EMBRYOPSIDA Pirani & Prado (crown group)
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; 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, 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 multilaminate]; spores trilete [?level]; 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 embryophytes.
Abscisic acid, ?D-methionine +; sporangium with columella; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; 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 in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour; spores trilete.
Sporophyte well developed, branched, free living, sporangia several; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response, passive control of leaf hydration; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells +, tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; leaf blade with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, lacking columella, eusporangiate [sporangia derived from periclinal divisions of several epidermal cells, wall multilayered]; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryo with roots arising lateral to the main axis [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root cap +; tracheids with scalariform-bordered pits; leaves spirally arranged, 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, root apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, 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, spiral, 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; 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, embryo axis straight, so 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.
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, secondary veins pinnate, overall growth ± diffuse, venation hierarchical-reticulate, 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 binucleate at dispersal, mature male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, 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 [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], 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).
MONOCOTYLEDONS / MONOCOTYLEDONEAE / LILIANAE Takhtajan
Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans, benzylisoquinoline alkaloids 0, hemicelluloses as xylans; root apical meristem?; root epidermis developed from outer layer of cortex; trichoblast in atrichoblast [larger cell]/trichoblast cell pair, the former further from apical meristem, in vertical files, or hypodermal cells dimorphic; endodermal cells with U-shaped thickenings; cork cambium in root [uncommon] superficial; root vascular tissue oligo- to polyarch, medullated, lateral roots arise opposite phloem poles; primary thickening meristem +; vascular bundles in stem scattered, (amphivasal), closed, vascular cambium 0; tension wood 0; vessel elements in root with scalariform and/or simple perforations; tracheids only in stems and leaves; sieve tube plastids with cuneate protein crystals alone; stomata parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf base sheathing, sheath open, petiole 0, blade linear, main venation parallel, main veins joining successively from the outside at the apex, transverse veinlets +, unbranched, vein/veinlet endings not free, margins entire, Vorläuferspitze +, colleters + ["intravaginal squamules"]; inflorescence terminal, racemose; flowers 3-merous [6-merous to the pollinator?], polysymmetric, pentacyclic; P = T, each with three traces, median T of outer whorl abaxial, aestivation open, members of whorls alternating, [pseudomonocyclic, each T member forming a sector of any tube]; stamens = and opposite each T member [primordia often associated, and/or A vascularized from tepal trace], anther and filament more or less sharply distinguished, anthers subbasifixed, endothecium from outer secondary parietal cell layer, inner secondary parietal cell layer dividing; G , with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; fruit a loculicidal capsule; seed testal; endosperm with distinct nuclear and chalazal chambers, embryo long, cylindrical, cotyledon 1, apparently terminal, with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous, hypocotyl short, (collar rhizoids +); cotyledon with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial; no dark reversion Pfr -> Pr; duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost.
[ALISMATALES [PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: ethereal oils 0; raphides + (druses 0); leaf blade vernation variants of supervolute-curved, (margins with teeth, teeth spiny); endothecium develops directly from undivided outer secondary parietal cells; tectum reticulate with finer sculpture at the ends of the grain, endexine 0; (septal nectaries + [intercarpellary fusion postgenital]). Back to Main Tree
Age. Magallón and Castillo (2009, which consult for more details) suggest ca 162 m.y. for relaxed and 126.5 m.y. for constrained penalized likelihood datings of the divergence of Alismatales from other monocots; Bell et al. (2010) estimate ages of (147-)136, 118(-107) m.y.; another estimate is ca 131 m.y. (Janssen & Bremer 2004), while estimates were (123-)128(-133) m.y. in Merckx et al. (2008a), (156-)138(-130) m.y. in Nauheimer et al. (2012: sampling), ca 108.1 m.y. in Xue et al. (2012), and 137-116 m.y. in Mennes et al. (2013).
Chemistry, Morphology, etc. Although raphides occurring in bundles and largely filling the cells containing them are common in this clade, druses may at least sometimes be found along with them (e.g. Prychid et al. 2008). For useful comments of the typology of endosperm development, see Floyd and Friedman (2000).
ALISMATALES Dumortier Main Tree.
(Cyanogenesis + [triglochinin]); starch grains pteridophyte-type, amylophilic; inflorescence scapose; anthers extrorse; tapetum amoeboid, cells uninucleate; carpels with completely unfused canals, styles +, stigma dry [common]; embryo (chlorophyllous), large, cotyledon large; seedling with hypocotyl and root well developed, collar rhizoids +. - 14 families, 166 genera, 4560 species.
Age. Crown-group Alismatales are dated to 124-111 m.y. by Wikström et al. (2001), ca 128 m.y. by Janssen and Bremer (2004) and around 103 m.y. by Bremer (2000b); Magallón and Castillo (2009) suggested ca 147 m.y. and 126 m.y., Bell et al. (2010) ages of (138-)122, 102(-93) m.y., and Magallón et al. (2013) suggested an age of around 122.6 m.y.; estimates were (133-)123(-97) m.y. in Merckx et al. (2008a), (146-)138(-130) m.y. in Nauheimer et al. (2012b) and 134-90 m.y. in Mennes et al. (2013).
See Stockey 2006 for a review of fossils that have been placed in Alismatales; see also Araceae below.
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...
Evolution. Divergence & Distribution. Les et al. (2003) discuss the distributions of a number of the hydrophytic taxa of this clade; most of them are likely to be rather young. Furness (2013) optimised a number of palynological characters in Alismatales (surface sculpture, microsporogenesis, tapetum type); those connected with hypohydrophily in marine members are homoplasious.
Ecology & Physiology. Alismatales include the only fully submerged marine angiosperms (Larkum et al. 2006 for an entry into the recent literature on "seagrasses" - loosely, all marine angiosperms; also Wissler et al. 2011 and below). Alismatales also include many other aquatics and hydrophytes and plants of marshy habitats, and this may well be the ancestral condition for the group as a whole (for Araceae, see Nauheimer et al. 2012). It is not surprising that a number of taxa lack vessels.
Bacterial/Fungal Associations. The apparent absence of mycorrhizae in many Alismatales may be because many of its members grow in water, either rooted in the mud or free-floating; mycorrhizae are usually absent in such situations (e.g. Safir 1987). However, the mycorrhizal status of Tofieldiaceae is unclear, and Araceae occupy a variety of habitats, being common in well-watered to aquatic environments.
Plant-Animal Interactions. Caterpillars of Pyralidae-Schoenobiinae are found on aquatic monocots, as are larvae of Chrysomelidae-Donaciinae (Powell et al. 1999; Jolivet 1988; esp. Kölsch & Pedersen 2008); the latter, at least, are found on aquatic plants in general and so are also to be found on Nymphaeaceae, Haloragaceae, etc.
Chemistry, Morphology, etc. The root stele is often tri- to pentarch. A number of wholly aquatic Alismatales lack vessels in any part of the plant (Cheadle 1944). When the leaves are petiolate, the vascular bundles are in an arc; inverted bundles are also common. Riley and Stockey (2004) describe the venation of a number of net-veined members of this order in considerable detail; such leaves usually have tertiary veins.
The bract subtending the flower and the abaxial tepal may be fused or otherwise developmentally linked, so producing a hybrid organ, or the bract may be lost, in some Alismatales, and both phenomena can occur in the one genus (Buzgo 2001; Remizowa et al. 2013a, b). In some other Alismatales the flowers may be pseudanthial (Soltis et al. 2005; Remizowa et al. 2011). Is the pollen endexine ever lamellate (it is in Acorus)? It has been said that Alismatales, inc. Araceae, are the only monocots with green (chlorophyllous) embryos (Seubert 1993), although they are also found in some Amaryllidaceae-Amaryllidoideae-Amaryllideae. Although endosperm is usually not well developed in seeds here, when it occurs it at least sometimes contains starch as a reserve (Dahlgren et al. 1985).
For seedling morphology, see Tillich (1985), for pollen, see Grayum (1992), Furness and Banks (2010), for ovules, see Igersheim et al. (2001), and for carpel evolution, see J. M. Chen et al. (2004a).
Phylogeny. Basal relationships in Alismatales are summarized by Les and Tippery (2013). Tofieldiaceae were placed here with only moderate support (Källersjö et al. 1998; Chase et al. 2000a); sometimes sister to the rest of the order (Graham et al. 2006, but sampling; Iles et al. 2013: support weak) or sister to Araceae (Tamura et al. 2004b). However, Tamura et al. (2004a), Janssen and Bremer (2004), Givnish et al. (2006b), Chase et al. (2006: strong support), Soltis et al. (2011: little support, but sampling), Nauheimer et al. (2012b) and others since have all placed Araceae as sister to all other Alismatales, and Tofieldiaceae sister to the remaining taxa; this topology is followed here. For relationships between other Alismatales, see Les et al. (1997: the rest of the tree here is largely based on this), also Y. Kato et al. (2003), J.-M. Chen et al. (2004b), G. Petersen et al. (2006c: 2 mitchondrial and 1 chloroplast genes), Liu and Li (2010) and Nauheimer et al. (2012b).
However, there are a number of uncertainties. Thus G. Petersen et al. (2006c) did not even recover a monophyletic [Hydrocharitaceae + Alismataceae + Butomaceae]. The tree in Janssen and Bremer (2004) is largely similar to that below, but the positions of Aponogetonaceae and Scheuchzeriaceae are not entirely certain, and this is discussed below under the former. For the relationships of Maundia, ex-Juncaginaceae, see below, however, von Mering and Kadereit (2010) were not sure of the exact position of Maundiaceae, and they also found weak support for a clade [Araceae + Tofieldiaceae]. For details of relationships in the main sea-grass clade, see also below; these remain particularly uncertain.
For a possible [Acorus + Alismatales] relationship, see Acorales.
Classification. Many small families have been described in Alismatales because the adaptations associated with the aquatic habitat are so striking. As relationships get further clarified in the [Juncaginaceae [Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]] clade, some consolidation of the small families there may be in order. A more restricted circumscription of Alismatales has also been suggested given uncertainty of the relationships of Acoraceae and Tofieldiaceae, although Acoraceae are always in the same immediate clade as the reduced Alismatales and Petrosaviaceae have only very rarely jumped outside the clade; this entails the recognition of a Potamogetonales as well (Les & Tippery 2013).
Previous Relationships. Most of the taxa here included in Alismatales have been recognised as being related, thus most are in Engler's (1892) Helobieae + Spathiflora and Cronquist's (1981) and Takhtajan's (1997) Alismatidae. However, in some classifications a group Spadiciflorae included all those taxa with a spadix, e.g. Cyclanthaceae, Araceae and Arecaceae, families that are now placed in three immediately unrelated orders, Pandanales, Alismatales and Arecales, while Engler (1892) linked Pandanaceae, Arecaceae and Cyclanthaceae. The relationships of Tofieldiaceae have been unclear, although they have usually been placed in a quite different part of the monocots, having a flower that fitted into the concept of the old Liliaceae sensu latissimo (see below, also Dahlgren & Clifford 1982; Tamura 1998).
Includes Alismataceae, Aponogetonaceae, Araceae, Butomaceae, Cymodoceaceae, Hydrocharitaceae, Juncaginaceae, Maundiaceae, Posidoniaceae, Ruppiaceae, Potamogetonaceae, Scheuchzeriaceae, Tofieldiaceae, Zosteraceae.
Synonymy: Alismatales Dumortier, Aponogetonales Hutchinson, Arales Dumortier, Butomales Hutchinson, Cymodoceales Nakai, Elodeales Nakai, Hydrocharitales Dumortier, Juncaginales Hutchinson, Lemnales Link, Najadales Dumortier, Orontiales J. Presl, Pistiales Richard, Posidoniales Nakai, Potamogetonales Dumortier, Ruppiales Nakai, Scheuchzeriales B. Boivin, Tofieldiales Reveal & Zomlefer, Vallisneriales Nakai, Zosterales Nakai -- Alismatidae Takhtajan, Aridae Takhtajan - Aropsida Bartling, Hydrocharitopsida Bartling, Najadiopsida Hoffmannsegg & Link
ARACEAE Jussieu, nom. cons. Back to Alismatales
Cyanogenic glucoside triglochinin, flavone C-glycosides +; dimorphic root hypodermis +; sieve tube plastids also with starch; pseudopetiole bundles scattered; stomata unorientated, also anomo- ["basal" genera] and tetracytic; inflorescence dense, flowers sessile [spadix], unbranched, inflorescence bract well developed; flowering period up to weeks, floral bracts, bracteoles 0; flowers 2-3-merous, in latter case median member of outer whorl of T adaxial, T ± hooded, with single trace, free (connate); (microsporogenesis simultaneous); pollen (often starchy), ektexine +; septal nectaries 0; carpels (basally) ascidiate, fusion usu. congenital, loculus with secretory trichomes, style at most short, stigma also wet; ovules ± unvascularized; fruit a berry; testa multiplicative, ³5 cells across, often parenchymatous, or with exotesta and/or endotesta and mesotesta lignified, tegmen collapsed; x = 16; cotyledon not photosynthetic, (collar rhizoids or collar roots +).
117[list]/4095 (5422 est.) - 8 subfamilies below. Mostly tropical, but few Africa-Madagascar and Australia.
Age. Crown-group Araceae have been dated to (132-)122(-112) m.y. by Nauheimer et al. (2012b); other dates include 98-89 m.y. (Wikström et al. 2001), ca 128 m.y. (Janssen & Bremer 2004) or to (114-)89, 79(-55) m.y.a. (Bell et al. 2010).
Distinctive pollen assigned to Pothooideae-Monstereae has been found in Early Cretaceous deposits of the late Barremian-early Aptian of some 110-120 m.y. old in Portugal (Friis et al. 2004); other pollen types that may also be Araceae were found at the same place (see also Hesse & Zetter 2007); however, Mayoa portugallica, one fossil involved, may be an individual of Laganella, an euglenid alga... (Hoffmann & Zetter 2010). The site is now, alas, developed. Nevertheless, macrofossils apparently of Araceae-Aroideae (a decidedly non-basal clade) have been discovered in deposits of a similar age in Portugal (Friis et al. 2010). Bogner et al. (2005) described a rather later (72 m.y. old: Late Campanian) spadix with perfect, tepalline flowers and a stout, conical, stigma/style from Alberta, Canada, and pollen fossils of a similar age from Eastern Siberia have been identified as Lasioideae (Hoffmann & Zetter 2010). See also Wilde at al. (2005), Bogner et al. (2007), and Herrera et al. (2008) for leaf fossils.
[Gymnostachydoideae + Orontioideae]: stomata parallel; parallel veins in 2(+) orders; tectum ± continuous, ovules straight, 1-2/carpel, inner integument 3-4 cells thick, ± multiplicative; seedling with cataphylls.
Age. The age for this node was estimated as (115-)96(-73) m.y. by Nauheimer et al. (2012b).
1. Gymnostachydoideae Bogner & Nicolson
Foliar vascular bundles with fibre sheaths and girders; leaves two-ranked, linear, leaf margins minutely toothed; inflorescence branched, green "spathe" at each branching point, spadices many; flowers 2-merous [outer pair of T lateral]; A thecae forming tip above slit; G 1, ascidiate, loculus lacking secretory trichomes stigma dry; ovule 1/carpel, apical, pendulous, unitegmic, micropyle naked, parietal tissue?; testa 0; endosperm copious, green, with starch, embryo green; n = 12; collar rhizoids 0.
1/1: Gymnostachys anceps. East Australia (map: from Mayo et al. 1997).
2. Orontioideae Mayo, Bogner & Boyce
Flavonols +, glycoflavones 0; vessels 0; (collenchyma in cortical bands), bundle-associated fibre strands +/0; (laticifers + - Orontium); (biforine raphides +); (stomata anomocytic); leaves spiral, with weakly differentiated pseudopetiole, blade and (pseudo)midrib, cross veins +; inflorescence bract large, coloured [spathe] (0); flowers 2-3-merous; (A also ventrifixed); ovary inferior (not - Orontium), secretory trichomes 0 - Symplocarpus; ovules 1-2/carpel, ± basal, (hemianatropous - Orontium), outer integument 22+ cells across, (lobed - Symplocarpus), inner integument 5-10 cells across; endosperm ± 0; n = 13-15.
3/6. Temperate East Asia, W. and E. North America (map: from Mayo et al. 1997).
Age. The age for crown-group Orontioideae is estimated at (77-)53(-28) m.y. by Nauheimer et al. (2012b). The fossil Spixiarum kipea, from the Crato formation in Brazil, is dated to 115-112 m.y., so if included in the crown group (a possibility: Coiffard et al. 2013b) this age would be rather discordant.
Synonymy: Orontiaceae Bartling
[Lemnoideae [[Pothoideae + Monsteroideae] [Lasioideae [Zamioculcadoideae + Aroideae]]]]: nucellar tissue disappears during ovule maturation, endothelium +.
Age. The age for this node was estimated as (113-)104(-93) m.y. by Nauheimer et al. (2012b).
3. Lemnoideae Engler
Floating aquatic herbs; roots monarch (0); collenchyma and bundle fibres 0; vessels 0; (prophyll 0); biforine raphides +; stomata anomocytic [on adaxial surface only]; plant made up of thalloid stem-leaf units, primary vein alone; (spathe 0), spadix not discernable; P 0; A 1-2, (monothecal), wall with secondary parietal layers not dividing; pollen trinucleate, mixed with raphides, globose to ellipsoid, ulcerate, spiny; G 1, stigma funneliform; ovules 1-7/carpel, (straight), (outer integument to 4 cells across), (nucellar cap 2 cells across); embryo sac bisporic [chalazal dyad], 8-nucleate [Allium-type]; fruit an achene [sort of]; seed operculate [operculum tegmic], testa ca 4 cells across; endosperm starchy, copious, chalazal haustorium +, embryo undifferentiated; n = 10, extensive polyploidy and dysploidy; hypocotyl and primary root 0, cotyledonary sheath broad and photosynthetic.
5/37. World-wide (map: Hultén 1962; Meusel et al. 1965; Landolt 1986: "absence" in tropical America and Africa may be due to undercollecting; Fl. Austral. 39: 2011). [Photo - Wolffia.]
Age. Crown-group Lemnoideae are estimated to be (88-)73(-59) m.y.o. by Nauheimer et al. (2012b).
Synonymy: Lemnaceae Gray, nom. cons., Wolffiaceae Bubani
[[Pothoideae + Monsteroideae] [Lasioideae [Zamioculcadoideae + Aroideae]]]: shoots consisting of reiterated sympodial units, branching from the axil of the penultimate foliar organ outside the inflorescence spathe; leaves with clearly differentiated pseudopetiole, blade and (pseudo)midrib, base with lateral (auriculate) flanges, (ligule +); inflorescence bract large, coloured [spathe], peduncle +; (calcium oxalate crystals, inc. raphides, mixed with pollen); endosperm sparse to copious; seedling cataphylls +/0.
Age. The age for this node was estimated to be (107-)97(-87) m.y. by Nauheimer et al. (2012b).
[Pothoideae + Monsteroideae]: stem usu. aerial, plants (hemi)epiphytes, climbers; (separate stem cortical vascular system +); (vessels in stem); H- or T-shaped trichosclereids + (0); styloids +; fibres ensheathing bundles; leaves two-ranked [Pothos] or spiral, elliptical to complex, higher-order venation reticulate, pseudopetiole apically geniculate; crystals often surrounding the embryo.
Age. The age for this node was estimated at (94-)81(-68) m.y. by Nauheimer et al. (2012b).
4. Pothoideae Engler
Climbers and epiphytes common; (main axis monopodial); (biforine raphides +); (leaves 2-ranked), fine venation reticulate, ("petile" flattened); spathe not enclosing spadix, ± reflexed; flowers 2-3-merous; anther thecae often forming tip above slit; (pollen 3-4 porate - Anthurium); ovules 1-2/carpel, basal/parietal, apotropous, outer integument 6-8 cells across, inner integument 6-8 cells across, parietal tissue?; spathe persistent in fruit; (outer integument not multiplicative), (inner integument ca 6 cells across - Pothos); endosperm with starch, (embryo green); n = (10) 12 (14-15); (seedling internodes long; very short unifacial part of cotyledon).
4/900: Anthurium (825), Pothos (70). Tropical America, Madagascar to South and Southeast Asia, Malesia and N.E. Australia (map: from Mayo et al. 1997). [Photo - Flowers, Fruits.]
Age. Crown-group Pothoideae are some (77-)65(-56) m.y.o. (Nauheimer et al. 2012b).
Synonymy: Pothaceae Rafinesque
5. Monsteroideae Schott
(Fibres only capping bundles); trichosclereids + (0); spathe often deciduous; flowers 2(-3 - Spathiphylleae)-merous; P often 0; pollen inaperturate, or sulcus extended or encircling, (ektexine dissected - 0); style with abundant trichosclereids; ovules 1-4(-many)/carpel, often basal, (hemianatropous); spathe soon deciduous in fruit; seed often embedded in mucilage; endosperm + [Spathiphylleae] or 0; n = 12, 14, 15, 21 [much polyploidy, n = 30 common].
12/360: Rhaphidophora (100: paraphyletic), Rhodospatha (75). Tropical South and Southeast Asia to the Pacific, South America (Africa) (map: from Mayo et al. 1997).
Age. The age of crown-group Monsteroideae is (64-)55(-47) m.y. (Nauheimer et al. 2012b).
Synonymy: Monsteraceae Vines
[Lasioideae [Zamioculcadoideae + Aroideae]]: plant tuberous or rhizomatous; ?leaves spiral.
Age. The age of this node is estimated at some (101-)90(-80) m.y. (Nauheimer et al. 2012b).
6. Lasioideae Engler
(Rooted aquatics), often prickly; sieve tube plastids with a little starch; fibres ensheathing or capping bundles; petiole long, warty, aculeate, or strikingly coloured, ± geniculate apically; spathe often spirally twisted, inflorescence flowering basipetally; P (0 [Pycnospatha], 4-9); A (-12), anthers with oblique pore-like slits; pollen grains lacking starch, sulcus with lamellate ectexine and thick bilayered endexine [outer: flakes or lamellae; inner: spongy]; G 1 [2-3(-16)], 1 (-6) locular, placentation various, inc. basal-diffuse; ovules 1-2(-many - esp. Cyrtosperma)/loculus, apotropous, ana-campylotropous, ?parietal tissue; seed surface usu. lamellate or warty, exotesta papillate, inner part of mesotesta and endotesta both lignified; endosperm thin (0), embryo green, curved; n = 13.
10/58. Pantropical (Africa - Lasimorpha) (map: from Mayo et al. 1997).
Age. Crown-group Lasioideae can be dated to some (38-)26(-15) m.y.a. (Nauheimer et al. 2012b).
Synonymy: Dracontiaceae Salisbury, Lasiaceae Vines
[Zamioculcadoideae + Aroideae]: plants monoecious (dioecious); spathe differentiated into tube plus blade, spadix differentiated into zones with staminate and carpellate flowers, flowers opening simultaneously in each zone, flowering period usu. 2-4 days; flowers imperfect; pollen inaperturate [omniaperturate].
Age. This node can be dated to (97-)87(-77) m.y. (Nauheimer et al. 2012b).
7. Zamioculcadoideae Bogner & Hesse
(Leaves compound, petiole geniculate, fine venation reticulate - Zamioculcas); staminate flowers: A (connate), introrse to extrorse; pollen also encircling sulcate, columellae winding and forming a sort of internal tectum as well as the external tectum, endexine lamellate, intine thin, (calcium oxalate crystals mixed with pollen); pistillode +; carpellate flowers: G , placentation axile; ovule one/carpel, ascending, ?parietal tissue; seeds almost lacking endosperm; n = (14), 17.
3/21. Africa, Kenya to Natal (map: from Mayo et al. 1997).
Age. The age of crown-group Zamioculcadoideae has been estimated to be (42-)23(-6) m.y. by Nauheimer et al. (2012b).
Habit various, (epiphytes); (glucomannans +); laticifers +, articulated, (anastomosing), (0); collenchyma in cortical bands or bundle-associated strands (0); fibres variously associated with bundles; biforine raphides + [H-shaped in T.S., wall thick, except for papillae at the two ends, lignified, cell contents mucilaginous] (0); leaves very variable, (parallel veins of different orders), (vein endings free); (inflorescences several together), (spadix with sterile zones); P 0; staminate flowers: A connate (not - Philodendron), connectives thick, (anthers introrse; anthers dehiscing by pores); pollen (trinucleate), (mixed with raphides) (spiny, smooth, striate, etc.), (in tetrads), ectexine thin, sporopollenin 0, or +, ektexine thin, wall with polysaccharides, endexine bilayed, (thick, spongy), intine massive; pistillode +; carpellate flowers: staminodes +, (G 1?, [2-4(-47)], placentation parietal, apical, basal, (styles connate); ovules 1-many/carpel, straight, (outer integument not multiplicative [Arisaema]), parietal tissue absent-3 cells across, base broad, massive [Theriophonium]; (endosperm with starch), chalazal haustorium +, unicellular, (storage cotyledons), (embryo green); n = 7+, but 13, 14, 17 common; (cotyledon sheath photosynthetic, bifacial [e.g. Colocasia, Philodendron, Xanthosoma], even leafy; collar rhizoids +).
68/2305: Philodendron (500), Homalomena (500), Arisaema (170), Amorphophallus (150), Alocasia (140), Schismatoglottis (120), Xanthosoma (60), Cryptocoryne (50). Tropical and warm temperate (the latter - Arum and relatives) (map: from Mayo et al. 1997, distribution attributable to Calla alone in green). [Photo - Flowers.]
Age. Crown-group Aroideae are some (92-)82(-73) m.y.o. (Nauheimer et al. 2012b).
Synonymy: Arisaraceae Rafinesque, Caladiaceae Salisbury, Callaceae Bartling, Colocasiaceae Vines, Cryptocorynaceae J. Agardh, Philodendraceae Vines, Pistiaceae C. Agardh
Evolution. Divergence & Distribution. Evidence suggests that all eight subfamilies of Araceae had diverged before the K/T boundary, early evolution in the family possibly occuring in Laurasia (Nauheimer et al. 2012b: see table S4, esp. S5 for 140+ dated nodes and further discussion of diversification in the family).
It has been estimated that Alocasia, centred in Borneo, diversified ca 13.5 or 19.3 m.y.a. (stem group ages are ca 10 m.y. more), and there were many subsequent dispersal events through the whole Southeast Asian/Malesian region (Nauheimer et al. 2012a: m.l. trees with little support).
For the possible base chromosome number of the family, see Cusimano et al. (2012 and references).
Ecology & Physiology. For epiphytism in Araceae, where it mostly occurs in Anthurium (ca 1/4 of its species), see (Zotz (2013).
Plant-Animal Interactions. Araceae are not much liked as food by butterfly caterpillars (Ehrlich & Raven 1964). A number of species of galerucine beetles (Aplosonyx) have been found feeding on laticiferous Aroideae from South East Asia where they make circular trenches in the leaves to interrup the latex flow and then eat out the portion of the leaf so isolated - it looks as if there are paper punch holes in the blade (Darling 2007); galerucines are known from other monocots and beetle herbivory in Araceae may be geographically more widespread.
Pollination Biology & Seed Dispersal.
Gibernau (2003, 2011) summarizes information on pollinators. More or less unpleasant (to us) odours are common in Araceae, as is evident from common names like skunk cabbage (Symplocarpus foetidus) and dead horse arum (Helicodiceros [Dracunculus] muscivorus), and pollination by flies and beetles - the latter may be the plesiomorphic condition in the family (Sannier et al. 2009; c.f. Bröderbauer et al. 2012: uncertain) - is common. Schiestl and Dötterl (2012) argue that the ability to detect particular volatile organic compounds in aroid-pollinating scarab beetles developed in the Jurassic, while the plants they pollinate evolved in the Cretaceous/Paleocene; an example of the quite common disconnect between the evolution of the pollinator and that of the plant. In addition, the beetles seem to have no particular preferences for compounds unique to the plant (Schiestl & Dötterl 2012). Caladium is a member of a clade characterised by being pollinated by dynastine scarab beetles (Mayo & Bogner 1988; Maia & Schlindwein 2006; see also Maia et al. 2010 - Philodendron). The volatiles produced by Arum attract insects in search of brood sites - the odour of A. palaestinum is that of rotting fruit, and it attracts Drosophila flies (Linz et al. 2010; Urru et al. 2011; Nauheimer et al. 2012a: fruit flies and Alocasia). Punekar and Kumaran (2010) describe the pollination of Indian species of Amorphophallus. A nectar-like but sometimes foul-tasting exudate may be produced by stigmatic hairs, etc., as in Anthurium (Daumann 1931; see also Fahn 1979), and this attracts pollinators; Croat (1980) discussed pollination in this speciose neotropical genus. Some species of neotropical Araceae, including members of both Anthurium and Spathiphyllum, are pollinated by euglossine bees (orchid bees) which show fair visitor specificity despite the apparently unspecialised flowers - the scent boquets of the attractants are different (Roubik & Hanson 2004; Hentrich et al. 2010b; Schiestl 2012).
The spathe of Aroideae is usually differentiated into tubular and blade-like portions. The fertile flowers are restricted to the basal part of the spadix, hence being more or less enclosed by the sometimes inflated tubular portion of the spathe. Inflorescences that trap the pollinator have evolved perhaps ten times or more in the family (Bröderbauer et al. 2012). Pollinators, particularly flies, attracted by the color of the blade, or the smell, or even the dangling apical portion of the spadix (e.g. some Arisaema) may be temporarily trapped inside the tubular portion by hairs, radiating sterile flowers, etc., but they are released when the staminate flowers open and they get covered with pollen (see Bröderbauer et al. 2012).
Thermogenesis has been detected in the inflorescences of Araceae. It is caused both by proteins that uncouple the components of the glycolytic pathway and by the mediation of an alternative oxidase, the net result being that glycolysis results in heat, not energy in the form of adenosine triphosphate, and rates of respiration can be very high (Gibernau et al. 2005; Watling et al. 2006; Onda et al. 2008; Barthlott et al. 2008 and references; Chouteau et al. 2009; Seymour 2010). The heat may volatilize compounds that attact pollinators, and/or provide a warm roost for them inside the spathe.
For a discussion on the evolution of the distinctive pollen that characterises most Aroideae, see Hesse (2006b). In a number of members of this subfamily the pollen is extruded from the anthers in almost toothpaste-like threads; the anthers of several genera open by pores. The arborescent South American Montrichardia has "explosive" pollen; the massively thick intine swells to an elongated structure ca 400 µm long within a few seconds, perhaps aiding its attachment to the pollinator, a hairless dynastid beetle (Weber & Halbritter 2007). A discriminant analysis of thirteen putatively pollinator-related characters, but not pollen surface, identified bee- and also less sharply differentiated beetle- and fly-pollinated morphologies (Gibernau et al. 2010; Gibernau 2003 for references), although how such analyses would fare if pollinator groups were not assumed is unclear. Grayum (1986) had earlier looked at features of the pollen surface and how they might correlate with pollinators; smooth pollen and beetle pollination were linked, as were spiny pollen and fly pollination, etc. Sannier et al. (2009: but see their caveats, Lemnoideae, Gymnostachys not included, only 2 Orontioideae, etc.) looked at pollinator and pollen across the whole family, and also suggested there was some correlation of pollen morphology and pollinator.
Raphides, prismatic calcium oxalate crystals, and other crystals from the walls of the anther may become mixed with the pollen (Barabé et al. 2004b; Barabé & Lacroix 2008b, Coté 2010; Coté & Gibernau 2012); their exact function is unclear. In Monsteroideae there are numerous trichosclereids in the stylar tissue and the spathe is deciduous; the trichosclereids may protect the exposed ovary against insects (there can be a variety of crystalline forms in different cells and tissues of the one plant - see Coté 2009). A variety of crystals is also found in the ovary (Coté & Gibernau 2012).
Understory Araceae in the Neotropics are a particularly important source of food for bats (Lobova et al. 2009).
Ecology & Physiology. The original habitat for the family is likely to have been more or less marshy (Nauheimer et al. 2012b). Climbers and epiphytes are notably common in Pothoidaeae and Monsteroideae, particularly in the former; all told, about 400 species of New World Araceae are climbers (Gentry 1991), rather fewer in the Old World (see also Benzing 1990). The leaves of climbers are often strongly heteroblastic, the leaves of a plant in the climbing phase being simpler than when it becomes reproductive. Monstereae are frequently epiphytic and often have seeds embedded in pulp, whether from the testa, trichomes, or the inner pericarp, perhaps to aid in their adhesion to branches (Mayo et al. 1998). Many Araceae are plants of shaded conditions, and net-veined leaves and fleshy fruits are associated with this habitat (Givnish et al. 2005). Interestingly, members of Aracaeae (they were hemiepiphytic) surveyed by Fisher et al. (1997) all developed signifcant root pressure.
Vegetative Variation. Vegetative variation in Araceae is considerable. Although many Araceae appear to be monopodial, the stem is usually a complex sympodium built up of repeating units each made up of expanded and reduced leaves and a terminal inflorescence (Engler 1877, translated by Ray & Renner 1990; Ray 1987b, 1988).
The leaves are very variable, both in gross morphology and in development (Ray 1987a for gross morphology). A number of taxa have fenestrate or apparently compound leaves produced by localised cell death. The leaves of Monstera, the swiss cheese plant, are fenestrate (see Melville and Wrigley 1969), while compound-leaved taxa include Zamioculcas and Dracontium. The leaves of Zamioculcas appear to be truly compound, with localised development of the blastozone, the marginal leaf meristem, producing the individual leaflets, while in Dracontium localised cell death results in what is an initially simple leaf blade with entire margins separating into a complex structure with numerous "leaflets". Such leaves may be huge, thus in Dracontium gigas the dissected foliar part is up to 4 m in diameter and is born on a petiole ca 5 m tall (Bown 2000). The leaves of Anthurium are notably variable, being entire to deeply lobed or even compound. Pulvini occur on the petiole of taxa like Dracontium. Details of basic leaf development vary considerably. Scindapsus develops in a "typical" monocot fashion, i.e. from the leaf base (Troll & Meyer 1955; Bharathan 1996; Doyle 1998b), while in Arisaema, Orontium, and Zamioculcas the blade develops from the upper part of the leaf primordium, i.e., they are similar in this to broad-leaved angiosperms (see also Periasamy & Muruganathan 1986 for Arisaema development).
The highly reduced vegetative body of Lemnoideae is variously interpreted as being some combination of leaf and shoot. Wolffia and Wolffiella lack both roots and veins in the thallus, and the thallus of the former may be less than 2.5 mm across; it is the smallest flowering plant known (see Lemon & Posluszny 2000b). The reproductive parts have been thought to represent either a reduced but perfect flower or a very highly reduced inflorescence; given the phylogenetic position of Lemnoideae, the former is perhaps more likely. The aquatic Pistia has a much less unconventional plant body, and its inflorescence, although reduced, is basically similar to that of other Aroideae; vegetative shoots are monopodial (Lemon & Posluszny 2000a). Both Lemnoideae and Pistia have supernumerary axillary buds which increases the complexity of their branching patterns. Although the early Tertiary fossil Limnobiophyllum seems "intermediate" between Lemnoideae and Pistia (Stockey et al. 1997), those two groups are not at all close in molecular phylogenies, and the fossil is to be assigned to Aroideae along with Pistia itself; there are yet other unrelated fossil floating aquatics in Araceae (Stockey et al. 2007). The Pistia lineage is quite old, 90-76 m.y. (Renner & Zhang 2004).
Genes & Genomes. DNA substitution rates are particulaly high in the free-floating Araceae, Lemnoideae and Pistia (Nauheimer et al. 2012b). The mitochondrial genome of Spirodela has been substantially rearranged, and it shows no syntenty with any other mitochondrial genomes (Wenqin Wang et al. 2012).
Chemistry, Morphology, etc. Raphides in those taxa that have been studied are twinned calcium oxalate crystals, H-shaped in transverse section, and often with lateral barbs (Sakai & Hanson 1974); Lemna, etc., also have such raphides. Raphides develop earlier than druses, at least in Amorphophallus, and may help protect young tissue, as well as aiding in regulating calcium (Prychid et al. 2008).
Xylem and phloem are mixed in the medulla of roots of Monstera, Heteropsis and Philodendron (Huggett & Tomlinson 2010): I do not know the distribution of this distinctive feature. Gonçalves et al. (2004) noted that some taxa with perfect flowers may have collenchyma at the apex or base of the petiole; their comparative data is of collenchyma presence at the middle of the petiole. This may perhaps explain the apparent conflict in the literature. Thus although Keating (2000b) recorded collenchyma for a few members of Lasioideae and Pothoideae, Gonçalves et al. (2004) failed to find it for some of the same taxa.
Ray (1987b) questioned whether all taxa have axillary buds; he considered such buds sometimes to be much displaced from the leaves with which they are normally associated. In addition to Gymnostachys, I have seen one taxon (unnamed, from Thailand) with a leaf blade that had softly dentate/spinulate margins. For leaf development, see Troll (1955) and Kaplan (1973). The former found that the blade of Typhonodorum and Orontium developed from the upper part of the leaf, while the latter thought that the blade of the leaf of Zantedischia developed from the lower part of the leaf, but noted that its leaf, and that of other (unnamed) Araceae he had examined, developed acropetally like the lamina of most broad-leaved angiosperms...
Buzgo (2001) suggests that from the point of view of floral development Orontium is more like core Araceae than is Lysichiton or Symplocarpus. Orontieae have a long internode (not always obvious) between the base of the spike and the subtending leaf or spathe and there may be common A-C primordia (Buzgo 2001). The sterile flowers that are often found between the staminate and carpellate zones of the inflorescences of many Aroideae develop in a variety of ways, but whether this implies that there are correspondingly different evolutionary pathways is unclear (c.f. Barabé et al. 2004a). When flowers are 2-merous, the outer pair of tepals are lateral. Some taxa have binucleate tapetal cells (Wunderlich 1954). For a discussion on the evolution of the distinctive pollen that characterises most Aroideae, see Hesse (2006b). Pseudomonomery has been documented for the family (Eckardt 1937; see Buzgo 2001). See Buzgo (2001) for discussion on the gyneocial construction of [Gymnostachydoideae + Orontioideae]; the gynoecium often has a single loculus.
Variation in ovule morphology is considerable but confusing. Gymnostachys has no micropyle since the integuments do not cover the nucellus, Pistia is exostomal, and other taxa are bistomal. The ovules of Pothos macrophyllus are shown by Buzgo (2001) to be anatropous and apotropous, although Pothos is described in the same paper as having straight ovules (the former is correct). In a number of taxa the ovules are reported to be tenuinucellate while the nucellus of Pistia is "very well developed" and appears to be in radial files (Mercado-Noriel & Mercado 1978), a nucellar cap and integumentary endothelium may be present, and so on. Clarificiation is needed. Thus Parameswaran described Theriophonum minutum as being tenuinucellate, but drew a complete layer of cells below the nucellar epidermis, while Jüssen (1929) noted that Spathiphyllum had a doubled epidermal layer, but that is not evident from the illustrations; in general it is difficult to match statements of nucellus type with the illustrations there. The megaspore that germinates is often micropylar in other than Aroideae and Calloideae, where it is chalazal, although not in e.g. Lysichiton (Grayum 1991).
The uninucleate chalazal endosperm haustorium of Arum maculatum is reported to be 24,576 n (Werker 1997). Maheshwari and Khanna (1957) and Tobe and Kadokawa (2010) describe the endosperm as being cellular, but it can be interpreted as being an extreme form of helobial (see also Acorales). The seeds of Pothoidaeae and Monsteroideae are described as frequently being ana-campylotropous (Seubert 1997). Mercado-Noriel and Mercado (1978) describe the seeds of Pistia as having large amounts of perisperm as well as some endosperm. Variation in seedling morphology is great; in some taxa the roots are green, and in others they are always white (Tillich 1985, 2003b). The "cataphylls" of the seedlings of Orontium are relatively long, linear structures (Tillich 2003b). Chromosome number is especially variable in Cryptocoryne (Aroideae).
Much information is taken from Mayo et al. (1997, 1998); see also Bown (2000); see also Dring et al. (1995: chemistry), Behnke (1995a: sieve tube plastids), French (1998: stem anatomy, extremely variable), Ertl (1932: venation and petiole anatomy, more normal monocot venation may be common in the basal subfamilial pectinations), Keating (2000b: collenchyma, 2003a: general anatomy, b: leaf anatomy, 2004 a: classification, b: raphides), Gonçalves et al. (2004: collenchyma), Carlquist and Schneider (2013: vessels), Maheshwari and Khanna (1956), Swamy and Krishnamurthy (1971), and Tobe and Kadokawa (2008: good summary, 2010: endosperm development), all embryology, Gatin (1921: seedlings, unfortunately Gatin died before he could make more than this "première contribution"), Tillich (1985, 2003b: seedlings), Seubert (1993: starch grains, seeds and seedlings, very variable), Bogner and Petersen (2007: chromosome numbers), and Bliss and Suzuki (2012: genome size in Anthurium, substantial variation, little correlation with anything). For floral morphology, see Barabé and Lacroix (2008a) and Poli et al. (2012), both Anthurium, Barabé and Lacroix (2008b: Anaphyllopsis), Barabé et al. (2012: Syngonium), Fukai (2004: Arisaema) and Barabé (2013: general, but much on Lasioideae), for locular hairs, see French (1987). For pollen, see Grayum (1991, 1992: much variation), Weber et al. (1999), Jayalakshmi (2004: phylogenetic framework inadequate), van der Ham et al. (2005: Amorphophallus and relatives), Hesse (2006a, b: summary, phylogenetic framework reasonable); also Barabé et al. (2004: anther crystals) and French (1986 and references: endothecial thickenings).
For a general bibliography of Lemnoideae, see Landolt (1980), for embryology, Maheshwari (1954), cytology, Urbanska-Worytkiewicz (1980), morphological details, Landolt (1986, 1998), and for chemistry, etc., see Landolt and Kandeler (1987). See Barabé et al. (2011) for floral meristicity of Lasioideae, Hesse (2002) for pollen morphology (the sulcus may be unique among angiosperms, and Seubert (1997) for seed morphology and anatomy. See Buzgo and Endress (1999) for Gymnostachys).
Phylogeny. Mayo et al. (2013) summarize recent phylogeneticn work on the family. Early hypotheses of phylogeny based on restriction site analysis (French et al. 1995) suggested rather pectinate relationships in the family, but a consensus tree of morphological characters (Mayo et al. 1997) showed somewhat less resolution. However, relationships have turned out to be pectinate, although of course that is in part because of what we have decided to call subfamilies. In most analyses the clade [Gymostachydoideae + Orontioideae] is sister to the rest of the family, and Lemnoideae are strongly supported as sister to the remainder, although Isles et al (2013) recovered a topology [Gymostachydoideae [Orontioideae + the rest]], although support was weak and sampling poor. Barabé et al. (2004a: little support) found that Lasioideae were not clearly separated from Aroideae. Although a trnL-trnF phylogeny (Rothwell et al. 2004) placed Callopsis and Asterostigma (both Aroideae) outside a clade with 100% jackknife support that included other Aroideae, Lemnoideae and Pothoideae, Tam et al. (2004: trnL-F sequences, Calla not examined) again suggest the phylogeny is rather pectinate, as do Cabrera et al. (2008: five chloroplast genes). The topology that Cabrera et al. (2008) present, quite well supported, is used here (see also Nauheimer et al. 2012b). There are two areas of continued interest.
1. The exact position of Zamioculcadoideae needs confirmation, but they can reasonably be excluded from Aroideae. There is no strong molecular support for a clade [Zamioculcadoideae + Aroideae] (e.g. Nauheimer et al. 2012b), but that clade does have some morphological features in common (see above). Bogner and Hesse (2005) raised the group [Zamioculcas + Gonatopus] to subfamilial status as Zamioculcadoideae. Stylochaeton has the same pollen as most Aroideae and it has simple leaves (Hesse et al. 2001); it is sister to other Zamioculcadoideae (see also Nauheimer et al. 2012b), so its reasonable inclusion does in the subfamily (see Cabrera et al. 2008) does make it notably less distinctive morphologically. The phylogeny of Cusimano et al. (2011) is largely similar to that of Cabrera et al. (2008); the former recognise a Zamiocalcadoideae s. str. It may be of interest that the pollen of Lasioideae, at least, has a lamellate endexine rather like that of Zamioculcadoideae.
2. Calla palustris, in early (prior to ed. 7) versions of this site placed in a separate subfamily, seems best included in Aroideae for now. Barabé et al. (2004a) found that it was embedded in Aroideae, although without strong support (see also Nauheimer et al. 2012b: well embedded, but nodes involved with poor support). Calla came out in a clade of Aroideae along with other rooted aquatics/marsh plants in molecular analyses (see Cabrera et al. 2008), but its position was unclear in both morphological and restriction site analyses. Calla and Aroideae both have laticifers, but the former has bisulcate pollen with sporopollenin and a tectate-columellate ektexine, perfect flowers, etc. (Ulrich et al. 2013) - and it has a much more northerly distribution (see the Map above), overlapping with that of other Aroideae only in Western Europe and N.E. North America. The ovules have parietal tissue, but so do those of some other Aroideae (Ariopsis, Arum). Its perfect flowers and many features of the pollen would represent reversals, it acropetal flowering is unique (c.f. Cusimano et al. 2011; Ulrich et al. 2013; see Barabé 2013 for floral morphology, other Aroideae have perfect flowers, albeit atypical). Its phylogenetic position needs confirmation before one can understand its morphology.
In Orontioideae, Orontium is sister to the rest of the subfamily (e.g. Nauheimer et al. 2012b). Tam et al. (2004) discuss relationships within Pothoidaeae and Monsteroideae; Carlsen and Croat (2013) begin to disentangle relationships in Anthurium, the classical sections being a poor guide. For the phylogeny of Lemnoideae see Les et al. (2002), Rothwell et al. (2004), and Nauheimer et al. (2012b), relationships being [Spirodela [Lemna + The Rest]]; for speciation there, see Crawford et al. (2006). Urospatha is sister to other Lasioideae (Nauheimer et al. 2102b).
Cabrera et al. (2008) offer a number of suggestions about tribal relationships in Aroideae; Nauheimer et al. (2012b) found little support for relationships between many of the tribes; Callopsis was sister to the rest of the subfamily, but support was weak. For a phylogeny of Philodendron, see Gauthier et al. (2008); Homalomena may be part of the same clade. Yeng et al. (2013) focus on Southeast Asian Homalomena, which form a clade that is quite separate from the New World species of the genus, anf the latter do indeed seem to be closer to (sister to) Homalomena. Cusimano et al. (2010) and Ohi-Toma et al. (2010) discuss relationships within Areae, particularly Typhonium and related genera, while Espíndola et al. (2010) focus on Arum. Gonçalves et al. (2007) discuss the phylogeny of the Andean Spathicarpeae, a clade in which the spathe is adnate to the spadix; many of the species grow in very dry and/or high conditions. For relationships around Schismatoglottidae, see Wong et al. (2010); Alocasia, see Nauheimer et al. (2012a); and for those in Amorphophallus, Sedayu et al. (2010).
Classification. For a tribal classification, see Cabrera et al. (2008) and especially Cusimano et al. (2011), however, a few genera immediately basal to their Aroideae s. str. and Zamioculcadoideae s. str. are unplaced, and a broad circumscription of both subfamilies is adopted here (see also Mayo 2013 et al. for the classification of the family). For a checklist and bibliography, see Govaerts and Frodin (2002) and the World Checklist of Monocots, and for several keys and much more, see CATE-Araceae. There are lots of monotypic genera!
Thanks. I am grateful to Monica Carlsen and Richard Keating for discussions about Araceae and to Simon Mayo for comments.
[Tofieldiaceae [[Alismataceae [Butomaceae + Hydrocharitaceae]] [Aponogetonaceae [Scheuchzeriaceae [Juncaginaceae [Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]]]]]]]: mycorrhizae uncommon [?Tofieldiaceae]; inflorescence a raceme; carpels free, plicate or mostly so; fruit a follicle; endosperm helobial.
Age. This node has been dated to 112-107 m.y. by Wikström et al. (2001) or (134-)118, 103(-89) m.y.byb Bell et al. (2010).
TOFIELDIACEAE Takhtajan Back to Alismatales
Steroidal saponins, chelidonic acid +; vessels?; fibres mixed with phloem; sieve tube plastids also with polygonal crystals; endodermal cells with U-shaped thickenings [distribution around here?]; stomata anomocytic; also prismatic crystals +; leaves equitant and isobifacial [oriented edge on to the stem], two-ranked; inflorescence bracts +, (flower single - Isidrogalvia); floral bracts +, ± foliaceous (0), calyculus below individual flowers (not some Tofieldia); T free (basally connate), with one trace [Tofieldia], median member of outer whorl adaxial [Tofieldia] or not; A (9-12 - Pleea; adnate to base of P; basally connate), introrse to latrorse, (filaments with three traces - some Isidrogalvia); tapetum glandular; microsporogenesis simultaneous; pollen di(trichotomo)sulcate (monosulcate - Isidrogalvia); septal or tepal nectaries +; G stipitate, carpel periphery completely postgenitally fused, (placentation parietal), (style + - Isidrogalvia); ovules 5-many/carpel, ana-campylotropous, (unitegmic), (nucellar cap +), hypostase +, integumentary obturator +; (embryo sac with long chalazal extension), antipodal cells not multinucleate; fruit also a septicidal capsule ["ventricidal" capsule], (P persistent); seeds with terminal appendages, obliquely stacked; phlobaphene +, tegmen thin; ?embryo; n = (14) 15 (16), chromosomes 0.9-2.5 µm long; radicle 0?.
3-5[list]/31: Isidrogalvia (14). S.E. U.S.A., N. South America, N. temperate (map: see Hultèn 1961; Meusel et al. 1965; Hultén & Fries 1986; Fl. N. Am. 26: 2002; Campbell 2010). [Photo - Flowers] [Photo - Flowers.]
Age. Crown-group Tofieldiaceae are dated to ca 100 m.y. (Janssen & Bremer 2004); other age estimates are 80-75 m.y. (Wikström et al. 2001) and (95-)64, 61(-35) m.y. (Bell et al. 2010).
Chemistry, Morphology, etc. The leaves of Tofieldia may lack palisade mesophyll (Kao 1989). Branching in Tofieldiaceae needs study. Remizowa et al. (2005) suggest that the first two leaves of axillary shoots in Tofieldia (the prophyll and the next leaf) are both adaxial; this would be very unusual, if true. Generalised comparisons between the calyculus of Tofieldiaceae, made up of two or three connate scales, with the spathe of Hydrocharitaceae and pseudowhorls of bracts in Alismataceae have been made (Remizowa and Sokoloff 2003; Remizowa et al. 2006b). Remizowa et al. (2010a) found that the calyculus is usually supplied by three vascular traces, but in Tofieldia pusilla it is basal on the pedicel and supplied by a single trace - part bract and part calyculus?
The nectaries of Tofieldiaceae may be unique. They are triradiate, being borne on the inner bases of the connate carpellary stipes (Remizowa et al. 2006a and references), and so appear to be the perfect "intermediate" between the septal nectaries found in many other monocots and the nectary-less condition.
For general information, see Ambrose (1975, 1980), Zomlefer (1997b), Tamura (1998 - as Nartheciaceae), and Campbell (2010), for the single-flowered Harperocallis, described from Florida in 1968 but recently synonymized in Isidrogalvia, c.f. McDaniel (1968) and Remizowa et al. (2011b), for sieve tube plastid type, see Behnke (2000, 2003), for inflorescence and floral morphology, see Remizowa and Sokoloff (2003) and Remizowa et al. (2006a, b, 2010b, 2013b), for ovary morphology, see Sterling (1979), for general embryology, see Cave (1968 and references), and for ovule development, see Holloway and Friedman (2008).
Phylogeny. Pleea is sister to the rest of the family (Tamura et al. 2004b; Azuma & Tobe 2011; Iles et al. 2103). Pleea is the only genus that has two stamems opposite members of the outer tepaline whorl and single stamens opposite members of the inner whorl - as in a few Alismataceae, Butomaceae and Hydrocharitaceae (Azuma & Tobe 2011). There is a fair amount of phylogenetic structure in the rest of the family, but little in the way of morphology to support most of the genera. L.-Y. Chen et al. (2013) found that Isidrogalvia was embedded in Petrosaviaceae, which is rather remarkable, although they did not comment on its position.
Classification. For a checklist of the family, see World Checklist of Monocots.
Previous Relationships. Tofieldiaceae have often been included in other families. Dahgren et al. (1985) placed them, along with representatives of Nartheciaceae and Petrosaviaceae, in Melianthaceae, Tamura (1998) placed them in Petrosaviaceae (along with Nartheciaceae), and Cronquist (1981) considered Tofieldia to be an archaic genus of his broadly-drawn Liliaceae. Tofieldiaceae were included in Melanthiales by Takhtajan (1997). Isidrogalvia was placed in Nartheciaceae by Tamura et al. (2004b; c.f. Azuma & Tobe 2011).
[[Alismataceae [Butomaceae + Hydrocharitaceae]] [Aponogetonaceae [Scheuchzeriaceae [Juncaginaceae [Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]]]]]]: plant rooted aquatic (with floating stems), leaves emergent; stem with lacunae; little oxalate accumulation; raphides and druses 0 (prismatic crystals +); bulliform cells 0 [?this level]; plant glabrous; inflorescence scapose; pollen grains trinucleate; carpel fusion via the central floral axis, partial at the carpel periphery; endosperm 0; seedling collar and collar rhizoids +.
Age. The divergence of the two main clades above is dated at 91-81 m.y.a. by Wikström et al. (2001: note topology), ca 107 m.y.a. (Janssen & Bremer 2004), or a little younger, at (115-)96, 83(-66) m.y. (Bell et al. 2010: note topology).
Evolution. Divergence & Distribution. L.-Y. Chen et al. (2013: disregard ages in Table 1) thought that the most recent common ancestor of this clade inhabited Eurasia.
Ecology & Physiology. All members of this clade grow in more or less marshy and sometimes saline conditions, and are common in all aquatic environments in which angiosperms grow except fast-flowing rivers. J.-M. Chen et al. (2004b) discuss the evolution of various life forms in the group - parallelisms are common.
More particularly, the clade is notable for the number of taxa it contains that can tolerate salt concentrations of 200mM (Flowers er al. 2010), and it includes all fully marine angiosperms. These are generally called sea-grasses, although not all are particularly grass-like, while true grasses like Spartina and Puccinellia, which can dominate in estuaries, are not usually included in this ecological group (for the evolution of salt tolerance in Poaceae, see Bennett et al. 2012). The extreme halophytic habit has evolved more than once, probably two or three times - once in Hydrocharitaceae and again in the [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]] clade, although then there would be reversals in the latter group (Les et al. 1997; Les & Tippery 2013). Tomlinson (1974b) described the vegetative morphology of sea grasses. He noted that in some taxa branching patterns were remarkably precise; roots were initiated within apical meristems, and were themselves unbranched, although a few taxa did have branched roots.
Sea-grasses are very important ecologically. There are only about 55 species all told, of which a few are Hydrocharitaceae and the rest are members of the [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]] clade. Like mangroves, sea grasses are most diverse in the area from the western Pacific to east Africa, less so in the Americas and west Africa (e.g. Tomlinson 1986). It is unclear how many times adaptations to the marine habitat have evolved; at least twice, but individual species of the [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]] clade in particular may tolerate a range of salinities (Barbour 1970), while Maundiaceae and many Juncaginaceae happily grow in salt marshes.
Touchette (2007) discussed the physiological problems faced by marine angiosperms, particularly problems with Na, Cl, and P concentrations, while Invers et al. (1999) examined carbon acquisition via dissolved bicarbonates. For the effect of submerged angiosperms in general on oxygen concentration of the water, see Caraco et al. (2006). Sulphated phenolic compounds are common in sea-grasses (McMillan et al. 1980), and probably arose in parallel; their function is unclear, although they may be involved in adaptation to life in the marine habitat. Wissler et al. (2011) compare gene expression in Posidonia and Zostera with that in grasses and broad-leaved angiosperms; the approach is interesting, but the sampling is too poor to say much about specific adaptations to the marine habitat.
The sea-grass ecosystem is of great ecological importance: In brief, it is very productive, supports a considerable amount of diversity, does not suffer from much herbivory, captures much sediment, and stores much carbon (Orth et al. 2006; Kennedy et al. 2010 for summaries). Sea-grasses occupy ca 22,800,000 ha, and they often grow in monodominant stands made up of clones that may be very extensive indeed (see Cymodoceaceae below). These stands are susceptible to attack by pathogens such as Labyrinthula, a heterokont protist that caused eel-grass wasting disease (Rasmussen 1998), but they are usually little grazed (e.g. Smith 1981; Waycott et al. 2009; Arnaud-Haond et al. 2012). The growth of sea grasses is highly modular, and members show an allometric scaling of their parts, the sizes of leaves, fruits, shoots and rhizomes all being correlated: species with thin rhizomes grow fast and have short-lived leaves; plants with thicker rhizomes grow more slowly, but have longer-lived leaves and more inter-module integration (Tomlinson 1974b; Duarte 1991). For general accounts of sea grasses, see Hemminga and Duarte (2000), Green and Short (2003: inc. distribution maps, etc.), and Larkum et al. (2006); see also Clade Asymmetries.
The gross primary productivity of sea-grass communities is around 1903 gCm2y-1 (like that of mangroves) and global primary productivity is 628 TgCy-1, while their net ecosystem production (1211 gCm2y-1 and globally 400 TgCy-1) is substantially higher than that of mangroves because of a relatively low respiration rate. Sea-grasses are responsible for 1.13% of all marine primary productivity; they bury 27-44 TgCy-1, some 12% of the total C storage in the marine ecosystem - and yet they occupy less than 0.2% of the area of the oceans (Duarte et al. 2005: macroalgae excluded, area occupied 0.3 x 1012 m2 [30,000,000 ha]; Duarte 2011). Indeed, this burial estimate may be only one half the actual amount (Fourqueran et al. 2012). Although the amount of carbon in sea-grass plants themselves is small, that stored in the soil/trapped sediment, which can be up to 11 m thick in the Mediterranean, is larger than that in the soild of most forests and comparable with that in mangroves. Estimates of global carbon storage by sea-grasses range from 4.2-8.4 or 9.8-19.8 Pg C, depending on the assumptions made, which is somewhat over 0.5% the global total (Fourqueran et al. 2012). Indeed, sea grasses trap not only sediment but allochthonous carbon, too, and when thinking about sea-grass communities as carbon sinks, then an estimate of 169-186 g C m-2 yr-1 seems reasonable - net community production of ca 120 g plus 41-66 g of allochthonous C (Kennedy et al. 2010: higher areal estimate below).
Importantly, estimates of areas occupied by sea-grass communities range from 22.8x106 (Waycott et al. 2009) to 30 x 106 (Duarte et al. 2005) to ca 40 x 106 ha, gross primary productivity is 3595 gCm2y-1 and global primary productivity is 1438 TgCy-1, while net ecosystem production is 1585 gCm2y-1 and globally 634 TgCy-1, substantially higher than either mangrove or seagrasses. Estimates of C burial are 60.4-70.0 TgCy-1 (Duarte et al. 2005). Furthermore, a substantial amount of sea-grass carbon moves into other marine ecosystems, including the deep sea (Suchanek et al. 1985). Not surprisingly, estimates vary. Mcleod et al. (2011) suggest a carbon burial rate of (100-)138(-176) g C m-2 y-1 (range 45-190), total carbon burial of 48-112 Tg C y-1), for a sea-grass area of 17.7-60.0x106 ha). Importantly, carbon may be sequestered for 4,000 years or more in the anoxic sea-grass soils (Orem et al. 1999; Serrano et al. 2011, 2013).
Estimates of the ecosystem services provided by sea-grasses are about $20,000/ha y-1. This value is twice or more those for mangroves, saltmarshes, and coral reefs (Orth et al. 2006). However, sea-grass ecosystems are under considerable pressure from humans and occasional pandemic diseases (Orth et al. 2006).
Pollination Biology & Seed Dispersal. The remarkable pollination devices of water-pollinated Alismatales, both marine and freshwater, have been much discussed (e.g. Cox 1988: review; Cox et al. 1991: computer simulation of underwater pollination; Cox & Humphries 1993: Cymodoceaceae; Les et al. 1997: phylogeny and hydrophily; see also Pettit et al. 1980; Les et al. 2006; Remizowa et al. 2012b). These include staminate flowers that detach from the parent plant and rise to the surface, the floating flowers themselves transporting pollen to the stigma; pollen variously aggregated and forming masses especially on the water surface; and underwater pollination (hypohydrophily) where the pollen grains are sometimes very much elongated or aggregated to form elongated strands, so increasing the chances of pollination. The progamic phase, the time between pollination and fertilization, is notably short in most of this clade, as in at least some other aquatic angiosperms (see Williams et al. 2010: I have not tried to optimize this). These adaptations are so striking that the flowers and inflorescences in particular, but also the vegetative bodies, of the plants appear very different both from one another and from Alismatales with more conventional life styles.
Sea grasses in particular can be very widely dispersed, whether as fruits or plant fragments, perhaps for hundreds of kilometres (Kendrick et al. 2012).
Chemistry, Morphology, etc. Thickened (nacreous) walls occur in the sieve tubes of a variety of seagrasses (Kuo 1983). Resting buds are produced sporadically throughout this group. Non-medullated roots are quite common, occurring in e.g. Butomaceae, Alismataceae, Limnocharitaceae (Stant 1964, 1967), Aponogeton, Triglochin, Potamogeton, although roots of e.g. Posidonia are medullated (von Guttenberg 1968). Remizowa et al. (2010b) discuss carpel fusion in the clade; when carpels are adnate to the central floral axis, they are often free laterally (see also Nymphaeaceae) and there is no compitum. There are a number of reports of sex chromosomes, e.g. in Phyllospadix (Harada 1956). At least some mitochondrial genes show an accelerated rate of change in aquatic Alismatales (G. Petersen et al. 2006).
Den Hartog (1970) gave a comprehensive taxonomic account of the marine Alismatales. Much general information is taken from Tomlinson (1982); see Zindler-Frank (1976) for oxalate accumulation and and Wilder (1975) for vegetative branching, inflorescence morphology, etc.; Sokoloff et al. (2013c and references) describe the rather scattered distribution of taxa with air canals in the testa. There have been extensive cytological studies in the group, see e.g. Harada (1956), Uchiyama (1989), Sharma and Chatterjee (1967), and Costa and Forni-Martins (2003).
Phylogeny. For a phylogeny of the whole group as well as detailed studies of most of the families within it, see Les and Tippery (2013: main tree 167 taxa, rbcL).
[Alismataceae [Butomaceae + Hydrocharitaceae]] : apical meristems of vegetative axes bifurcating; axillary squamules +; C-glycosyl flavones +; inflorescence branches determinate; P = K + C, members of both whorls with many traces; (androecium with trunk bundles; stamen pairs opposite K); placentation laminar; (ovules many/carpel); seeds exotestal; chromosomes (0.8-)2-13.6 µm long.
Age. The age of this clade is mid-Cretaceous, some (127+-)103.6(-74) m.y. (L.-Y. Chen et al. 2012a: 95% HPD), or ca 47 m.y.a. (Janssen & Bremer 2004).
Evolution. Divergence & Distribution. L.-Y. Chen et al. (2013) thought that the ancestor of this clade inhabited Eurasia.
Ecology & Physiology. A few plants in this clade are reported to have CAM photosynthesis (Keeley 1998).
Chemistry, Morphology, etc. The prophylls of Limnocharis (Alismataceae) and Vallisneria (Hydrocharitaceae) may not be in the normal adaxial position (Wilder 1975). Islam (1950) sugested that both Alismataceae and Hydrocharitaceae had tenuinucellate ovules.
For floral development, see Posluszny et al. (2000) and Charlton and Ahmed (1973), for tepal vasculature, see Glück (1919), and for cytogenetics, see Feitoza et al. (2009).
ALISMATACEAE Ventenat, nom. cons. Back to Alismatales
Plant with latex; (cormose, stoloniferous); (unicellular or stellate hairs); flavone and phenolic sulphates, tannins + (0); rhizome with endodermis; (vessels 0); stomatal subsidiary cells with parallel divisions; leaves two-ranked to spiral, involute, with pseudopetiole and midrib, apical subepidermal pore +, primary veins merge or not with each other, (inverted vascular bundles); (plant mon- or dioecious); inflorescence branches whorled; C more or less crumpled in bud, thin, evanescent; nectary at base of C, A, or from staminodes or carpel flanks; A 3-many, centrifugal or centripetal, (outer members staminodial), also latrorse, endothecium with base-plate thickenings; pollen pantoporate (0-3 porate - Caldesia), spinose; G 2-many, ± free or connate basally, with residual floral apex, partly ascidiate, placentation also basal-lateral, (infra-stylar extra-gynoecial compitum/pollen tube growth - level?); ovules one-many/carpel, apotropous [when 1], (parietal tissue absent), (nucellar cap ca 2 cells across - e.g. Sagittaria); embryo sac bisporic [chalazal dyad], 6-nucleate [variant of Allium-type], (monosporic, 4-nucleate [Oenothera-type]); fruit also an achene; exotesta with outer wall thickened, (thin-walled, cells with upturned ends [Limnocharis]; with glandular hairs), tegmen ± obliterated or walls ± thickened; basal cell of suspensor enlarged; embryo strongly curved; n = (5-)7-8(-13), chromosomes 2.4-14.4 µm long.
15[list]/88. Pantropical, also temperate (map: see den Hartog 1957; Hultèn 1961; Meusel et al. 1965; Haynes & Holm-Nielsen 1997; Fl. Austral. 39: 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photo - Flower, Echinodorus Flower, Fruit, Sagittaria Flower, Limnocharis vegetative, Hydrocleis flower.]
Age. L.-Y. Chen et al. (2012a: 95% HPD) estimated the age of crown group Alismataceae as Upper Cretaceous, some (109.2-)79.4(-68.6) m.y.a..
Evolution. Divergence & Distribution. Ages for separations within the clade are given by L.-Y. Chen et al. (2012a), and there are also biogeographical reconstructions.
Pollination Biology & Seed Dispersal. In at least some species of Ranalisma and Sagittaria the pollen tubes grows down the style, out through an opening at the base of the ovary, into the floral axis and thence into adjacent carpels (X.-F. Wang et al. 2002, 2006, 2011).
The individual fruitlets of Limnocharis separate from the axis and float; seeds that they contain may be dispersed by this means.
Chemistry, Morphology, etc. For leaf development in Sagittaria, in which the blade develops from the upper part of the leaf, see Bloedel and Hirsch (1979). Both leaf form and flower type (staminate, carpellate) are extremely plastic in taxa like Sagittaria latifolia (Dorken & Barrett 2004).
Although there are often many carpels and stamens, organ initiation is basically whorled. Anther initiation may be centrifugal or centripetal; there are common stamen primordia (Sattler & Singh 1977). Alisma and relatives have granular, not spinose pollen and nuclear not helobial endosperm. The pollen often contains starch. The pores of the pollen grains have very irregular margins. The carpels may initiate first in the antesepalous positions, sometimes on gynoecial bulges; or the carpels may be in many whorls (looking spiral!) and completely covering the axis (Singh & Sattler 1972, 1973, 1977a; Charlton 2004 and references; Rudall 2008). Alternatively, there may be a single whorl of carpels with a large, residual floral axis in the center, as in the old Limnocharitaceae (e.g. Leins & Stadler 1973); there the carpels are connate laterally, there are many ovules per carpel, and placentation is laminar.
General information is taken from Haynes et al. (1998b: as Alismataceae and Limnocharitaceae) and Hooper and Symoens (1982: as Limnocharitaceae); for general morphology, see Charlton and Ahmed (1973), for vegetative anatomy, see Stant (1964), for floral development, see Leins and Stadler (1973), Charlton and Ahmed (1973), Charlton (1991 and references), Wang and Chen (1997) and K.-M. Liu et al. (2002), for embryology, see Dahlgren (1934b) and Johri (1936 and references, both with discussion on number of cells in the embryo sac), for endothecium, see Manning and Goldblatt (1990), and for cytogenetics, see Feitoza et al. (2010).
Phylogeny. Details of the relationships between and within Alismataceae and the old Limnocharitaceae are still rather unclear (Soros & Les 2002; Y. Kato et al. 2003; J.-M. Chen et al. 2004a, b; L.-Y. Chen et al. 2012a; von Mering & Kadereit 2010; Lehtonen 2009 for a summary). Echinodorus is polyphyletic (Soros & Les 2002; see also Lehtonen & Myllys 2008). Morphological analyses yield poorly supported basal pectinations with Butomopsis, Hydrocleys, and Limnocharis successively sister to the remainder of the clade; Alismataceae in the old sense then form a well supported clade (Lehtonen 2009: several characters show continuous variation). In an analysis with comprehensive sampling and using ITS plus three chloroplast genes a well-supported clade [Luronium, Damasonium, Baldellia, Alisma] was sister to the rest of the family, but with only moderate to weak support along the basal part of the backbone, and this clade was not recovered in smaller study using additional chloroplast genes, or was in a different position when mitochondral genes were used (L.-Y. Chen et al. 2012a).
Classification. Alismataceae include the "old" Limnocharitaceae (first recognized by Takhtajan in 1954) here, and they certainly have much in common. If Limnocharitaceae were segregated, Alismataceae would have practically nothing by which they could be recognised.
Synonymy: Damasoniaceae Nakai, Limnocharitaceae Cronquist
[Butomaceae + Hydrocharitaceae]: ovary loculi with secretions.
Age. The divergence of these two families is dated to ca 88 m.y. before present (Janssen & Bremer 2004).
Phylogeny. Butomaceae were embedded in Hydrocharitaceae in a rbcL analysis of Y. Kato et al. (2003), but this position has not been confirmed.
BUTOMACEAE Mirbel, nom. cons. Back to Alismatales
Plant monopodial; flavonols?; stomata variable; leaves ± two-ranked; inflorescence umbellate, with subtending bracts, (floral bracts 0), prophylls 2, lateral; flowers protandrous; T petal-like, but whorls not identical; A 9, some latrorse; pollen monosulcate; nectar from carpel flanks; G 6, fusion postgenital, stigma ± decurrent; chalazal cells ± hypertrophied, surounding nucellar cells radially arranged; air canals in testa, outer walls of exotestal cells thickened and with encrustations, tegmen persists; embryo and color?; cell at end of suspensor enlarged; n = 7, 8, 10, 11, 12, etc., chromosomes 3.7-8.3 µm long.
1[list]/1: Butomus umbellatus. Temperate Eurasia, naturalised in N.E. North America (map: from Hultén & Fries 1986). [Photo - Habit © D. Woodland, Inflorescence © E. Parnis.]
Chemistry, Morphology, etc. Stant (1967) reports crystals "in the form of small rods" in the diaphragm cells surrounding the air spaces in the stem; she also suggests that the leaf of Butomus is equivalent to the petiole of Alismataceae (Limnocharitaceae.
For the position of the prophyll, see Eichller (1875). There appear to be C-A primordia, with a pair of stamens differentiating first, and then a single stamen adaxial to that pair (Singh & Sattler 1974). The basal cell of the endosperm may remain undivided but become hypertrophied, or there may be some free nuclear divisions (Fernando & Cass 1996).
Much information is taken from Cook (1998); see Roper (1952) and in particular Fernando and Cass (1996) for embryology and Charlton and Ahmed (1973) for plant morphology.
HYDROCHARITACEAE Jussieu, nom. cons. Back to Alismatales
Branching?; flavone and phenolic sulphates +; vessels 0; endodermis obscure or thick-walled; stomata ?type; (prophyll lateral); leaf (margins spiny), base sheathing [?type] or not; inflorescence subtended by 2 often connate bracts; androecium with trunk bundles?, (A introrse); pollen inaperturate, exine thin to none, (spinulate), trinucleate; nectaries 3, staminodial (0); G inferior, carpel closure by secretion only, laterally ± free, placentae [= carpel walls] much intruded, style single, short, stigmas usu. branched, papillate adaxially; ovules 1-many/carpel, outer integument often ³3 cells across, micropyle bitegmic, parietal tissue 1-2(-more?) layers across, nucellar cap 2-3 cells across (absent); fruit often ± fleshy, dehiscence irregular; stone cells in mesotesta and endotesta, all testal cells ± thickened except the outermost wall, or exotestal, endotegmen with tuberculate inner wall alone persisting; chalazal endosperm haustorium, unicellular suspensor haustorium; n = notably variable, chromosomes (0.8-)2-10 µm long; cotyledon bifacial; extensive loss of mitochondrial genes.
18[list]/116 - four groups below. World-wide (map: blue, marine Hydrocharitaceae; red, freshwater members - see Hultèn 1961; Hultén & Fries 1986; Fl. N. Am. 22: 2000; FloraBase 2005; Fl. Austral. 39: 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012: van Steenis & van Balgooy 1966; den Hartog 1970 for marine taxa).
Age. Crown group Hydrocharitaceae are dated to ca 75 m.y. (Janssen & Bremer 2004), while L.-Y. Chen et al. (2012b) suggest a rather younger crown-group age of (72.6-)65.5(-54.7) m.y..
1. Hydrocharitoideae Eaton
Foliar vascular bundles inverted; leaf vernation involute or convolute, pseudopetiole +, blade broad, ligules +, basal, adaxial or paired lateral [totally enclosing young leaves]; plants monoecious; staminate flowers: A 1-6; pollen tectate-columellate, with (minute) spines; carpellate flowers: (C 0); G [3-9], (carpels basally ascidiate - Limnobium); ovules straight, (micropyle bistomal); exotestal cells much enlarged; n = 7-11, 13-15.
2/5. Temperate and subtropical.
[Stratiotoideae [Anacharidoideae + Hydrilloideae]]: roots unbranched; leaf blade ± linear; plant dioecious; ; (ovules straight).
2. Stratiotoideae Luersson
Plant floating; leaves tristichous, in rosettes, margins strongly spiny; staminate flowers: A many, adaxial 5-17 fertile, others staminodial; pollen baculate, tectum incomplete; carpellate flowers: staminodes +; G 6, in 2 whorls, outer opposite K, (carpels basally ascidiate); n = 10+.
1/1: Stratiotes aloides. Eurasian.
Synonymy: Stratiotaceae Schultz Sch.
[Anacharidoideae + Hydrilloideae]: plant monopodial; submerged; inflorescences axillary, emersed or not; placentae usu. not much intruded; ovules usu. few/carpel; (fruit indehiscent).
3. Anacharidoideae Thomé
Root trichoblasts 0 [Blyxa]; leaves whorled to spiral, (usually opposite when scales), (blade broad - some Ottelia); (flowers perfect [Apalanthe, Ottelia); staminate flowers: released, usually as buds; P 3 + 3 (3); A 3 (+ 3 staminodes) or 6, (dorsifixed; pollen with discontinuous exine, little or no sculpturing); carpellate flowers: hypanthium +, usu. long; P 3 + 3; staminodes +; G [3(-20+)]; (carpel walls much intruded); (ovules many/carpel), (micropyle bistomal, outer integument to 4 cells across, parietal tissue 1-4 cells across; nucellar cap 2-3 cells across; antipodal cells persist; fruit a capsule, indehiscent or irregularly dehiscent; seeds usually <30; n = ?6, 8, 9, 11, 12, 14, etc.
7/38. Tropical to temperate, esp. America.[Photo - Habit © D. Woodland, Blyxa Habit, Flower © M. Clayton.] and Egeria.
Synonymy: Blyxaceae Nakai, Elodeaceae Dumortier, Otteliaceae Chatin, nom. illeg.
4. Hydrilloideae Luersson
(Marine); root trichoblasts 0 [Vallisneria]; leaves (spiro)two-ranked or whorled, (blade broad, pseudopetiole + - Halophila), colleters + [Enhalus]; (plant monoecious - often Naias); perianth biseriate and undifferentiated, uniseriate, (0); staminate flowers: (released as buds); A 1-3, (1 staminode); (pollen inaperturate), (exine 0); carpellate flowers: hypanthium +; staminodes (2-)3; G [2-9], (carpel walls much intruded), (stigmas commissural), (filiform, smooth); (micropyle bistomal), (obturator +); fruit fleshy, capsular, or dehiscing irregularly; (air canals in testa), (exotegmic tuberculae +); n = 6-8, 10, 12, 15.
8/61: Naias (40), Vallisneria (12). Tropical and subtropical, especially Old World; Naias subcosmopolitan. [Photo - Hydrilla, © H. Wilson, Halophila, Enhalus, flower, © from D. Les website], Thalassia, fruit, © from D. Les website.]
Synonymy: Enhalaceae Nakai, Halophilaceae J. Agardh, Hydrillaceae Prantl, Najadaceae Jussieu, nom. cons., Thalassiaceae Nakai, Vallisneriaceae Dumortier
Evolution. Divergence & Distribution. L.-Y. Chen et al. (2012b: see more dates, also ancestral areas) suggest an Asian origin for the family. Thus both Hydrilloideae, the sea-grass clade, and the sea-grass genera themselves may have originated in the India-China-Celebes area; the crown-goup age of the sea-grass clade is only (41.3-)19.4(-15.9) m.y. However, Y. Kato et al. (2003) had suggested an age for this last node of (130-)119(-108) m.y., strongly disagreeing with these other dates, while He et al. (1991) proposed a Cretaceous age and Gondwana origin for Ottelia.
Ecology & Physiology. Hydrocharitaceae such as Hydrilla and Egeria have C4 photosynthesis with the metabolic compartmentalisation needed occurring within single cells (Bowes et al. 2002 for references).
Vegetative Variation. Marine taxa are rhizomatous, with leaf-bearing short shoots (see Tomlinson 1974b for a summary). Taxa like Elodea have leaves borne all along the stem, while others have whorled leaves; Stratiotes aloides forms floating rosettes in the summer, and the plant sinks to the bottom of the water in winter, rising to the surface in the summer. Leaf shape and margin also vary a great deal.
Pollination Biology & Seed Dispersal. Pollination mechanisms in Hydrocharitaceae include entomophily, anemophily, epi- and hypohydrophily, and selfing. Parallelism is pervasive, and sex expression of the flowers/plants is very labile, whatever the tree (e.g. see L.-Y. Chen et al. 2012b). Hypohydrophily has evolved at least twice (e.g. Naias, marine genera), and staminate flowers that detach from the plant and rise to the surface of the water perhaps five times (Les et al. 2006 and references). In a number of species the hypanthium elongates greatly, and the carpellate flower opens onto the surface of the water. Pollination in those taxa where the staminate flowers are released may be epi- or hypohydrophilous. Small detached staminate flowers borne above the surface of the water on reflexed sepals can be caught by the carpellate flowers; these flowers may have two stamens (Nechamandra), three stamens and three erect staminodes that act as little sails (Lagarosiphon), or six stamens (Appertiella). Hydrilla is wind pollinated, the pollen being released explosively by the anthers as they reach the surface in little gas bubbles produced by the submerged staminate flower, while in Elodea the pollen, similarly produced from submerged flowers, floats. In other taxa the hypanthium does not elongate, the carpellate flowers having long pedicels, again, detached staminate flowers are caught by the carpellate flowers. Examples are Maidenia (= Vallisneria) and the marine Enhalus; in the former, there are at most 24 pollen grains per staminate flower. In the marine Halophila the pollen is released in chains, and pollination is underwater. The insect-pollinated Blyxa has secondary pollen presentation. For more details, see e.g. Ernst-Schwarzenbach (1945), Cook (1982, 1996, especially 1994-1995), and Tanaka et al. (2013: details of pollen and stigma morphology).
Chemistry, Morphology, etc. The plants may be tanniniferous. Hydrocharis, apparently alone in the group, has a root epidermis that is of inner epidermal origin.
Growth and branching in Hydrocharitaceae needs more study. In species like Enhalus and Stratiotesthe first leaves produced after the cotyledon are at right angles to it, whereas in most others these leaves are borne in the same plane as the cotyledon (Haccius 1952a). Axillary buds along the stems are commonly precocious (Wilder 1975), and pseudodichotomous branching, often interpreted as being the result of this precocious axillary branching, is also quite common (Tomlinson 1974b, 1982). Posluszny and Charlton (1999) described the extremely complex branching in Hydrocharis morsus-rana, suggesting that it has components of flower/inflorescence morphology. They thought that the sheathing bracts, separated by a short internode, might be comparable to the first two leaves on a branch. Tanaka et al. (1997) noted that flowers and axillary branches frequently arise from the same axil, and there is also variation in bracteole number and position (lateral, paired, etc.: Eichler 1875).
The anthers sometimes lack an endothecium (Ernst-Schwarzenbach 1945). Elodea is shown as having its carpels opposite the inner perianth whorl (Eichler 1875). The staminodes of Vallisneria are opposite the petals/inner P and V. spiralis, at least, has commissural stigmas (Les et al. 2008). The carpels are best interpreted as being more or less free from each other laterally but adnate to the receptacular wall abaxially (Weberling 1989 for references, esp. Kaul 1968). The ovary in at least some taxa is filled with mucilage, but it is unclear if there are intra-ovarian trichomes (Rudall et al. 1998c, c.f. Oriani & Scatena 2012). Blyxa has notably short chromosomes (Uchiyama 1989). The mitochondrial nad1 intron 2 is absent in two representatives of this family (Gugerli et al. 2001); the extent of this loss is unclear.
General information is also taken from Cook (1998), Haynes et al. (1998a), and Haynes and Holm-Nielsen (2001); for ovules, etc. see Kausik (1940a), Islam (1950) and Govindappa and Naidu (1956), for testa anatomy, see Shaffer-Fehre (1991a, b), and for pollination mechanisms, see Cook (1982, and especially 1994-1995), these correlate with pollen morphology and phylogeny, see Tanaka et al. (2004).
Phylogeny. Tanaka et al. (1997: two genes) found a series of quite well-supported nodes; the ultimate groupings recognised there are similar to those of Les et al. (1997). Les et al. (2006) in a four-gene analysis of all genera bar one, and including morphological characters, again found largely similar relationships: Hydrocharitoideae were sister to the rest of the family (support not given because only a single outgroup was used), and then Stratiotoideae, but with only moderate support (72% bootstrap, all characters), and then the clade [Anacharidoideae + Hydrilloideae] (52%); however, the monophyly of all four subfamilies was strongly supported.
Analysis of an eight-gene supermatrix by L.-Y. Chen et al. (2012b) yielded an appreciably different tree. Basic relationships are [Stratiotoideae [Anacharidoideae [Hydrocharitoideae + Hydrilloideae]]]. The position of Stratiotoideae was largely driven by mitochondrial data, otherwise support for the backbone of the tree was strong, but that for the particular position of Hydrilla poor (L.-Y. Chen et al. 2012b). Les and Tippery (2013) noted the variety of topologies that had been found for the four subfamilies; they themselves found the relationships [Hydrocharitoideae [Anacharidoideae [Stratitoideae + Hydrilloideae]]], althought support was weak, as it was for the monophylyy of Anacharidoideae and Hydrilloideae.
Within Hydrilloideae, Naias was strongly supported (98%) as sister to Hydrilla in the combined analysis, although not in all individual molecular analyses, yet the two are notably distant in the tree in the morphological analysis (Les et al. 2006). Within Hydrilloideae, there is a "marine" clade: [Enhalus [Halophila + Thalassia]]. Despite the obvious morphological differences between Naias and other Hydrocharitaceae, Posluszny and Charlton (1999 and references) noted that both branching and seed anatomy link them, however, Liu and Li (2010) found Naias to be sister to the other Hydrocharitaceae that they examined, while L.-Y. Chen et al. (2012b) found the relationships [sea-grasses [Naias [Hydrilla + the rest]]].
For a phylogeny of Vallisneria, see Les et al. (2008).
Classification. There are eleven family names available for the eighteen genera in Hydrocharitaceae, reflecting the variety of pollination mechanisms and vegetative adaptations to the aquatic life style. I follow the subfamilial classification suggested by Les et al. (2006).
[Aponogetonaceae [Scheuchzeriaceae [Juncaginaceae [Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]]]]]: primary root poorly developed; calcium oxalate crystals of any sort absent; bracts 0; P members with a single trace; pollen reticulate; parietal tissue ³2 cells across; suspensor unicellular, cell large; chromosomes (0.5-2.3(-4.5) µm long.
Age.The first branch in this clade (Aponogetonaceae versus the rest!) is dated to ca 98 m.y. (Janssen & Bremer 2004).
Evolution. Divergence & Distribution. L.-Y. Chen et al. (2013) thought that this clade began to diverge in Eurasia.
Chemistry, Morphology, etc. A number of taxa in this clade have a radicle that is lateral and exogenous in origin (Yamashita 1970, 1972, 1976).
For a summary of much information about the families here, see Sokoloff et al. (2013c); see Markgraf (1936) for general floral studies in the "simplest Helobiae".
Phylogeny. Aponogetonaceae and Scheuchzeriaceae are sister taxa and in turn are sister to the other members of the group in a rbcL analysis of Y. Kato et al. (2003) and also in Liu and Li (2010). The positions of Aponogetonaceae and Scheuchzeriaceae are sometimes reversed, as in Janssen and Bremer (2004, see also L.-Y. Chen et al. 2013). Relationships between these two families were unclear in von Mering and Kadereit (2010), while Nauheimer et al. (2012b), Iles et al. (2013) and Les and Tippery (2013) recovered the relationships followed here.
Classification. There is a plethora of small families in this clade, again because of the very distinctive floral and vegetative morphologies that have evolved in connection with the aquatic habitat its members favour. Maundiaceae are recognised below, further increasing the number, but rationalization may well be in order (see A.P.G. III 2009); Hydrocharitaceae as circumscribed above would be a model to follow.
APONOGETONACEAE Planchon, nom. cons. Back to Alismatales
Plant with a short rhizome or corm, apical meristems of vegetative axes bifurcating [?all]; vessels 0; laticifers +, articulated; ?stomata; leaves spiral, vernation involute, with pseudopetiole, blade and midrib, primary veins merge with each other, tertiary veins few, apex of old leaves with pore; plants usu. monoecious or dioecious; flowers sessile [inflorescence spicate); (flowers monosymmetric); P (1-4); staminate flowers: (A 16³), (stamen pairs +), (anthers introrse); microsporogenesis also simultaneous; pollen monosulcate, reticulum uniform, muri broad, (micro)echinate; pistillode ?; carpellate flowers: (P 0); staminodes +; G 2-9, free, alt. P, septal nectaries + (0), placentation basal; ovules 1-12/carpel, (unitegmic - integument 5-6 cells across), nucellar cap ca 2 cells across; T etc. persistent in fruit or not; seed coat mucilaginous, air canals in testa, exotesta protective or not, endotegmen tanniniferous, or undifferentiated and translucent; embryo green or not, radicle sublateral, exogenous (0); n = ?12, 16, 19, etc., chromosomes 0.7-2.3 µm long; cotyledon bifacial.
1[list]/50. Old World, esp. South Africa, largely tropical and warm temperate, suspected of being introduced in parts of Southeast Asia-Malesia - localities not on map) (map: from van Bruggen 1985, 1990). [Photo - Aponogeton Flower © H. Wilson, Habit © R. Kowal.]
Evolution. Divergence & Distribution. The distinctive pollen of Aponogeton has recently been reported from western Greenland and North America in deposits as old as 82-81 m.y. (Grímsson et al. 2013), hence the origin and diversification of the clade is difficult to ascertain.
Pollination Biology. Madagascan and Indian species of Aponogeton can be hybridized (Yadav 1995; see also Grímsson et al. 2013).
Chemistry, Morphology, etc. For cell death and the development of the fenestrate leaves of Aponogeton madagascariensis, see Wright et al. (2009).
It has been suggested that a bract may form an hybrid organ with a tepal, so making the flower slightly monosymmetric; separate bracts were not seen (Buzgo 2001). More pronounced monosymmetry occurs in flowers in which only two perianth members develop; these appear to be the abaxial pair, and in a monocot flower with "normal" orientation these would be members of the inner perianth whorl, and the median member of the outer whorl of stamens is abaxial (see Singh & Sattler 1976b); a parallelism with Maundia (Sokoloff et al. 2013c).
Some information is taken from van Bruggen (1990, 1998); for leaf development, see Gunawardena et al. (2004), for embryology, see Sâné (1939), embryo development, see Yamashita (1976), and for floral morphology, see Remizowa et al. (2010b).
Phylogeny. For the phylogeny of the genus, see Les et al. (2005) and Les and Tippery (2013). The Australian Aponogeton hexatepalus, with six tepals (surprise!) and quite distinctive pollen, is sister to the rest of the genus.
[Scheuchzeriaceae [Juncaginaceae [Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]]]: sulphated phenolic acids [flavonoids] +, leucanthocyanins, flavones 0; leaf ± linear, ligulate, base with auricles; filaments shorter than the anthers, anthers ± sessile; pollen inaperturate; carpels with complete postgenital fusion [sampling!], nectary 0.
Chemistry, Morphology, etc. For the distribution of sulphated compounds, see especially McMillan et al. (1980).
There has been much discussion about the nature of the perianth - or whether there is a perianth, or if it is an "abaxial outgrowth" of the stamens - in the flowers of many members of this clade. It seems to me that flowers in which the perianth member seems to come from the back of a stamen probably represent an extreme form of the perianth-stamen association that is common in monocots.
SCHEUCHZERIACEAE F. Rudolphi, nom. cons. Back to Alismatales
Plant irregularly sympodial; cyanogenic glucoside triglochinin +, flavonoids 0; stem endodermis +; stomata tetracytic; leaves two-ranked, with apical pore, intravaginal squamules as hairs; inflorescence bracts +, ± foliaceous; pollen in dyads, grains three-nucleate, inaperturate; G 3(-6), opposite outer T, basally connate, fusion usually congenital, placentation parietal; ovules (1) 2/carpel, subbasal, outer integument ca 4 cells across, inner integument ca 2 cells across, parietal tissue 4-5 cells across, (nucellar cap 2 cells across); T persistent in fruit; testa smooth, mesotesta many layered, cells with thick walls; embryo green; n = 11, chromosomes 0.8-2 µm long; cotyledon not photosynthetic.
1[list]/1: Scheuchzeria palustris. N. Temperate to Arctic (map: see Hultén 1961; Fl. N. Am. 22: 2000). [Photo - Habit.]
Chemistry, Morphology, etc. Although Scheuchzeriaceae are chemically like Juncaginaceae, they are not otherwise particularly similar. Some information is taken from Haynes et al. (1998b); see Stenar (1935) for embryology.
[Juncaginaceae [Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]]]: flowers rather small, closely aggregated, inconspicuous; P-A pair with single vascular trace, [P often adnate to A]; G free; carpels the dispersal unit; endosperm nuclear.
Evolution. Divergence & Distribution. The character "ovule one/carpel" is placed at this node by Remizowa et al. (2012b), q.v. for the evolution of a number of characters in this part of the tree. For the evolution of syncarpy around here, see Sokoloff et al. (2013d).
Chemistry, Morphology, etc. The nature of the small, tepal-like structures closely associated with the stamens found in many members of this clade has occasioned much discussion. Sattler (1962) and Singh (1965) considered the perianth and androecium of Potamogetonaceae to be distinguishable although there was but a single trace to each P/A pair. This tepal-like structure is called a retinaculum by some, and then considered to be some kind of enation, not tepalline; indeed, von Mering and Kadereit (2010) suggest that the clade [Maundiaceae + the rest] may be characterized by a flower that lacks a perianth (several taxa there entirely lack a perianth of any sort). Rudall (2003b, see also references) suggested that the flowers of all or many of the taxa in this group were some kind of pseudanthia. Here these structures are considered to be tepals, being extreme examples of the close association between a tepal and its opposing stamen that is common in monocots.
Phylogeny. Iles et al. (2009, 2013) and von Mering and Kadereit (2010) suggested that Juncaginaceae are paraphyletic; indeed, the separation of Maundia from the rest of the family in fact clarifies gynoecial variation within Juncaginaceae s.l.. However, von Mering and Kadereit (2010) were not sure of the exact position of Maundiaceae, and they also found weak support for a clade [Araceae + Tofieldiaceae].
JUNCAGINACEAE Richard, nom. cons. Back to Alismatales
Apical meristems of vegetative axes bifurcating [?all]; O- and C-glycosyl flavones, cyanogenic glucoside triglochinin +; stem endodermis + or 0; (laticifers - Lilaea); stomata also tetracytic, subsidiary cells with parallel divisons; leaves spiral, ± unifacial (2-ranked, isobifacial, equitant), (ligules - Triglochin); (plant dioecious - Tetroncium), (flowers polygamous); (flowers sessile), bracts 0 (+); flowers 1-4-merous, (monosymmetric), "P" 0-4, 6; A 3-8; G 1 [3-10], weakly connate, fertile carpels opposite inner P, (alternating with an outer whorl of sterile carpels), (placentation parietal - Tetroncium), (styluli long - some Lilaea [= Triglochin]), stigma penicillate; ovules 1-few/carpel, basal, outer integument ³3 cells across, parietal tissue 4-6 cells across; fruit schizocarpic or achenial, (hooked, winged), T persistent or not; exotesta and entegmen with cuticle, otherwise crushed; (endosperm +), embryo ?colour, with short thick hypocotyl, primary root lateral, exogenous; n = 6, 8, 15, etc., chromosomes 0.6-1.1 µm long.
3[list]/15. Cosmopolitan, but largely coastal (map: see Hultèn 1961; Meusel et al. 1965; Hultén & Fries 1986; Fl. N. Am. 22: 2000; FloraBase 2004; Köcke et al. 2010). [Photo - Habit, Fruit.]
Evolution. Divergence & Distribution. Stem-group Juncaginaceae are dated to ca 82 m.y., the crown group to ca 52 m.y. (Janssen & Bremer 2004).
Chemistry, Morphology, etc. Imperfect flowers may lack a perianth (female flowers of Lilaea) and have a single stamen and carpel; to a certain extent the number of parts in the flower is connected with flower size (Buzgo et al. 2006). The abaxial median tepal is somewhat bract-like (Buzgo 2001; Buzgo et al. 2006; Remizowa et al. 2010b). Stamens of the outer tepal-stamen unit may be outside tepals of the inner tepal-stamen unit (Dahlgren et al. 1985; Endress 1995b). There is no evidence of pseudanthia; terminal flowers are close to being peloric (Buzgo et al. 2006). Seedlings of Triglochin have two-ranked leaves.
Some information is taken from Arber (1925: general), Agrawal (1952: embryology), Haynes et al. (1998b: general), and von Mering (2013: Tetroncium); for alternative interpretations of the gynoecium, see Igersheim et al. (2001).
Phylogeny. Tetroncium is sister to the rest of the family (good support), and Lilaea is embedded in Triglochin (von Mering & Kadereit 2008).
Classifictaion. For a classification of the family, see von Mering and Kadereit (2008).
Synonymy: Heterostylaceae Hutchinson, Lilaeaceae Dumortier, Triglochinaceae Berchtold & J. Presl
[Maundiaceae [[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]]: vessels 0; carpels ascidiate [sampling!], ovule 1/carpel, apical, pendulous, straight.
Phylogeny. For discussion of the position of Maundiaceae, see Les and Tippery (2013).
MAUNDIACEAE Nakai Back to Alismatales
Outer vascular bundles of scape inverted; stomata ?anomocytic; leaves triangular, ligule 0; flowers sessile [inflorescence spicate]; flowers monosymmetric by reduction; bracts/bracteoles 0; P 2, tranverse-abaxial, (-4 [terminal flowers]), clawed, (with three traces); A (4-)6, with separated thecae; G [(3-)4], laterally ± free, cruciform, styluli marginal, recurved; outer integument 3-4 cell layers across, with air canals, inner integument ca 2 cells across, parietal tissue 4(?+) cells across, nucellar coenocyte + [cell walls of tissue immediately distal to vascular bundle break down]; fruit not a schizocarp, T persistent; testa obliterated; n = ?
1/1: Maundia triglochinoides. East Australia (map: from Australia's Virtual Herbarium, viii.2009).
Chemistry, Morphology, etc. There may seem to be twice as many stamens as tepals, but this is because the anther thecae are separated. See von Mering and Kadereit (2010) for the interpretation of the androecium; as they note, similar stamens are found in Posidoniaceae and Zosteraceae. Sokoloff et al. (2013c) described the morphology of Maundia in detail, noting i.a. variation in floral diagrams.
[[Posidoniaceae [Ruppiaceae + Cymodoceaceae]] [Zosteraceae + Potamogetonaceae]]: submerged marine aquatics; rhizome with endodermis; epidermis chlorophyllous, stomata 0; hydrophily + [water pollination]; flowers imperfect; fruit ± drupaceous; embryo with massive elongated hypocotyl, also prominent in seedling, base of hypocotyl [collar] much enlarged.
Age. Janssen and Bremer (2004: c.f. topology) suggest that the first split within this clade can be dated to ca 73 m.y., and they also give other divergence dates within it; see also Coyer et al. (2013: again, c.f. topology).
Evolution. Divergence & Distribution. Les et al. (1997) observed that halophily might have evolved once and at this node, and was subsequently lost, or twice, depending on how optimisation was carried out; Australia figures prominently in scenarios for the evolution of halophily (e.g. Les et al. 1997; L.-Y. Chen et al. 2013). Similarly, whether vessels and stomata are lost in parallel several times, and/or are lost and then regained, is unclear; the stomata of Potamogetonaceae have a rather odd development, perhaps suggesting that there they have been reacquired.
Pollination Biology & Seed Dispersal. Underwater pollination, hypohydrophily, is particularly common here and pollination mechanisms throughout the group have been much studied (e.g. Pettit et al. 1980; Cox 1988; Cox et al. 1991; Remizowa et al. 2012b).
Ecology & Physiology. For the ecology of seagrasses, see the discussion above.
Chemistry, Morphology, etc. There are many questions about plant growth, for which, see Tomlinson (1974b). Inflorescence and flower morphology in this clade can also be difficult to interpret. For some details of morphology, anatomy, etc., although not of the non-marine members, see Larkum et al. (2006); stomata are absent even on the carpels (Sokoloff et al. 2013c).
Phylogeny. This clade is only poorly supported in molecular studies (Les et al. 1997), but the relationships above were again found by Les and Tippery (2013). Cymodoceaceae was found to be sister to the other families of this group by Nauheimer et al. (2012b). L.-Y. Chen et al. 2013) did not recover a [Posidoniaceae [Ruppiaceae + Cymodoceaceae] clade, rather, Cymodoceaceae were either very paraphyletic or polyphyletic, depending on one's interpretation of the tree, and they are paraphyletic in Isles et al. (2013). Janssen and Bremer (2004) found a clade [Ruppiaceae [Zosteraceae + Potamogetonaceae]
For phylogenies of several of the genera included here, see Waycott et al. (2006) and Les and Tippery (2013).
[Posidoniaceae [Ruppiaceae + Cymodoceaceae]: leaves two-ranked; P 0; anthers with apical development of the connective; pollen filiform.
Age. For a possible date for this node of ca 27 m.y., see Coyer et al. (2013: c.f. topology).
Phylogeny. Ruppiaceae are sister to [Posidioniaceae + Cymodoceaceae] in a rbcL analysis of Y. Kato et al. (2003). Relationships are generally unclear in the studies of Liu and Li (2010) and Les and Tippery (2013).
POSIDONIACEAE Vines, nom. cons. Back to Alismatales
Stem monopodial; unlignified fibre strands from leaf sheaths copious, persistent; inflorescence branched, branches with bracts, flowers sessile [ultimate units spicate]; flowers usu. perfect, bracteate, bracts unvascularized; A 3, thecae more or less separate, deciduous, connective broad, shield-like; pollen smooth, exine 0; G 1, stylulus 0, stigma complex; ovule sessile, campylotropous, with an outgrowth of fused integuments opposite the micropyle, outer integument ca 6 cells across, inner integument ca 4 cells across, parietal tissue ca 10+ cells across; fruit a fleshy follicle, surrounded by persistent connective; first cleavage of zygote vertical; n = 10, dimorphic; seedling with primary root, root hairs few, or root 0.
1[list]/9. Mediterranean, temperate Australia (map: see den Hartog 1970).
Evolution. Ecology & Physiology. Clones of Posidonia oceanica in the Mediterranean may be up to 15 km across and thousands to tens of thousands of years old (estimates were up to 200,000 years, but that conflicts with the recent sea level changes in the Mediterranean); dissemination by fragments of plants was taken in to consideration (Arnaud-Haon et al. 2012).
Chemistry, Morphology, etc. The morphology of the ovules is distinctive and basically uncategorizable (see also Remizowa et al. 2012b). Ma et al. (2012) described embryo sac development; it is monosporic and 4-nucleate; two of the nuclei fuse and form a diploid polar nucleus. This should be confirmed, as should the plane of division of the zygote, which was described as being vertical but looks almost oblique (Ma et al. 2012).
Information is taken from Kuo and McComb (1998: general) and Remizowa et al. (2012b: floral morophology); for germination, see Kuo and Kirkman (1997).
[Ruppiaceae + Cymodoceaceae]: leaves serrulate; flowers monosymmetric by reduction; A 2.
RUPPIACEAE Horaninow, nom. cons. Back to Alismatales
Plant often in brackish or fresh water; roots unbranched; sulphates?; endodermis?; leaves 1-veined, sheath not ligulate, ± auriculate [= "stipule"]; inflorescence spicate; flowers perfect; pollen elongate-arcuate, triaperturate; G (2-)4(-16), stipitate, stylulus 0, stigma ± peltate; ovules also lateral, micropyle bistomal, parietal tissue ca 7 cells across; fruit an operculate drupelet; testa 2-layered, exotegmen cells large with branched protuberances from the walls, all becoming crushed; endosperm helobial, primary root lateral, exogenous; n = 8-12, 15, dimorphic, chromosomes 0.7-4.4 µm long.
1/1-10. More or less world-wide, apparently quite frequently gowing well away from the sea in all continents (map: see Hultén 1961; Fl. N. Am. 22: 2000; Heywood 1978 [for some of the southern hemisphere]; Ito et al. 2010; Fl. Austral. vol. 39: 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012).
Phylogeny. Both hybridisation and long distance dispersal are likely in Ruppiaceae (Ito et al. 2010).
Evolution. Seed Dispersal. The fruits are eaten by water birds.
Chemistry, Morphology, etc. Although Haynes (1978; see also Haynes et al. 1998a) described the ovules as being campylotropous, they are shown as being straight by Gamerro (1968) and Posluszny and Sattler (1974). I follow the latter for the interpretation of stamen morphology; they mention that parietal tissue is about 1 cell across - but c.f. Haynes et al. (1998a). Ovule morphology needs to be cleared up.
Phylogeny. Ito et al. (2010) look at the biosystematics of this difficult group in which cytological variation is considerable.
Classification. Ruppiaceae are only doubtfully distinct from Cymodoceaceae (Les et al. 1997).
CYMODOCEACEAE Vines, nom. cons. Back to Alismatales
(Plant monopodial); (roots branched); distinctive cyclitols; rhizome with central stele; (sieve tubes with thick nacreous walls - Halodule); leaves two ranked, (blade terete - Syringodium), (apex serrulate); plant monoecious or dioecious; flowers in cymose groups enclosed by bracts, or solitary; staminate flowers: A connate, (apical appendages 0 - Syringodium); (microsporogenesis simultaneous - Thalassodendron); (pollen smooth), (exine 0); carpellate flowers: G 2, stylulus +, (stigmatic branches 2, 3, long; fruit achene or drupelet, 1 (2) seeded; testa 0; n = 7, 8, 10, 12, 14-16, chromosomes <7µm long; (seed viviparous - Amphibolis), seedling with tuft of root hairs.
5[list]/16. More or less tropical (to warm temperate), Australia in particular (map: see den Hartog 1970; van Baloogy 1975; Australia's Virtual Herbarium xii.2013). [Photo - Habit]
Chemistry, Morphology, etc. This family needs work. For Remizowa et al. (2011) the flowers of Cymodoceaceae represented racemose partial inflorescences. Tomlinson (1982) described Thalassodendron as having a basal, anatropous ovule, but Takhtajan (1985) and Tomlinson and Posluszny (1978) described the ovules of Syringodium as being apical and straight. Pollen of Amphibolis is up to 5 mm long. Cymodocea is viviparous, and the cotyledon is at most small (e.g. Arber 1925: C. antarctica).
Additional information is taken from Kuo and McComb (1998: general) and McConchie et al. (1982: floral morphology); for cyclitols, see Drew (1983) and for chromosomes, see Kuo (2013: ?Thalassodendron).
[Zosteraceae + Potamogetonaceae]: roots unbranched; leaf with apical pore, (sheath closed); plant mono- or dioecious.
Age. Estimates of the time these two clades diverged range from ca 100 m.y. (Y. Kato et al. 2003) to ca 47 m.y. (Janssen & Bremer 2004).
ZOSTERACEAE Dumortier, nom. cons. Back to Alismatales
Main stems monopodial; also flavone sulphates +; rhizome cortex with unlignified fibrous strands (not Phyllospadix) and vascular bundles; sieve tubes with thick nacreous walls; leaves two-ranked, ligule +, (sheath closed); plant ± dioecious; inflorescence with spathe and spadix, spadix axis flattened, flowers in two ranks, alternating on adaxial surface; flowers monosymmetric by reduction, bracts 0; (T 0); staminate flowers: P 1; A 1, anther thecae separate, joined by connective; pollen filiform, (binucleate), smooth, exine 0; pistillode 0; carpellate flowers: staminode +, G 1, ± asymmetrical, stylulus +, stigmatic branches 2, long, ± fimbriate; ovule with outer integument to 7 cells across, parietal tissue absent, 2 nucellar layers laterally, podium massive, postament +; fruit achenial, ribbed; exotestal cells ± anticlinally and periclinally elongate, other cells persist, ± thickened or not, tegmen degenerates; n = 6, 9, 10, chromosomes 0.9-1.6 µm long; no primary root.
2[list]/14. Temperate to subtropical (map: see den Hartog 1970; van Balgooy 1975).
Age. Divergence may have started within Zosteraceae ca 33 m.y.a. (Y. Kato et al. 2003) or ca 23.3. m.y.a. (Coyer et al. 2013).
Evolution. Ecology & Physiology. The age of a clone of Zostera marina in the Baltic was estimated at more than 1,000 years (Reusch et al. 1999).
Chemistry, Morphology, etc. Sulphated flavononids have not yet been detected from Posidonia (Heglmeier & Zidorn 2010: summary of phytochemicals). All leaves on a plant are similar in morphology.
Tomlinson (1982) suggested that the staminate flowers had two, bisporangiate/monothecal anthers. The course of endosperm development is unclear.
General information is taken from Kuo and McComb (1998) and Tomlinson and Posluszny (2001), reproductive morphology from Soros-Pottruff and Posluszny (1994: Phyllospadix).
Phylogeny. For relationships in Zosteraceae see Y. Kato et al. (2003), Les et al. (2001) and in particular Coyer et al. (2013); Phyllospadix is sister to the rest of the family.
Classification. For generic limits, see Les et al. (2001)
POTAMOGETONACEAE Berchtold & J. Presl, nom. cons. Back to Alismatales
Often freshwater plants, (± marine, submerged); (apical meristems of vegetative axes bifurcating - Zannichellia); sulphated compounds 0, (vessels + - non-marine taxa), (flavone sulphates + - Zannichellia); (stomata +, development odd); leaves spiral, 2-ranked or opposite, vernation involute, (with pseudopetiole, midrib and blade), primary veins merge with each other, (margin serrulate), (with apical pore), ligule basal, sheathing, (adnate to leaf base), auricles 0; flowers sessile [inflorescence spicate], (inflorescence bracts + - "subtending spathe"); (plant monoecious); flowers (perfect), (2-)4-merous; P clawed,
adnate to A; A 1-4; pollen (trinucleate); G (1-)4(-8), alternating with P, ± stipitate, partly ascidiate, stigma ± expanded;
4[list]/102: Potamogeton (60). Worldwide, esp. temperate (map: see Hultén 1961; Meusel et al. 1965; Haynes & Holm-Nielsen 2003; Kaplan 2008; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photo - Habit, Potamogeton Inflorescence.]
Age. Divergence wthin Potamogetonaceae may have begun ca 25 m.y.a. (Janssen & Bremer 2004).
Evolution. Pollination Biology & Seed Dispersal. Cross-pollination is by wind, or by pollen floating on the surface of the water. Nunes et al. (2012) suggested that Potomageton illinoensis might have a hyperstigma.
Potamogeton in particular is a very important source of food for ducks in North America; the fruit floats and is photosynthetic.
Chemistry, Morphology, etc. There is great variation in the leaf base, including the ligules (often called stipules), and in leaf shape both within and between species; some taxa of Potamogeton are heterophyllous, with submerged and floating leaves differing greatly in form. Potamogeton tends to have trilacunar nodes, and there has been some debate as to whether the ligule is "really" a stipule (Colomb 1887; Sinnott & Bailey 1914).
There has been debate as to the nature of the ovule, which is often more or less campylotropous, sometimes because of an ingrowth of the carpel wall (Takaso & Bouman 1984; Nunes et al. 2010), Posluszny and Tomlinson (1977) suggested that staminate flowers of Zannichellia had a single anther with up to 12 sporangia, although other interpretations seem possible; the anthers are sessile. Remizowa et al. (2011) thought that the flowers of Zannicellia might represent racemose partial inflorescences...
Much general information is taken from from Haynes (1978) and Haynes et al. (1998b); see also Posluszny (1981) and Charlton and Posluszny (1991) for floral morphology, Kaplan et al. (2013) for chromosome numbers, not Zannichellia.
Phylogeny. The morphologically very distinctive Zannichellia, which alone in the family commonly has flavone sulphates, is rather weakly embedded within Potamogetonaceae (Les et al. 1997) or sister to the rest of the family (Les & Tippery 2013). Potamogeton itself is para- or polyphyletic (Les & Haynes 1995); for the phylogeny and evolution of Potamogeton in particular, see Lindqvist et al. (2006).
Synonymy: Hydrogetonaceae Link [status?], Zannichelliaceae Chevallier, nom. cons.