple, see Refulio-Rodriguez and Olmstead (2014).
SCHLEGELIACEAE Reveal Back to Lamiales
Woody shrubs or vines, often epiphytes, (large trees); pericyclic sheath sclereidal; nodes 1:3; petiole bundle solid or (almost)annular, with wing bundles, pericyclic lignification 0; sclereids +; stomata variable; lamina margins entire or serrate/spiny; (inflorescence branched); flowers quite large; nectaries on outside of K; staminode +/0; nectary vascularized from carpellary bundles/0; placentae swollen, (placentation intrusive parietal, placentae uni- or bilobed); fruit a berry, K persistent to ± accrescent; seeds compressed or angular; exotestal cells with scalariform thickenings on the inner periclinal wall or mucilaginous with outer periclinal wall absent; endosperm +/0, cotyledons slightly over half the length of the embryo; n = 20; seedlings epigeal and phanerocotylar, cotyledons lobed.
4[list]/28: Schlegelia (15), Gibsoniothamnus (11). Mexico to tropical, esp. N.W., South America, Antilles (map: from Gentry 1980; Tropicos iii.2014). [Photo - Flower, Flower, Fruit.]
Chemistry, Morphology, etc. For wood anatomy, see Gasson and Dobbins (1991); there are no obvious differences in wood anatomy between Schlegeliaceae and Bignoniaceae. Schlegelia may have anomocytic or paracytic stomata, while those of Gibsoniothamnus are anisocytic or cyclocytic. There are often quite conspicuous "glands" on the lower surface of the lamina - these are hairs with the normal lamialean structure of radially-arranged cells in the head. Gibsoniothamnus may be anisophyllous (c.f. Thomandersia). Winged seeds have been reported for a.g. Schlegelia (Fischer 2004b), but the combination of winged seeds and baccate fruits seems rather improbable; Gentry (1973) described the seeds of Schlegelia as being angular. I have not seen the Cuban Synapsis.
Some information is taken from Burger and Barringer (2000), Barringer (2004: Gibsoniothamnus), and Fischer (2004b: under Scrophulariaceae), all general, Leinfellner (1973: gynoecium of Schlegelia), and Armstrong (1985: floral anatomy). Gibsoniothamnus parvifolius: Herrera 672, - leaf, stem, seed; G. allenii: McPherson 11069 - leaf, seed; Schleglia darienensis: Neill et al. 11411 - seed.
Previous Relationships. Schlegelia and relatives have usually been included in Bignoniaceae or in Scrophulariaceae s.l., being "transitional" genera between the two (Cronquist 1981).
LENTIBULARIACEAE Richard, nom. cons. Back to Lamiales
Herbs, rosette-forming and other growth forms; carnivorous [insectivorous]; (verbascoside 0 - Utricularia); primary root reduced immediately after germination, lateral roots lacking a root cap [?always]; plants often Al-accumulators, little oxalate accumulation; ?cork; vessel elements?; stomata also anisocytic; hairs variously secreting mucilage and digestive enzymes; leaves spiral, lamina margins entire, vernation circinate [Pinguicula heterophylla], or leaves apparently 0 and vegetative plant body not easily categorizable; K 5-partite, polysymmetric, or divided into 2 lobes, C quincuncial [abaxial lobe outside the others in bud - asscending cochlear], with an abaxial spur, nectar produced by glandular hairs; A 2 [the abaxial pair], (± free - Pinguicula), filaments stout [always?], thecae confluent, (superposed), epidermal cells ephemeral; tapetal cells 2(-3)-nucleate; staminode 0; pollen (grains tricellular), (4-10-zonocolporate - Pinguicula); G placentation free-central or basal, style hollow, short [up to as long as the ovary, often 0], stigma with broad lobes, (sensitive), (one lobe only), wet; ovules (2endosperm starchy, (U-shaped), 0, embryo green, with cotyledons (1, some Pinguicula], or minute, undifferentiated [Utricularia]; germinal hypogeal [some Pinguicula]; n = 7-12+.
3[list]/330: Utricularia (220), Pinguicula (80), Genlisea (30). World-wide, introduced into Hawaii? (map: from Hultén 1958, 1962, 1971; Taylor 1989). [Photo - Flower.]
Age. Crown-group Lentibulariaceae have been dated to (41-)38, 28(-25) m.y. (Wikström et al. 2001) or ca (54-)42, 37(-28) m.y. (Bell et al. 2010).
Evolution. Ecology & Physiology. As befits their carnivory, Lentibulariaceae are notably prominent in acid habitats including those of the ephemeral flora of African inselbergs (Seine et al. 1996). Details of the morphology of Lentibulariaceae as it relates to their carnivorous proclivities are given by Lloyd (1942) and Juniper et al. (1989) in particular, while Peroutka et al. (2008b) discuss aspects of their functional biology.
Pinguicula, which alone among Lentibulariaceae has roots and embryos with cotyledons (the latter, not all species), has fly-paper traps. According to the english summary of Titova (2012: p. 1162) the cotyledons of P. vulgaris have the "ability to flap and digest insects". Secretory glands throughout the family are attached to single epidermal cells and have no contact with vessels.
Genlisea has long, spirally-twisted, structures rather like eel traps; prey are passively trapped as they swim up the spiraling branches, their exit being blocked by backwardly-pointing hairs. Some species of Utricularia have non-suction traps rather like those of Genlisea, but most have suction traps. For the morphology of these suction traps, see Reifenrath et al. (2006 and references; Merl 1915). These traps are found in species of Utricularia growing both in water and in moist soil. Many species have sensitive hairs the stimulation of which leads to the rapid opening of the trap, water being sucked in. Jobson et al. (2004) and Laakkonen et al. (2006) suggest a possibly associated change in cytochrome c oxidase that may increase respiratory capacity so providing the energy needed for the rapid changes involved in the movements of the traps. Vincent et al. (2011) distinguish between a slow, energy-dependent phase in which water is pumped out of the trap, the trap becoming deformed and elastic enegy being stored in the trap body, and a fast but passive phase in which the trap door opens and closes in less than a millisecond, water and contained prey rushing inside. Spontaneous opening of traps without stimulation by prey is common (Adamec 2011 and references).
There is a diverse microbial community in the traps, perhaps a mutualistic association, that may aid in the uptake of phosphorus by the plant (Sirová et al. 2009). Carbon recently fixed by the plant may end up in the young traps (Sirová et al. 2010) and is perhaps used by the microbes there. Indeed, some Utricularia may eat aquatic algae, especially if the water is very acid; algae may predominate in traps in such environments (Peroutka et al. 2008a) and nitrogen from 15N-labelled phytoplankton may move into the plant (Alkhalaf et al. 2009). However, the relationship between plant and algae - and potential animal prey, too - is for the most part unclear (Jobson & Morris 2001; Alkhalaf et al. 2011; Adamec 2012) On the one hand, it has been suggested that the plant may even support the microbial community nutritionally when there is no prey in the traps (Adamec 2011), on the other, a number of the bacteria in the traps are able to fix nitrogen, even if the high nitrogen concentration in the traps represses this activity (Sirová et al. 2014).
Vegetative Variation. It can be difficult to understand the vegetative morphology of some species of Utricularia in particular. The embryo is undifferentiated, and although some exceptions are mentioned by Plachno and Swiatek (2010), even there cotyledons and radicle are not apparent. Small fragments of the "leaves" or the cut peduncle can regenerate the whole plant (Merl 1915), ordinary roots do not occur in Genlisea and Utricularia, and the suction bladder-traps in the latter have no parallel in other flowering plants (see e.g. Sattler & Rutishauser 1990; Plachno & Swiatek 2010 for development). Chormanski and Richards (2012) describe the construction of U. gibba in detail; the plant is made up of stolons and dichotomously-branching leaf-like structures that bear the traps. Indeed, Kaplan (1997, vol. 2: chap. 14, 17; e.g. also Lloyd 1942) suggested that the various structures bearing traps in Lentibulariaceae are all basically foliar in nature. For instance, the spiralling, positively geotropic passive traps of Genislea are borne in the same phyllotactic sequence as its leaves, and the prolonged apical growth of these traps is like that of the leaves of some species of the morphologically much less problematic Pinguicula. In addition to the traps, there are quite commonly other leaf-like structures in Utricularia, and U. kuhlmannii was even described as having odd pinnate leaves by Merl (1915).
Genes & Genomes. Pinguicula can have a long branch (Refulio-Rodriguez & Olmstead 2014). Mutation rates in the matK gene in Genilsea in particular, and also Utricularia, are about the highest in all angiosperms (Müller et al. 2004), and that of other genes is also high (Jobson et al. 2003). At the same time, some species of Genlisea, e.g. G. margaretae, have the smallest genomes known from angiosperms (Greilhuber et al. 2006), although there is substantial variation (50 fold) within the family. Ibarra-Laclette et al. (2013, see also 2011) found that almost all the non-genic DNA in the tiny genome of U. gibba had been lost, yet gene number and overall functionality seemed unchanged from that of genomically more obese plants. At the same time, there was evidence of three rounds of genome duplication beyond the palaeohexaploidy event of the core eudicots.
Chemistry, Morphology, etc. In Pinguicula a single antipodal cell may persist, enlarge, and divide (Kopczynska 1964). The integument may be multiplicative in Genlisea (see Merl 1915); testa morphology in Utricularia is very variable.
"Nutritive tissue" is described from the chalazal end of the ovule, the funicle, and the placenta, i.e., at both ends of the developing embryo, but it is not recorded from Pinguicula. In some taxa of Utricularia, at least, the embryo sac more or less escapes from the ovule and apparently takes nutrients from the placenta, and nuclei from the placenta have been found in the aggressive micropylar endosperm haustorium (Farooq 1966; Khan 1970 and references). There seems to have been no recent work on this system, and it is not even mentioned in Fischer et al. (2004b).
For additional general information, see Goebel (1891: Utricularia), McPherson (2008: Pinguicula, 2010), and the Carnivorous Plants Database, for some chemistry, see Damtoft et al. (1994), for vegetative morphology, see Brugger and Rutishauser (1989) and Rutishauser and Isler (2001), for pollen, see Rodondi et al. (2010: Pinguicula), and for seeds and embryos, see Stolt (1936), Kausik (1938), Farooq (1965), Farooq and Bilquis (1966 and references), Degtjareva et al. (2004a), and Takhtajan (2013: also seedling and young plant).
Phylogeny. For the phylogeny of Lentibulariaceae, see Jobson et al. (2003), Müller et al. (2004, 2006b), and also Müller and Borsch (2005a). Cieslak et al. (2005) and Degtjareva et al. (2006) discuss the phylogeny and evolution of Pinguicula and Reut and Jobson (2010) that of Utricularia subgenus Polypompholyx; for an account of Genlisea, see Fleischmann (2012).
Classification. For a classic revision of Utricularia, see Taylor (1989).
Synonymy: Pinguiculaceae Dumortier, Utriculariaceae Hoffmannsegg & Link
[Thomandersiaceae + Verbenaceae]: inflorescence racemose; staminode +; 3³ ovules/carpel; endosperm 0.
THOMANDERSIACEAE Sreemadhavan Back to Lamiales
Shrub or small tree; 2-indolinone alkaloids +; phloem stratified; pericyclic fibres massively thickened, ?short; nodes 1:3; petiole bundles forming a ring or incurved C-shaped; stomata anisocytic; leaves ± heterophyllous, lamina with flat glands abaxially, (margins deeply lobed), petiole swollen at apex and base; K with nectaries on the outside; pollen 5-6-colpate; nectary vascularized by carpellary traces; gynoecial vasculature 8-shaped; ovules 1-3/carpel, hemianatropous; capsule loculicidal, K accrescent; seed with cup-shaped expansion of funicle, hilum rather large; seed coat with ascending-imbricate scales or warts, exotesta palisade, not lignified, up to 6 layers of cells in the warts; embryo strongly curved, cotyledons complexly folded, thin-foliaceous; n = ?
1/6. W. and C. Africa (map: from Wortley et al. 2007a).
Chemistry, Morphology, etc. The flat glands mentioned above are dark-drying and up to 3 mm across, and are quite different from the lamialean glandular hairs with their radially-segmented heads which also often occur on the abaxial surface of the lamina.
Despite the presence of structures sometimes described as jaculators, fruit dehiscence is not explosive, unlike Acanthaceae. The seed, with its prominent hilum, sits in a thin, cup-like expansion of the funicle. Inside the seed coat described above is a layer of much crushed cells, in turn above a layer of a few less crushed cells; the outer layer of the endosperm has a distinct outer periclinal cell wall. I am not sure exactly how the cotyledons are folded. Study of the development of the ovule, embryo, and endosperm and of seed anatomy might well be profitable.
For alkaloids, see Ngadjul et al. (1995), and for general details, see Wortley et al. (2005a and especially 2007a). Thomandersia hensii: de Wilde & Jongkind 9400, seed, stem; Ngok Bamak et al. 1263, leaf; T. laurifolia: Dibata 30, seed; Thomandersia sp.: Reitsma et al. 1819, leaf, stem.
Previous Relationships. Thomandersia was previously usually included in Acanthaceae; aside from its rather different fruits, it does not have swollen nodes, cystoliths, etc.
VERBENACEAE Jaume Saint-Hilaire, nom. cons. Back to Lamiales
Vines, shrubs, or trees (perennial to annual herbs); 4-carboxy-iridoids +; (pits vestured); petiole bundles arcuate (also medullary, associated with median bundle); needle crystals common; stomata diacytic, (anomocytic); stems often square; eglandular hairs unicellular; lamina margins entire; (flowers sessile); flower often rather weakly monosymmetric; space between K and C [water calyx]; (A of two lengths, but free), ± sessile [so usu. included], (filaments +), (staminode 0); tapetal cells 2-4-nucleate; pollen (colpate, por[or]ate), exine thickened near apertures; G also 1 (4), collateral, placenta on the margin of the carpel, otherwise position various, style short [to 1/2 length of corolla tube], (long), stigma capitate (bilobed, oblique), with conspicuous stigmatoid tissue, wet; ovules 2/carpel, apotropous, integument 5-9 cells across, obturator +; (antipodal cells multinuclear); K persistent, enclosing fruit; seeds not dispersed separately; testa thin-walled; cotyledons spatulate; n = 5-12+.
31[list]/918. Pantropical (to warm temperate), but mostly New World, esp. S. South America. In Europe, Verbena officinalis may be native only from S. Europe and eastwards (map: from van Steenis & van Balgooy 1966; Hultén 1971; Lebrun 1977; Meusel et al. 1978; Brummitt 2007; Australia's Virtual herbarium 12.2012).
1. Petreeae Briquet
Shrubs and vines; flowers ± polysymmetric; K much enlarged, petal-like (not Petrea brevicalyx); G 1; fruit indehiscent, fleshy.
1/12. Mexico to the Amazon Basin.
Synonymy: Petreaceae J. Agardh
[Duranteae [[Casselieae + Citharexyleae] [Priveae [Rhaphithamnus [Neospartoneae [Verbeneae + Lantaneae]]]]]]: fruit loculicidal, two-partite.
2. Duranteae Bentham
Trees to herbs; eglandular hairs multicellular; (flowers sessile), (± polysymmetric); (A 2 + 2 staminodes); G 1().
6/192: Stachytarpheta (130). S. U.S.A. to Argentina, (Africa to India).
Age. The age for this node may be at least 42 m.y. (Nie et al. 2006).
Synonymy: Durantaceae J. Agardh
[[Casselieae + Citharexyleae] [Priveae [Rhaphithamnus [Neospartoneae [Verbeneae + Lantaneae]]]]]: ?
[Casselieae + Citharexyleae]: ?
3. Casselieae Troncoso
Inflorescences axillary; (staminode 0); (G 1 [adaxial carpel]).
3/14. Mexico and the Caribbean to Argentina.
4. Citharexyleae Briquet
Axillary inflorescences 0.
3/135: Citharexylum (130). S. U.S.A. to Argentina. [Photo - Flower.]
[Priveae, Rhaphithamnus [Neospartoneae [Dipyrena [Verbeneae + Lantaneae]]]]: flowers ± sessile; stigma bilobed (oblique, capitate).
5. Priveae Briquet
?1/21. Pantropical-warm Temperate.
6. Rhaphithamnus Miers
Inflorescences axillary; fruit indehiscent, fleshy.
1/2. Chile, Argentina.
[Neospartoneae [Dipyrena [Verbeneae + Lantaneae]]]: flowers sessile.
7. Neospartoneae Olmstead & O'Leary
(Ephedroid shrubs); plant glabrous; inflorescences axillary (terminal) inflorescences 0); (staminode +); G 1.
3/6. Argentina, Chile, S. to Patagonia.
[Dipyrena [Verbeneae + Lantaneae]]: staminode 0.
8. Dipyrena Hooker
Fruit of two bilocular pyrenes.
1/1: Dipyrena juncea (Gillies & Hooker) Ravenna. Temperate Chile, Argentina.
[Verbeneae + Lantaneae]: staminode 0.
Age. An estimate of the age of this node is (40-)39, 29(-18) m.y. (Bell et al. 2010); another is (31-)28, 20(-17) m.y. (Wikström et al. 2001).
9. Verbeneae Dumortier
(Iridoids from deoxyloganic acid); lamina margin often serrate; (inflorescence unbranched); (A 5 - Verbena); fruits also septicidal [four pyrenes]; n = 5, 7, 10.
3/260: Verbena (200), Junellia (48). Mostly American, Eurasia to Africa.
10. Lantaneae Endlicher
Ethereal oils +; stomata anisocytic; (inflorescence often ± capitate), rarely terminal; G 1 [Coelocarpum, with [G 2], probably sister to rest], "style short", stigma entire; (ovule 1/carpel - Lantana); (endosperm + - Lantana).
9/275: Lippia (120), Lantana (100). Mostly New World
Synonymy: Lantanaceae Martynov
Evolution. Divergence & Distribution. The family appears to be of tropical South American origin (Olmstead 2013). O'Leary et al. (2012; see also Thode et al. 2013) reconstructed the evolution of characters and fruit; there is a trichotomy [Lantaneae + Dipyrena + Verbeneae], so if there is a clade including the first two, it will lack the apomorphies of Lantaneae. Exactly where Rhaphithamnus and Coelocarpum end up on the tree (see below) will also affect our understanding of character evolution.
Pollination Biology & Seed Dispersal. Lu-Irving and Olmstead (2013) estimated that fleshy fruits had been derived from dry fruits at least five times in Lantaneae alone.
Plant-Animal Interactions. Gall-forming fruit flies of the Tephretidae-Tephrellini are found here (and on Acanthaceae and Lamiaceae: Korneyev 2005).
Chemistry, Morphology, etc. Petraea (and Nashia) have polysymmetric flowers (Jabbour et al. 2008). An endothelium is only poorly developed (Johri et al. 1992). For the position of the carpels, see Sattler (1973). The ovules are described as being attached to the margins of the carpel (Junell 1934); two-chambered mericarps or stones may contain an ovule/seed from both carpels (Sanders 2001); indehiscent fruits are fleshy (O'Leary et al. 2012). Pericarp anatomy is more complex (Ryding 1995). The testa of at least some Verbenaceae has the hypodermal layer(s) thickened (Rohwer 1994a).
For general information, see Sanders (2001), Atkins (2004) and Brummitt (2007), for iridoids, see von Poser et al. (1997 - also Soltis et al. 2005b), for hairs and stomata, see Cantino (1990), for the megagametophyte, see Rudall and Clark (1992), and for exine thickening, see Chadwell et al. (1992).
Phylogeny. Marx and Olmstead (2007) found that Petraea and Duranta, both woody, were successively sister to the rest of the family. Marx et al. (2010) present a comprehensive phylogeny of the family, although, as they noted, sampling within the big genera needed to be improved. A couple of genera remained unplaced: Dipyrena may be close to Verbeneae while Rhaphithamnus may be close to Priveae, although branches within the latter are rather long; the position within Lantaneae of Coelocarpum, morphologically plesiomorphic, was also uncertain (Marx et al. 2010). The topology above was also recovered by Yuan et al. (2010b), the position of Rhaphithamnus being unclear while that of Dipyrena was consistently sister to the [Verbeneae + Lantaneae] clade, and Thode et al. (2013).
For relationships around Verbena, see Yuan and Olmstead (2008), while within the Lantana-Lippia complex, Aloysia formed a basal grade and members of the animal-dispersed Lantana with their pyrene-type fruits were polyphyletic (Lu-Irving et al. 2009, esp. 2014; Lu-Irving & Olmstead 2013).
Classification. For the circumscription of the family, see especially Cantino (1992a, b), and for a tribal classification, see Marx et al. (2010).
The whole Lantana-Lippia complex, speciose although it may be, could perhaps be reduced to a single genus, the larger genera currently recognised being para- or polyphyletic (Lu-Irving et al. 2009, see also 2014). Marx et al. (2010) suggested that nine genera could be recognised in the complex, but whatever taxonomic solution is adopted major generic adjustments in this area will be needed. Earlier taxonomists had used fruit characteristics to delimit genera, and fruit evolution has turned out to be highly homoplasious (Lu-Irving & Olmstead 2013). I provisionally include Glandularia, with about 100 species, within Verbena; Junellia is also part of this complex. The limits of genera around Junellia have been redrawn (O'Leary et al. 2009); for a revision of Junellia in the old sense, see Peralta et al. (2008).
Previous Relationships. Verbenaceae have often been considered very close to Lamiaceae, q.v. for differences. For Avicennia, also once included in Verbenaceae, see Acanthaceae; Phrymaceae are also separate.
[Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]] : ?
LAMIACEAE Martynov, nom. cons.//LABIATAE Jussieu, nom. cons. et nom alt. Back to Lamiales
Herbs (trees, vines); diterpenoids, betaines, C4-decarboxylated iridoids, trisaccharide esters of verbascoside [?level] +; cork also deep-seated; (pits vestured); (nodes 1:2); petiole bundles arcuate (annular); stomata diacytic (anomocytic); stem often square; (eglandular hairs unicellular; stellate); lamina vernation variable, margins toothed; inflorescence branches cymose; A (2), staminode 0 (+); tapetal cells multinucleate; pollen 3-colpate, exine not thickened near apertures; G , style (unequally) bifid, stigma inconspicuous, not expanded, dry (wet); ovules 2/carpel, borne on inner side of carpel margin, apotropous, integument 5-9 cells across; fruit indehiscent, K persistent; testa usu. thin, exotestal cells elongated or not, thickened on radial and often inner walls, (hypodermal cells sclerenchymatous).
236[list]/7173 - 7 subfamilies below. World-wide (map: from Vester 1940; Hultén 1971; Van Balgooy 1975; Lebrun 1979; Frankenberg & Klaus 1980). [Photos - Collection, Fleshy fruit.]
Age. Estimates of the age for the clade [Callicarpa, Ajugoideae, Lamioideae] are (36-)33, 26(-23) m.y. (Wikström et al. 2001) and (50-)49, 38(-27) m.y. (Bell et al. 2010).
1. Symphorematoideae Briquet
Lianes; ?diterpenoids; inflorescences capitate, of 3-7-flowered cymes, involucrate; flowers polysymmetric, (monosymmetric), ± sessile; K 5-8, C 5-16; A 4-18; nectary 0; G imperfectly 2-locular; ovules apical, pendulous, straight, funicle 0; embryo sac ± on surface of ovule; fruit dry or subdrupaceous; ?endosperm; n = 12, 14, 17, 18.
3/27. India, Sri Lanka, South East Asia, Malesia.
Synonymy: Symphoremataceae Wight
[Viticoideae [Ajugioideae [Prostantheroideae [Nepetoideae [Scutellarioideae + Lamioideae]]]]]: ovules subbasal, ± erect, anatropous.
Age. An estimate of the age for the clade [Callicarpa, Ajugoideae, Lamioideae] is (50-)49, 38(-27) m.y. (Bell et al. 2010).
2. Viticoideae Briquet
Often woody; (hairs branched); (leaves palmately compound); nectary 0 or poorly developed; fruit a drupe; ?endosperm.
10/376-526: Vitex (250), Premna (50-200). Tropical, esp. South East Asia-Australia.
Synonymy: Viticaceae Jussieu
[Ajugioideae [Prostantheroideae [Nepetoideae [Scutellarioideae + Lamioideae]]]]: ?
Age. An age for this clade is (30-)28, 17(-15) m.y. (Wikström et al. 2001).
3. Ajugoideae Kosteletzky
(Aromatic, no terpenoids, etc.); flowers (4 [Aegiphila] merous), also polysymmetric or 1-lipped [lobes 0:5 - Teucrium]; pollen exine with branched (simple, granular, etc.) columellae; nectary slight-0 (+); (antipodal cells numerous); nutlets reticulate, (fruit a drupe, K coloured, accrescent); endosperm several-layered/0, cotyledons investing embryo [?common]; n = 7, 10, 13, 14, 16+.
24/1115: Clerodendrum (150), Teucrium (250), Aegiphila (120), Rotheca (50-60), Ajuga (40-50). Cosmopolitan, but many temperate, and esp. South East Asia to Australia.
Synonymy: Aegiphilaceae Rafinesque, Ajugaceae Döll, Siphonanthaceae Rafinesque
[Prostantheroideae [Nepetoideae [Scutellarioideae + Lamioideae]]]: ?
4. Prostantheroideae Luersson
(Aromatic); (shrubby); (microphyllous); flowers polysymmetric (monosymmetric), 4-8 merous; (staminodes 2); (disc 0); endosperm +; n = ?
16/317: Prostanthera (100), Hemigenia (50), Pityrodia (45). Australia.
Synonymy: Chloanthaceae Hutchinson
[Nepetoideae [Scutellarioideae + Lamioideae]]: fruit a schizocarp, dry, (indehiscent).
5. Nepetoideae Kosteletzky
Commonly aromatic [volatile terpenoids, rosmarinic acid], nepetoidin A and B [caffeic acid esters], (distinctive seed fatty acids) +, betaine concentration low, iridoid glycosides, acteosides 0 (+); stem endodermis +; calyx with epidermal prismatic calcium oxalate crystals; (A 2, unithecate); pollen hexacolpate, tricellular; style gynobasic; exocarp with mucilaginous cells producing hygroscopic spiral fibrils; endosperm development highly asymmetric, the two haustoria lying close to each other, 1-layered [0?], cotyledons investing embryo; n = 6+; frequently attacked by Puccinia menthae.
105/3675: Salvia (900+), Plectranthus (300), Hyptis (280), Thymus (220), Nepeta (200+), Clinopodium (100), Isodon (100), Micromeria (70), Ocimum (65), Platostoma (45), Aeollanthus (40), Hedeoma (40), Lepechinia (40), Origanum (40), Pyconostachys (40). World-wide, but esp. (warm) temperate.
Age. Diversification in the Nepetoideae is estimated to have begun (63.7-)57.6, 52.3(-42.3) m.y.a. (Drew & Systma 2012a).
Synonymy: Glechomaceae Martynov, Mellitidaceae Martynov, Menthaceae Burnett, Monardaceae Döll, Nepetaceae Berchtold & J. Presl, Salviaceae Berchtold & J. Presl, Saturejaceae Döll
[Scutellarioideae + Lamioideae]: stem endodermis +; calyx ribbed, fibrous [large amounts of fibrous tissue associated with the veins].
6. Scutellarioideae Caruel
(Aromatic, no terpenoids, etc.); (leaves spiral); inflorescence racemose; K strongly two-lipped, (rotate, coloured - Holmskioldia), lobes rounded; (C 0:5); (style ± terminal - Wenchengia); seeds tuberculate; endosperm various; n = 12+.
5/380: Scutellaria (360). ± Cosmopolitan.
Synonymy: Salazariaceae F. A. Barkley, Scutellariaceae Döll
7. Lamioideae Harley
(Aromatic), laballenic fatty acid and related compounds [l.a. = CH3(CH2)10CH=C=CH(CH2)3COOH]; (calyx mesophyll with narrow prismatic calcium oxalate crystals); (stamens 4, about the same length - Pogostemon and relatives); style gynobasic; (ovule with glandular hairs - Leonurus, Teucrium); embryo sac with micropylar lobe longer and broader than chalazal lobe; nutlets hardly reticulate; endosperm several-layered, embryo spatulate; n = 6+.
63/1260: Stachys (300), Phlomoides (150-170), Sideritis (140), Leucas (100), Phlomis (50-90), Pogostemon (80), Eremostachys (5-60). Esp. Europe and Africa to Asia, some cosmopolitan, but v. few Antipodean.
Synonymy: Melissaceae Berchtold & J. Presl, Stachydaceae Döll
And 10 genera unassigned, including Callicarpa (140: hairs branched/stellate; flowers polysymmetric, 4-5(-7)merous; C free; stigma lobes relatively broad; fruit a drupe) and Tectona (4: tree; flowers polysymmetric).
Evolution. Divergence & Distribution. Diversification within Mentheae (Nepetoideae; ca 2,300 species, about a third of the family) is estimated to have begun ca 46 m.y.a., perhaps in the Europe/Mediterranean area (Drew & Systma 2012a). Mentheae include Salvia, the limits of which are unclear, although the clade is very speciose in the New World; there have been several independent movements to Africa and the Old World (Will & Claßssen-Bockhoff 2014). The ca 60 species of Lamiaceae endemic to Hawaii represent a major diversification there. Although they are currently placed in three separate genera, they are all polypoids with fleshy fruis and are derived from within dry-fruited west North American (or areas slightly to the south) Stachys (Lamioideae); they probably represent but a single introduction to the islands (Lindqvist & Albert 2002; Roy et al. 2013; see also the silversword alliance - Asteraceae). Prostantheroideae are an Australian radiation of often shrubby and small-leaved plants growing in dry conditions.
Ecology & Physiology. Thymol, the essential oil 2-isopropyl-5-methylphenol and known from some Nepetoideae, at least, not only is bactericidal but it also seems to encourage nodulation of legume seedlings, which has implications for communty development (McKenna et al. 2013).
Pollination Biology & Seed Dispersal. Species in the very big, primarily New World-Mediterranean Salvia often have only two unithecate anthers. The connective is expanded and forms a lever arm that is involved in pollination; when the lever arm is hit, the other end, with the single theca, pivots and comes down on the back of the pollinator. As in other members of the family, pollination is predominantly by large insects and birds (Claßen-Bockhoff et al. 2003: summary of early literature). Claßen-Bockhoff et al. (2004a, b) described stamen development in Salvia, and Walker and Sytsma (2007) suggested that the distinctive stamen with its lever arm might have evolved three times via a bithecate condition with the thecae at opposite ends of an extended connective; the common ancestor of all unithecate clades had two "ordinary" stamens. Taxa like the 4-stamened Melissa and Lepechinia are at the base of the part of the tree that includes Salvia, and there are other taxa with two stamens immediately below the clades containing Salvia (Walker & Sytsma 2007); a number of other Mentheae, mostly New World, also have two stamens (Drew & Sytsma 2012a).
Reith et al. (2007) described details of pollination in Salvia pratensis, and Wester and Claßen-Bockhoff (2006, 2007, 2011) focus on pollination by birds. There are over 300 bird-pollinated species of Salvia, and these are largely restricted to the New World; flowers with an ornithophilous syndrome in fact encompass a remarkable amount of variation (Wester & Claßen-Bockhoff 2011). In low Mediterranean shrublands, megachilid bees are important pollinators of Lamiaceae (Petanidou & Ellis 1996).
Drew and Sytsma (2012b) discussed the evolution of dioecy within the New World genus Lepechinia; it seems to have occurred at least three time there.
The calyx is an integral part of the dispersal mechanism of the disseminule, whether being brightly coloured and helping to attract frugivores, as in Clerodendrum, having hooked hairs or being itself hooked (Priva and some species of Salvia respectively), or forming a kind of catapult mechanism (Scutellaria) or a wing. Various kinds of calcium oxalate crystals are found in the sepals, perhaps protecting the nutlets against insect predators (Ryding 2010b). Myxocarpy, the nutlets producing mucilage and so adhering to their disperser or anchoring the nutlet in the ground, is common in Nepetoideae (Pammel 1892; Ryding 1992); Yang et al. (2012) discuss the general importance of surface mucilage in propagules. Large genera like Lamium (Lamioideae) and Teucrium (Ajugoideae) have myrmecochorous nutlets (Lengyel et al. 2010).
Plant-Animal Interactions. The leaf beetle Phyllobrotica (Chrysomelidae) eats plants from Scutellarioideae, Lamioideae and Viticoideae, but not members of Nepetoideae - or Verbenaceae (Farrell & Mitter 1990). Larvae eat the roots, adults the above-ground parts, which they can decimate. Gall-forming midges of the Tephretidae-Tephrellini are found here (and on Acanthaceae and Verbenaceae: Korneyev 2005), as are gall-forming wasps of the Cynipidae-Cynipinae (Redfern 2011) and agromyzid dipteran leaf miners (Winkler et al. 2009).
Economic Importance. Chia, Salvia hispanica, has nutritious seeds very high in alpha-linolenic acid; it was a major crop in the Aztec empire (Ayerza & Coates 2005).
Chemistry, Morphology, etc. Trisaccharide esters of verbascoside are found in Lamiaceae alone, but disaccharides are found there as well as in Verbenaceae, Oleaceae and Orobanchaceae in particular (Mølgaard & Ravn 1988). For the distinctive allenic fatty acids, see Aitzetmüller et al. (1997).
Bailey (1956) noted the vegetative nodes of Lamiaceae and "Verbenaceae" might be two trace, one gap. The distribution of such nodes needs to be clarified; Marsden and Bailey (1955) described such nodes in Clerodendron trichotomum in considerable detail. Species of Lamioideae and Scutellarioideae, but not Nepetoideae, tend to have relatively massive ammounts of fibrous tissue associated with the veins in the calyx, e.g. with the tertiary veins (Ryding 2007, 2010b).
There is further discussion of other asterids with polymerous flowers like those of Symphorematoideae elsewhere (see the euasterid clade). The pollen grains of at least some Lamiaceae become very much flattened as they dry out (Halbritter & Hesse 2004). The ovules are described as being attached (just) to the false septae (Junell 1934); there is variation in ovule attachment within the family. Many Lamiaceae have a single layer of sclerenchymatous, bone-shaped cells on the inside of the mesocarp, others have thicker pericarp walls, and the cells are often crystalliferous (Ryding 1995). The exotestal cells of the seed are thickened, particularly on their inner periclinal and anticlinal walls (Rohwer 1994a). Some Lamiaceae have asymmetric development of the endosperm such that the two haustoria come to lie very close to each other (Ram & Wadhi 1964 for references). This distinctive development may be restricted to Nepetoideae (further studies are needed), but it is also to be found in many Acanthaceae. Wunderlich (1967b) suggests that there is no endosperm in mature fruits of Nepetoideae.
For a comprehensive treatment of Lamiaceae, see Harley et al. (2004), for fatty acids in the seed, see Badami and Patil (1981), for betaine distribution, see Blunden et al. (1996: widespread, but Verbenaceae and other Lamiales?), for secondary metabolite evolution, see Grayer et al (2003) and Wink (2003), for hairs and stomata, see Cantino (1990), for leaf anatomy in Mentheae, see Moon et al. (2009a), for some floral development, see Endress (1999) and Naghiloo et al. (2014), for ovules, which have a vascular supply, see Guignard (1893), for gynoecial morphology and embryology, see Junell (1934), for seedlings, see Vassilczenko (1947: cotyledons in Lamiaceae s. str. usu. cordate to hastate), for pollen, ovules and seeds, see Wunderlich (1967b), for the megagametophyte, see Rudall and Clark (1992), for nutlet micromorphology, see Moon et al. (2009b: Mentheae) and especially Ryding (2010a and references), for nutlets in Stachys, see Salmaki et al. (2009), and for proteinaceous inclusions in the nucleus, see Speta (1979). Moon et al. (2008a, b) surveyed pollen morphology especially of Salviinae and other Mentheae.
Phylogeny. Bootstrap support for the family is 100% (Wagstaff et al. 1998); however, although Congea (Symphorematoideae) may be sister to the rest, major relationships within the family remain unclear. Bendiksby et al. (2011) recovered a set of relationships [Callicarpa [Prostantheroideae [[Symphorematoideae + Viticoideae] [[Cornutia, Gmelina, Tectona, Premna] [Nepetoideae [Garrettia [Scutellarioideae + Lamioideae]]]]]]], mostly with strong support, although sampling was mediocre and analyses of individual markers apparently yielded different topologies. These relationships differ from those in the classification above mainly in the position of Prostantheroideae and in the paraphyly of Viticoideae (c.f. Bramley et al. 2009).
For relationships in Viticoideae, see Bramley et al. (2009); Vitex itself is paraphyletic. For the phylogeny of the Australian-centered Chloantheae (Prostantheroideae), see Conn et al. (2009) and for that of Prosanthera itself, with the classical (Bentham!) morphologically-circumscribed infrageneric taxa not standing up too well, see Wilson et al. (2012). For the relationships around the para/polyphyletic Clerodendrum (Ajugoideae), see Steane et al. (1999, 2004).
Within Nepetoideae, the large New World-centred Salvia, with over 900 species, is probably polyphyletic, Rosmarinus, and some other mostly quite small genera also being involved (Walker et al. 2004; Walker & Sytsma 2007; Moon et al. 2010) - alas for "Scarborough fair". Jenks et al. (2013) looked at relationships within the speciose (500+ species) New World subgenus Calosphace and found that many sections were not monophyletic, relationships following geography rather than morphology - hence much parallel evolution. Moon et al. (2010) and Drew and Systma (2012a) have begun to circumscribe major clades within the huge Mentheae. Major changes in our ideas of relationships in Menthineae and in the limits of the subtribe are needed; species of Clinopodium are scattered through much of the tree (Bräuchler et al. 2010; Drew & Sytsma 2011). Drew and Sytsma (2011, 2012b) explored the limits and relationships of Lepechinia. Nepetoideae also include the large tribe Ocimeae which has synthecous, dorsifixed anthers (Paton et al. 2004). Ocimeae in turn include the large genus Hyptis; the other genera of Hyptinae are embedded in a paraphyletic Hyptis (Pastore et al. 2011); however, there is little resolution along the backbone of the tree, so major clade limits there are unclear.
For phylogenetic relationships in Lamioideae, see Wagstaff et al. (1995), Scheen et al. (2010), who found that Cymaria might be sister to the rest of the subfamily, Bendiksby et al. (2011) who added Acrymia to Cymaria, although support for the sister group position of the combined clade was low, and Chen et al. (2014), who preferred to exclude the two from the subfamily on morphological grounds, although they included the odd genus Holocheila. For relationships of the ca 60 species of lamioid mints endemic to Hawaii, see Lindqvist and Albert (2002; Roy et al. 2013); recognition of the three genera in which they are placed makes Stachys paraphyletic (see also Roy & Lindqvist 2012; Roy et al. 2013), but this aside, the limits of Stachys are difficult to determine (see also Scheen et al. 2010; Bendiksby et al. 2011), and there may have been ancient hybridization in Stachydeae (Salmaki et al. (2013)). Leucas is also highly paraphyletic (e.g. Scheen & Albert 2009), while relationships within Phlomidae have been evaluated by Mathiesen et al. (2011) and Salmaki et al. (2012). See Scheen et al. (2007) for relationships around Physostegia.
Wenchengia has spiral leaves and a more or less terminal style and it was initially unclear where it should be placed (Cantino & Abu-Asab 1993). However, a position sister to all other Scutellarioideae is strongly supported (Li et al. 2012).
Classification. The classification here is based on that of Harley et al. (2004); see Cantino and Sanders (1986) for the distinctions between the two biggest subfamilies, Lamioideae and Nepetoideae. The implied subfamilial phylogeny above is for convenience only, to help in working through character variation. Note that the circumscription of Viticoideae is more narrowly drawn than in Cantino et al. (1992), some genera included there not being assigned to subfamilies here. For tribal limits in Lamioideae, see Scheen et al. (2010) and Bendiksby et al. (2011).
In general, generic limits need attention, thus in both Stachys and Leucas characters associated with pollination prove unreliable indicators of clades (Scheen et al. 2010); the former genus in particular may have to be considerably expanded or pulverised (Salmaki et al. 2013). Clerodendrum has been dismembered (Steane & Mabberley 1998; Yuan et al. 2010a); Harley and Pastore (2012) reworked generic limits in Hyptidinae, and Coleus is to be included in Plectranthus. How Salvia is to be treated presents a challenge - perhaps Rosmarinus, Thymus, Mentha, and Origanum are to be included (Walker et al. 2006; Walker & Sytsma 2007), however, Mentheae are so big that sampling will have to be improved to get at generic limits, although these are evidently suspect. There are many other places where generic/clade rearrangements are to be expected, as in Chloantheae (Prostantheroideae: Conn et al. 2009). All the floral characters used to distinguish genera in Menthineae turn out to be homoplastic, and Clinopodium in particular is polyphyletic (Bräuchler et al. 2010).
Previous Relationships. Lamiaceae and Boraginaceae have always been considered distinct, but their similar gynobasic styles and fruits with four separate nutlets (and also some chemistry) have invited comparisons between the two, and they were often placed fairly close to each other, as by Cronquist (1981), where both are in Lamiales. However, there are numerous differences (chemistry, leaf insertion, floral symmetry, ovule morphology, etc.) between the two, and the radicle in Boraginaceae points upwards in fruit while in Lamiaceae it points downwards.
As their alternative name Labiatae implies, Lamiaceae have always been considered as an "eminently natural" family, being immediately recognisable because of their herbaceous habit, paired, serrate leaves, square stems, monosymmetric flowers, gynobasic style, and four nutlets. However, the gynobasic style and the four nutlets may have evolved more than once (Cantino 1992a), and a considerable number of ex-Verbenaceae must now be included in Lamiaceae (see Junell 1934 for important early work on the gynoecium; Cantino et al. 1992a, b). Those two families, previously considered close but separate, are now more easily distinguishable morphologically than before.
[Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]] : inflorescence racemose; (protein crystal stacks in nucleus).
Chemistry, Morphology, etc. Note that there may be chemical differences within Phrymaceae s.l., thus Mazus has iridoids while Mimulus does not (Hegnauer & Kooiman 1978). However, sampling is poor - and needs to be expanded. For nuclear protein crystals, see Albach et al. (2009).
Phylogeny. There is still some doubt as to relationships in this clade, in particular, whether genera like Mazus are to be included in a broadly-circumscribed Phrymaceae, or not (Oxelman et al. 2005; Tank et al. 2006). However, Xia et al. (2009), Albach et al. (2009), Schäferhoff et al. (2010) and Fischer et al. (2012) have all found support for the paraphyly of Phrymaceae, with Mazus and Lancea forming a clade separate from that containing the rest of the family (see also Nie et al. 2006), so dismemberment is in order.
The woody Paulownia, Brandisia and Wightia that have been associated with Bignoniaceae and/or Scrophulariaceae in the past are to be placed in this clade. Thus Brandisia is to be included in Orobanchaceae (Bennett & Mathews 2006; esp. McNeal et al. 2013; Q.-M. Zhou et al. 2014). There is some support for the placement of Paulownia as sister to Lamiaceae (Olmstead et al. 2000) or with Phrymaceae interpolated between it and Orobanchaceae (some analyses in Albach et al. 2009). A position sister to Orobanchaceae is on balance more likely (Olmstead et al. 2001; Mueller et al. 2001; Hilu et al. 2003; Müller et al. 2004: Wortley et al. 2005a [80% bootstrap]). Although chloroplast data did not link Wightia with Paulownia, ITS and combined analyses did, albeit the support was not very strong and in the latter analyses Orobanchaceae were not monophyletic (Q.-M. Zhou et al. 2014).
MAZACEAE Reveal Back to Lamiales
Annual or perennial herbs; iridoids +; cork?; vessel elements?; pericyclic fibres 0; leaves opposite (spiral), margins toothed; flowers with very well developed lower lip; anther thecae divergent, staminode 0; stigma sensitive; integument 5-6 cells across; (fruit indehiscent); n = 19.
3[list]/33: Mazus (30). Central Asia and North China to the Antipodes, rather scattered, but esp. China (map: from Barker 1991; AgroAtlas viii.2012 - India, Malesia esp. vague).
Chemistry, Morphology, etc. Mazus has 1:1 nodes and lacks a pericyclic sheath. For more information, see under Phrymaceae, but little is known about this clade.
Phylogeny. Fischer et al. (2012) found that the monotypic Central Asian Dodartia, usually included in Phrymaceae, was sister to Mazus (support good).
[Phrymaceae [Paulowniaceae + Orobanchaceae]]: ?
Age. The age of this node is around 67 m.y. (Wikström et al. 2001).
PHRYMACEAE Schauer, nom. cons. Back to Lamiales
Annual or perennial herbs (woody); (iridoids 0); cork?; vessel elements?; lamina (punctate), margins toothed (entire); (inflorescence fasciculate), (inflorescence branches cymose), (flowers single); K tubular, toothed, subplicate-ribbed (4-, 3-lobed), (C polysymmetric; 2 + 0 - Mimulus douglasii); A (2), anthers subreniform, thecae confluent; (pollen tricellular), (6-8-colpate; each colpus with 2 orae; spiraperturate; tricolpate); nectary +/0; (fertile carpel 1), (placentation parietal, near-basal), stigma broadly 2-lobed (1-lobed; shortly 2-fid), sensitive (not); ovules (1-)many/carpel, straight, integument 3-7 cells across; (fruit indehiscent), K persistent; (seeds with pedestals); endosperm +/almost 0, cotyledons convolute; n = 7-12, 14-16, 22, etc.
13[list]/188: Erythranthe (111), Diplacus (46). ± World-wide, esp. temperate and W. North America and Australia, but few humid tropics (map: from Meusel et al. 1978; Barker 1982; Hong 1983, 1993; India-Southeast Asia-Antipodes very inaccurate.). [Photos - Collection, Mimulus Flower.]
Age. The crown age may be ca 40 m.y. (Nie et al. 2006: Fig. 2, probably low end of range); Phryma separated from most of the rest of the family (the divergence of Peplidium is older) some 49.4-32.3 m.y.a..
Evolution. Divergence & Distribution. Although Phryma represents an old clade, its well-known East Asian - E. North American disjunction happened a mere ca 6-2 m.y.a. (Nie et al. 2006, q.v. for other estimates).
Genes & Genomes. There is extensive polyploidy and aneuploidy (both happening 10+ times) in North American Mimulus, but neither is associated with the evolution of major clades (Beardsley et al. 2004).
Chemistry, Morphology, etc. Whipple (1972) described the nodes of Phryma as having three traces coming from a single gap; the ovules were described as being apotropous and hemitropous.
For general information about other genera included here, see Fischer (2004b: Scrophulariaceae p. pte), for some chemistry, see Q.-M. Zhou et al. (2014), for pollen, see Argue (1980, 1981) and Chadwell et al. (1992); for Phryma, see Whipple (1972), Venkata Ramana et al. (2000: embryology), and Cantino (2004: general). For floral development in Mazus, see Rawat et al. (1988).
Phylogeny. Phryma and Mimulus and its relatives make up this unexpected clade (Beardsley & Olmstead 2000, esp. 2002; Beardsley et al. 2001, 2004; Beardsley & Barker 2004; Nie et al. 2006). Is Cyrtandromoea to be placed here? (see discussion in Gesneriaceae above under Phylogeny).
Classification. For a conspectus of the family, see Barker et al. (2012); Mimulus has had to be dismembered. For a monograph of Mimulus old style, species of which are the subjects of many evolutionary studies, see Grant (1924) and Thompson (2005).
Previous Relationships. Phryma was previously placed in a monotypic family on account of its distinctive morphology, or allied with Verbenaceae. Mimulus and other genera were included in Scrophulariaceae s.l.
Botanical Trivia. The mostly Australian Glossostigma is scarcely bigger than Lemna, while small plants of Mimulus jepsonii may consist only of cotyledons, a pair of foliage leaves, and a flower (T. Livschultz, pers. comm.).
[Paulowniaceae + Orobanchaceae]: ?
Age. An estimate of the age of this node (Paulownia sister to Buddleja) is (58-)48, 38(-26) m.y. (Bell et al. 2010); Bremer et al. (2004) suggest an age of ca. 64 m.y. while is the age in Wikström et al. (2001).
PAULOWNIACEAE Nakai Back to Lamiales
Woody*, trees, climbers or stranglers, deciduous; iridoids +, (cornosides +); cork cambium outer cortical; nodes 1:1; hairs uniseriate-branched to stellate*; petiolar bundle annular; lamina margins entire*; inflorescence branched, ultimate units cymose; flowers large; K ± valvate, leathery*, deeply lobed, space between K and C [water calyx], C hairs uniseriate with tapering terminal cell; anther thecae head-to-head or parallel and apically confluent, endothecium massive, extending across connective, staminode 0; pollen tricolpate; nectary vascularized; placentae massive, style hollow, head expanded or not, stigma punctate, hollow; seed pedestals +, seeds winged (several sinuous wings - Paulownia); exotesta cells broad, with complex reticulate thickenings; endosperm +; n = 19, 20.
2/8. South East Asia to east Malesia (map: from Hu 1959, Paulownia alone). [Photo - Flower]
Chemistry, Morphology, etc. The phylogenetic significance of the wood anatomical differences between Catalpa (Bignoniaceae) and Paulownia (Dos Santos & Miller 1993) is unclear.
Erbar and Gülden (2011) noted that the terminal flowers in an inflorescence of Paulownia might have five stamens - peloria. The ad- -> abaxial direction of development of members of the calyx and the corolla whorls is unusual in Lamiales (Erbar & Gülden 2011), although observations are limited.
For additional information, see Schilling et al (1982: verbascoside, etc.), Fischer (2004b: as Scrophulariaceae), and Q.-M. Zhou et al. (2014: general).
Wightia is very poorly known; in the characterization above, possible apomorphies that refer to both genera have an asterisk, the rest refer to Paulownia alone.
Phylogeny. For a discussion on the relationships of Paulownia and Wightia, see above; the latter genus is only provisionally included here.
Previous Relationships. Paulownia is superficially like Catalpa (Bignoniaceae) and both have been shuttled back and forth between "Scrophulariaceae" and Bignoniaceae. Paulownia has endosperm and lacks the distinctive ovary and seed anatomy of Bignoniaceae (Armstrong 1985; Manning 2000; Lersten et al. 2002); on the other hand, Catalpa is definitely to be included in Bignoniaceae. Wightia has often been associated with Paulownia in the past (Q.-M. Zhou et al. 2014 and references).
OROBANCHACEAE Ventenat, nom. cons. Back to Lamiales
Plant turning black on drying (not); (mannitol +), cork?; head of glandular hairs lacking vertical partitions; lamina margins often toothed to deeply lobed; C with abaxial-median or abaxial-lateral lobes outside others [quincuncial, descending cochlear] in bud; placentae paired-stipitate; seed with exotestal cells variously thickened on the inner walls.
99[list]/2060. World wide, but especially N. (warm) temperate and Africa-Madagascar.
1. [Rehmannia + Trianeophora]
Plant rhizomatous; leaves spiral; bracts ± foliaceous, (bracteoles 0); (staminode +); stigma sensitive; n = ?
2/7. China (map: from Flora of China vol. 18. 1998; green = R. glutinosa, also cultivated).
Synonymy: Rehmanniaceae Reveal
[Lindenbergieae [Cymbarieae [Orobancheae [Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]]]]: stomata do not close; placentation parietal.
2. Lindenbergieae T. Yamazaki
Bracts ± leaf-like, bracteoles usu. 0; A thecae on connective arms; testa usu. with hook-shaped thickenings adnate to surface; n = 16.
1/12. N.E. Africa to N. Philipines (map: see Hjertson 1995).
Age. Bremer et al. (2004) suggested that the age of this node can be put at around 48 m.y., the age in Wolfe et al. (2005) was ca 52.2 m.y..
Synonymy: Lindenbergiaceae Doweld
[Cymbarieae [Orobancheae [Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]]]: ?
Hemiparasitic herbs (shrubs); ectomycorrhizae 0; orobanchin +, little oxalate accumulation, 6- and/or 8-hydroxylated flavone glycosides 0; leaves spiral to opposite; (K ± free), C (tube development intermediate), (aestivation imbricate); staminode 0 (1), anther thecae parallel or ± confluent, sagittate to inverted U-shaped, often hairy, with tails or basal awns, (thecae unequal), (tapetum amoeboid); pollen often starchy, commonly tricolpate, surface retipilate, (polyporate); ([G 5]), (placentation axile), (placentae [2, bilobed] 4 [-6], [much divided]), stigma clavate to capitate; ovule (>1/carpel), unvascularized or not, variants of anatropous, integument (2-)4-7(-12 )cells across, (embryo sac protrudes beyond the micropyle); (antipodal cells persistent); capsule loculicidal to septicidal, (indehiscent); (seed pedestals +); (seed with elaiosomes), (cells of seed wings with reticulate thickenings on anticlinal walls), (cells of layers other than the exotesta thickened and lignified); endosperm +, (walls thickened; reserves starch; mannose-rich polysaccharides; 0); (perisperm +, 1-layered), embryo often small (minute, undifferentiated); (germination via germination tube).
96/2040. World wide, but especially N. (warm) temperate and Africa-Madagascar (map: from van Steenis & van Balgooy 1966; Hultén 1971; Meusel et al. 1978; Hong 1983). [Photo - Plant, Collection.]
3. Cymbarieae D. Don
5/16. E. North America (1 sp.), Eurasia. n= 8.
[Orobancheae [Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]]: ?
4. Orobancheae Lamarck & de Candolle
Holoparasitic; (A free from C - Eremitilla); pollen variable, (heteromorphic); n = ?
12/180: Orobanche (150). North temperate, North Africa.
Synonymy: Aeginetiaceae Livera, Phelypaeaceae Horaninow
[Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]: ?
5. Brandisia J. D. Hooker & Thomson
Shrubs to lianas; hairs stellate; anther thecae long-ciliate; n = ?
1/13. Burma to China.
[Rhinantheae [Buchnereae + Pedicularidae]]: ?
6. Rhinantheae Lamarck & de Candolle
(Holoparasitic); n = 9-14.
18/540: Euphrasia (170-350), Bartsia (50), Rhinanthus (45). ± Worldwide, but esp. Eurasian.
Synonymy: Euphrasiaceae Martynov, Melampyraceae Hooker & Lindley, Rhinanthaceae Ventenat
[Buchnereae + Pedicularidae]: ?
7. Buchnereae Bentham
(Holoparasitic); (axillary 3-flowered cymes); n = 12, 14, 19+.
16/350: Buchnera (100), Alectra (40), Harveya (40), Sopubia (40). Tropics, inc. Australia.
Synonymy: Buchneraceae Lilja, Cyclocheilaceae Marais, Nesogenaceae Marais
8. Pedicularidae Duby
(Anther thecae unequal or single); n = 8, 11-15, etc.
16/857: Pedicularis (600-?800), Castilleja (160-200), Agalinis (45). Mostly northern hemisphere, some to South America and the Caribean.
Synonymy: Pedicularidaceae Jussieu
Evolution. Divergence & Distribution. Orobanchaceae may have diversified north of the Tehys Sea, pehaps in eastern Asia (Wolfe et al. 2005). It has been suggested that the evolution of holoparasites with minute dust seeds - which may have evolved three times or so - was driven by the expansion of grasslands in the middle of the Tertiary (Eriksson & Kainulainen 2011; see also McNeal et al. 2013). The age of around 31.5 m.y. for the adoption of the holoparasitic habit in Epifagus may not be too terribly far off the mark, but the sister taxon used in the estimation (Digitalis) is a distant outgroup so the agreement of 31.5 m.y. with anything is more likely to be coincidental.
Orobanchaceae are unusual in that the non-parasitic Lindenbergia is much less diverse than its sister group, which is parasitic, a size relationship that is the reverse of that common in parasitic:non-parasitic sister clades, however, most Orobanchaceae are only hemiparasitic (Hardy & Cook 2012).
Euphrasia has a North Temperate - circum-Pacific distribution and is basically bipolar; much dispersal seems to have been involved in attaining this range (Gussarova et al. 2008). Diversification within the large genus Castilleja is becoming better understood. There is a speciose West North American/Central/South American perennial clade - some 120 species - derived apparently quite recently from an annual ancestor; polyploidy is common in the perennials, but not in the annuals (Tank & Olmstead 2008, 2009). Annuals have dispersed more than once to South America (Tank & Olmstead 2009).
Ecology & Physiology. Hemiparasitism appears to have evolved once (McNeal et al. 2013), while holoparasites have evolved from hemiparasites perhaps three times (dePamphilis et al. 1997; Nickrent et al. 1998; Young et al. 1999; Schneeweiss et al. 2004a; Bennett & Mathews 2006; esp. McNeal et al. 2013). The hemiparasitic Harveya obtusifolia is well embedded in a holoparasitic clade of the genus; whether there has been reversion in life style or yet more independent acquisitions of the holoparasitic habit in that part of the family is unclear (Morawetz & Randle 2009; species not included by McNeal et al. 2013); Morawetz et al. (2014) incline to the latter position. However, the distinction between the two life styles is not sharp. Species like Striga linearifolia and Alectra sessiliflora are close to being holoparasitic, and Tozzia alpina may live underground for a decade or so before producing photosynthetic, fertile above-ground shoots (McNeal et al. 2013).
Some Orobanchaceae, particularly the hemiparasitic taxa with chlorophyll, take up largely water, nitrogen, etc., from their hosts, others take up organic material as well; iridoid glucosides, pyrrolizidine and quinolizidine alkaloids, etc., may also move from host to parasite (e.g. Adler & Wink 2001; Hibberd & Jaeschke 2001; Shen et al. 2005 [also host selection]; Rasmussen et al. 2006 and references). Much of the carbon may move through the xylem (Tesitel et al. 2010); Batashev et al. (2013) note that phloem companion cell morphology in Orobanchaceae is very distinctive. Movement of (secondary) metabolites may also be from parasite to host. Some of the severe effects on the host caused by the parasite may be due in part to the breakdown of the iridoid glucoside of the parasite and the release of the cytotoxic iridoid aglucone, perhaps caused by the host's ß-glucosidases, themselves common because they are involved in the host's cyanogenic defence pathway (Rank et al. 2004). For other information on parasitism in the family, see Irving and Cameron (2009 and references).
Alder (2000, 2002, 2003) found a complex relationship between hosts and parasite, the annual Castilleja indivisa. Association with Lupinus in particular led to a decrease in herbivores eating the parasite (sometimes), more visitors by pollinators, increased seed set, etc., when compared with other hosts. These effects were mediated by the movement both of alkaloids and nitrogenous compounds (increase in growth s.l.) from the lupin to the parasite; alkaloids acted as a deterrent to herbivores and indirectly increased visits by sensitive pollinators who were no longer put off by half-eaten inflorescences (Adler 2000).
Host specificity, and the formation of races specific to particular hosts, is well-known in Orobanche in particular. Incompatability between the host and parasite is first evident in the endodermal region, at least in Orobanche (Thorogood & Hiscock 2010).
For the role of strigolactones, exuded from host roots, in stimulating germination of seeds of some species of Orobanchaceae, see Tsuchiya and McCourt (2009) and Akiyama et al. (2010 and references). There are recent suggestions that germination is in part controlled by maternal genes in persistent maternal (nucellar) tissue (Plakhine et al. 2012). Haustoria of several different types are formed soon after germination, some forming a connection with xylem only, others with both xylem and phloem, nevertheless, haustoria may have but a single origin within Orobanchaceae (Fischer 2004b for a summary).
Stomata in this family seem to be perpetually open (Stewart & Press 1990; Smith & Stewart 1990), even in the apparently autotropic Lindenbergia, sister to most other Orobanchaceae; the situation in Rehmannia and relatives (see below) is unknown. The stomata remain open despite the presence of large amounts of abscisic acid, which normally would be expected to result in their closure (Jiang et al. 2010; other papers in Folia Geobotanica 45(4). 2010). Perpetually-open stomata are common in hemiparasitic plants in general because they increase the transpiration flow in the parasite so faciltating movement of water, nutrients, etc., from the host (e.g. Phoenix & Press 2005).
The effects of hemiparasitic Orobanchaceae on the general community can be considerable. They may increase overall diversity if they parasitize dominant species, as in some grasslands, or decrease it, if they attack less common species. The hemiparasites, particularly the annuals, increase nutrient cycling in communities in which they grow, perhaps particularly in the Arctic. The litter they produce is relatively rich in nutrients, nutrients not being resorbed as the plant senesces. Their litter often decomposes more rapidly than that of other species in the community; overall, the positive ecological effects of the litter can counteract the negative effects of parasitism (Quested et al. 2003; Phoenix & Press 2005; Watson 2009; Fisher et al. 2013).
Pollination Biology & Seed Dispersal. Pedicularis is particularly common in montane-alpine areas in the Northern Hemisphere, and although there are very many species, actual numbers are uncertain (Mill 2001). Variation in floral morphology in the genus is very great, yet pollination is predominantly by bumble bees (Macior 1982). Some species have a corolla tube ca 10 cm long or more, or there may be an asymmetric, proboscis-like extension of the upper lip (the galea) that is formed from the two adaxial corolla members (e.g. Li 1951 and references). There are some 600 species of Pedicularis in the Sino-Himalayan region that are likely to be pollinated by bumble bees, of which over fifty species are known from the Hengduan region of China alone (Williams et al. 2009). Species with red, long-tubed flowers and growing at higher elevations may lack nectar and be pollinated by pollen-collecting bumble bees, which raises the question of the function of these very long tubes - effectively they are pedicels, the plants not having long inflorescence axes (Huang & Fenster 2007). Character displacement, in which sympatric taxa differ more than would be expected, so reducing the chances of pollen being deposited on the wrong stigma (pollen interference), seems to be one component in the generation of the exceptional diversity of the genus in the Hengduan Mountains (Eaton et al. 2012); sympatric species sharing the same pollinating bee tend to deposit and pick up pollen from different parts of the bee's body, but if one species of Pedicularis is particularly common, this will help ensure pollinator constancy (Huang & Shi 2013). For comments on the floral evolution of the genus, see Macior (1982, 1984) and Ree (2005a); pollen morphology - there is quite extensive variation - is linked with corolla morphology and pollinator type (Hong Wang et al. 2009a). For other literature on pollination, see Kampny (1995: as Scrophulariaceae).
For myrmecochory in seeds of Melampyrum and Pedicularis) in particular, see Lengyel et al. (2009, 2010). Eriksson and Kainulainen (2011) discuss the distinctive dust seeds of many parasitic Orobanchaceae (also in Ericaceae-Monotropoideae, myco-heterotrophic taxa in general, etc.); Lathraea squamaria, parasitic on Corylus, has relatively large seeds, perhaps connected with the need of the seedling to reach the relatively deep roots of their future host.
Plant-Animal Interactions. Agromyzid dipteran leaf miners have diversified on the hemiparasitic Orobanchaceae (Winkler et al. 2009), and larvae of Nymphalinae-Melitaeini butterflies are commonly found on them (also on Plantaginaceae, but not on Scrophulariaceae: Wahlberg 2001).
Genes & Genomes. The chloroplast genome of the holoparasitic members may be very small - it is only 45 kb in Conopholis americana (Wicke et al. 2013). The genome may become extensively rearranged, but a few genes remain functional (Wicke et al. 2013); the IR has been lost more than once (Wolfe et al. 1992; Jansen & Ruhlman 2012).
Horizontal nuclear gene transfer from Sorghum and its relatives to Striga (but not Orobanche) has been demonstrated, the transferred host genes functioning in the nucleus of the parasite (Yoshida et al. 2010).
For the evolution of nuclear genome size in the family, see Weiss-Schneewiess et al. (2005); genome size is reduced after polyploidization. Unlike chloroplast genomes, nuclear genomes of holoparasitic taxa are much larger - to almost 10x - than that of the free-living Lindenbergia, although the nuclear genome of the hemiparasite Schwalbea is only slightly larger than that of Lindenbergia. Orobanche has many more repetitive DNA clusters contributing to genome size increase (Piednoël et al. 2012). Gruner et al. (2010) suggested that a facilitating factor for this increase was rootlessness; root growth in taxa with large nuclear genomes is reduced, but of course root growth in holoparasistic taxa is minimal.
For chromosome numbers and karyotype evolution in Orobanche and relatives, see Schneeweiss et al. (2004c).
Economic Importance. A number of Orobanchaceae, e.g. Striga and Alectra species of the tropical clade (see below), are very serious parasites primarily on legume and grain crops in warmer and drier areas and especially in sub-Saharan Africa, where they are still spreading. Striga parasitizes monocots, affecting ca 40% of the cereal producing areas and causing average losses in yield of 30-90%, especially on poorer soils. A single plant of Striga can produce up to 100,000 seeds which can remain viable for about 20 years (Scholes & Press 2008; see also Ejeta & Gressel 2007; Yoshida & Shirasu 2009; Irving & Cameron 2009). Alectra vogelii can cause the complete loss of legume crops it infects (Morawetz & Wolfe 2009), while Orobanche parasitizes eudicot crops in more or less temperate parts of the world.
Chemistry, Morphology, etc. Orobanchaceae have orobanchin, a phenylpropanoid ester of caffeic acid, and silicic acid, and their iridoids are derived from the aucubin pathway (Thieret 1971; Rank et al. 2004); c.f. Gesneriaceae. For fatty acids in the seeds of Orobanche, see Velasco et al. (2000).
Fischer (2004b) noted that a collar-like base of the corolla tube persists after the rest has fallen off - is this a family character? Corolla aestivation is interesting in this clade. The abaxial-lateral pair of corolla lobes commonly envelops the adaxial-lateral lobes, while in Euphrasia and its relatives the abaxial lobe also envelops this latter pair of lobes - both forms of quincuncial aestivation; in a number of other Orobanchaceae, the abaxial lobe envelops all other lobes, i.e. ascending cochleate aestivation (Armstrong & Douglas 1989). For floral development, see Armstrong and Douglas (1989), Endress (1999). Greilhuber (1974) observed endomitotic polyploidization in the cells of the inner tapetum in some genera - but not in Pedicularis, Melampyrum, and Plantaginaceae. The chalazal haustorium of Melampyrum is massive and binucleate (Takhtajan 2013).
The recently-described Eremitilla is very distinctive morphologically, i.a. the stamens are free from the corolla tube and the anther thecae are more or less embedded in the expanded filament apex (Yatskievych & Jiménez 2009).
For general treatments, see Terekhin and Nikitcheva (1981), Fischer (2004b: Scrophulariaceae p. pte), Demissew (2004: Cyclocheilaceae), Harley (2004: Nesogenaceae), the Parasitic Plants website (Nickrent 1998 onwards) and Heide-Jørgensen (2008); for floral development, see Canne-Hilliker (1987), for corolla aestivation, see Eichler (1875) and Armstrong and Douglas (1989), for pollen, see Minkin and Eshbaugh (1989), Lu et al. (2007) and Zare et al. (2014: heteromorphism in Orobancheae), for ovules and seeds, see Takhtajan (2013), for ovules of Cyclocheilon, etc., see Junell (1934), for embryology, see Krishna Iyengar (1940b), Tiagi (1963) and Arekal (1963) and references, and for seed morphology, see Musselman and Mann (1976), Joel et al. (2012) and M.-L. Liu et al. (2013: Pedicularis).
Phylogeny. For the delimitation and composition of the family, see Young et al. (1999), Wolfe et al. (2005), Bennett and Mathews (2006), etc. In a rather restricted phylogenetic analysis, Rehmannia (previously in Gesneriaceae) had been associated with Oreosolen (Albach et al. 2007), in Scrophulariaceae s. str. (Oxelman et al. 2005), but this may be a rooting problem. In a rather more extended study, Rehmannia was sister to Orobanchaceae, while Oreosolen indeed linked with Verbascum and relatives, forming part of a north temperate group in Scrophulariaceae (Jensen et al. 2008b). In a tree found by Oxelman et al. (2005), Rehmannia linked very weakly with Phryma, Paulownia, Mazus and Lancea, as well as with genera of Orobanchaceae.
Recent work suggests that Rehmannia and Trianeophora, both East Asian, form a strongly supported clade that is sister to the rest of the family - i.e. Lindenbergia and the rest (Xia et al. 2009; see also Albach et al. 2009; Fischer et al. 2012). Albach et al. (2007) had recorded the presence of iridoids in Rehmannia, although these are at best very uncommon in Gesneriaceae, and also at least some mannitol, a polyol not occurring in Scrophulariaceae s. str. but found i.a. in some Orobanchaceae. However, [Rehmannia + Trianeophora] did not immediately link with other Orobanchaceae in some analyses in Q.-M. Zhou et al. (2014). Rehmannia is not known to be hemiparasitic; it has a racemose inflorescence, its flowers lack bracteoles, the two abaxial-lateral corolla lobes are outside the others (as is common in Orobanchaceae), and its stigma lobes are sensitive. Trianeophora has bracteoles, it may have a staminode, but its floral aestivation is similar, if quite variable (Wang & Wang 2005: close to Digitalis). Phytochemistry also links Triaenophora closely with Rehmannia (Jensen et al. 2008b). Rehmannia has 1:3 nodes and petioles with arcuate + wing bundles, both very common in Lamiales (pers. obs.).
Lindenbergia may be sister to the rest of the family (e.g. Wolfe et al. 2005; Albach et al. 2009, but sampling limited; Fischer et al. 2012) or it may link more particularly with a small group of parasitic taxa (Bennett & Mathews 2006: support weak). Recent work places it sister to the rest of Orobanchaceae with overall rather strong support (McNeal et al. 2013; some analyses in Q.-M. Zhou et al. 2014). Lindenbergia is autotrophic (Hjertsen 1995) and has tricolporate pollen rather like that common in Lamiales, while the pollen of many other Orobanchaceae is tricolpate and retipilate (Minkin & Eshbaugh 1989; Bennett & Mathews 2006).
Other than that, one summary of relationships is [holoparasitic clade [Castilleja, Pedicularis, etc. [Euphrasia, Rhinanthus, etc. + tropical clade]]] (Bennett & Mathews 2006). R. G. Olmstead (pers. comm. 2003) noted that the inclusion in the tropical clade of Nesogenes (Nesogenaceae) and Cyclocheilon and Asepalum (Cyclocheilaceae), all poorly known, was likely (see also B. Bremer et al. 2002 for Cyclocheilon). There was strong support for Nesogenes (the only taxon of this group included) being sister to the shrubby Radamea (Bennett & Mathews 2006; McNeal et al. 2013), and these two genera belonged to a strongly supported tropical clade (Bennett & Mathews 2006). In a more comprehensive analysis, ex Cyclocheilaceae and Nesogenaceae are sister to this tropical clade, within which there was some resolution of relationships (Morawetz & Randle 2009, esp. Morawetz et al. 2010); Nesogenes was sister to Graderia and in a clade that includes Striga (Morawetz et al. 2010; see also Fischer et al. 2012). In a study focussing on Acanthaceae, McDade et al. (2012) found a fascinating set of relationships, [Rehmannia [Lindenbergia [Cyclocheilon + the rest]]], although support for the position of Cyclocheilon (see also below) was not that strong.
The position of the woody liane Brandisia is unstable and the genus is isolated (Bennett & Mathews 2006; esp. McNeal et al. 2013). Wightia, with which it has been linked, is not immediately related, but it does belong somewhere in the clade [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]] - see above).
Inclusion of Nesogenes, and in particular Cyclocheilon and Asepalum considerably increases the morphological diversity of Orobanchaceae. Cyclocheilon and Asepalum lack much in the way of a calyx, the calyx being at most a minute rim, but have large bracteoles enveloping the flower bud (c.f. Acanthaceae-Nelsonioideae). They are also shrubs with red roots [?always]; the flowers are single in the leaf axils; the exine is thickened near the apertures; the placentation is axile or parietal, with 1-5 apotropous ovules/carpel, endothelium?, the funicles are long and the stigma is lingulate. The fruit is a capsule or schizocarp; there is no endosperm. Although Harley (2004) notes similarities between the pollen of Cyclocheilaceae, Nesogenaceae (both have tricolpate pollen, that of Nesogenes is perhaps also pilate) and Orobanchaceae, nothing is known of stomatal closure and parasitism in these plants. Clarification of their relationships and their ecology is needed to help our understanding of the evolution of parasitism in Orobanchaceae.
A recent study that included ca 2/3 the genera of Orobanchaceae and used both nuclear and plastid genes yielded a rather strongly supported phylogeny that is the basis for the groupings above, although Lindenbergia was not basal in the PHYB + PHYA analyses and the position of Brandisia was unclear (McNeal et al. 2013).
For a re-evaluation of relationships of genera in the old Rhinantheae, see Tesitel et al. (2010 - also other papers in Folia Geobotanica 45(4). 2010); Scheunert et al. (2012) suggest that Rhinanthus itself is not monophyletic (see also Bennett & Mathews 2006). For a phylogeny of Pedicularis, see Ree (2005), for that of Euphrasia, see Gussarova et al. (2008), of Orobanche and relatives, see Schneeweiss et al. (2004a, c) and Park et al. (2008), and of Castilleja, see Tank and Olmstead (2008, 2009). For further details of relationships, see dePamphilis (1995) and Olmstead and Reeves (1995). Tank et al. (2006) summarize ideas on relationships within the family.
Classification. See McNeal et al. (2013) for the tribal classification that is followed here - ex Cyclocheilaceae (Cyclocheilon and Asepalum) were absentees. Although a number of genera were not sampled, they are small and will have only a marginal effect on species numbers. Thus 12 genera from the old Buchnereae (Fischer 2003) were not examined, but they include a mere 25 species.
See Hjertsen (1995) for a monograph of Lindenbergia; Tank et al. (2009) provide a phylogenetic classification of Castillejinae.
Previous Relationships. Hemiparasitic genera like Euphrasia and Pedicularis used to be considered intermediates between holoparasitic Orobanchaceae and Scrophulariaceae s.l. (e.g. Boeshore 1920). Rehmannia has often been linked with Titanotrichum and included in Gesneriaceae (Xia et al. 2009 for references).
Botanical Trivia. The purple-flowered Lathraea clandestina is one of the few parasitic plants cultivated for its horticultural merit.
Thanks. To David Tank for useful comments; Robert Mill also caught a number of mistakes around here.