EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; flavonoids + [absorbtion of UV radiation]; chloroplasts lacking pyrenoids; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.

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

All groups below are crown groups, nearly all are extant; characters mentioned are those of the common ancestor of the group.


Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.


Sporophyte branched, branching apical, dichotomous; sporangia several; spore walls not multilamellate [?here].


Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].


Branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].


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


Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; 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.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

ANGIOSPERMAE Lindley / MAGNOLIIDAE Takhtajan  Back to Main Tree

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine +, thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, much larger than ovule at time of fertilization; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Age. Age estimates of crown-group angiosperms vary considerably, although most are in the range (210-)150-140(-130) m.y. (e.g. Doyle 2001; Sanderson & Doyle 2001; Wikström et al. 2001; Aoki et al. 2004; Davis et al. 2004a; Sanderson et al. 2004; Bell et al. 2005; Leebens-Mack et al. 2005; Moore et al. 2007; Soltis et al. 2008: a variety of estimates; Moore et al. 2010). Bell et al. (2010: note topology) suggest ages of (199-)183(-167) and (154-)147(-141) m.y. (see also Magallón 2009) and Iles et al. (2014) ages of (167.7-)158.7(-151) m.y. ago. Some recent estimates based on molecular data tend to be substantially older than others, Magallón (2008 and references) and Magallón & Castillo (2009) noting ages of 182-158 m.y. and 130 or 242 m.y. respectively, i.e. mostly Lower to Middle Jurassic or older, indeed, Smith et al. (2010: see esp. Table S3) suggested that crown-group angiosperms were (270-)228, 217(-182) m.y.o., and there are ages of 275-215.6 m.y. in Magallón (2010), (280, 252-)246, 209(-186) m.y. in Zeng et al. (2013) and ca 279 m.y.a. in Z. Wu et al. (2014). Yet again, other ages are somewhat younger, e.g. (240-)205(-175) m.y. in Clarke et al. (2011: other dates), (256-)198(-163) m.y. in N. Zhang et al. (2012, similar in Xue et al. 2012), (257.9-)208.7-193.7(-157.7) m.y. in Magallón et al. (2013) for this clade and around 195.4-185.3 m.y. in Naumann et al. (2013); see also Schneider et al. (2004).

Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see below).

Evolution. Divergence & Distribution. Thinking specifically of possible apomorphies for flowering plants, presence of vessels is placed at the [Austrobaileyales + the rest] node. However, the distinction between vessels and tracheids can be very hard to make (e.g. Carlquist 2012). Amborella lacks much in the way of obvious vessels (Feild et al. 2000b; c.f. Carlquist 2012), in Nymphaeaceae and Cabombaceae vessel morphology may be quite distinctive (Carlquist & Schneider 2009; Schneider & Carlquist 2009), and vessels are absent in Hydatellaceae, so vessels may have arisen some three times in the basal part of the angiosperm tree.

Routley et al. (2004) find protogyny to be very common in "basal" angiosperms (Amborellaceae inapplicable, variable in eudicots and above Alismatales in monocots - see also Endress 1994b). Sage et al. (2009) suggest that the basic condition of the angiosperm stigma may have been dry. Staedler et al. (2009; see also Wang et al. 2011) thought that the presence of an extragynoecial compitum could be an apomorphy of angiosperms, and then it would have to be lost at least twice; Armbruster et al. (2002) and Wang et al. (2011) discuss the complex patterns of gains and losses of various kinds of compita. In Amborellaceae and some other ANITA-grade angiosperms, including Hydatellaceae, the stigma has multicellular papillae. Endress (2001a) notes i.a. that the carpels (?of the ancestral angiosperm) may have uniseriate hairs - in Trimeniaceae and Nymphaeales the apical cell of these hairs is elongated and tanniniferous.

Whether or not an 8-nucleate embryo sac and triploid endosperm are synapomorphies for all angiosperms or only for those angiosperms in the [[magnoliid + Chloranthaceae] [other angiosperms]] clade has been unclear (Friedman 2001a, b, 2006; Baroux et al. 2002). Friedman et al. (2003a, esp. b) and Friedman and Williams (2003, 2004) incline towards the latter hypothesis - see especially Friedman and Ryerson (2009). If Nymphaeales are sister to Amborellales (but see below), then diploid endosperm may be the ancestral condition, with triploid endosperm evolving in parallel in Amborella and in the [[magnoliid + Chloranthaceae] [other angiosperms]] clade.for endosperm development, see Williams and Friedman (2004 and references) .

The morphology of those gymnosperms - currently largely unknown - on the angiosperm stem clade will affect the level at which some of the angiosperm apomorphies above are to be pegged. For example, if reticulate-perforate pollen is optimized to the second node on the tree (see Friis et al. 2009 for a discussion), it makes the pollen morphology of the common ancestor of all angiosperms ambiguous. The "standard view" is that the ancestor of flowering plants had monosulcate pollen (e.g. Walker & Walker 1984; Doyle 2013), but pollen of Amborella is anaulcerate. Complicating our understanding of the morphology and ecology of the immediate angiosperm ancestor, the early-diverging Nymphaeales are in many respects highly autapomorphic aquatics. The placement of features such as details of sugar transport in the phloem is frankly speculative. Finally, for features such as parietal tissue/nucellus only one (Nymphaeales) to three cell layers across above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where higher up on the tree changes in these features occurs. The polarity of many angiosperm characters remains unclear (e.g. Friedman & Floyd 2001; Ronse De Craene et al. 2003).

For a survey and evaluation of floral morphology and systematics, see Matthews and Endress (2012). For further discussion on evolution and diversification, see e.g. Bachelier and Friedman (2011: female gametophyte competition within a single ovule and angiosperm evolution), X.-F. Wang et al. (2011: pollen tube growth/compitum development), Williams (2008, 2009, 2012a, esp. 2012b: pollen tube/male gametophyte development, nucellus, etc.), Taylor and Kirchner (1995: carpel evolution), Hickey and Taylor (1995) and Rudall (2013), both evolution of the flower, Wing and Boucher (1998: ecology), Donoghue (2004: general), Whitney (2009: stronger selection for divergent flower than fruit morphology). For woodiness and wood anatomy, see S. Kim et al. (2004a) and Herendeen et al. (1999: a useful table), for changes in phyllotaxy, Ronse De Craene et al. (2003), for the evolution of the perianth, etc., see e.g. Hasebe (1999), D. Soltis et al. (2005a, b), for carpellary fusion, see Sokoloff et al. (2013), for endosperm, see below, for stigma type, Thien et al. (2009), and for variation in embryo size, see Verdú (2006). For microsporogenesis evolution, see especially Furness et al. (2002b) and Taylor and Osborn (2006), for pollen micromorphology, see Sampson (2000), Doyle (2005: c.f. topologies of the trees used, 2008) and Taylor and Osborn (2006). For various aspects of early angiosperm evolution, see below.

Genes & Genomes. Genome size in many angiosperms is small, indeed, 1-1.4 picograms is the estimated ancestral nuclear C value for angiosperms (Masterson 1994; Leitch et al. 2005), although there are some notable exceptions (e.g. a few Liliales and Asparagales). It is smaller than that of extant gymnosperms, although genomes in Gnetaceae & co. are smaller than those of the others (Leitch et al. 2005; Nystedt et al. 2013). At this level genome size and ploidy level seem not to be connected. For genome duplication in stem-group angiosperms, see e.g. Karlgren et al. (2011). For the evolution of the IR/LSC junction in the chloroplast genome, see R.-J. Wang et al. (2008), for chloroplast genome evolution, see Kua et al. 92012). Evans and Rees (1971) discuss variation in the length of the mitotic cycle, with that in eudicots being ca 4 hours longer than that in monocots (interphase, G1, is involved, 16 species sampled). For B-function genes, etc., see S. Kim et al. (2004b) - synonymization: AP3 and PI with DEF and GLO.

Chemistry, Morphology, etc. Some taxa in the ANITA grade (Amborellales, Nymphaeales and Austrobaileyales) have been surprisingly little studied. Thus root morphology, cork development, etc., are unknown in Amborellaceae, an absence of knowledge complicated by the very distinctive "aquatic" morphology and anatomy of Nymphaeales.

The mycorrhizal condition of the ANITA grade is largely unknown, as is that of Canellales, Piperales, and most of Laurales; mycorrhizae are absent in Nymphaeales (and Ceratophyllales), as might be expected for aquatic groups (Landis et al. 2002; B. Wang & Qiu 2006). However, the ancestor of Magnoliophyta as a whole is likely to have had vesicular-arbuscular mycorrhizae, indeed, this condition may well have been a feature of all seed plants, if not still deeper in the tree. The triperpenoid oleanane is widely distributed in angiosperms, but in no other extant seed plants (Taylor et al. 2006). An arsenite transporter controlled by the single-copy ACR3 gene and promoting arsenic tolerance is found throughout land plants other than flowering plants, as found when searching whole-genome and and EST databases (Indriolo et al. 2010), so its loss is another apomorphy.... Boyce at al. (2004) noted that the lignification of the primary cell wall was heavy in ANITA-grade angiosperms (and in Drimys, a magnoliid) and gymnosperms, less in eudicots, and this had implications for ion-mediated xylem flow. However, the sampling is very preliminary. p-hydroxybenzaldehyde, a component of many lignins, is apparently absent from broad-leaved angiosperms - at least from magnoliids and eudicots (Towers & Gibbs 1953), but is present in the monocots sampled and in some living gymnosperms (and also some Myrtaceae, etc.). For mannans, etc., see Popper and Fry (2004); Austrobaileya has mannans, although two other members of the order sampled lack them, Nymphaea also has mannans, but other Nymphaeales and Amborella were not sampled. Pribat et al. (2010) discuss the distribution of a folate-dependent phenyanaline hydrolase, which may be correlated with major plant groups when sampling is improved.

Furuta et al. (2014) describe how the sieve tube nucleus becomes non-functional; autolysis occurs, and the nuclear contents are released into the cytoplasm where they are degraded. Axial parenchyma is notably slight to absent in Amborellales, Austrobaileyales, Laurales, and Chloranthales (Herendeen et al. 1999). Leaf traces make connections only with xylem produced during the first year (Tomlinson et al. 2006); c.f. Pinales. Stomatal morphology and development in many members of the ANITA grade is notably variable (e.g. Upchurch 1984; Rudall & Knowles 2013). Leaf teeth of the chloranthoid type, with a central vein joined by branches from above and below and then proceeding to a thickened apex, may be plesiomorphic within angiosperms and synapomorphic for them (Doyle 2007).

For pollen characters of angiosperms of the ANITA grade, and also magnoliids, see Doyle (2007). The pollen morphology of Amborellaceae is not well understood and there is much variation in microsporogenesis and pollen morphology in Nymphaeales, Amborellaceae, etc. (e.g. Furness et al. 2002), and some of the pollen characters may be incorrectly placed on the tree. For pollen tube growth, see e.g. Abercrombie et al. (2011). For tapetum type and orbicule production, see Verstraete et al. (2014 and references).

Lauraceae, Degeneriaceae and Magnoliaceae, at least, develop a massive, multiseriate suspensor during embryogenesis (Wardlaw 1955). For the evolution in endosperm development, see above). Seedlings/young plants with decumbent lignotubers and sympodial growth are common in the ANITA grade and in Chloranthaceae, although not in the aquatic Nymphaeales, and early angiosperms may have been smallish trees (Feild et al. 2003, 2004; Feild & Arens 2005); most eudicots have seedlings/young plants that are at least initially erect. Our knowledge of the dark reversal of P[hytochrome]fr → Pr may be a bit skimpy, but the general pattern of the ability of the plant to do this seems interesting (Kendrick & Hillman 1971). For 1C values (converted to 2C values here, see Plant DNA C-values Database, consulted vi.2013 (also Bennett & Leitch 2010).

Phylogeny. The balance of evidence is tilting towards the hypothesis that angiosperms are sister to a clade that includes all extant gymnosperms, however, given the uncertainty in our knowledge of the relationships between the major seed-plant clades, direct links to them are provided here: Cycadales, and Pinales; for a general discussion, see seed plant evolution.

Within early-diverging angiosperms, Donoghue and Mathews (1998) listed 16 different hypotheses of relationships that involved the first three nodes, but Amborellaceae alone have often been found to be sister to other angiosperms (not an hypothesis that Donoghue and Mathews included!), Nymphaeales sister to the rest, then Austrobaileyales - the ANITA grade (e.g. Mathews & Donoghue 1999, 2000; Qiu et al. 1999, 2000, 2001 [checked for long-branch attraction - none], 2005, 2006a, 2006b [some analyses], 2007; P. Soltis et al. 1999, 2000; Parkinson et al. 1999; Zanis et al. 2002; Magallón & Sanderson 2002; Kim et al. 2003; Borsch et al. 2003, 2005; Hilu et al. 2003; Nickerson & Drouin 2004; Aoki et al. 2004; P. Soltis & D. Soltis 2004; Müller et al. 2006a; Hansen et al. 2007; Duarte et al. 2008; McCoy et al. 2008; Zeng et al. 2014; Drew et al. 2014; Wickett et al. 2014: transcriptome analyses; Sun et al. 2014: chloroplast and nuclear data; etc.). For other studies, see Ruhlman et al. (2007), Jansen et al. (2007) and Moore et al. (2007). Graham et al. (2000), Cai et al. (2006), Jansen et al. (2006b), Bausher et al. (2006), Chang et al. (2006), Wu et al. (2007), Huang et al. (2010: c.f. rooting), Moore et al. (2011: position not as stable as one might like...) and Iles et al. (2014).

Of the topologies depicting relationships between early-diverging angiosperms, by far the commonest is one in which the ANITA grade (the acronym varies) is basal to all other flowering plants (e.g. E. K. Lee et al. 2011). However, Goremykin et al. (2003a), using complete chloroplast sequences, but for only 10 angiosperms, suggested the relationships [[Amborellaceae + Calycanthaceae] [eudicots + monocots]], but poor taxonomic sampling with resultant long-branch attraction may be responsible for these results (D. Soltis & P. Soltis 2004; Jansen et al. 2004; Stefanovic et al. 2004; Degtjareva et al. 2004b; D. Soltis et al. 2004); monocots were represented by the highly derived Poaceae. Goremykin et al. (2004) found the same general result when adding Nymphaea; it linked with Amborella - which was still not sister to all other angiosperms. However, this study, too, suffers from the same sampling problem; grasses are highly derived monocots (see Kuhl et al. 2004 for the very distinctive genome of Poaceae). Indeed, even when looking at complete chloroplast sequences of just a few flowering plants, the inclusion of Acorus, breaking up the long branch leading to Poaceae, had a major effect (Stefanovic et al. 2004), although there are also questions about the models used in the analyses (Lockhart & Penny 2005; Goremykin et al. 2005). Morton (2011: nuclear Xdh gene) found weak support for Ceratophyllaceae as sister to all other angiosperms, although otherwise much of the structure in her tree was similar to that of other studies mentioned here; in the massive parsimony analysis of Goloboff et al. (2009) relationships [Ceratophyllum [[Amborella + Nymphaeales] other angiosperms]].

There have been persistent suggestions that there is an [Amborellales + Nymphaeales] clade. This topology was perhaps particularly prominent in some analyses of mitochondrial genes, e.g. Qiu et al. (2006b), although there were several unexpected if poorly supported relationships elsewhere in their preferred tree (e.g. Qiu et al. 2010; see also Qiu et al. 2000, 2005, 2006a). Sun et al. (2014) also found this topology in most of their mitochondrial analyses. Soltis et al. (2007; data from D. Soltis et al. 2000) found that the relationships obtained depended on the method of analysis; Bayesian analysis favoured [Amborellaceae + Nymphaeaceae], while parsimony yielded [Amborellaceae + The Rest], while Goremykin et al. (2012) suggested that a wrongly specified substitution model would produce the latter result. Indeed, what kinds of characters are analysed may be important. Goremykin et al. (2009b) found an [Amborella + Nymphaea] clade after removing a relatively few (500) highly variable positions from the analysis, and although criticized by Drew et al. (2014), other studies hint more or less strongly that rate heterogeneity may be an issue (Barkman et al. 2000; Stefanovic et al. 2004; Leebens-Mack et al. 2005; Finet et al. 2010; Goremykin et al. 2013). In a comprehensive series of analyses, Xi et al. (2014) thought that the problem had to do with the rate of gene evolution, not amount of data. Concatenation results tended to give a clade [Amborellaceae + The Rest] unless fast-evolving sites were removed; if they were, an [Amborella + Nymphaea] clade was found, as in all their coalescent analyses. However, in a series of analyses of fairly well sampled transcriptome data, Wickett et al. (2014) found very little support for the [Amborella + Nymphaea] clade whatever the analytical method used.

Differing topologies may have little effect when thinking about angiosperm evolution, certainly for characters like the evolution of habit/habitat (c.f. Drew et al. 2014), but it does make one think about embryo sac evolution (Xi et al. 2014); such issues depend in part on how characters are optimised on the tree.

Sampling and analytical strategies may well be critical here, particularly when there are relatively few taxa each with very large amounts of data. In some cases large amounts of data may indeed be the solution, in others, perhaps quite surprisingly little data per taxon but improved sampling will do the trick (e.g. Rokas et al. 2005; Hedtke et al. 2006). Of course, exactly where sampling should be improved is important (Geuten et al. 2007), and each situation will have to be evaluated independently. The discovery that Hydatellaceae are sister to other Nymphaeales (Saarela et al. 2006) unexpectly did allow sampling in this area of the tree to be improved, but without affecting its topology. Fiz-Palacios et al. (2011) suggested a number (25+) of "non-conventional" relationships in their study on land plant diversification, but this, too may be a taxon sampling issue; I rarely mention these here. More data are not always an unmixed blessing, thus Barrett et al. (2012), using whole chloroplast genomes of monocots, found that adding data did not necessarily result in asymptotically stabilizing support values, rather, these continued to fluctuate even when there was quite a lot of data and relatively small further amounts were added. Finally, some kinds of DNA data may be positively misleading when it comes to understanding relationships (Duvall & Ervin 2004; Qiu et al. 2005; Duvall et al. 2006, 2008b; G. Petersen et al. 2006b). Mitochondrial data tend to give odd topologies, and horizontal transfer is notably common in mitochondrial genomes (Sanchez-Puerta et al. 2008, 2011; Hao et al. 2010; Wenqin Wang et al. 2012; c.f. Cusimano et al. 2008; Rice et al. 2013). With genome and transcriptome data being accumulated for considerable numbers of plants, issues surrounding how best to analyse the massive amounts of data being accumulated become central (see below).

There are convenient summaries of the copious literature on relationships between the major angiosperm clades in e.g. P. Soltis & D. Soltis (2004), D. Soltis et al. (2005b) and Qiu et al. (2005). For information on broader patterns of relationships here, see especially the notes at the mesangiosperm node; for relationships higher up in the tree, see monocots, eudicots, pentapetalae/core eudicots, asterids, euasterids, and Escalloniales. The discussions focus on the usually rather conservative topologies of the trees in this site, but it will be clear that there is sometimes substantial uncertainty about details of relationships.

Classification. For bibliographic information on familial and ordinal names, etc., in angiosperms see Reveal and Chase (2011) and Reveal (2012).

Synonymy: Alismatidae Takhtajan, Arecidae Takhtajan, Aridae Takhtajan, Asteridae Takhtajan, Bromeliidae C. Y. Wu et al., Burmaniidae Heintzw, Caycanthidae C. Y. Wu et al., Catyophyllidae Takhtajan, Ceratophyllidae Doweld, Chloranthidae C. Y. Wu et al., Commelinidae Takhtajan, Cornidae Reveal, Dillenidae Reveal & Takhtajan, Ericidae C. Y. Wu et al., Hamamelididae Takhtajan, Iliciidae C. Y. Wu et al., Juncidae Doweld, Lamiidae Reveal, Lauridae C. Y. Wu et al., Liliidae J. H. Schaffner, Loranthidae Tieghem, Malvidae C. Y. Wu et al., Myrtidae J. H. Schaffner, Nelumbonidae Takhtajan, Nymphaeidae Takhtajan, Orchididae Heintze, Piperidae Reveal, Plumbaginidae C. Y. Wu et al., Polygonidae C. Y. Wu et al., Ranunculidae Takhtajan, Rosidae Takhtajan, Rutidae Doweld, Theidae Doweld, Triuridae Doweld, Winteridae Doweld, Zingiberidae Cronquist - Magnoliophytina Reveal - Magnoliophyta Reveal

[Amborellales + Nymphaeales]: ?

Age. Age estimates for this clade (if it exists) are (242.7-)150.1(-75.6) m.y. (Zhou et al. 2014).

AMBORELLALES Melikian, A. V. Bobrov & Zaytzeva  Main Tree.

Nodes 1:1; plant dioecious; hypanthium +; nectar from base of P?; A sessile, middle layer of anther wall from both secondary parietal cells [ wall type]; pollen anaulcerate [pore-like, operculum endexinous, margin poorly defined], ektexine cupulate [distinctive undulate, columella-less exine]; stigma with uniseriate multicellular papillae; ovule 1/carpel, outer integument annular [cap-shaped], nucellar cap 0; embryo sac bipolar, 9-nucleate, with three synergids, antipodal cells die very early, polar nuclei in chalazal region; fruit a drupelet; exotesta and exo- and endotegmen thick-walled, lignified; endosperm triploid, develops in chalazal half. - 1 family, 1 genus, 1 species.

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above). Of course, putting apomorphies here in particular is a distinctly dubious proposition, given both the position of the clade and the black hole of ignorance immediately basal to angiosperms.

Includes Amborellaceae.

Synonymy: Amborellineae Shipunov

AMBORELLACEAE Pichon, nom. cons. Back to Amborellales


Shrub or small tree; alkaloids?; cork?; axial parenchyma apotracheal diffuse; (some pits in tracheary elements lacking membranes); pericycle with hippocrepiform sclereids; mucilage cells 0; petiole bundles arcuate; (stomata anomocytic); ?tooth morphology; inflorescence cymose; flowers small; P spiral, basally connate, 5-8, with a single trace; staminate flowers: A 6-25, outer adnate to the base of P, vascular bundle branched near thecae; pistillode 0; carpellate flowers: staminodes 1-2; G 3-6, whorled; ovule ± median, pendulous, hemianatropous, sessile, micropyle endostomal; P persistent, stone surface sculpted; seed coat tanniniferous; germination hypogeal, seedlings/young plants sympodial; n = 13; horizontal transfer of atp1 gene.

1[list]/1: Amborella trichopoda. New Caledonia. [Photo - Leaves, Flower.]

Evolution. Divergence & Distribution. Assuming that New Caledonia finally became emergent 32 m.y.a. (Cluzel et al. 2012;Swenson et al. 2014 for references), proto-Amborella must have been hanging out somewhere else for a very long time.

Pollination Biology. Both insects and wind are effective pollinators (Thien et al. 2003). Stigmatic exudate may join all the stigmas of a single flower together, and pollination of ovules in more than one carpel from pollen landing on a single stigma is possible, i.e. there is an extragynoecial compitum (Williams 2009).

Genes & Genomes. The mitochondrial genome of Amborella contains genes from a number of land plants, including at least three different mosses, and such "foreign" genes may also migrate to the nucleus (Bergthorsson et al. 2004), although Goremykin et al. (2009) questioned that the evidence for these tranferson methodological grounds. However, the mitochondrial genome of Amborella is about seven times normal size and has acquired about three genomes worth of green algal DNA, two genomes worth of moss DNA, and one genome worth of angiosperm DNA (Rice et al. 2013). The algal DNA is similar to that of the trebouxiophyte Coccomyza, a component of lichens, perhaps suggesting that wounding of Amborella plants followed by uptake of mitochondrial DNA from associated epiphytes could be a mechanism facilitating this uptake. The angiosperm DNA came from Fagales, Oxalidales, Santalales, Ricinus (Malpighiales-Euphorbiaceae) and Bambusa (Poales-Poaceae) (Rice et al. 2013). Mitochondrial genomes like that of Amborella are as yet unknown from other angiosperms, although sampling is still poor, and one wonders what might be distinctive about Amborella that might lead to it alone being such "a graveyard of foreign genes" (Rice et al. 2013: p. 70).

Chemistry, Morphology, etc. For absence of aluminium accumulation, see Thien et al. (2003). Amborella lacks reaction wood, its stems tending to sprawl, especially when young; in terms of architectural models (Hallé et al. 1978) the plant conforms to Troll's model. Some pits of the tracheary elements lack membranes, so technically they are vessels; open conduits are made up of only two such cells (Feild et al. 2000b), but Carlquist (2012a: p. 107; see also 2012c) thought that these were artefacts, noting that "intact porose pits in end walls of Amborella can be found". Stomatal morphology is quite variable, although the brachyparacytic configuration is common (Carlquist & Schneider 2001). The leaves are described as being spiral at first (Cronquist 1981; Takhtajan 1997), but c.f. Posluszny and Tomlinson (2003).

The perianth is spiral and undifferentiated. There seems to be no agreement on pollen morphology; Sampson (2000) and Hesse (2001) suggest that the pollen is not really tectate (see also Doyle 2000, 2001; Doyle and Endress 2000), and the aperture is difficult to categorise, as well as not always being present. Williams (2008, 2009) describes pollen tube development and fertilization. The ovule has been described as being orthotropous, anatropous, or intermediate (Tobe et al. 2000). Bobrov et al. (2005) show that the drupe of Amborella differs from a typical drupe in that the bulk of the woody layer is mesocarpial in origin, unlike the drupes of Laurales, etc. The nature of the "resinous" cavities in the mesocarp is unclear; although not observed by Bobrov et al. (2005), they were conspicuous in material I saw and are unlikely to be an artefact caused by re-expansion of dried fruits prior to study. The seed coat appears to have thin, unlignified walls, as might be expected in such a fruit, although some lignification has been reported (Tobe et al. 2000).

Friedman (2006; c.f. Tobe et al. 2000) described a very distinctive embryo sac for Amborella; a third synergid cell arises from a cell division that also produces the female gamete. In other angiosperms the polar nuclei are sister to the egg nucleus (at one end) and the central chalazal nucleus (at the other), and the egg is produced by a nuclear division; however, the overall pattern is not necessarily fundamentally different since Amborella has a 9-nucleate embryo sac (c.f. Friedman 2006). Friedman and Ryerson (2009) discuss the evolution of the angiosperm embryo sac in detail. Porsch (1907) took the view that the micropylar and chalazal ends of the embryo sac were identical, but he had an "Englerian" concept of seed plant evolution, with Amentiferae being primitive. Porsch and others at that time (e.g. Nawaschin 1895) saw chalazogamy in Amentiferae (see Fagales here, also Ulmaceae) as being in some way intermediate between porogamy and non-angiospermy, where the female gametophyte has more than a single archegonium. However, the embryo sac of Amborella may be derived (Friedman & Ryserson 2999), and this is perhaps a little more likely if Amborella and Nymphaeales are sister clades (see Xi et al. 2014).

Additional information is taken from Bailey and Swamy (1948: general), Metcalfe (1987: anatomy), Philipson (1993), Sampson (1993: pollen), Yamada et al. (2001a: ovules), and Field et al. (2003: ecophysiology); for endosperm, see below. Chemistry?

Previous Relationships. Amborellaceae were included in Laurales by Cronquist (1981) and Takhtajan (1997).

EVOLUTION AND DIVERSIFICATION OF THE ANGIOSPERMS (This section is still under construction)

Below are some thoughts about the evolution of angiosperms. The first five sections are more introductory, while the others attempt to summarise aspects of angiosperm evolution and diversification. The evolution of flowers and fruits figure prominently in the mythology of angiosperm evolution and success, and they are indeed important (section 8), although not in any simple sense. Certainly, numbers of species is but one measure of success or importance, and in section 9 I discuss some physiological-ecological dimensions to angiosperm evolution, emphasizing aspects that seem to have had a major hand in shaping the global environment over the last 100 m.y. or more. This leads to section 10, where I turn to asymmetries in evolution, emphasizing relatively small groups of both plants and animals that seem to have had a disproportional (in terms of their species numbers) effect at scales from the global environment to the local community. When thinking of plants in this context, measures like primary productivity, biomass accumulation, and the like can be used as indicators of importance - and species-rich clades in the euasterids then barely have a walk-on part. In section 11 I attempt a summary. Needless to say, many very important topics are barely touched on, and this part of the site is very much under construction.

1. Important Caveats.

2. Angiosperms and Insects.

2A. Insects, Plants and Herbivory.

2B. Phytophagous Insects.

2C. Pollinating Insects.

3. Angiosperms and Fungi.

4. Evolution in Stem Group Angiosperms.

5. Cretaceous History of Angiosperms.

5A. Introduction.

5B. Early Angiosperm Evolution.

5C. Later Cretaceous Evolution.

6. Tertiary Diversification.

6A. Mostly Flowering Plants.

6B. Mostly Other Organisms.

6C. Latitudinal Gradients of Diversity.

8. Flowers, Pollination, and Evolution.

7A. Flowers, Pollination and Fertilization.

7B. Major Clades With Monosymmetric Flowers.

7C. Major Clades With Wind-Pollinated Flowers.

7D. A Cautionary Note.

8. The Physiological-Ecological Context of Angiosperm Evolution.

8A. Venation Density.

8B. Vascular Evolution.

8C. Wood and Litter Decay.

8D. Ectomycorrhizae and their Associates.

8E. C4 Photosynthesis, Grasses, and Grassland.

8F. Other.

9. Asymmetries in Evolution.

9A. Plant-Animal interactions.

9A1. Pollination.

9A2. Seed Dispersal.

9B. Carbon Sequestration.

10. In Conclusion.

1. Important Caveats.

When thinking about evolution in general, a well-supported phylogeny is of course a sine qua non, and there are several parts of the main tree here as well as in many orders where we know less than we would like. Beyond this, there are important issues of dating, understanding fossils, working out diversification rates, optimising characters on trees, etc., that need to be taken into consideration. I discuss some of these issues briefly below, but please consult the primary literature for details.

1. Dating is critical, but how best to do this remains a subject of intense discussion (e.g. Magallón and Sanderson 2001; Graur & Martin 2003; Pirie et al. 2005; Renner 2005b; Bell & Donoghue 2005; Magallón & Sanderson 2005; Rutschmann et al. 2007; Sanderson et al. 2004; Hengcheng Wang et al. 2009; Smith et al. 2010: molecular dating; Crepet et al. 2004: palaeontological dating; Magallón 2009; Milne 2009: sampling; Burleigh 2012; especially Sauquet et al. 2012; Magallón 2014). Many clade ages are not very reliable at this stage of our knowledge, and in several cases there are wildly different estimates for the same event. For instance, compare Wikström et al. (2001, 2004), Davies et al. (2004), Clarke et al. (2011) and Z. Wu et al. (2014) for angiosperm ages, Clarke et al. suggest a crown-group age in the Jurassic or earlier, Wu et al. an age in the mid-Permian. See also Sauquet et al. (2012) for Nothofagus, Crisp and Cook (2011) and Martínez et al. (2012) for cycads, and Barreda et al. (2010b, 2012) and Heads (2012) for Asteraceae (Waters et al. 2013 for a critique of the latter). Although many ages for clades are given on these pages (many dates, not all mentioned here, are conveniently assembled in Hedges & Kumar 2009), they should all be treated with extreme caution. The original papers should be consulted for details of methodology, the actual node to which the date refers, and the topology of the tree that is being dated.

Dates based on molecular, tectonic, and paleontological data can be in conflict, and the first two often give substantially older ages than the last, but c.f. Nymphaeales. In a study of different ways of calibrating, and two different ways of dating, Sauquet et al. (2011) found that the ranges of the means alone for each node varied by up to a factor of 10 (see also Parham et al. 2011). The relaxed ages given by Magallón and Castillo (2009) are often substantially older than the constrained ages - for example, the relaxed crown group age for angiosperms is about 242 m.y., and the constrained age about 130 m.y.. For useful discussions on dating, see also Magallón et al. (2013), Sytsma et al. (2014), etc..

Although it might seem that a clade living on a volcanic island must be younger than that island, there are several examples suggesting the contrary to be found in these pages (see also Heads 2011); island age cannot be used as either a maximum or minimum age without there being other evidence.

Fossil evidence is central to dating. However, fossils are of course nearly always more or less incomplete and so lack critical features, and to the extent that many fossils are stem-group members, they may lack the apomorphies of the crown group. Moreover, they cannot be expected to be simply "ancestral", rather, they may have evolved distinctive features of their own, and these, given the nature of seed plant evolution, may well be parallelisms, so perhaps suggesting links with unrelated groups in phylogenetic analyses, especially if these are widely ranging. Some studies have questioned what had previously seemed to be quite well established fossil identifications (e.g. Cook & Crisp 2005; Nothofagus; Biffin et al. 2010b: Araucariaceae). Fossils yield only a minimum age (Donoghue & Benton 2007), and fragmentary fossils in particular may be assignable to more than one node. The identification of fossils and their selection for calibration of molecular trees should be treated very carefully (e.g. Gandolfo et al. 2004; Graham 2010; Clarke et al. 2011; etc.). The fossil record is sure to have surprises, for example, Leefructus, from early Cretaceous deposits 125.8-122.6 m.y. old and assigned to stem Ranunculaceae (Sun et al. 2011) challenges many of our ideas of angiosperm evolution.

In Poaceae in particular there are problems. Amber fossils from the Cretaceous of Myanmar/Burma (Shi et al. 2012; see also Poinar 2004) dated to ca 98.8 m.y. suggest a substantially greater age for the clade and its diversification than is given by other dating methods. Such dates would change many other dates for flowering plant clades and cause a general rethinking of angiosperm evolution; Poinar (2011) recently reaffirmed the probable identity of this fossil as Poaceae-Pooideae. Other core eudicot angiosperm fossils have been found in these amber deposits (e.g. Poinar 2011, Poinar et al. 2007, 2008), so much hangs on their correct dating and the correct identification of the fossils. Even less extreme datings suggested by grass phytoliths from India had a substantial effect on age estimates, and hence on diversification rates (Christin et al. 2014).

2. Distributions are not easy to interpret, since there is abundant evidence that the present and past distributions of many plant and animal groups are very different. Early in the Tertiary the distributions of a number of tropical taxa like Nypa and Cyclanthaceae that are today rather restricted were much wider (e.g. Plaziat et al 2001; Smith et al. 2008), while in the Oligocene humming birds were flying about in Europe (Mayr 2004). Genera and families continue to be added to the list of groups in which past and present distributions are very different (e.g. Stull et al. 2012; Manchester et al. 2012; Grímsson et al. 2013), and it is well known that many taxa now restricted to Southeast Asia grew in Europe and North America in the Tertiary (e.g. Ferguson et al. 1997; Manchester et al. 2009).

Dates are of course essential when interpreting distributional patterns. In a number of clades, patterns that that seemed to reflect vicariance caused by plate tectonic events may be better explained by much more recent dispersal/migration events (e.g. Renner 2005b, de Queiroz 2005, Wen & Ickert-Bond 2009: summaries, also Higgins et al. 2003; Nathan 2006; Yoder & Nowak 2996; Carpenter et al. 2010; Gillespie et al. 2012a; Baker & Couvreur 2012a, b; Christenhusz & Chase 2012; c.f. in part Ladiges & Cantrill 2007; Heads 2008, etc.). Even Lars Brundin's hitherto iconic chironimid midge drift-determined distributions may need reinterpretation from this point of view (Krosch et al. 2011). Finally, Smedmark et al. (2014) emphasized how difficult it was to reconstruct biogeographical events if more than one resolution was allowed for nodes whose support was weak, but using a single tree in such reconstructions is inadvisable. For how organisms achieve the ranges that they have, about which we know little, see e.g. Schurr et al. (2009) and individual family accounts.

3. The apparently simple issue of species numbers is in fact not that straightforward. We have to be very careful even when discussing the size of extant clades. There are two aspects to this - what is really the clade of interest?, and, how many species does it contain?

A. I take it as axiomatic that comparisons between taxa simply because they have the same hierarchical rank are usually ill-advised, putting it mildly. Simplistic "major clade"-type comparisons are not enough (e.g. Smith et al. 2011, but see Ricotta et al. 2012 and Laenen et al. 2014: Fig. 1). As an example, Orchidaceae are often considered to be a highly diverse clade in terms of numbers of species when compared with other families. However, since they are sister to the rest of the Asparagales, the disparity in species number, although considerable, is only three-fold (ca 22,000 vs. 7,100: note that Sargent 2004 compared Orchidaceae with Hypoxidaceae, with 100-220 species), furthermore, Asparagales as a whole, with ca 29,000 species, are sister to commelinids, with some 23,500 or more species. Within Orchidaceae the largely epiphytic and often CAM Epidendroideae include most species (e.g. Gravendeel et al. 2004). So the related questions, "Are orchids really diverse, and if so, why?", are not easy to answer. Perhaps Epidendroideae, or a clade within them, is the hyperdiverse group. There are many other examples of extreme clade size imbalance throughout the tree in which categorical ranks are less than informative about evolution and diversification (see below for another example).

B. Estimates of the number of extant species of flowering plants vary by a factor of about two - 422,127 (Govaerts 2001) to 223,300 (Scotland & Wortley 2003) - and perhaps add 20% (Joppa et al. 2010).

4. The relationships of angiosperms to other seed plants remain unclear (see below), and thus so do the whens, whys and hows of their initial diversification (see Davies et al. 2004b; Friis et al. 2005; Frohlich & Chase 2007; Pennisi 2009; Lee et al. 2011). Here we can distinguish between the origin of the clade of which angiosperms are the only extant representative, i.e. stem angiosperms ("origin 1"), the origin of plants with carpels, tepals, and a heterosporangiate strobilus, i.e. the evolution of plants with flowers ("origin 2"), and finally, the origin of crown angiosperms, i.e. the clade represented by the immediate common ancestor of extant flowering plants ("origin 3"). Stem angiosperms presumably are of early Carboniferous age or even older, 350±35-305-275±35 m.y. old, if the angiosperm clade is sister to the clade including all living gymnosperms (e.g. Savard et al. 1994; Crane et al. 1995; Crane 1999; Magallón & Castillo 2009; Clarke et al. 2011), perhaps to a younger bound of Permian in age (Doyle 1998a). Even if crown angiosperms are as much as 270 to 182 m.y. old in age (Smith et al. 2010), they will still have a substantial stem history. For the bulk of this some 100 m.y. plustime plants along the angiosperm stem may well have had naked seeds and other features of extant gymnosperms. Although current evidence suggests that extant gymnosperms are monophyletic, when considering both extant and fossil taxa gymnosperms are paraphyletic with respect to angiosperms; angiosperms are derived from a gymnospermous ancestor. However, little progress has been made in identifiying plants that can be placed somewhere between origin 1 and 3 over the last forty years or more (Doyle 2012; c.f. X. Wang 2009; X. Wang & Wang 2010; see Mathews & Kramer 2012 for a way forward).

5. Many characters seem to come and go on the tree almost willy-nilly, which makes their optimisation a distinctly hazardous undertaking. Thus using either parsimony or maximum likelihood, making apparently reasonable assumptions about weighting gains over losses (or vice versa), or just using the rather simple models of evolution explicit in ACCTRAN or DELTRAN to place the character on the tree (e.g. Donoghue & Ackerley 1996; Cunningham et al. 1998; Omland 1997, 1999; Ree & Donoghue 1999; Polly 2001; Webster & Purvis 2001; Ronquist 2004; Crisp & Cook 2005; Remizowa et al. 2010b; Sokoloff et al. 2013d; O'Meara 2012; Gascuel & Steel 2014), may affect the position of synapomorphies on trees, and hence our ideas of evolution (see also Sannier et al. 2007; Sannier et al. 2011; Sundue & Rothfels 2013). Syme and Oakley (2012) suggest that tree-based and node-based methods give very different results when it comes to allowing reversals. And of course the very definition/circumscription of the feature of interest may be problematical.

Endosperm evolution, perhaps particularly in monocots, is a good example. Tobe and Kadokawa (2010) discuss endosperm morphology in terms of cellular and helobial types. However, this typological distinction, commonly employed in the literature, does not capture the subtleties of endosperm development (see especially Floyd et al. 1999; Floyd & Friedman 2000, 2001 for alternatives; Rudall et al. 2009b). The initial division of the endosperm is highly asymmetric in Araceae, with subsequent cell divisions initially occurring only in the micropylar chamber; the family is considered to have cellular endosperm (Tobe & Kadokawa 2010; see also Maheshwari & Khanna 1957: The chalazal cells here are sometimes massive, e.g. Paremeswaran 1959). But asymmetry in endosperm development characterizes helobial endosperm development, so Araceae could also be characterized as having a form of helobial endosperm; Acoraceae also show similar developmental asymmetry (Buell 1938). As to the importance of topological uncertainties, if Tofieldiaceae are sister to the rest of Alismatales, then where the change from "cellular" to "helobial" endosperm should be placed on the tree is unclear. Either one gain (apomorphy for order) and one loss (Araceae), or two gains (Tofieldiaceae, and above Araceae). But the problem is broader, since helobial-type development also occurs in the ANITA grade (e.g. Rudall et al. 2009b).

There is also variation in whether the chalazal (e.g. Nymphaeales) or micropylar (Amborella) domain gives rise to the bulk of the endosperm. The evolutionary history of nuclear endosperm development is unclear (Olsen 2004). There is also variation in e.g. nuclear endosperm development, as within Poaceae (Leroux et al. 2014)

Whether or not a triploid endosperm is a synapomorphy for all angiosperms or only for those angiosperms in the [[magnoliid + Chloranthaceae] [other angiosperms]] clade is unclear (Friedman 2001a, b, 2006; Baroux et al. 2002). Friedman et al. (2003a, esp. b) and Friedman and Williams (2003, 2004) incline towards the latter hypothesis - see especially Williams and Friedman (2004) and Friedman and Ryerson (2009). If Nymphaeales are sister to Amborellales (but see above), then diploid endosperm may be the ancestral condition, with triploid endosperm evolving in parallel in Amborella and in the [[magnoliid + Chloranthaceae] [other angiosperms]] clade - and the supporting argument here would be that Amborella has an embryo sac unique in the angiosperms. Simple parsimony, both ACCTRAN or DELTRAN, help little here since there are no outgroups.

6. Understanding the palaeoecological context of the evolution of angiosperms is a challenge. Seed plant physiology and its interaction with the environment s.l. has helped shaped stem- and crown-angiosperm diversification since the Permian. Since ecological contexts change over time, that of the early Tertiary diversification of angiosperms is likely to be quite different from those of the origins of stem- and crown-group angiosperms. The Tertiary context is initially connected with the bolide impact at the K/T boundary, although much of angiosperm diversity as we now appreciate it seems to be a phenomenon of the later Tertiary, and again the ecological context has changed.

Palaeontologists face this problem on a daily basis. Thus Rothwell et al. (2000) reconstructed the palaeoecology of the small, probably short-lived conifer Aethophyllum using a combination of evidence from the fossil, the palaeoenvironment, etc. (also e.g. Strömberg 2006). Although it is tempting to read the ecology of early angiosperms from that of extant taxa of the ANITA grade, this is hazardous (e.g. Wheeler & Baas 1991, 1993; Philippe et al. 2008); thus Little et al. (2010) challenge the reliability of aspects of leaf morphology, especially the presence of teeth, as palaeoclimatic indicators (for which, see e.g. Wolfe 1978). However, since the immediate relatives of angiosperms are unclear, working out how the ancestral crown angiosperm functioned will for now have to be a top-down process (Feild & Arens 2005, 2007).

Furthermore, most angiosperms are symbiotic systems at a variety of levels. Features ascribed to plants may well be the result of interactions between plants, fungi, and/or bacteria (Friesen et al. 2011), and this goes far beyond the ancient endosymbiotic events that resulted in chloroplasts and mitochondria. Importantly, basic angiosperm physiology is mediated by fungi and bacteria both in the soil and in the plant, and this shaped and continues to shape both the local and the global environments.

7. With time, the tree, distributions, apomorphies, and numbers of species, we can begin to think about diversification. Although diversification is mentioned frequently below, both it and the related term, adaptive radiation, are imprecise and can be difficult to estimate and interpret (e.g. Bengtsson 1998; Sanderson 1998; Davies et al. 2004; Ricklefs 2007; Olson & Arroyo-Santos 2009; Ackerly 2009; Wertheim & Sanderson 2010; Stadler 2011a, b; Drummond et al. 2012; Morlon 2014, etc.). In curves showing diversity in clades over time, what can seem like an abrupt radiation, with rapid diversification after a period when there was little apparent diversity - the "broom and handle" and "stemmy" patterns evident in many clades - may be the result of extinction, diversification after the extinction event resuming at a rate similar to that before the event even if the overall appearance of the tree is that of a radiation (Crisp & Cook 2009). Extensive sampling (>80%) is needed if accurate estimates of slowdowns in diversification are to be made (Cusimano & Renner 2010), extinction is hard to estimate (Rabosky 2010c), and diversification rates will automatically tend to increase towards the present. Simple experiments estimating future extinctions showed that these might affect estimates of clade size imbalance at nodes of up to ca 50 m.y.o. (Clarke et al. 2011). In general, estimating clade size imbalance is a remarkably tricky operation, especially in the near absence of fossils, the usual situation (Tarver & Donoghue 2011; see also e.g. Rabowsky 2010a, b). Even when there is an excellent fossil record, strategies like removing recently-radiating clades may be needed if one is to detect diversity loss in other clades (Morlon et al. 2011: whales, etc.; see also Stadler 2011b). Optimisation is also relevant here, i.e., how are so-called key innovations linked to particular nodes? Finally, diversity/species numbers make up just one way to measure success, and there are other measures such as dominance, biomass production and net primary productivity that are discussedbelow.

2. Angiosperms and Insects.

Associations between plants and insects may be close, whether the insects are herbivores, detritivores, or pollinators. The diversification of angiosperms appears to be broadly contemporaneous with the massive diversification of many insect groups that are now more or less dependent on them, although there is some argument as to just how closely linked the two were. Ehrlich and Raven (1964) provide an early statement of the idea of co-evolution; also see/c.f. Janzen 1980; Schemske 1983; Brouat et al. 2001; Futuyma & Agrawal 2009; Kato et al. 2010; Fordyce 2010; Janz 2011; de Vienne 2013 and others). The term "co-evolution" can include anything from situations in which changes in one member of the association is linked to changes in the other (cospeciation need not be involved), to cospeciation (which may not involve mutual evolutionary change), to key innovations and adaptive radiation. The reciprocal evolutionary change and diversification of co-evolving plant and insect or other animal groups seems to be quite uncommon, and usually involves vertical inheritance of parasites/endophytes (de Vienne et al. 2013), although there is quite close co-evolution in some examples of herbivory and parasitism (Winkler & Mitter 2008; Althoff et al. 2012, but c.f. some bruchids, etc.). Host switching is often associated with radiation of the insect on the new host (Fordyce 2010) and is quite common (de Vienne et al. 2013). Complicating our understanding of the interactions of insects and plants are the symbiotic bacteria and other organisms associated with insects (Frago et al. 2012; Zhu et al. 2014). However, some plant and insect groups are closely associated, and the question is, to what extent is/was the evolution of the two connected?

2A. Insects, Plants and Herbivory. Details of plant-insect relationships are discussed after individual orders and families. Plants have evolved mechanical and especially chemical defences against herbivory, and some insects have evolved ways of tolerating these defences - or they eat only plants with particular defences that they then coopt for their own defence (e.g. Termonia et al. 2001 for chrysomelid leaf beetles). Plant tissues are, however, for the most part rather nutrient-poor, and plant cell walls are made up of the rather indigestible cellulose and still more indigestible lignin (cellulose digestion in termites occurs via their association with protozoa). However, many insects and some other arthropods are able to break down cellulose walls independent of any mutualistic association with microorganisms, and this has implications for the evolution of land plants and their associated insects (Calderón-Cortés et al. 2012 for a summary of the literature).

What attracts an egg-depositing insect to one plant and prevents it laying eggs on another is often some aspect of plant chemistry (see Bernays & Chapman 1995 and Fernandez & Hilker 2007 [Chrysomelidae] for host plant selection). In general, more related plants do have more similar animals eating them (Weiblen et al. 2006; Futuyma & Agrawal 2009 for literature), simply because they will tend to taste similarly. In any one local area, related plants may show greater than expected diversity of traits involved in herbivore defence (e.g. Becerra 2007; Becerra et al. 2009; Kursar et al. 2009). Some herbivorous insects effectively track plant secondary metabolites and are found on whatever plant has a particular metabolite, independent of the phylogeny of the plant groups concerned (e.g. Winkler et al. 2009); glucosinolates and some alkaloids are examples. Glucosinolates are found in both Putranjivaceae (Malpighiales) and Brassicales, as are the pierid butterflies that are attracted to glucosinolates, while swallowtail butterflies are found on Rutaceae and Lauraceae, for example, the two having similar alkaloids.

Herbivorous insects may sequester secondary metabolites from the plant in the larva and/or adult stages, ensuring some measure of protection by so doing; they often have warning colouration, i.e., they are aposematic. They may also use plant metabolites for pheromones to attract mates, or these metabolites may simply act as oviposition cues, not being otherwise utilised by the insect (Brower & Brower 1964 on butterflies; Nishida 2002 for a review). Protective metabolites may be found in latex, or they may be translocated via the vascular tissue, or there may be other specialised tissues involved. Herbivorous insects that eat plants with such defences may show distinctive vein-cutting behaviours which stop the supply of any protectants to the plant tissue and enable the insect to eat it (see e.g. Dussourd & Eisner 1987; McCloud et al. 1995; Becerra et al. 2001; Dussourd 2009).

Within herbivores, there is a general decrease in host specificity both in temperate and tropical regions that follows the sequence: granivores > leaf miners > fructivores > leaf chewers = sap suckers > wood eaters > root feeders (Novotny & Basset 2005). Specialization in weevil-plant associations is similar: fruit and seed > wood > root and stem eaters (McKenna et al. 2009). How insect larvae feed, i.e., whether they are internal feeders like stem borers and whether they can tolerate raphides, or latex, etc., may be more conserved than associations between larvae and particular groups of plants or other types of feeding behaviours (e.g. Powell 1980; Peigler 1986; Powell et al. 1999: associations with latex-containing plants; Konno 2011: chemistry; Farrell & Sequiera 2001; Lopez-Vaamonde et al. 2003, 2006). Phylogenetic conservatism may be greater in groups in which the adults tend to remain close to plants in which they grew up, as with beetles, compared to the situation where the adult may fly away, as in many lepidoptera (Berenbaum & Passoa 1999).

Extant angiosperms show a correlation between woodiness and tannin frequency and a negative correlation between tannins (generalized defence) and alkaloids and other secondary metabolites (specific defence). Plants that were obvious or apparent to herbivores had generalized defences, while less apparent plants were more short-lived and had specific defences (e.g. Feeney 1976; Silvertown & Dodd 1996; see also Levin 1976; Mole 1993). (Insects that were specialized on their hosts ate the first group, generalized insects the second, and also the first - Endara & Coley 2010.) Similarly, "quantitative" defences are more generalised, polyphenolics and the like, and butterflies like Lycaenidae are the herbivores, while "qualitative" defences are highly toxic and butterflies like Nymphalidae are specialized herbivores (Fiedler 1996). Plants that were not apparent would need defences only against generalist herbivores (Endara & Coley 2010).

However, the nature and amount of the defensive compounds produced can also be explained, and perhaps more satifactorily, by the resource availability hypothesis, in which herbivore defence is thought of from a cost:benefit point of view (Endara & Coley 2010 for a summary). In particular, the growth rate of the plant affects the nature and amount of defences laid down, fast-growing plants needing less in the way of defence since their leaves are short-lived and would soon be replaced even if they had not been eaten (Endara & Coley 2010). Deciduous plants in general, with their rather thin leaves, will tend to be eaten by insects more than plants with long-lived xeromorphic leaves (e.g. Coley & Barone 1996; Arnold et al. 2001; Wilf et al. 2001; Lewinsohn et al. 2005). Defences are often linked with low concentrations of available nutrients since growth rae is slow and the leaves are long lived (Coley et al. 1985; Endara & Coley 2010). Connected with such ideas is the observation that herbaceous light-demanding taxa are more often attacked by biotrophic fungi, fungi needing living plant tissue (therefore probably not loaded with toxic substances) to prosper, whereas woody taxa, and especially those growing in shaded conditions, were more likely to be infected by necrotrophic fungi, fungi which first kill plant tissue before digesting it (García-Guzmán & Heil 2013). Ali and Agrawal (2013) summarized the curent state of knowledge about the generalist/specialist paradigm, noting how little was really known about details of the herbivore:plant interaction.

There is much discussion about possible correlations between geography, species richness, herbivory and defensive metabolites. Herbivory is often supposed to be greater in tropical than in temperate forests, and defences should be disposed likewise (Adams et al. 2011 and references; see also Agrawal et al. 2012). Novotny et al. (2006) suggested that individual species of temperate and tropical plants (controlled for phylogenetic relationships) supported a similar number of insect species, but since there were many more species of plants in the tropics, there would be many more species of insects there. However, there may be other patterns of association (c.f. Novotny et al. 2007 and Dyer et al. 2007), and an analysis of the food plants of Californian butterflies showed plant and butterfly diversity to be at most weakly correlated, whether the caterpillars had broad or narrow host plant preferences (Hawkins & Porter 2002). Indeed, two recent comprehensive analyses suggest that both herbivory and allocation of resources to plant defences tend to be greater at higher latitudes away from the equator (Moles et al. 2011a, b), while Salazar and Marquis (2012) noted that although the diversity of herbivores on Piper increased towards the equator, the amount of herbivory did not (see also Moles 2013).

More generally, Menken et al. (2009) suggest a correlation between species numbers, host specificity and feeding habits in lepidoptera in particular: internal feeders tend to be small, have higher host specificty, and show relatively little diversification (but c.f. sawflies on Salix/Populus - Nyman et al. 2006), while external feeders tended to be larger, show less host specificity, and formed more speciose clades. The plesiomorphic condition in lepidoptera is small size and internal feeding, features of the basal jawed clades and the basal Glossata such as Eriocraniidae (Menken et al. 2009; Imada et al. 2011), and overall the change in host plant preferencs has been from specialist to generalist (Menken et al. 2009). Along similar lines, Nylin et al. (2014) thought that transient polyphagy in nymphalid butterflies facilitated host-plant shift and subsequent diversification of the butterly that shifted.

To sumarize: The impact of insect/plant associations on plant diversification is still poorly understood (Futuyma and Agrawal 2009: also other papers in Proc. National Acad. Sci. U.S.A. 106(43)). In addition, symbionts, particularly bacteria, of the insect may affect its interaction with the plant (Frago et al. 2012). In some cases, diversification of plants can be linked to the development of particular defences, but this does not happen in any simple fashion; the mechanism by which insect diversification increases when feeding on angiosperms is also unclear (Janz 2011). However, a recent idea is to apply the ideas of island biogeography to the problem. With cecidomyiid gallers, at least, if host species are closer, insect diversity may go up because it is easier to switch hosts, and if ranges of insects are large and the plants are structurally complex, diversity also increases; clade age has little to do with it (Joy & Crespi 2012; for age, c.f. Brändle & Brandl 2002 [in part]; Farrell & Mitter 1994). We need to know more about both the timing of diversification and patterns of phylogenetic relationships in both groups, and evidence for the former in particular is often lacking (de Vienne et al. 2013), worse, there is uncertainty in both areas; this is discused further below.

2B. Phytophagous Insects. Phytophagous insects make up at least one quarter of all described species, and over half the beetles (Janz et al. 2006; Farrell 1998: ca one third of beetles; Hunt et al. 2007), although there are also very species-rich beetle clades that are neither herbivores nor decomposers (e.g. Barraclough et al. 1998). For a comprehensive phylogeny of all beetles, see Hunt et al. (2007). Clades of phytophagous insects may be more speciose that their non-phytophagous sister groups, ectophagous clades more diverse than their endophagous sister taxa, and clades that eat angiosperms more speciose compared to those that eat other plants (Mitter et al. 1988; Winkler & Mitter 2008), although in the first case, at least, the asymmetry may not be significant (Hunt et al. 2007).

Weevils are a particularly diverse group with some 62,000 species described, but perhaps 220,000+ species altogether. McKenna et al. (2009) suggest that crown-group diversification of major angiosperm-associated weevil clades was underway by the Aptian 125-112 m.y.a., and there was a "massive diversification" as angiosperms became floristically common. "Basal" Curculionidae show strong associations with monocots, but there is little evidence that early monocots were either particularly abundant or ecologically successful (Crane et al. 1995; Friis et al. 2004; J. A. Doyle et al. 2008; c.f. McKenna et al. 2009). Bark beetles are weevils that are decomposers; they are less speciose in clades that returned to conifers. Scolytinae and Platypodinae include the ambrosia beetles; parental care is almost universal here, and the weevils make tunnels in the wood and are associated with the ambrosia fungi (Ophiostoma, Ceratocystis: Ophiostomatales, ascomycetes). This association has evolved about seven times in these and related weevils and is unreversed (e.g. Farrell et al. 2001; Jordal et al. 2011). Scolytinae, Cossoninae, and Platypodinae are the three major clades of wood-boring (endophagous) weevils, a habit that originated independently in the three (Haran et al. 2013).

Chrysomelidae or leaf beetles, including the bruchids or seed beetles, are another very speciose herbivorous clade. Their origin has been dated to (86-)79-73(-63) m.y.a., well after the origin of the angiosperms (e.g. Gómez-Zurita et al. 2007).

There are at least 150,000 species of butterflies and moths (Lepidoptera) (Roe et al. 2009 for a summary), and larvae of about two thirds of these are herbivores, most being mono- or oligophagous (Bernays & Chapman 1994). Relationships among major groups of ditrysian insects - ditrysia also include the majority of moths, both Macro- and Microlepidoptera - have been unclear (Mutanen et al. 2010). Macrolepidotera have been linked with the microlepidopteran Pyraloidea (Regier et al. 2009), while Cho et al. (2011 and literature; see also Regier et al. 2009; Mutanen et al. 2010; Kawahara & Breinholt 2014) suggest that butterflies and large moths are not sister groups. The butterfly clade also includes a small clade made up of the mostly night-flying Hedylidae, the American moth-butterflies. Relationships among butterflies s.l. may be [Papilionidae [[Hedylidae + Hesperidiidae] [Nymphalidae [Pieridae [Riodinidae + Lycaenidae]]]]], although the position of Pieridae is unclear (Heikkilä et al. 2011; Kawahara & Breinholt 2014: pierids not included). Large moths may not be sister to butterflies; Kawahara and Breinholt (2014) link the former with much smaller pyraloid and gelechioid moths, and it is the combined clade that is sister to butterflies. Grimaldi (1999) suggested that diversification of lepidopteran clades with probosces began in the mid- to upper Jurassic; Labandeira et al. (1997) suggested somewhat older dates.

There are over 4,000 species of aphids (Hemiptera-Aphididae) feeding on plant sap, and they tend to be monophagous; again, diversification was Late Cretaceous/early Tertiary (von Dohlen & Moran 2000). Psyllidae (jumping plant lice), also Hemiptera-Sternorrhyncha and with around 2,000 species, also tend to be very host-specific. Ants, almost 12,000 species, also seem to have diversified in the late Cretaceous-early Eocene, 75-50 m.y.a..

Another set of close associations between plant and insect results in distinctive galls (see Shorthouse & Rohfritsch 1992 and Redfern 2011 for good introductions). There are anywhere from (21,000-)132,930(-211,000) species of of galling insects, the estimates partly depending on the numbers of flowering plants accepted because of the specificity of many galler/plant associations (?ref). The dipteran gall midges (Cecidomyiidae-Cecidomyiinae, see Roksam 2005 for a phylogeny) are the largest group of galling insects comprising perhaps 25% of galling insects in North America (Abrahamson & Weiss 1997). They are worldwide in distribution, but they show no particular patterns of host associations (Yukawa & Rohfritsch 2005: but see below for geography). The hymenopteran gall wasps (Cynipidae) may comprise as many as 50% of gallers locally and are north temperate; they are almost entirely restricted to eudicots (Ronquist & Liljeblad 2001). Smaller groups of gallers include psyllids (jumping plant lice, hemipterans) which are particularly common in Australia and on Fabaceae, at least in the Neotropics (Fernandes & Price 1991; Crespi et al. 2004; Espiritó-Santo & Fernandes 2007; Raman et al. 2005) and a couple of hundred species of aphids, also hemipterans (Wool 2004; J. Chen et al. 2013 for the phylogeny of hormaraphidine gallers), and some other insects, including and a few Lepidoptera, are also gallers.

In general, gall-inducing insects are commonest on sclerophyllous plants growing on poor soils in warm climates between 25 and 45o N and S, or perhaps more generally in species-rich communities, whether dry or wet, but not necessarily in tropical climates (Price et al. 1998; Yukawa & Rohfritsch 2005; see Price et al. 1987 for galling in an adaptive context). Other organisms may be directly involved in the establishment of galls, such as fungi in cecidomyid ambrosia galls (Rohritsch 2009 and references). Here the fungus gets its nutrients from the plant and is eaten by the midge larvae; indeed, cecidomyids may originally have been fungivorous (Roksam 2005). A whole network of parasites, hyperparasites and predators is all more or less dependent on gall larvae (Redfern 2011; see also figs and fig wasps).

2C. Pollinating Insects. There is much debate over the nature and extent of flower-pollinator co-evolution, the existence of wide-ranging pollination syndromes versus sometimes quite local guilds (S. D. Johnson 2010), and what exactly pollinators might see and respond to (Waser et al. 1996; Chittka et al. 1999; Fenster et al. 2004; Waser & Ollerton 2006; Raguso 2008; Ollerton et al. 2009a); see also the papers in Ann. Bot. 113(2). 2014. Rodríguez et al. (2004) and Horridge (2009) discuss the bee's point of view, the former, thinking about monosymmetry in particular, the latter more generally. Another strand of the discussion is the idea that pollination is effected as the plant exploits pre-existing perceptual/sensory biases of the pollinator, whether in pollination by deception (e.g. Schaefer & Ruxton 2009; Moré et al. 2013), where benefits are one-sided, or more commonly when both plant and pollinator are benefited (e.g. Chittka 1996; Schaefer & Ruxton 2009, 2010; Schiestl 2010; Schiestl et al. 2010; Schiestl & Dötterl 2012; Shresthra et al. 2013). Some "pollinator"-plant relationships may even be best thought of as a kind of commensalism, some bees (for example) scavenging pollen from flowers that have already been successfully visited by other pollinators (Linsley et al. 1973; Roubik 1989). Finally, several quite small but successful groups of pollinators that pollinate many species of plants make it difficult to maintain that other than general co-evolution of plant and pollinator is occurring, or even that much evolution of the pollinator is occurring at all (see esp. Thompson 2009; Guimarães et al. 2011, also below).

For the evolution of butterflies and moths, see above.

The evolution of bees is of particular importance, given the close involvement of many of them with angiosperm pollination (for bees and pollen, see Westerkamp 1996; for an account of all bee groups, see Michener 2007). Apoidea includes the spheciform wasps, since bees evolved from within the wasps, a group that feeds their larvae with insects (e.g. B. R. Johnson et al. 2013). The basic phylogenetic structure within Anthophila/Apiformes, the clade that includes all bees, is [Dasypodainae [[Meganomiinae + Melittinae] [[Andrenidae [Halictidae [Stenotritidae + Colletidae]]] [Apidae + Megachilidae]]]] (Cardinal & Danforth 2013), thus the old mellitids, there represented by Dasypodainae and [Meganomiinae + Melittinae], are paraphyletic, although they are monophyletic in Hedtke et al. (2014). Recent suggestions are that the age of stem-group bees is some (182-)149(-119) m.y., in line with some revisions of ages for the origin of angiosperms, with crown-group Megachilidae, a major clade including the leaf-cutting bees, starting to diversify (154-)126(-100) m.y.a. (Litman et al. 2011). The age of crown-group bees is estimated at (132-)123(-113) m.y. (Cardinal & Danforth 2013), all bee families having diverged by the K/T boundary. Estimates for stem Apidae are some 135-120 m.y.a. (Grimaldi & Engel 2005), with their initial diversification occurring in the early- to mid-Cretaceous 112-100 m.y. in association with the evolution of angiosperms (Grimaldi 1999, see also Engel 2000; Michez et al. 2009, 2012: discussion of fossils purporting to be bees; Grimaldi & Engel 2005; Almeida & Danforth 2009; c.f. Renner & Schaefer 2010).

Within Apidae, the somewhat over 1,000 species of at least primitively eusocial corbiculate bees have the relationships [[Euglossini + Apini] [Meliponini + Bombini]] (Cameron 2004: morphology and behaviour-based trees conflict with those based on molecular data, the latter give the relationships above; also Cardinal et al. 2010; Cardinal & Danforth 2011; Danforth et al. 2013; Martins et al. 2014). Crown-group Apidae are dated to (95-)87(-78) m.y. (Cardinal & Danforth 2011). Corbiculate bees are estimated to be (89-)77(-66) m.y.o. (Martins et al. 2014, q.v. for other estimates). Within the corbiculate clade, the crown group of the stingless, rather speciose and highly eusocial meliponines is dated to (61-)58(-56) m.y. and (56-)51(-48) m.y., that of orchid bees (euglossines), (35-)28(-21) m.y. and (38-)26(-17) m.y., bumble bees (Bombini), (31-)21(-12) m.y. and (48-)26(-14) m.y., and of honey bees (30-)22(-16) m.y. and (29-)22(-17) m.y. (see Cardinal & Danforth 2011 and Martins et al. 2014 respectively); another estimate of crown group euglossine diversification is 42-27 m.y. (Ramírez et al. 2010).

These general relationships are consistent with the appearance of bees in the fossil record. The earliest fossil bee, perhaps sister to other Apoidea, was found in amber of Upper Albian (probably Early Cenomanian, (99.4-)98.8(-98.2) m.y. - Shi et al. 2012) from Burma (Poinar & Danforth 2006); it is also quite small, being ca 5 mm long, in line with the often rather small Cretaceous flowers. However, this insect may be some kind of predatory wasp (Ohl & Engel 2007). A fossil from Late Cretaceous (96-74 m.y.a.) New Jersey amber was assigned to the extant genus Trigona, a highly derived eusocial stingless bee (Apidae-Meliponini: Michener & Grimaldi 1988); both its age (now estimated at 70-65 m.y.) and its relationships - it is now placed in Cretotrigona, and is a crown or stem meliponine - have been re-evaluated (Engel 2000). Both Apidae and Megachilidae, derived long-tongued bees, are known from Baltic amber of Eocene age (Danforth et al. 2006 and references). Note that colour perception is not an apomorphy for bees (Chittka 1996).

3. Angiosperms and Fungi.

Mycorrhizae..Complicating any simple story about the evolution of mycorrhizal relationships is the fact that fungi are associated with the gametophytic generation in liverworts, hornworts and even pteridophytes, but with the sporophytic generation in seed plants (Desiró et al. 2013). In a number of basal clades mucoromycotes are the fungi associated with the gametophytes. Embryophytes and fungi established associations very early in the Silurian/Devonian (Selosse & Tacon 1998; Nebel et al. 2004). Both Mucoromycotina and Glomeromycota can form mycorrhizal associatons with gametophytes of the same species of hornworts (Desirò et al. 2013), in different groups of liverworts (e.g. Field et al. 2012, 2014), and from early vascular planrs of the Rhynie Chert (Strullu-Derrien et al. 2014). Mycoheterotrophic associations are also found in some gametophytes of free-sporing plants, especially lycophytes and ferns. However, mosses in particular - but not Takakia - usually lack mycorrhizal associations (Read et al. 2000; Kottke & Nebel 2005; Duckett et al. 2006b; Ligrone et al. 2007; Wickett & Goffinet 2008; Stenroos et al. 2010; Pressel et al. 2008, 2010).

Endogone-like fungi (Mucoromycotina) form mycorrhizae with some liverworts (Treubia, Haplomitrium), hornworts (e.g. Bidartondo et al. 2011; Field et al. 2014), and early vascular plants from the 407 m.y.o. Rhynie Chert (Strullu-Derrien et al. 2014). In liverworts, mucoromycete fungi are found in the thallus - Haplomitrium even lacks rhizoids entirely - although the relationship between plant and fungus seems to be one of mutualism (Field et al. 2014). Interestingly, the genome of the glomeromycote Rhizophagus irregularis has a number of similarities with those of Mucoromycotina (Tisserant et al. 2013). In general, the nature of the plant-fungus association in many non-seeding plants can be rather different from the classic ectomycorrhizal or vesicular arbuscular mycorrhizal associations, and all these early plant-fungus relationships are perhaps best called paramycorrhizal associations (Kenrick & Strullu-Derrien 2014).

The evolution and ecological significance of mycorrhizae have been widely discussed (see Malloch et al. 1980; papers in Allen 1992; Read et al. 2000; Landis et al. 2002; Egger & Hibbett 2004; Taylor et al. 2009; Field et al. 2014, etc.), as has the morphology of the plant/fungus interface (e.g. Peterson & Massicotte 2004; Peterson 2013 and references) and how the fungus uses the 10% or more of photosynthesate that it gets from the plant (Leake et al. 2004). However, given the depth that plant roots commonly grow and the sampling of studies on mycorrhizae, much of the rhizosphere remains very poorly understood from the point of view of general plant-fungal interactions (Pickles & Pither 2013: ectomycorrhizae in particular). Being mycorrhizal is not a simple either/or matter, and the one species of plant may have a variety of associations with fungi, although relatively few plants routinely form both ecto- and endomycorrhizal associations (Poole & Sylvia 1990; Molina et al. 1992 for some examples).

Aquatic plants, hardly surprisingly, often lack mycorrhizae (see Safir 1987 and Radhika & Rodrigues 2007 and references for records; de Marins et al. 2009), but the frequent absence of mycorrhizae in Caryophyllales, Proteales, etc., is somewhat surprising. Epiphytic taxa are not often mycorrhizal (Janos 1993; see other papers in Mycorrhiza 4(1). 1994; Desirò et al. 2013; Kato & Tsutsumi 2013), but c.f. Ericaceae and Orchidaceae at least (e.g. Kottke et al. 2008; Martos et al. 2012). Overall some 18% of flowering plants may lack mycorrhizae, and a further 12% are only facultatively mycorrhizal (Molina et al. 1992). For comprehensive surveys on mycorrhizal associations. see Brundrett (2008: updated online resource, 2009) and Akhmetzhanova et al. (2012) in particular.

For the economics of the exchange between the two partners - mostly sugars from the plant, but a greater variety of metabolites from the fungus, see Wyatt et al. (2014). Associations between plant and fungus/fungi can become very close. Myco-heterotrophic flowering plants, commonest in monocots, lack chlorophyll entirely and are very largely nutritionally dependent on the activities of their associated fungi; for the taxonomically scattered associations between glomeromycotes and myco-heterotrophic plants, from lycophytes to angiosperms, see Merckx et al. (2012). Myco-heterotrophic Ericaceae and Orchidaceae have modified ectomycorrhizal associations (e.g. Perotto et al. 2012).

Mycorrhizae often affect various aspects of root architecture such as root thicknesss, root branching, and the development of root hairs (Baylis 1975; Schweiger et al. 1995 and references), although any connection between root attributes and mycorrhizal status/response to mycorrhizal establishment is difficult to make (Maherali 2014). Benefits accruing to the partners may be similarly various (Newsham et al. 1995). The development of root hairs or of a vesicular arbuscular mycorrhizal association may be alternative ways for a plant to obtain phosphorus when it is in short supply (Schweiger et al. 1995 and references). Other distinctive root morphologies like dauciform roots, roots appearing carrot-shaped because they are densely covered by long root hairs, are responses of the plant to nutrient-poor conditions (e.g. Schweiger et al. 1995; Playsted et al. 2006; Gao & Yang 2010).

Endomycorrhizae or vesicular-arbuscular mycorrhizae (VAM) are very widespread. They are found in about 70% of seed plants, 80% of all land plant species, 92% of plant families (Blackwell 2011). Just how many times VAM associations evolved in land plants is unclear; obviously, it depends in part on the very definition of mycorrhizae (see below)! Mycorrhizae have not often been found in fossil gymnosperms, but have recently been reported from Upper Permian Glossopteris (Harper et al. 2013).

Glomeromycota are usually the fungi involved in VAM associations (Schüßler et al. 2001), but see above. Their hyphae are aseptate and intracellular, often forming vesicles or branching structures (the arbuscules) within the cells. There is substantial variation both in the morphological details of the fungus-plant association (e.g. Smith & Smith 1997; Peterson & Massicotte 2004) and in the proportion of fungal biomass inside and outside the plant, which depends on the group of Glomeromycota involved (Maherali & Klironomos 2007). Sexual reproduction in Glomeromycota seems to be very uncommon. The spores are multinucleate, the nuclei in any one spore not having any immediate common ancestor, so the unit of selection may be the individual nucleus (Jany & Pawlowska 2010). Hyphae from different mycelia can fuse, making the nuclear mix yet more complex (Giovannetti et al. 2004). However, Rhizophagus irregularis, which has been studied in some detail, has a number of genes involved in sexual reproduction, so how glomeromycetes reproduce is an open question (Tisserant et al. 2013 and references).

Some 290 species of Glomeromycota have so far been described (Öpik et al. 2010; Merckx et al. 2012), and all form VAM. Recent surveys suggest both that the dispersal of the fungi may be limited, partly because their spores are relatively large and not dispersed by wind (Tedersoo et al. 2014b), and also that the diversity of Glomeromycota has been considerably underestimated, but even if there are 1,000 or even many more species (Kivlin et al. 2011; see also Pickles & Pither 2013 for cautionary comments), that is still far fewer than the probably 200,000 species or so of plants colonized (Rinaldi et al. 2008). There is some evidence for host specificity or at least host preferences of the fungus (Gosling et al. 2013), while Wenner et al. (2014) found that related species (same genus, subfamily) of Asteraceae tended to be most similar in their associated fungi (here Glomeromycota were in a minority). Many plants form associations with several species of fungus, ecological specialists and generalists forming associations with different fungi (Öpik et al. 2009, 2010). A single plant can form different associations sequentially (van der Heijden et al. 2006) or unrelated species of plants may be colonized by the one fungus (Kottke et al. 2008; Walder et al. 2012). Overall, the diversity of VAM fungi was not correlated with the that of its hosts (Tedersoo et al. 2014b).

In VAM associations, nutrient uptake by the plant - especially of phosphorus, although recent work adds nitrogen - is increased, and water uptake is improved (Read 1991; Allen 1992; Govindarajulu et al. 2005; Leigh et al. 2009 and references; Tian et al. 2010; Bonfante & Genre 2010); Gosling et al. (2013) found that the diversity, but often not colonization rate, of VAM fungi was affected by the concentration of soil phosporous. VAM fungi obtain at least carbohydrates from the plant (Helber et al. 2011; see also Walder et al. 2012), and Tisserant et al. (2013) noted that the colonization of plants by VAM might result in a 20% net increase in photosynthesis (Kaschuk et al. 2009: crop - Fabaceae - systems). Indeed, glomeromycetes seem to be unable to break down and utilize complex biopolymers (Tisserant et al. 2013). VAM also have substantial beneficial effects on soil structure (Taylor et al. 2009), improving drainage, and hence weathering, and also playing an important role in phosphorus uptake by scavenging for it more efficiently (S. E. Smith et al. 2011). Maherali & Klironomos (2007) found that ecosystem functioning was improved if all three major types of Glomerophycota were in the one community. However, since a single fungus individual can be associated with more than one plant, and because hyphae from different individuals may fuse, a potentially quite large number of plants from the same or different species may be put in indirect contact with each other (Giovannetti et al. 2004), and so it becomes a very complex calculation to estimate the costs and benefits accruing to the parties involved (Walder et al. 2012). How changing carbon dioxide concentrations in the atmosphere might affect the soil carbon storage activities of VAM is unclear (Verbruggen et al. 2012 and references).

Although few details of the establishment of VAM interactions are known (Whitfield 2007), a number of the genes involved are the same as those involved in establishment of nodulation in the nitrogen-fixing clade (e.g. Maillet et al. 2010 and references, also the Fabales page). The invasion of plant tissue by the fungus may be similar to the establishment of parasitism (Bonfante & Genre 2010). Initial attraction of the fungus to the plant, and also hyphal branching, is mediated by strigolactones secreted by the root (Akiyama 2010 and references). These strigolactones may initially have been involved in rhizoid elongation in the gametophyte (Delaux et al. 2012).

The VAM association is probably of very long standing, and may even be a feature of the common ancestor of all land plants (see also Baylis 1975; Redecker et al. 2000b; Kottke & Nebel 2005; Duckett et al. 2006b; Ligrone et al. 2007; Parniske 2008; B. Wang et al. 2010), or at least of a major subset of vascular plants. However, just how many times VAM associations evolved in land plants is unclear.

Ectomycorrhizae grow on many fewer species of plants. Estimates vary: 2,500-3,000 species (Smith & Read 2008), 5,600 species of angiosperms + 285 species of gymnosperms (Brundrett 2009), or ca 8,000 species (Rinaldi et al. 2008: gymnosperms included). There is a strong phylogenetic signal in the plants that form ECM associations (e.g. Alexander & Lee 2005), and this is discussed below. ECM seed plants are generally woody, although there are some herbaceous taxa, perhaps particularly in Arctic-Alpine environments (e.g. Newsham et al. 2009). Basidiomycetes are frequent ECM associates, but Pezizales and other ascomycetes like the widespread Geococcum are also quite common and Zygomycota are also involved.

Many more species of fungi are involved in ECM than in VAM associations. Conservative estimates are 7,750 species of fungi, and although the figure may be as high as 20,000-25,000 (Rinaldi et al. 2008; Tedersoo et al. 2012), Tedersoo et al. (2014b) suggest caution in estimating funbgal richness. Pickles and Pither (2013) discuss the need to sample throughout the soil column, but Anderson et al. (2013) found that mycelium frequency decreased with depth. In both temperate and tropical ECM communities the fungi involved are often quite widespread, tropical lowland ECM associations being as diverse as those in more temperate climates (Henkel et al. 2012: Dicymbe-Fabaceae; Brearley 2012: Dipterocarpaceae). Generally there is little host specificity, but in some communities, for example, those in the tropics where ECM plants are uncommon, ECM fungus host specificity may be quite high (Timling & Taylor 2012; M. E. Smith et al. 2013 and references). Furthermore, Tedersoo et al. (2013: Salicaceae) found that phylogenetic relationships of the host had a strong effect on ECM richness and community composition (see also Pölme et al. 2013).

Overall, temperate and boreal areas have the highest ECM fungal diversity, and its is there that their associated plants dominate (Wardle & Lindahl 2014; Tedersoo et al. 2014b), and other groups of soil-dwelling organisms show a similar pattern, perhaps connected with the substantial vertical stratification of soils in ECM-dominated communities (Tedersoo et al. 2012). African and Malagasy ECM woodlands showed relatively less diversity, the same ECM fungi being found on unrelated species and at different successional stages (Tedersoo et al. 2011). Of course, until the advent of molecular methods, identification of the fungi depended on their being cultivable and undergoing sexual reproduction, and although Sebacinales can now be identified using molecular data, some remain unculturable (Tedersoo et al. 2010b).

In Boletales, at least, ECM associations may have evolved in the ecological context of soils low in nitrogen (and high in organic material) as the result of activities of brown rot fungi, a number of which are also Boletales (and other fungi: Eastwood et al. 2011).

There is probably an evolutionary sequence, white rot fungi → brown rot fungi → ECM, with development of ECM associations in Boletales, at least, being favoured by the ecological conditions (e.g. low nitrogen) that result from the activities of brown rot fungi a number of which are also Boletales (and other fungi: Eastwood et al. 2011; see also Floudas et al. 2012). Hibbett et al. (2000) suggested that white-rot fungi might also be derived from within ECM clades. White rot and brown rot fungi, both lignin decomposers, although the former are more efficient, are widely scattered through Agaricomycota (Eastwood et al. 2011).

For a survey of ECM-plant relations, see Itoo and Reshi (2013). ECM hyphae form a complete sheath investing the rootlets and a Hartig net of hyphae penetrating between the exodermal/cortical cells, indeed, the fungal sheath forms the interface between the plant and the soil, not the root itself (e.g. Taylor et al. 2009). The fungal hyphae are septate and are not intracellular except in Ericaceae and Orchidaceae. Usually the Hartig net involves simply the outermost layer of cells, but sometimes, as in Pinaceae, the hyphae penetrate more deeply (Brundrett 2004). There are other ECM variants, such as tuberculate mycorrhizae, clusters of roots surrounded by hyphae (Smith & Pfister 2009). ECM help in the aquisition of nitrogen and phosporous by the plant, obtaining them from material as diverse as pollen, from dead nematodes by breaking down chitin, and from the weathering of rocks (e.g. L. L. Taylor et al. 2009, 2011; Averill et al. 2014); nitrogen can be transferred to the plant in an organic form, e.g. as glutamine (Alexander 1989; Newbery et al. 1997; Michelsen et al. 1998; Read & Perez-Moreno 2003; Cairney & Meharg 2003; Lindahl & Taylor 2004; Martin & Nehls 2010; Bonfante & Genre 2010; but c.f. Persson & Näsholm 2001: common in plants in vitro). ECM fungi may retain nitrogen in their mycelium, perhaps especially when the supply of photosynthesate from the plant is high, and the result is soil with very low N concentrations that is unfavourable for the growth of non-ECM plants (Näsholm et al. 2013).

VAM associations were not found beyond 74o N in the Canadian Arctic (Olsson et al. 2004) and were very uncommon just below the Artic Circle in Alaska, contrasting strongly with the diversity of other ecological groupings of fungi, although the disparity in numbers of clones was somewhat less (Taylor et al. 2013). Indeed, more recent work suggests that VAM are found to 820 N while ECM and ERM are found to only 790 N, being limited by the ranges of their mostly woody hosts (Newsham et al. 2009). Recent work suggests that the diversity of ECM fungi increases in mid to high northern latitudes and ERM fungi also show a diversity increase towards the poles, in both cases consistent with the distribution of their seed plant associates (Wardle & Lindahl 2014; Tedersoo et al. 2014b).

At least some ECM fungi are very similar to or identical with ericoid mycorrhizal fungi (ERM); both can be more or less saprotrophic and take up nitrogen in an organic form (e.g. Michelsen et al. 1996; Jonasson & Michelsen 1996; Hashimoto et al. 2012). Consistent with this idea, Vrålstad et al. (2002) and others have found fungal isolates from ECM and ERM plants, and also from those with dark septate endophytes, to be more or less intermixed on phylogenetic trees and showing little phylogenetic divergence (see also Perotto et al. 2012). Consequently, Vrålstad (2004; see also Brundrett 2004) suggested that ECM and ERM formed a single ecological guild, one of whose characteristics is the uptake of organic nitrogen by the plant (c.f. in part Lindahl et al. 2002: opposition between decomposer and mycorrhizal fungi; Talbot et al. 2008: VAM; Inselbacher et al. 2012). Most ERM are dominated by ascomycetes (Read 1996; Tedersoo et al. 2006: hypogeous fungi are derived from ascomycete ECM fungi), and Leotiomycete fungi, ascomycetes that are commonly ERM, become more diverse towards the poles and of course their ericaceous associates are also common there (Wardle & Lindahl 2014; Tedersoo et al. 2014b). Although basidiomycetes of the Sebacinales-B group may form associations with both Ericaceae and Orchidaceae, different species are involved (Setaro et al. 2012).

Not only are mycorrhizal fungi not necessarily restricted to a single species of plant and a single species of plant can form more than one kind of mycorrhiza, but individual mycorrhizae may form simultaneous associations with more than one plant, and quite commonly with more than one species of plant. McGuire (2007b) described the ECM network in Dicymbe forests in Guyana, and this was established even as the seed germinated. Villareal-Ruiz et al. (2004) persuaded a single fungal mycelium to form an ECM with Pinus sylvestris and an ERM with Vaccinium myrtillus at the same time. The fungal associates of Arbutus menziesii (Ericaceae-Arbutoideae), from Pacific North America and with arbutoid mycorrhizae, are diverse and occur on other angiosperms growing in the same area, and in particular on ECM Pseudotsuga (Pinaceae) (Kennedy et al. 2012), and similar lability has been shown by the ascomycete Rhizoscyphus ericae, often an ERM on the hair roots of north temperate Ericaceae, and ECM on Pinus growing together with these Ericaceae (Grelet et al. 2010; see also Villarreal-Ruiz et al. 2004). Mycorrhizal woodlands and savannas of Africa and Madagascar are noted both for the relative uniformity of their mycorrhizal fungi and the fact that one species of fungus can form associations with species of plants in different families and at different successional stages of the vegetation (Tedersoo et al. 2011).

The result is the formation of complex mycorrhizal networks (e.g. Villareal-Ruiz et al. 2004; Simard & Durall 2004; Selosse et al. 2007b; Kennedy et al. 2012). Weiß et al. (2011) found the same nuclear LSU sequences of basidiomycetous Sebacinales in taxonomically unrelated plants growing in different areas, sometimes the association was mycorrhizal, sometimes endophytic, and they suggested that Sebacinales might play an important role in ecosystem integration. All kinds of land plants may be involved. Liverwort gametophytes can form associations with fungi that are also ECM on the flowering plant on which the liverwort is found. Examples include Marchantia/mycorrhizal fungus/Podocarpus and the myco-heterotrophic chlorophyll-less Cryptothallus/the basidiomycete Tulasnella/Pinus-Betula (Read et al. 2000; Bidartondo et al. 2003; Kottke & Nebel 2005 and references). Rhizoscyphus ericae also forms mycorrhizal associations with Jungermanniales-Schistochilaceae, leafy liverworts (Pressel et al. 2008).

Interestingly, extant forests made up of VAM trees tend to be more diverse than forests with ECM trees (Malloch et al. 1980; McGuire 2007a), and there are rather few angiosperms in ECM-dominated communities in temperate and in particular boreal areas (see below). Laliberté et al. (2013) discuss the diversity of vegetation associated with ECM in terms of the youth of the soils; tropical soils are older, more strongly weathered. However, tropical ECM dipterocarp-dominated forests are as diverse as tropical forests anywhere, and ECM heathlands in southwest Australia, for instance, are also diverse (Read 1991, 1996; Page et al. 2012). The overall relationship between numbers of species of plants and of fungi in ECM-dominated communities is opposite to that in both VAM associations and also the modified ECM associations in Ericaceae (ERM). Even if there are 1,000 or even many more species of Glomeromycota (Kivlin et al. 2011; Pickles & Pither 2013), they colonize 200,000 species or so of plants (Rinaldi et al. 2008). Estimates of numbers of species of ECM fungi range from 7,750 (conservative) to 20,000-25,000 (Rinaldi et al. 2008; Tedersoo et al. 2012); numbers of species of ECM seed plants are arond 8,000 (Rinaldi et al. 2008: including ERM species, excluding Orchidaceae).

Endophytic fungi, fungi growing inside plants, have been placed in four groups. Class one endophytes are ascomycete clavicipitaceous fungi and occur in grasses with which they form very close associations (e.g. Schardl 2010). Class two endophytes pervade all the tissues of the plant; the fungi involved are not particularly speciose. Class three endophytes are restricted to shoots and are very diverse. Class four endophytes, dark septate endophytes, are restricted to roots (Rodriguez et al. 2009). Transmission of endophytes may occur via the seed (vertical transmission), as is common in class one endophytes in particular, or via fungal spores (horizontal transmission), more common in other endophytic associations (Arnold 2008).

Endophytic fungi are likely to be found in all seed plants (Rodriguez et al. 2009; Hoffman & Arnold 2010; Friesen et al. 2011), perhaps particularly in Poaceae and Ericaceae (e.g. Petrini 1986, other papers in Fokkema & van den Heuvel 1986; Saikkonen et al. 2004). The number of species of endophytic fungi is likely to be very large. Thus Arnold et al. (2001) found 418 morphospecies of class three endophytes in only 83 leaves of two species of tropical trees, Ouratea (Ochnaceae) and Heisteria (Erythropalaceae) (see also Bills & Polishook 1994; Frohlich & Hyde 1999; Arnold & Lutzoni 2007 and other articles in Ecology 88[3]. 2007). Gazis et al. (2012) even described a new class of ascomycete fungi based on endophytes growing in the sapwood of Peruvian Hevea. Note that the "fine endophytes" described as growing in the roots of some Arctic plants (Newsham et al. 2009) are considered to be VAM.

Most endophytes are Ascomycota. Fungi living inside lichens, endolichenic fungi may be phylogenetically close to these endophytic clades; these are different from the mycobionts whose association with algae constitutes the lichen thallus (Arnold et al. 2009b). Other fungal groups are involved. Sebacinales (basidiomycetes) are particularly diverse ecologically and are common endophytes (Weiß et al. 2009) as well as producing the distinctive modified ECM of Ericaceae and Orchidaceae. Trichoderma has different kinds of associations with plants, and endophytes may become saprotrophic or mycoparasitic on the death of the host plant (Chaverri & Samuels 2013). Grass endophytes are perhaps derived from fungi that are insect pathogens, and some species of fungi are both pathogen and endophyte (Spatafora et al. 2007; Sasan & Bidochka 2012), and endophytic fungi are often more related to pathogens and other endophytes than to saprotrophic fungi (U'Ren et al. 2009). Endophytic fungi are also at least sometimes derived from necrotrophic fungi, parasitic fungi that first kill the host cell before digesting it (Delaye et al. 2013; García-Guzmán & Heil 2013).

In other than class one endophytes, details of what the fungi are doing, let alone of any advantages accruing to the parties involved, are poorly understood (e.g. see Jumpponen 2001: dark septate endophytes; Jumpponen & Jones 2009: phyllosphere; Rodriguez et al. 2009: summary; Chaverri & Samuels 2013: Trichoderma). Fungi may affect seed germination and survival (U'Ren et al. 2009), and endophytic associations are probably at least intermittently mutualistic (Carroll 1988, 1995); they may often be involved in facilitating stress tolerance in plants (Rodriguez & Redman 2008). Movement of nitrogen from caterpillars with the ubiquitous insect pathogen Metarhizium (related to grass class 1 endophytes) to switch grass (Panicum virgatum, so not Poöideae) and a bean (Phaseolus vulgaris, Fabaceae-Faboideae), plants in which the fungus is also an endophyte, has been demonstrated (Behie et al. 2012). Van Bael et al. (2009) found that leaf-cutting ants seemed to dislike plants with numerous endophytes (nitrogen-fixing bacteria, esp. Klebsiella, are also an integral part of this system - Pinto-Tómas et al. 2009). Endophytic fungi have also been implicated in the protection of the host plant against fungal pathogens (Martin et al. 2012: in vitro; Raghavendra & Newcombe 2013). Dark septate endophytes may be involved in the uptake of nitrogen (Newsham et al. 2009; Newsham 2011).

Further Complexities. Associations between plants and fungi are ubiquitous. There are several characteristic "plant" metabolites such as indolizidine (swainsonine) and ergoline alkaloids that are synthesized by fungal or bacterial associates of the plant; these are toxic to animals and presumably protect the plant (e.g. Popay & Rowan 1994; Gunatilaka 2006; Markert et al. 2008: Convolvulaceae; Pryor et al. 2009: Fabaceae; Wink 2008); Celastraceae and especially Poaceae are also distinctive in this regard. Endophytes of Picea (spruce) produce several metabolites toxic to the eastern spruce budworm (Findlay et al. 2003; Sumarah et al. 2010). Such compounds behave as if they were endogenous plant metabolites (Zhang et al. 2009; Friesen et al. 2011). Of course, "true" secondary metabolites like terpenoids and quinolizidine alkaloids are produced more or less exclusively in mitochondria and/or chloroplasts - i.e. in a bacterial endophyte whose association with the plant is of very long standing (Wink 2008).

From what has been said above, it is clear that sharp distinctions between different types of fungal associations can be hard to draw (Gao & Yang 2010; esp. Vrålstad 2004; Perotto et al. 2012; Peterson 2012), and the line between mutualism - or at least prolonged symbiosis - and parasitism is a fine one (Eaton et al. 2010 and references). Fungi and plants interact in yet other situations, for example, several hundred species of fungi have been found in the phyllosphere, the above-ground surface of the plant, of the temperate Quercus macrocarpa (Jumpponen & Jones 2009).

Fungi associated with plants may have endosymbionts themselves. Mycorrhiza-plant associations often include bacteria as additional partners, whether growing on the surface of the mycelium and synthesising crucial metabolites or living within the hyphae; bacteria are involved both in the establishment and the functioning of ectomycorrhizae (Frey-Klett et al. 2007). Thus the bacterium Candidatus Glomeribacter gigasporarum (near Burkholderia) is found in the VAM fungus Glomus (Castillo & Pawlowska 2009, 2010; Bonfante & Genre 2010). Such bacteria can affect the growth of the fungi, and they may be vertically transmitted like the fungi themselves (Bianciotto et al. 2003; Hoffman & Arnold 2009). Numerous bacteria (mostly Proteobacteria) and a diversity of fungi are known to be involved, although the relationship sometimes seems to be rather casual (Hoffman & Arnold 2010). However, bacteria can be integral to ECM associations, whether facilitating the establishment of the association (mycorrhiza helpers) or as integral to its subsequent functioning (Frey-Klett et al. 2007 and references); they have also been implicated in fixing nitrogen (Paul et al. 2007). Even viruses in endophytes may affect the ability of the host plant to grow in particular conditions (Márquez et al. 2007).

Organisms other than fungi are endophytes, most notably, plants may have a variety of endophytic bacteria. Obvious examples here are nitrogen-fixing bacteria (see the N-fixing clade), but a variety of other bacteria are involved as are plants other than members of the N-fixing clade (e.g. Hardoim et al. 2008; Lemaire et al. 2011b). As with fungi, the line between parasite and pathogen is not sharp, and bacteria may move from e.g. hemipterans associated with plants to the plants themselves (Caspi-Fluger & Zchori-Fein 2010). Bacteria, like fungi, are also found in the phyllosphere, some 7,300 bacterial OTUs being found on 57 species (ca 420 OTUs/tree) from Barro Colorado Island, Panama, and the estimate of bacterial OTUs from that island alone was some 11,615 species (Kembel et al. 2014: use of current phylogeny does not affect results - S. W. Kembel pers. comm. xi.2014). Some of these bacteria are known to affect the growth of the plant, whether by fixing nitrogen, detering pathogens, or the like (Kembel et al. 2014 for references).

The net result of all these associations is that plants are microcosms or some kind of complex chimaeras, as Herre et al. (2005) noted, referring to tropical plants and their endophytic fungi in particular.

4. Evolution in stem group angiosperms. (This section needs lots of work.)

The angiosperm stem group diverged from other seed plants (origin 1 above) by the late Paleozoic (Moldowan et al. 1994; E. L. Taylor et al. 2006). Candidates for fossil relatives of stem-group angiosperms include Corystospermales (Pteruchus, Ktalenia, etc.: Frohlich & Parker 2000), Bennettitales, and Caytoniales (poorly known in the younger Mesozoic). Other pteridosperm groups that have been linked with angiosperms are Pentoxylon and glossopterids, and at least some of the latter had multiflagellate male gametes (Nishida et al. 2004: Soltis et al. 2008 for some references). And if crown-group angiosperms are 270 to 175 m.y.o. (see below), then we may need to think about a different set of gymnosperm/pteridosperm reproductive structures when thinking of the evolution of the angiosperm flower that if crown-group angiosperms are Cretaceous in origin.

A phylogenetic association between Cycadeoids or Bennettitales - "fossil beehives" - and angiosperms has long been mooted (see also Doyle 2006 and Hilton & Bateman 2006 for cladistic analyses and literature). Interestingly, the triterpenoid oleanane, found pretty much throughout angiosperms, also occurs in Bennettitales (Moldowan et al. 1994; E. L. Taylor et al. 2006). Seed morphology and anatomy in particular, but also pollen morphology, suggest that Bennettitales, Erdmanithecales, and Gnetales should be placed together in the BEG group; Erdmanithecales persisted into the Late Cretaceous and Gnetales are still extant (Friis et al. 2007, 2009a: four new genera in this complex, 2013; Mendes et al. 2010). Some sort of relationship between Gnetales and angiosperms has long been suggested (see below). The BEG group has radiospermic ovules that lack a cupule, a vascularized nucellus but not a vascularized integument, and seeds with an outer sarcotesta, a sclerotesta, and a layer inside that (Rothwell & Stockey 2002). Morphological phylogenetic analyses often suggest a connection between the "flower" of Bennettitales and those of angiosperms (Rothwell et al. 2008a, 2009; Crepet & Stevenson 2009, esp. 2010), but c.f. relationships among angiosperms, and the tree topology is sensitive to change of one character state in one taxon. Indeed, in some morphological analyses Bennettitales do not group with the anthophytes and are associated with cycadofilicalean plants, extant gymnosperms are also not monophyletic, and Gnetales are sister to angiosperms (Crepet & Stevenson 2009, 2010).

The envelopment of the seed to produce a fruit-like structure must have happened independently in the Bennettitales and angiosperms (Rothwell & Stockey 2010). Furthermore, the reproductive morphologies of some of the early (Upper Triassic) Bennettitales are rather different from those of later fossils (e.g. Pott et al. 2010), and the interpretation of the complex reproductive structures of the group is not easy (see Crane & Herendeen 2009 for careful analyses). Rothwell et al. (2009) and Rothwell and Stockey (2013) strongly questioned the idea of a close relationship between Bennettitales and Gnetales, noting i.a. that the former had spiral, not decussate, insertion of parts, the nucellus formed a plug in the micropyle, and there was no pollen chamber. Gnetaceae & co. themselves are far from having a flower, and the consensus of molecular studies is that they are best placed sister to or inside Pinales (see below). Overall, the BEG clade seems to have little to do with angiosperm origins.

The challenge is to think of how the heterosporangiate strobilus with short internodes that is the angiosperm flower might have evolved from the separate male and female strobili of most gymnosperms. X. Wang et al. (2007; X. Wang 2009, 2010b) thought that the early to mid Jurassic Schmeissneria, previously placed in Ginkgoales, was angiospermous, having closed carpels. Another mid-Jurassic fossil, Xingxueanthus, also is supposed to have had closed carpels as well as a style (Wang & Wang 2010). X. Wang and Wang (2010) toyed with the idea that angiospermy may have arisen more than once and considered these plants to be stem-group angiosperms; see also Wang (2009) for pre-Cretaceous angiosperm diversification and extinction. X. Wang (2010a) provided detailed descriptions of other possible pre-Cretaceous angiosperms; carpels may consist of an axis (= placentae) subtended by bracts (= carpel walls: see also Guo et al. 2103; Liu & Ni 2013).

Rudall and Bateman (2010) suggested that the morphology of crown group conifers, being highly derived, might be of little help in thinking about that of the ancestors of angiosperms. This turns the problem over to the interpretation of fossil remains, and here there has been little progress over the last forty years or more. Similarities between the ovules of some Magnoliaceae and the cupules of Caytonia (e.g. Umeda et al. 1994) are probably superficial; features like the lobing of the integuments which induced this comparison seem to have little significance, certainly there is no suggestion that the two integuments of angiosperm ovules are of fundamentally different natures (e.g. Endress & Igersheim 2000; Endress 2005c). The ovule-bearing structures of Caytonia can be linked with the carpels of extant angiosperms by invoking appropriate morphological gymnastics (Doyle 2006 for literature, also Doyle 2008b; Doyle & Donoghue 1986a, b, 1992; Doyle & Endress 2010; etc.), but it does not make for satisfactory reading. In a comprehensive review on the bearing of fossil data on the origin of the flower, Doyle (2008b, see also Taylor & Taylor 2009) concluded that our understanding of the fossil record was insufficient to help much in understanding angiosperm origins.

Thinking about morphology in the context of what is known about development affects how one interprets fossils. Baum and Hileman (2006) proposed a developmental genetic model for the evolution of the flower which may help in the interpretation in the significance of particular fossils, and this and other models are summarized by Bateman et al. (2011b). Frohlich and Parker (2000) suggested that the heterosporangiate strobilus evolved in pteridosperms like Corystospermales from a male strobilus on which ectopic ovules developed - their "mostly male" theory of the origin of angiosperm flowers. LEAFY/FLORICAULA genes were likely to be associated with male reproductive structures, they suggested, and NEEDLY genes with female. However, work on the expression of LFY/FLO and NLY orthologs suggest that both genes are expressed in early-stage primordia, but the former are then expressed in ovules and microsporangia while the latter are expressed in the ovuliferous scale, aril, microsporophylls, etc. The expression of both genes in both male and female cones is not consistent with the "mostly male" theory (Vásquez-Lobo et al. 2007 and references; Moyroud et al. 2010; Tavares et al. 2010; see also Bateman et al. 2011b). Mathews and Kramer (2012; c.f. Kelley & Gassner 2009 for a more conventional approach) analyse ovule development in seed plants and floral development in angiosperms to think how these structures might have evolved; i.a. they suggest that evolution is less the change in form of pre-existing structures than the assemblage of new developmental modules in the context of homeosis, heterotopy, and heterochrony.

Chanderbali et al. (2010) found that genes involved in microsporangium, etc., production in at least some gymnosperms are also expressed in the perianth of angiosperms; only a few genes involved in ovular expression are also expressed there. S. Kim et al. (2004b) age the split that gave rise to the paleo AP3 and PI genes to around (297-)290-230(-213) m.y., well before the origin of crown angiosperms. Jiao et al. (2011) suggested that there was a whole genome duplication in these stem group plants - estimates of peak ages are (245-)236, 234(-225) m.y.a., the first half of the Triassic, although the overall spread of ages is 275-150 m.y., which gives the imagination pretty free rein. For other studies plotting the evolution of genes involved in floral morphology and development, see the Amborella Working Group (2013) - some 70% of the genes involved were present in the most recent common ancestor of extant seed plants, others are still older, There have indeed been dramatic changes in the expressions of some genes during land plant evolution (e.g. Banks et al. 2011), but where on the tree these changes occurred is unknown. Thus Szövényi et al. (2010: ca 30% of the genome mapped) noted that a total of only ca 5% of the genes in Funaria hygrometrica were expressed uniquely in the sporophytic and gametophytic generations, but in Arabidopsis ca 5% of the genes were differentially expressed in the gametophyte alone and ca 25% in the sporophyte alone. Gene expression in neither bryophyte generation was like that in the Arabidopsis gametophytes, but where in the tree between Funaria and Arabidopsis this shift might have taken place is unknown. For other such studies, see Lang et al. (2010) and Zhu et al. (2012).

Nearly all extant angiosperms are distinctive because of their hierarchical-reticulate venation, while that of many fossil seed plants and monilophytes is not hierarchical and is dendritic (open), often dichotomizing. Roth-Nebelsick et al. (2001) thought that the reticulate venation in seed ferns like Glossopteridales and Giganopteridales might be linked with the development of a drier climate; some of the latter group may even have leaves with a quasi-hierarchical organization.

To summarise: ideas of relationships between angiosperms and other seed plants remain in limbo (Feild & Arens 2005, 2007; Taylor et al. 2009). In particular, it is unclear which seed ferns and relatives are to be linked with the stem-group of angiosperms, regardless of whether extant gymnosperms are monophyletic or paraphyletic or where Gnetales go on the tree (e.g. Rudall & Bateman 2010). The basic issue is of course that only morphology can allow us to infer what the immediate ancestors of crown-group angiosperms might be, and morphology-based trees tend to have only a few characters, even if their sampling in terms of potentially relevant taxa can be quite extensive (e.g. Rudall et al. 2013). Are morphology-based trees credible?

5. Cretaceous History of Angiosperms.

Evolution. Divergence & Distribution. 6A. Introduction. The most comprehensive reviews of Cretaceous angiosperm history are those of Friis et al. (2006a, 2010a, 2011 in particular), on which this section draws heavily; see also Krassilov (1997), Dilcher (2010), Taylor (2010: focus on genes possibly involved), Doyle and Upchurch (2014), etc.. Doyle (2008b), Specht and Bartlett (2009), Endress (2010a), Doyle and Endress (2010), and others provide surveys of the floral morphology and biology of extant "basal" angiosperms. Hu et al. (2012) list early records of pollen, tabulate pollen morphology and suggest possible pollinators of ANITA-grade angiosperms, magnoliids, "basal" eudicots and monocots, and finally optimise a number of pollen and floral characters on the tree.

If the ages of some 270 to 175 m.y.a., so certainly Jurassic, if not earlier, mid-Permian (see above) for crown angiosperm origins are correct, we have a series of problems. We need to rethink the ecological context of the evolution of angiosperms and of the insects associated with them and we may need to understand how angiosperms persisted as a presumably not very diverse clade for 50 m.y. or much, much more - or only 23 m.y. (Z. Wu et al. 2014).

There are also very differing narratives for later angiosperm evolution. Some suggest that angiosperms achieved ecological dominance by the end of the Cretaceous; others suggest that tropical rainforest as we know it had barely developed then, and that Cretaceous angiosperms were ecologically and physiologically rather unlike many of their Tertiary successors. As to events at the Cretaceous-Tertiary (K/T) boundary, some suggest that the bolide impact had a major effect only on North American plants, any more global effect being more muted; others suggest there were major changes in vegetation structure and composition at the K/T boundary and in the early Tertiary. Similar tensions are evident in the literature on the evolution of mammals, insects, and other animals.

6B. Early Angiosperm Evolution. Leaving these problems aside for the time being, unambiguous angiosperm fossils from before the Lower Cretaceous are few. The pollen of angiosperms is distinctive. Although there are a number of reports of pre-Cretaceous angiosperm pollen, some can be dismissed because of incorrect dating or contamination (Hochuli & Feist-Burkhardt 2013 for literature). However, there are several pollen types from the Middle Triassic (ca 243 m.y.a.) of northern Switzerland that are similar to angiosperm pollen, being monosulcate, columellate, semitectate and reticulate, but with a very thin nexine (Hochuli & Feist-Burkhardt 2013). Pollen grains of this type are from plants that seem to have grown in a variety of habitats, so it is a little difficult to explain the absence of angiosperm megafossils from the Jurassic if the pollen really was from angiospermous plants. Hochuli and Feist-Burkhardt (2013) reasonably elect to consider these grains to be pollen of relatives of stem-group angiosperms. Other grains from the Triassic and Jurassic are remarkably like the very distinctive pollen of Acanthaceae-Tricantherinae (see also Tripp & McDade 2014b).

Fossil pollen from the Cretaceous Valanginian-Hauterivian 141-132 m.y.a. has also been attributed to angiosperms, although if columellate pollen is ancestral in angiosperms, there may be connections with the Triassic reticular-columellar Crinopolles pollen type (Doyle 2001; Zavada 2007). Nevertheless, diversification of angiosperms was well under way by 137 m.y.a. as judged by these pollen remains, but it was 10-30 m.y. or more before crown group diversification really got going (e.g. Feild & Arens 2005). Thus in the Barremian-Aptian ca 125 m.y.a. there are some 140-150 taxa recorded from Portugal alone (e.g. Friis et al. 1999, 2000a, 2010b). All in all, a remarkably diverse flora, even if recent work suggests that a younger age for at least some of this material, perhaps Albian and ca 112 m.y.o. (Heimhofer et al. 2005, 2007).

Although practically none of these fossils can be assigned to extant families, 85% of them represent plants of the magnoliid type or are somewhat monocot-like (Friis et al. 1997a, 1999, 2001; Heimhofer et al. 2007 - see also Doyle et al. 2008 for an evaluation of early fossils putatively of monocot origin; Friis et al. 2010a). Doyle (2001) noted the abundance of families with ascidiate carpels and exotestal seeds in these floras - and in extant members of the ANITA grade and Chloranthaceae. Doyle and Endress (2010) should be consulted for possible phylogenetic placements of a number of mostly magnoliid and ANITA-grade Cretaceous fossils, albeit the constraint tree used has a rather different topology that that of the main tree here.

Moore et al. (2007) suggest some time between 148.6-135.5 m.y.a. for a rapid separation of the Chloranthales, magnoliid, monocot, eudicot and Ceratophyllales clades (see also Sun et al. 2011), although other dates are somewhat younger. There are fossils assignable to Chloranthaceae from the late Barremian ca 130 m.y.a. onwards, with some being very like extant Hedyosmum (e.g. Crepet & Nixon 1996; Friis et al. 2006b for references). Pollen data suggest that monocots/magnoliids split in the early Aptian-mid Albian 125-105 m.y.a. (Heimhofer et al. 2005; Hochuli et al. 2006). Magnoliids diversified somewhat later for the most part (Friis et al. 1997a, 2006b for reviews); Lauraceae are prominent in the fossil record, and include the somewhat younger Early Cenomanian Mauldinia (Drinnan et al. 1990). This has distinctive condensed monosymmetric inflorescences quite unlike those of other Lauraceae, yet its flowers are very like those of extant members of the family. Jud and Wing (2012) thought that monocots and eudicots might have diverged 125-119 m.y.a., initial angiosperm diversification having occurred within a mere 5-10 m.y. before that.

There are several hypotheses about the ecological preferences of early angiosperms (see also vascular evolution). Most include the idea that conditions were disturbed (e.g. Heimhofer et al. 2005; Berendse & Scheffer 2009 for a summary; Bond & Scott 2010; Boyce et al. 2010). Other than that, suggestions as to the conditions these plants faced vary. The first angiosperms may have been rather small (Friis et al. 2010b) tropical trees with sympodial growth that tolerated shady, humid and disturbed ("dark and disturbed") conditions, or similar environments (e.g. Feild 2005; Feild & Arens 2005, 2007; Coiffard et al. 2006; Berendse & Scheffer 2009 for a summary); later there was movement into into more open conditions (e.g. Feild & Arens 2007; Bond & Scott 2010). There are suggestions that angiosperms initially grew in semi-arid (e.g. Stebbins 1965, 1974; Hickey & Doyle 1977) or at least seasonally arid (Bond & Scott 2010) conditions, and some early leaf floras from Portugal do have leaves that are small in size and xeromorphic in appearance (Friis et al. 2010b). Early nymphaealean-type plants are likely to have grown in aquatic or marsh-like habitats (e.g. G. Sun et al. 2008), while Coiffard et al. (2012) emphasized that 5/11 genera they examined that grew in the first stage of the rise to dominance of angiosperms were aquatics, and they "competed with charophytes". They did not say that the ancestral angiosperm was aquatic, but Goremykin et al. (2012) do think that this is likely. However, both very xeromorphic and aquatic plants are likely to be derived; in aquatics, loss of cambial activity may be difficult to reverse (). In any event, whether Nymphaeales are sister to Amborellaceae or not will have little effect on ancestral reconstructions of habitat preferences. It also seems unlikely that the angiosperm progenitor was a "diminutive, rhizomatous to scrambling herb" (Taylor & Hickey 1992, p. 137: an extension of the palaeoherb hypothesis), although some early angiosperms may have been herbs, certainly aquatic herbs (e.g. Friis et al. 1999 and references).

Whatever habitats angiosperms first favoured, there is a consensus that they were soon components of disturbed, mesic communities (Hickey & Doyle 1977) with well lit or open conditions (e.g. Royer et al. 2010), and mention of flood-plain like habitats is common (e.g. Wing & Boucher 1998; Coiffard et al. 2008). Aethophyllum, a small (but hardly herbaceous), fast-growing conifer (?Voltziales), had occupied similar habitats in the lower middle Triassic (Rothwell et al. 2000). How woody the early angiosperms were is unclear; Philippe et al. (2008) suggested that they might have had cambium, but there were no thick-walled fibres and in general cell walls were thin (see also Amborella); they are likely to have been shrubby plants (Hickey & Doyle 1977). In any event, any climatic niche (habitat) evolution that occurred then may have been slow (Smith & Beaulieu 2009). Growth rates of early angiosperms may have been high and reproduction rapid compared with gymnnosperms (Doyle & Hickey 1976; Bond 1989; Wing & Boucher 1998; Verdú 2002), although if the plants were any size there was unlikely to be quick nutrient turnover via litter decomposition (Liu et al. 2014). The reproductive cycle was relatively short, with a short time between pollination and fertilization; the development of callose plugs and callose in the pollen tube wall probably allowed the pollen tube to grow faster, callose synthase genes are also expressed in at least some gymnosperms, but not in the pollen tube, and some angiosperms do not have callose in the pollen tubes (Abercrombie et al. 2011). , seeds were small (see below), the plants were small, overall, there was a short pre-reproductive period and short overall generation time (e.g. Williams 2008, 2009; Crepet & Niklas 2009 Bond & Scott 2010).

The flowers of early angiosperms are small and rather generalised (see e.g. Crane et al. 1995; Doyle & Donoghue 1986a; Friis & Crepet 1987; Friis & Endress 1990; Friis et al. 2000, 2006b, 2010b; Endress 2001a; Weberling 2007; Doyle 2008b; Doyle & Endress 2000, 2010, 2011). The stamens of fossils are often wedge-shaped, with a massive apex, stout filaments and connectives, and anthers open by laterally-hinged valves (e.g. Crepet & Nixon 1996; Endress 2008c and references; Endress 2011a) - although perhaps not in the earliest angiosperm fossils. Dry stigmas and protogyny were probably the common condition (e.g. Sage et al. 2009; Endress 2010a). These small flowers were probably aggregated into inflorescences to attract pollinators (Friis et al. 2006b). The carpels are likely to have had few ovules, Doyle (2012) and others suggesting that the ancestral state is to have a single ovule, the stamens produced only a few pollen grains, but there is no evidence of nectaries [check] (e.g. Crepet et al. 1991; Dilcher 2000; Friis et al. 2006b). However, quite "derived" features are early evident. Thus Sinocarpus, from the Barremian-Aptian 139-122 m.y.a., had carpels that were apparently connate at the base (Leng & Friis 2003), and inferior ovaries were surprisingly common (e.g. Crane et al. 1995; Friis et al. 1999).

If extant magnoliid and ANITA-grade angiosperms are any guide, distinctions between different kinds of floral parts might be hard to make. Distinguishing perianth and prophylls and bracts can be difficult in extant angiosperms, there can be intermediates between perianth and stamens, the numbers of parts and their arrangement vary, etc. (Buzgo et al. 2004; Taylor et al. 2008; Endress 2008a; Doyle & Endress 2011 and references).

The seeds of early angiosperms were dry (but see Eriksson et al. 2000a, esp. b) and mostly rather small compared with those of extant gymnosperms (Tiffney 1986a; also Haig & Westoby 1991; Linkies et al. 2010); the seed contents, probably mostly endosperm reserve, were a mere 2-3 mm3. A small size is perhaps to be expected since plant and seed size are quite strongly linked (e.g. Eriksson et al. 2000; Moles et al. 2005b). The embryos themselves are likely to have been small to minute (measured as the embryo:seed ratio), resulting in a period of morphological dormancy before a plantlet developed and germination could occur (Forbis et al. 2002; Linkies et al. 2010). Indeed, seeds of plants in the ANITA grade are mostly notably smaller than those of extant gymnosperms (e.g. Moles et al. 2005a), and the embryo is small.

It was early recognized that angiosperm leaves are very different from those of most other vascular plants (Hickey & Doyle 1977). Some early fossils had leaves with a multistranded midrib, they were simple, with entire margins and irregular venation. However, the regularity of the venation increased, blades having several orders of venation, as well as teeth, and compound leaves became more common. Vegetative evolution was a major element in early angiosperm diversification (Hickey & Doyle 1977), and an increase in venation density coupled with ordered hierarchical-reticulate venation and the evolution of vessels with simple perforation plates can be linked to increased photosynthesis, transpiration and all that that implies, which includes the spread of l.t.r.f. (e.g. Boyce et al. 2009; Boyce & Lee 2010; Feild et al. 2011b; Boyce & Leslie 2012; Feild & Brodribb 2013; see also below). These developments may have been a two-step process, the first happening ca 100 m.y.a., the second perhaps at the end of the Cretaceous.

Many older plant fossils have very distinctive character combinations (e.g. Feild & Arens 2005; Fries et al. 2011 and references). For example, Archaefructus, probably an aquatic herb that lived in the Barremian-Aptian at least 124 m.y.a. (Sun et al. 2002), has been interpreted as having perfect flowers that are unlike those of any extant angiosperms - there is no perianth, the receptacle is very elongated, the stamens are paired, and the carpels are conduplicate - or these "flowers" are inflorescences, the paired stamens representing staminate flowers that lack any other structures (see also Zhou et al. 2003; Friis et al. 2003b; Ji et al. 2004; Doyle & Endress 2007; also Crepet et al. 2004 for analyses of this and other early fossil angiosperms). Whatever the interpretation, Archaefructus is unlikely to be sister to all extant angiosperms (c.f. Sun et al. 2001; Crepet et al. 2004), recent morphological work suggesting that it could be a member of Nymphaeales (Doyle & Endress 2007, 2010a; Doyle 2008b). Of course, some fossils, perhaps including Archaefructus itself, may represent quite distinct but now extinct clades (von Balthazar et al. 2008). Hyrcantha, also more or less aquatic, is also from Barremian-Aptian deposits in China (Dilcher et al. 2007); it has leaves with sheathing stipules and partly connate carpels with apparent resin bodies at their apices. Fossils from the Aptian/Albian ca 112 m.y.a. continue to have odd assemblages of characters (see also Friis et al. 1995). For a critical re-evaluation of the North American Potomac floras, large Aptial to Albian in age (125-100 m.y.o.), see Doyle and Upchurch (2014). Plants from the beginning of this period are largely assignable to the ANITA grade, Chloranthaceae, and Ceratophyllum areas, while towards the end of this period magnoliids, Platanales, and Buxales predominate.

Quite a variety of strange-looking putative angiosperms have been discovered in deposits from northeastern China, and although the identities of a number are disputed (Sun et al. 2006), new fossil finds from this area continue to challenge our understanding of angiosperm evolution (e.g. Sun et al. 2011: see eudicots below). Perhaps more remarkably, fossils ascribed to Sarraceniaceae (asterids-Ericales) have been described from deposits about the same age as those in which Archaefructus was found (Li 2005); this does seem something of a stretch.

As to what pollinated these early angiosperms, Labandeira (2010 and references) suggested that many pollinating clades of Hymenoptera, Diptera, and Lepidoptera originated around Late Barremian/end Albian some 125-100 m.y.a.. Early angiosperms are likely to have been pollinated by insects (Hu et al. 2008), although Hu et al. (2012 and references) suggest that pollination by both insects and wind (ambophily) may also have occurred. Thermogenic (beetle) pollination is found in some extant members of many "basal" lineages, including Araceae, although not it is not known from most Laurales, Amborellales, and Acorales (Thien et al. 2000; Seymour et al. 2003; Seymour 2010). Beetles are quite common pollinators of ANITA and magnoliid angiosperms, including Calycanthaceae (Laurales), and are attracted to haplomorphic flowers lacking definite symmetry signals (Leppik 1957); of course, other factors such as scent and thermogenesis are also involved. B. Wang et al. (2013) review the possible role of beetles in the pollination of early angiosperms, noting that beetles such as Scarabaeoidea and Chrysomeloidea that were likely to have been involved had evolved by or at the early Cretaceous. One factor to remember is that the flowers of early angiosperms are generally small, often just a few millimetres across.

Pollen seems initially to have been produced in rather low quantities, yet it may have been an early source of food for the pollinator, pollen being found in coprolites (Friis et al. 1999). Nectar is unlikely to have been a common reward at this time, although "food bodies" have been reported in 115-100 million year old flowers from Lower Cretaceous Burmese amber (Santiago-Blay et al. 2005). The few dispersed pollen morphs and the diversity of pollen morphs associated with plant remains suggests some kind of insect pollination (Friis et al. 1999). Pollenkitt, produced by tapetal degeneration and rich in plastid-derived lipids, helps pollen grains stick together, but pollen of early flowers is not often clumped (Doyle et al. 1975; Hu et al. 2008). There is no signal of an increase in protein content of the pollen of extant representatives of basal angiosperm clades that suggests bee pollination (Roulston et al. 2000), and bees are unlikely to have been pollinators of early flowers; certainly, their diversity then was low (e.g. Grimaldi & Engel 2005). Bee larvae obtain their fat from pollenkitt (Renner 2010 and references).

Dispersal of disseminules is initially likely to have been by wind (Wing & Boucher 1998). However, Eriksson et al. (2000b) sampled some 100 taxa from the Barremian-Aptian (132-112 m.y.a.), and even then ca 25% were animal dispersed, although they were small, very like the abiotically-dispersed propagules that predominated in early angiosperms (see Tiffney 1984; Eriksson 2008; Dilcher 2010, in part; Sussman et al. 2013).

In the Portugese Late Barremian-Aptian 124-112 m.y.a. climate and environment were unstable, which might have favoured angiosperms if they were adapted to disturbed habitats (Heimhofer et al. 2005); angiosperms diversified towards the end of this period, and the following Albian was a warmer and drier time (see also Coiffard et al. 2006, 2007). Tricolpate pollen, the signal of eudicots, has been reported from the Late Barremian-Early Aptian some 125-120 m.y. (e.g. Magallón et al. 1999; Sanderson & Doyle 2001), although if the relationships of Leefructus from early Cretaceous deposits 125.8-122.6 m.y. old in China and assigned to stem Ranunculaceae (Sun et al. 2011: no associated pollen) is confirmed, these ages will have to be revised. In west Portugal and elsewhere tricolpates are initially in low numbers, but in the Early Albian ca 112 m.y.a. angiosperms, including tricolpates, diversified rapidly (Heimhofer et al. 2005; Friis et al. 2006b for references). The functional advantage of tricolpate pollen may be that the grains germinate faster, even if they remain viable for a shorter time than monoaperturate pollen (e.g. Furness & Rudall 2004). Somewhat younger (120-110 m.y.) monocot pollen has been identified as Araceae-Pothoideae (Friis et al. 2004; see also Doyle et al. 2008: Friis et al. 2010), although some early monocot pollen records have been questioned (Hoffmann & Zetter 2010). Overall monocot fossils are not very common, but being a predominantly herbaceous group they may have fossilized less well. Fossil angiosperm wood is known from deposits of up to about 120 m.y.a. (Aptian), although its assignment to extant clades is not easy (Oakley et al. 2009).

6C. Later Cretaceous Evolution. The Late Cretaceous begins ca 99.6 m.y.a. with the Cenomanian, the sea during this period being about one hundred and fifty meters above its present level. I also include somewhat earlier dates in this section, the period from 110-80 m.y.a. encompassing the so-called Cretaceous Terrestrial Revolution (KTR: Lloyd et al. 2008; Benton 2010; Meredith et al. 2011). A long-term warming trend from the early Aptian culminated in the Cenomanian-Turonian thermal maximum ca 99 m.y.a. (Heimhofer et al. 2005). Atmospheric CO2 concentrations were about 1,600 p.p.m. around the Jurassic-Cretaceous boundary, possibly the highest concentrations since their dramatic deline in the late Devonian ca 360 m.y.a., but then declined. Global temperatures show a similar overall trend (Shi & Waterhouse 2010; Franks et al. 2013).

This period has been characterised as one in which major changes in the terrestrial vegetation occurred (e.g. Crepet 2008; Coiffard & Gomez 2011, 2012). Some low latitude floras were dominated by angiosperms even in the Cenomanian-Turonian (Coiffard & Gomez 2012 for references). Mid-latitude floras were also changing considerably, fossil woods becoming notably more common (Philippe et al. 2008; Wheeler & Lehman 2009), although angiosperms seem to have been relatively minor components of the vegetation until the end of the Cretaceous (Coiffard & Gomez 2012). Over a period of about 49 m.y., - m.y.a., angiosperms spread latitudinally from the more tropical environments they initially inhabited (Axelrod 1959; Hickey & Doyle 1977; Wing & Boucher 1998; Hemihofer et al. 2005 for further references), moving polewards in the early Late Cretaceous (Pott et al. 2012 and references); abundance increased in a similar fashion. There were a significant number of eudicots in mid-latitude North America in the Albian-Turonian, ca 100 m.y.a., although again tey were slightly earlier at lower latitudes, S of palaeolatitude 30 N (e.g. Crane & Lidgard 1989, 2000; Lupia et al. 1999), and they replaced free-sporing plants (see also Fiz-Palacios et al. 2011: "continuous replacement"), but not conifers (see e.g. Wing & Boucher 1998; Lupia et al. 1999); cycads may also have declined. The decline of cycads and Bennettitales (cycadophytes, an ecological grouping) might be linked with the contemporaneous decline in herbivorous stegosaurian dinosaurs, but there is no indication of any even loose relationships between early angiosperms and dinosaurs (Barrett & Willis 2001; Butler et al. 2009 and references). In Australia, angiosperm pollen had increased from a low level in the middle Albian ca 105 m.y.a. to about 35% of the total spores at the end-Cretaceous, while pollen of free sporing plants dropped from 80% to 45% during the same period. However, not all fern families behaved the same, and there are differences between Australia and North America (Nagalingum et al. 2002).

Many early angiosperms grew in shady or disturbed flood plain-type habitats (e.g. Feild & Arens 2005, 2007; Coiffard et al. 2006, 2007; Miller 2013: 105 m.y.a. Albian). Areas where conifers remained common seem to have become more restricted, and ecological factors such as slow seedling growth, details of leaf construction, narrow stomatal apertures (ca 2 µm: Walker 2005), etc., may explain this (e.g. Bond 1989). At the same time, they have a very high leaf area index of up to 21 (Maguire et al. 2005), and many of these features in extant conifers make them formidable competitors with angiosperms in well-lit conditions on soils that are other than nutrient-rich (Brodribb et al. 2012).

Pollen suggests that core eudicots may have been around since the Albian 125-112 m.y.a., and many major euasterid, rosid and monocot clades seem all to have radiated by around 90 m.y.a. at the latest (e.g. Sanderson et al. 2004; Jian et al. 2008 and references; Wang et al. 2009). Flowers assignable to a variety of asterid groups and also to Saxifragales (ovary inferior, crowned by a nectary, styles more or less separate, i.e. they look very like the old woody Saxifragaceae) being especially common, as are Ericales (Friis et al. 2006b). Indeed, Saxifragales, although now not very speciose, may also represent an ancient and rapid radiation (Fishbein et al. 2001; Fishbein & Soltis 2004; Jian et al. 2008).

Fossils referable to extant angiosperm families appear in east North America around 115-90 m.y.a., and by some 85 m.y.a. their diversity had increased considerably (Crane and Herendeen (996; also Lidgard & Crane 1988; Friis & Crepet 1987; Friis & Endress 1990; Crepet et al. 2004, etc.). Crepet (1996, 2008) noted the first appearance of many largely core eudicot characters beginning in the Albian, but especially the Cenomanian/Turonian some 96-88 m.y.ago. The diversity of floral form in the Turonian of east North Americas is very considerable, magnoliids, rosids and asterid-Ericales all being represented (e.g. Crepet & Nixon 1996). Rosids in particular were common in the Late Cretaceous (Friis et al. 2010b), and diversification of the major rosid clades may have occurred (114-)108-91(-85) m.y.a., and that of Fabidae and of Malvidae very soon after, (113-)107-83(-76) m.y.a. (Hengchang Wang et al. 2009). The origins of several clades within Malpighiales and Ericales whose representatives now are major components of lowland tropical rainforest (l.t.r.f.) are also to be pegged to the Mid Cretaceous or slightly later, dates in the former being some time in the late Aptian/Albian, (119.4-)113.8(-110.7)/(105.9-)101.6(-101.1) m.y. ago (Davis et al. 2005a: high and low estimates). Initial malpig diversification was rapid, and relationships have been hard to disentangle (Wurdack & Davis 2009; but c.f. Xi et al. 2012). Crown group Menispermaceae have been dated to around 109.1-106.3 m.y.a. (W. Wang et al. 2012), and this family is now most common in tropical rain forests where it is prominent in the liane element of the vegetation; l.t.r.f. is probably its ancestral habitat (W. Wang et al. 2012). However, Burnham (2009) noted that there were few fossils of climbers through most of of the Mesozoic, although a few angiosperm climbers are known from the Cretaceous; wood fossils of lianes from the Cretaceous-Palaeogene are dominated by Ranunculales and Vitaceae-Vitoideae, the latter being Tertiary in age (Smith et al. 2013).

Pollinating insects, as well as lizards, snakes, and perhaps modern bird and mammal orders, all diversified more during the KTR (Benton 2010), although dinosaurs seem to have been unaffected (Lloyd et al. 2008). The evolution of bees, now major pollinators of angiosperms, and other insect pollinators, seed dispersers (esp. ants) and herbivores, is particularly important. Diversification of ants, mosses, beetles and hemipterans occurred along with that of rosid angiosperms 108-83 m.y.a. (Hengchang Wang et al. 2009). Angiosperm flowers from the Cenomanian-Turonian 110-90 m.y.a. have a variety of quite specialized zoophilous morphologies, and nectar secretion became common (Crepet 1996, 2008; Hu et al. 2008); Citerne et al. (2010) suggested that 93.5-89 m.y.a. in the Turonian was a period of floral innovation and evolution of pollinators. Sympetaly and monosymmetry (evidence for the latter is indirect, seeds assignable to Zingiberales: Rodríguez-de la Rosa & Cevallos-Ferriz 1994) appear in the Late Cretaceous (Friis 1985; van Bergen & Collinson 1999; Friis et al. 2003a). By the mid-Cretaceous pollen became more abundant and is quite often found in clumps, suggesting that the pollinators were becoming more specialized (Hu et al. 2008; Leslie & Boyce 2012).

Bee diversification began (132-)123(-113) m.y.a. (Cardinal & Danforth 2013; ca 112 m.y.a.: Grimaldi 1999; ca 125 m.y.a.: Ronquist et al. 2012), with families diverging by the beginning of the Tertiary; most diversification occurred within the last 100 m.y. (see also Engel 2000; Grimaldi & Engel 2005). Crown-group Xylocopinae bees are dated to around 90-85 m.y.a. (Cardinal et al. 2010; Cardinal & Danforth 2013), although there was little immediate diversification of the four main clades that originated then (Rehan et al. 2013). Early bees are likely to have been oligolectic (Litman et al. 2011 and references: note early ages for bee diversification; also Sedivy et al. 2012; c.f. e.g. Moldenke 1979), with individual species of bees visiting relatively few species of flowers, and these might be related. Several species of bees might pollinate a single plant species, and the floral morphology of the latter is likely to have been rather unspecialized (see below). However, there is no obvious signal of an increase in protein content of the pollen of extant representatives of angiosperm clades that had probably evolved by then that might suggest a shift to bee pollination (Roulston et al. 2000).

Initial divergence within butterflies s.l. (Papilionoidea) may also have been around 110-95 m.y.a. (Heikkilä et al. 2011). Most subfamilies of ants were diversifying by the late Cretaceous (Moreau et al. 2008). Locally, herbivory was quite prominent (Labandeira et al. 2002b). The sugar-rich fruits of angiosperms may have provided a habitat for budding yeasts such as Saccharomyces cerevisiae; they have a genome duplication ca 100 m.y.a. that is perhaps connected with their ability to exploit this habitat (Wolfe & Shields 1997; Conant & Wolfe 2007). (For the evolution of yeasts able to grow in nectar, etc., largely a Tertiary phenomenon, see Guzmán et al. 2013.)

Nectary evolution is of particular interest since nectar is a major pollinator reward in extant angiosperms. A flower, the Rose Creek fossil from the Cenomanian some 96-94 m.y.a., is certainly a core eudicot although not identifiable to an extant family (Basinger & Dilcher 1984). Relatively large compared to the flowers of other Cretaceous angiosperms, it has five stamens that are somewhat unexpectedly opposite the petals and is the earliest fossil flower with a nectary (Friis et al. 2011). With the advent of the core eudicots by (121-)115-109(-101) m.y.a. nectar produced by receptacular nectaries may have become a major reward for pollinators (Friis et al. 2006b), although receptacular or ovarian nectaries are also found in Proteales (even some fossils of the now wind-pollinated Platanaceae are described as having nectaries) and Buxales. Septal nectaries may be an apomorphy for monocots, being scattered throughout that clade, and are certainly found in Alismatales; they may have evolved by 120 m.y.a. or earlier. Many Laurales have paired glandular biodies at the base of the stamens that may provide some reward to the pollinator, and these appeared around 127-89 m.y.a. (see Laurales). Other kinds of nectaries are found in angiosperms other than monocots and core eudicots.

Around 108-94 m.y.a. (Late Albian) the venation density of angiosperms had become markedly greater than that of non-flowering plants and ANITA-grade angiosperms (Feild et al. 2011b; c.f. Bond & Scott 2010 in part). Atmospheric CO2 concentration was in its long decline from the late Jurassic-early Cretaceous to the later Oligocene ca 40 m.y.a., bottoming out only in the Pleistocene (Shi & Waterhouse 2010; Franks et al. 2013); this provides the background against which changes in venation density and stomatal size (see below), both increasing photosynthetic efficiency, played out. In these early changes venation density increased above 2.5-5 mm/mm2, and the path length for water transport inside the leaf (from vein to stomatal pore) equalled the internal diffusion path of CO2 (from stomatal pore to chloroplast); stomata were still quite large (e.g. de Boer et al. 2012).

Friis et al. (2006a; see also Heimhofer et al. 2005) note a dramatic increase of phylogenetic diversity and ecological abundance of angiosperms at this time. However, even up to the Cenomanian ca 96 m.y.a. there are many fossils that probably belong to the ANITA-magnoliid grade (e.g. Coiffard et al. 2006; Kvacek & Friis 2010; Friis & Pedersen 2011). Later in the Cretaceous angiosperm diversity was increasing, being high even close to the Arctic Circle (Hofmann et al. 2011), and angiosperms may have achieved at least some measure of ecological dominance (Friis et al. 2006b). Large trees first appear in the fossil record in the Late Albian to Cenomanian (ca 90.6 m.y.), and trends like increasing seed size were already evident, probably connected with the increasing size of woody plants (e.g. Eriksson et al. 2000a; Forbis et al. 2002; Linkies et al. 2010), thus a general increase in fruit size occurred at about 85-75 m.y.a. (e.g. Eriksson et al. 2000a; Dunn et al. 2007).

Plants with distinctive pollen assignable to the Normapolles complex and comparable with that of a group of extant Fagales were both diverse and ecologically prominent in rocks from east North America to western Asia from the Late Cenomanian/Early Turonian ca 93.5 m.y. ago. Of the other pollen provinces, the southernmost was characterized by Nothofagites pollen, probably also from plants that would be included in Fagales (e.g. Pacltová 1981 for a review; Kedves & Diniz 1983; Friis et al. 2006b, 2010b).

Just how ecologically dominant angiosperms had become in the later Cretaceous remains unclear. Through much of the earlier Cretaceous, any dominance of angiosperms may have tended to be restricted to fluvial or disturbed environments. Areas with ever-wet tropical humid climates seem to have been initially rather restricted (see also Boyce et al. 2009, 2010; Boyce & Lee 2010; Feild et al. 2009a). Even if there was tremendous phylogenetic diversification in the later Cretaceous and early Tertiary, this later transformative ecological change (e.g. Feild et al. 2011b) should not lead to the underestimation of the effects of the KTR.

The evolution of those clades of parasitic and myco-heterotropic angiosperms that live in l.t.r.f. or similar conditions is of particular interest. Stem-group Rafflesiaceae are estimated to have diverged from other Malpighiales some 95 m.y.a., divergence within the family beginning (95.9-)81.7(-69.5) m.y.a. (Bendiksby et al. 2010); this might suggest the presence of l.t.r.f., the habitat to which Rafflesiaceae are all now largely restricted, before the latter time. Although Naumann et al. (2013, q.v. for discussion) estimate the stem age of Rafflesiaceae to be only ca 65.3 m.y.a., around the Cretaceous/Tertiary boundary, they think a number of parasitic associations are of Cretaceous age, for instance, the Aristolochiaceae-Hydnoroideae, although the crwon-group age of the two may not be that different. Myco-heterotrophic clades of Dioscoreales often grow in similar habitats, and some are estimated to have diverged (118-)109-79(-68) m.y.a., with the myco-heterotrophic habit being established well before the beginning of the Palaeocene (Merckx et al. 2008a, 2010).

Coiffard and Gomez (2009: p. 164) suggest that the Late Cretaceous was the "dawn of modern angiosperm forests", but their Turonian forests of ca 90 m.y.a. grew primarily in disturbed and/or riparian-type habitats (see also Jud & Wing 2013); Platanaceae, found along channel margins in the Cenomanian, had spread onto flood plains in the Turonian. Bond and Scott (2010) suggest that until the Mid or even Late Cretaceous angiosperms were mostly small herbs to small trees of the understory growing in dryish conditions, perhaps rather weedy plants (Feild et al. 2011b), and analyses using variables like leaf area and vein density, plant height and seed size, suggest angiosperms were mostly not canopy trees, seed size remaining small (Jud & Wing 2013). In parts of Campanian (83.6-72.1 m.y.a.) North America, angiosperms seem to have lived in rather species-poor and open woodland (Lehman & Wheeler 2001; Wheeler & Lehman 2001, 2009). The trees, up to 1.3 m across, may have produced Normapolles pollen (Lehman & Wheeler 2001), now commonly associated with ectomycorrhizal Fagales, so a diverse forest might not be expected, however, identifications suggested for these woods rarely include Fagales (Wheeler & Lehman 2009). In the Albian-Cenomanian of Europe ca 100 m.y.a. angiosperms were most evident in backswamp, flood plain, levee, and braided river habitats (Coiffard et al. 2006), and trees up to 2 m in diameter have been found in Late-Cretaceous riparian swamps (Parrott et al. 2013). The deciduous habit was relatively common in these flood plain habitats ((Wolfe 1987).

By ca 80 m.y.a. angiosperms came to make up ca 40% of both floristic diversity and abundance even at higher latitudes (Crane & Lidgard 1989; Lupia et al. 1999; see also Nagalingum et al. 2002), and there was an end-Cretaceous rise to dominance of angiosperms in Patagonia (Iglesias et al. 2011). Pollen data suggest that monocots and magnoliids grew largely in the area between ca 500N and 20oS, and this pollen was probably mostly from members of Arecaceae (Crane & Lidgard 1989). Conifer pollen and also spores from "bryophytes" and "pteridophytes" decreased in diversity, although gnetalean pollen was quite diverse at rather lower latitudes in the mid-Cretaceous (Crane & Lidgard 1989). However, Strömberg et al. (2013) suggested that in the Late Cretaceous (ca 73 m.y.a.: Wyoming) angiosperms were not notably abundant compared with other co-occurring vascular plants, but they did vary considerably in niche optimum and niche breadth. (Similarly, non-polypodiaceous ferns dominated Late Campanian (73 m.y.) North American fern prairies, but Polypodiales, less dominant, were quite diverse [Wing et al. 2013].) Angiosperms may have formed a canopy at least locally by the end-Cretaceous (e.g. Upchurch & Wolfe 1987; Crane & Lidgard 1990; Boyce et al. 2010), but how diverse that forest was is unclear. In their discussion of Cretaceous angiosperm ecology, Wing and Boucher (1998: p. 379) concluded that at the end of the Cretaceous, diversification of flowering plants represented "the evolution of a highly speciose clade of weeds but not necessarily a major change in global vegetation", while Eriksson et al. (2000) suggest that Late Cretaceous vegetation was open, rather dry (leaf size was relatively small - Upchurch & Wolf 1987), and disturbed by herbivores (see also Schönenberger 2005; Wing et al. 2012). Fires were relatively common throughout the Cretaceous, and they may have encouraged/been encouraged by a rather shrubby, low stature vegetation with a relatively short life cycle (Bond and Scott 2010; Bond & Midgley 2012).

There was a second major increase in angiosperm venation density at the end of the Cretaceous (Maastrichtian) ca 70 m.y.a., and only then did trees having a venation density around 10 mm/mm2 or more similar to that of plants in the most productive l.t.r.f. today appear (Brodribb & Feild 2009; Feild et al. 2011b). This was accompanied by a decrease in stomatal size and an increase in stomatal number, which together increased stomatal gas exchange capacity; specifically, the intake of CO2; photosynthesis could increase yet water loss stayed more or less the same (e.g. de Boer et al. 2012; see also Boyce & Zwieniecki 2012). Modelling suggests that the increase in evapotranspiration enabled by these changes in leaf venation may well have helped in the spread of l.t.r.f. (Boyce & Lee 2010). The maps at the end of Willis and McElwain (2014) show the extent of the changes; earlier changes presumably had different causes, e.g. continental drift.

There was an increase in the net diversification rate of mammals around 100 m.y.a. and again around 80 m.y.a. at the end of the CTR, followed by a decrease (Meredith et al. 2011). Indeed, Meredith et al. (2011: p. 523) observed that the increase in diversity of angiosperms to 80% during the CTR 125-80 m.y.a., was "a key event in the diversification of mammals and birds". Examination of the teeth of multituberculate mammals suggests that a radiation began ca 85 m.y.a. in which the adoption of a more herbivorous diet may be associated with the increasing prominence of angiosperms (G. P. Wilson et al. 2012).

It has been suggested that diversification of mosses accelerated in the Cretaceous as rates decelerated for liverworts (an initial increase there was Jurassic in age: Feldberg et al. 2014; Laenen et al. 2014) and gymnosperms (Fiz-Palacios et al. 2011 but c.f. Cooper et al. 2012; Laenen et al. 2014 for problems with the study). Diversification in the speciose pleurocarpous mosses, about 40% of all mosses, seems to have been early-Cretaceous and rapid, with subsequent semi-stasis. Many mosses, especially members of Hypnales, are epiphytic (Shaw et al. 2003b; Newton et al. 2006, 2007; see also Kürschner & Parolly 1999), and their initial radiation is at about the same time as the early rise of the angiosperms during the KTR (Laenen et al. 2014). However, Porellales, largely leaf-epiphytic liverworts, diverged from the terrestrial Jungermanniales in the Jurassic, and they, too, show enhanced diversification compared to other liverworts in the Cretaceous and early Tertiary (Heinrichs et al. 2007; Feldberg et al. 2014; see also Ahonen et al. 2003; Forrest & Crandall-Stotler 2004). Lejeuneaceae initially diversified in the Cretaceous, and neither here nor Cephaloziineae was there change in rate through the Tertiary (R. Wilson et al. 2007a, b; Feldberg et al. 2013). Cooper et al. (2012) suggested that although many liverwort families diverged in the Cretaceous and other splits in liverworts were very much older, much divergence within the families was Tertiary. Diversification of polypod ferns began in the Cretaceous (Schneider et al. 2004; Schuettpelz & Pryer 2009), perhaps associated with the evolution of a distinctive new photosystem that allowed them to grow in shady conditions (Kawai et al. 2003). The initial evolution of epiphytism in ferns can be dated to the mid-Cretacous or near the K/T boundary (but c.f. Trichomanes), even if much diversification was a Tertiary phenomenon (Dubuisson et al. 2009; Schuettpelz & Pryer 2009). The question is, to what extent can "the ecological opportunities provided by humid megathermal forests" (Feldberg et al. 2014: p. 1) that seems to have driven the diversification of these epiphytes, etc., be translated to the existence of tropical rainforest?

To conclude. Hypotheses of the evolution of the taxa in early angiosperm-dominated rainforests span the spectrum. The "museum" hypothesis is that centers of diversity are not centers of origin, rather, they are in areas in which there has been little disturbance over the last 50-100 m.y. (Stebbins 1974). It has also been suggested that many clades persisted largely unaffected across the K/T boundary, or there was initial rapid diversification which slowed down as global cooling occurred ("ancient cradle"), or there was a progressive increase in diversification rate towards the present, the "recent cradle" theory (see Couvreur et al. 2011c for references). The ancient cradle hypothesis is consistent with the suggestion by Fiz-Palacios et al. (2011: c.f. ages) that the diversification rate of angiosperms was constant through the Cretaceous, while Couvreur et al. (2011c) found that the rate for palms held more or less constant for some 65 m.y. after their origin ca 100 m.y.a., right across the K/T boundary. Palms are iconic plants of l.t.r.f. today, so either the rainforest of 100 m.y.a. was rather different from that of today (see e.g. Feild et al. 2011b), or l.t.r.f. of "modern" aspect remained very restricted in extent for millions of years, or there are methodological problems with the analyses (see e.g. Quental & Marshall 2010). However, Coiffard and Gomez (2009) suggest that early palms may have been swamp plants plants like living basal Arecales (their examples were Calamus, Nypa, and Mauritia). Annonaceae (Couvreur et al. 2011a; see also Erkens et al. 2012), Araceae (Nauheimer et al. 2012) and the liverwort groups Lejeunaceae (R. Wilson et al. 2007) and Cephaloziineae (Felberg et al. 2012) show a similar constant rate of diversification. The diversification rate of the main clades of ants may have been constant (Pie & Tschá 2009, but c.f. Moreau & Bell 2013), and rather surprisingly, given text-book accounts, mammal diversification seems to have been little affected by the end-Cretaceous extinction event (Bininda-Emonds et al. 2007; Meredith et al. 2011; G. P. Wilson et al. 2012; but c.f. O'Leary et al. 2013).

Of course, these scenarios are not mutually exclusive. Certainly, many major angiosperm clades diversified well after the palms, mostly in the Tertiary, and these include families like Fabaceae, and woody Fabaceae are now prominent in tropical forests, and perhaps even Myristicaceae. Most of the diversification of the more herbaceous members of the euasterids, including that of Asteraceae, is also a Tertiary phenomenon.

6. Tertiary Diversification

Atmospheric CO2 concentrations continued to fall throught the Tertiary (Arakaki et al. 2011). Global temperatures were high at the beginning of the Tertiary, and then declined, although with pronounced if sometimes short-term increases.

6A. Mostly Flowering Plants. The end-Cretaceous bolide impact that occurred ca 65.5 m.y.a. seems not to have been accompanied by widespread fires (Belcher 2010). Nevertheless, it caused up to 80% loss of plant species, at least in some places in North America (Upchurch & Wolf 1987), although other estimates are around 25-33% (Nichols & Johnson 2008; cf. Salas-Leiva et al. 2013). There was concomitant extinction of diet-specific herbivorous insects as evidenced by a survey of the types of leaf damage caused by herbivores (Labandeira et al. 2002a, b; Wilf 2008). The severity of the impact seems to have depended in part on physical location (K. R. Johnson & Ellis 2002). Elsewhere, as in New Zealand the iridium anomaly associated with the bolide impact was followed by a thin layer high in fungal remains (Vajda & McLoughlin 2004), while in both hemispheres there were fern spikes (and, in the Netherlands, a bryophyte peak) after the impact (Saito et al. 986; Vajda & McLoughlin 2007 and references; Nichols & Johnson 2008). Evidence from Australia is unclear (e.g. Macphail et al. 1994; Hill & Brodribb 2006). However, in Patagonia in particular, and perhaps elsewhere the Southern Hemisphere, changes at the K/T boundary were rather muted (Wilf et al. 2013).

"Sudden ecosystem collapse" did occur, at least locally in North America, even common plants not transgressing the Cretaceous/Tertiary boundary (Wilf & Johnson 2004: p. 347); they estimate 30-57% extinction of the flora (data are from pollen) in southwest North Dakota. The familial composition of Early Tertiary forests in North America does differ from that of their Late Cretaceous counterparts (e.g. K. R. Johnson 2002; Wilf & Johnson 2004). However, no major plant group is known to have disappeared at the end of the Cretaceous (Nichols & Johnson 2008), and by and large the main pollen genera persisted across the K/T boundary, even if species did not (Tschudy & Tschudy 1986). Several clades of heterosporous water ferns failed to cross the boundary, although some extant clades are known fossil from the Cretaceous (Collinson et al. 2013). Both insect-pollinated and/or evergreen taxa of seed plants suffered more than wind-pollinated and/or deciduous taxa (Collinson 1990; McElwain & Punyasena 2007). As just mentioned, groups like Annonaceae, Arecaceae, and Araceae seem to how constant diversification rates across the K/T boundary, suggesting that the bolide had relatively slight effect overall on them, although some clades, at least, show a relatively high diversification rate soon after their origin (literature summarized by Couvreur et al. 2011a). Menispermaceae, today often plants of the l.t.r.f., showed a burst of diversification close to the K/T boundary (Wang et al. 2012). Seed ferns survived until well into the Palaeocene in Tasmania (McLoughlin et al. 2008). Complicating interpretation of the data, an imbalance between macrofossils (high extinction) and sporomorphs (low extinction) has been noted across the Triassic-Jurassic boundary, and that can be explained by factors that make the latter record less sensitive (Mander et al. 2010).

Groups other than plants and dinosaurs suffered; there are estimates of about 60% loss of butterfly diversity at the K/T boundary (Wahlberg et al. 2009), a mass extinction of birds in western North America, but perhaps elsewhere, too (Longrich et al. 2011), and a 83% extinction of snakes and lizards in North America (Longrich et al. 2012). Although crown-group placental mammals may be entirely Tertiary in age (O'Leary et al. 2013), and ant diversification may be little affected (but see above for other opinions). Although marine extinctions were quite common (Schulte et al. 2010; Ohno et al. 2014), both the cause(s) of K/T extinctions and even their extent remain particularly problematic for some (see Science 328: 973-976. 2010).

Estimates of the time that vegetation took to recover from the impact range from only a few thousand years in New Zealand (Vajda & McLoughlin 2007) to over a million years years (McElwain & Punyasena 2007), depending on the location of the forests. Recovery of algal primary productivity in marine ecosystems may have taken as little as the order of century or perhaps even less (Sepúlveda et al. 2009: Denmark), although most estimates of marine recovery are longer (literature in Wilf & Johnson 2004). North American snakes and lizards took perhaps 10 m.y. to recover their Late Cretaceous diversity (Longrich et al. 2012).

In North America initial recolonization may have been by swamp- and mire-loving plants, which survived the impact better (K. R. Johnson 2002; Labandeira et al. 2002b), indeed, mire vegetation was least affected by the impact (Nichols & Johnson 2008). The bolide impact in North Dakota adversely affected more species gowing along channels than those in the flood plain, and fast-growth ecological strategies were favoured: Leaves were thin and often deciduous, and there was a small increase in venation density from ca 3.5 mm/mm2 to ca 4.6 mm/mm2, i.e. ca 1.8 mm/mm2 (Blonder et al. 2014: compare this to the average difference between nonangiosperms and eudicots, ca 8 mm/mm2). This fast-growth strategy might allow the plants to deal better with changing light regimes (e.g. the "impact winter": Ohno et al. 2014 and refs.) and heterogeneities in resource availability (Blonder et al. 2014). Indeed, some time around the end of the Cretaceous there was a second shift in venation density in angiosperms, figures increasing to around 10 mm/mm2 or more as in plants of productive l.t.r.f. habitats, and this was coupled with a reduction in stomatal size and an increase in stomatal number (e.g. de Boer et al. 2012), but how this shift relates to those mentioned by Blonder et al. (2014) is uncertain, as are any long-term effects of the changes noted by the latter.

If the effect of the end-Cretaceous bolide impact on angiosperms is somewhat unclear, there were certainly major changes in angiosperm ecology and diversity in the early Tertiary. For angiosperm clades that crossed the K/T boundary, the average seed mass, initially rather low, increasing markedly (e.g. Tiffney 1986b; Collinson & van Bergen 2004; Sims 2010). This trend can be seen in Juglandaceae, with many winged disseminules, as well as in Fagaceae, which lack such disseminules (Tiffney 1986a); rather few Palaeocene fruits were fleshy (Collinson & van Bergen 2004). This increase in seed size may be linked primarily to a change in forest type, now closed and made up of tall trees with dense leaf venation, and/or to the evolution of the mammals, birds, and bats that dispersed the seeds (e.g. Tiffney 1984, 2004; Eriksson et al. 2000a, b; Mack 2000; Moles et al. 2005a, b; Eriksson 2008; Dilcher 2010); see Anderson et al. (2011) for the importance of fish as seed dispersers in the Amazon region. Large seeds are common in plants that at least initially grow in shaded habitats, providing reserves for the initial growth of the seedling, although they may also be favoured by dry conditions, or soils with low mineral nutrients, etc. (Leishman et al. 2000; Bolmgren & Eriksson 2005). Trees tend to have larger seeds than herbs; euasterids, many of which are herbaceous, tend to have small seeds (Eriksson & Kainulainen 2011). Seed-dispersing animals and the plants they dispersed may have diversified roughly in parallel (see below: e.g. Tiffney 1984, 2004; Wing & Tiffney 1987; Collinson & Hooker 1991; Dilcher 2000; c.f. Herrera 1989). The acquisition of fleshy fruits is not linked with notable increases in diversification of clades with them (Bolmgren & Eriksson 2010 and literature; c.f. Eriksson & Bremer 1991).

Seed mass of extant angiosperms currently drops quite abruptly (seven-fold) at the edge of the tropics (Moles et al. 2007: sampling in the tropics not very good). The reasons for this are unclear, but wind dispersal of smaller seeds in the open habitats that are more common outside the tropics may be involved (Lorts et al. 2008). The current prevalance of ectomycorrhizal forests and the often rather acid, humus-rich, and nutrient-poor soils that they favour in regions outside the tropics may also affect seed size, although temperate mast-fruiting ectomycorrhizal Fagaceae have notably large seeds while ectomycorrhizal Betulaceae-Betuloideae have small seeds. Indeed, Xiang et al. (2014) thought that relatively open habitats after the K/T boundary may have favoured the diversification of fagalean clades with winged disseminules, although such habitats are unlikely to have persisted.

In general angiosperm diversity in the tropics and warm temperate areas was rather low during the Palaeocene (Wilf 2008). However, by the middle Palaeocene (ca 61 m.y.) vegetation in France was diverse and also supported a diverse assemblage of herbivores, as in a number of sites far distant from the Mexican point of impact of the bolide (Wappler 2009 and references). In Colombia, the bolide event was reflected more by changes in ecological structure, less in extinction (De la Parra et al. 2007; see Graham 2010 for the vegetational history of Latin America). Fossils from the Late Palaeocene in Colombia imply that the basic familial composition of the forest was similar to that of current neotropical rainforest, although both plant and herbivore diversity were rather low (Jaramillo et al. 2006). This may reflect a rather belated recovery from the bolide impact and/or that the tropical rainforest ecosystem was just developing (Wing et al. 2009). Palaeocene and Eocene Patagonian vegetation was more diverse than its North American counterparts, and the diversity of herbivore damage in a fossil flora from the early Eocene in Argentina was appreciably greater than in comparable North American floras (Wilf et al. 2005; Iglesias et al. 2007; Wilf 2008; Wilf et al. 2011).

During the early Tertiary, angiosperms with their often dense veinlet reticulum and high leaf specific conductivity, and small and dense stomata (Watkins et al. 2010; Feild et al. 2011b; de Boer et al. 2012; Feild & Brodribb 2013), in turn associated with high rates of photosynthesis and transpiration, may have facilitated the rise to dominance and spread of widespread closed tropical forest with reliably high rainfall (e.g. Boyce et al. 2008, 2009, 2010; Boyce & Lee 2010). Venation density of angiosperm leaves had increased again around the Cretaceous-Maastrichtian, and only after this did tropical forests assume a more "modern" physiology (Brodribb & Feild 2009; Feild et al. 2011a, b). Fast decomposition of angiosperm litter, particularly associated with the deciduous habit (Knoll & James 1987, see also below), may also have speeded nutrient cycling and plant growth (Cornwell et al. 2008; Berendse & Scheffer 2009). There were also changes in wood anatomy during this period (Wheeler & Baas 1991); there is more discussion on such matters below. Jaramillo et al. (2010 and references) note that high levels of CO2 and high levels of soil moisture improve the performance of plants when temperatures are high, as earlier in the Tertiary, perhaps also another element in angiosperm success. Angiosperms began to dominate in the canopy in the Palaeocene (Jud & Wing 2013).

A late-Palaeocene Colombian flora ca 58 m.y.o. studied by Wing et al. (2009; see also Burnham & Johnson 2004) has a very high venation density and is the first fossil evidence of functional equatorial neotropical megathermal rainforest (= l.t.r.f.: Feild et al. 2011b). Such forests had a floristic composition overall quite similar to contemporary forests there (Jaramillo & Cárdenas 2013; see also Wing et al. 2009; Ricklefs & Renner 2012). Fossil record of l.t.r.f. as it is currently understood from Asia are from the early Eocene 52-50 m.y.a. of western India (Rust et al. 2010). Thus it is only in the early Tertiary, and perhaps in the Eocene rather than the Palaeocene, that vegetation takes on a more modern appearance, and a closed, multi-layered l.t.r.f. with climbers and a great variety of associated vertebrates and insects appears (e.g. Upchurch & Wolfe 1987; Wing 1987; Eriksson et al. 2000a; Morley 2000: general account; Pennington et al. 2006a; Crane & Carvell 2007: the early Tertiary fossil record; Burnham 2009: climbers). Tropical forests as we think of them, the "modern archetypal tropical rain forest" of Burnham and Johnson (2004, see their Table 1), with lianes, epiphytic ferns, bromeliads and orchids, both also with many epiphytic species, and angiosperms with large seeds and relatively large leaf blades with dense venation and entire margins, seem to be a Tertiary phenomenon (Upchurch & Wolf 1987; Schuettpelz 2006; Boyce et al. 2009: Schuettpelz & Pryer 2009; Watkins et al. 2010). In extant l.t.r.f. there are numbers of closely related species (= species in the same genus!) growing together (c.f. Turner et al. 2013), although both the extent of this phenomenon and its history are problematic.

Fires decreased, excluded by the closed forest in which there were few shrubs to support fire and in which the litter decayed quickly (Bond & Scott 2010; Bond & Midgley 2012); the Australian area may be an exception (He et al. 2011; Crisp et al. 2011; Crisp & Cook 2013).

During the Palaeocene-Eocene thermal maximum (PETM) of about 55 m.y.a., some 10 m.y. after the bolide impact, temperatures increased 3- even 8o or more - estimates vary - to mean annual temperatures (MAT) 31-34o C (e.g. Willis & MacDonald 2011). (Note that the MAT of L.t.r.f. today is ca 27.5oC, and photorespiration predominates over photosynthesis above 35o - Sun et al. 2012.) Over 2,000 gigatons of carbon were released in ca 10,000 years, the whole event lasting a mere 100,000-200,000 years (Zachos et al. 2008; McInerney & Wing 2011). Humidity, precipitation and so weathering all increased during this period (Zachos et al. 2001, 2008). Temperature swings slightly later at ca 53.5 m.y.a. may have been as or even more extreme (Sluijs et al. 2009).

In South America plant diversity and origination rates increased at about the time of the PETM, however, there is no evidence of thermal damage to the leaves (Jaramillo et al. 2010), and despite temperatures 5-70 above current values the l.t.r.f. there seems to have been largely unaffected (Jaramillo & Cárdenas 2013). In North America (Wyoming area), on the other hand, mesophytic plants, especially conifers, were temporarily replaced by species that could tolerate both increased temperature and decreased precipitation, and movement of floras and replacement of at least Cupressaceae and Podocarpaceae occurred elsewhere on the globe (Wing & Currano 2013). In west-central North America plant diversity and herbivore diversity and activity increased (Currano et al. 2008). Diversity was also very high in Late Palaeocene Gulf Coast floras, pollen diversity increasing ca 15% (Harrington & Jaramillo 2007). Major diversification of herbivorous beetles in particular and insects in general may have occurred (Farrell 1998; Wilf & Labandeira 1999; Wilf et al. 2001; Lopez-Vaaamonde et al. 2006), and Citerne et al. (2010) suggest that this was a period of floral innovation.

Evidence for extinctions at this time is unclear. The PETM may have caused some marine extinctions, and while there were shifts in the distributions of both terrestrial plants and animals, overall there seems to have been little extinction (Wing et al 2005; Willis & MacDonald 2011; Wing & Currano 2013; c.f. Mander et al. 2010). In parts of Europe there is evidence for episodic fires in a vegetation dominated by ferns and perhaps Fagales (Collinson et al. 2007). At the end of the Palaeocene there was a pronounced (ca 20%) decrease in palynological diversity in the then paratropical Gulf Coast floras (Harrington & Jaramillo 2007).

Although temperatures soon moderated, they then became gradually warmer, peaking during the Early Eocene Climatic Optimum of 52-50 m.y.a., when it was much warmer, wetter, and more temperate than it is now (e.g. Greenwood & Wing 1995; Upchurch et al. 2007; Zachos et al. 2001, 2008; Kroeger & Funnell 2011). Palm trees grew well inside the Arctic circle (Eldrett et al. 2009; Sluijs et al. 2009), and chrysomelid bruchine beetles, now restricted to palms, have been found from rather mountainous localities in Washington and Brisih Colombia in North America and Primorye, eastern Russia, in deposits of about Early Eocene Climatic Optimum in age(Archibald et al. 2014). The pollen diversity in a site from south Ellesmere Island (76o N) was equivalent to that of vegetation in the southeastern United States today (Harrington et al. 2011). This Arctic flora has also been compared with that of the Pacific Northwest, although overall there may be more similarity with eastern Asia floras, especially in the seasonality of precipitation (Schubert et al. 2012). Unique mixed deciduous broad-leaved and evergreen and deciduous conifer forests grew north of 65-70o N, and these were remarkably speciose considering that it was dark for about a third of the year (Collinson 1990; Jahren 2007 and references); there seems to have been some local endemicity (Harrington et al. 2011). Earlier, Wing (1987) had emphasized the uniformity and homogeneity of broad-leaved evergreen forests at ca 60o N, while Harrington and Jaramillo (2007) noted the mixture of families that are now temperate or tropical in their distribution in floras of the Gulf Coast in the late Palaeocene. In general, extratropical climates showed little seasonality, and this enabled plants which would seem to have mutually exclusive climatic preferences to grow together. In South America the tropical flora did not shift south when temperatures were high, rather a new kind of vegetation whose ecophysiology is unknown developed in paratropical areas below 24oS, and there the dissimilarity between tropical and extratropical floras increased (Jaramillo & Cárdenas 2013). Elsewhere, taxa whose ranges are now tropical then had much wider distributions (e.g. Wing 1987; Archibald et al. 2010; Plaziat et al 2001: Nypa; Smith et al. 2008: Cyclanthaceae; Herrera et al. 2011, Stephania; Collinson et al. 2012: survey of the middle Eocene Messel flora). Palm trees also grew well inside the Antrctic circle, too (Pross et al. 2012), with evidence of paratropical rainforest from off Wilkes Land in the early Eocene ca 51 m.y.a. (Pross et al. 2012).

A number of plant taxa now restricted to Southeast Asia were growing in Europe and North America at various times from the Palaeocene to the Miocene (e.g. Ferguson et al. 1997; Manchester et al. 2009: East Asian endemics), and there have been similar range changes in the Southern Hemisphere, for example in conifers (Wilf 2012). Southern temperate forests and Mediterranean vegetation are perhaps the best modern analogues of this rather aseasonal early vegetation. Both are notably speciose (Archibald et al. 2010), while Leslie et al. (2012) note that clade age of southern conifers is considerably greater than that of their northern counterparts, perhaps because of the persistence of milder, wetter habitats there (so shades of the early Tertiary) compared to the increased seasonality and climatic fluctuations that began to occur at the end of the Eocene in the north.

Species diversity of both animals and plants was probably at a maximum in later Eocene forests, partly because of the flatter global temperature gradients in a warmer earth (Jaramillo & Cárdenas 2013), and it has declined since (Archibald et al. 2010, 2013). Early Eocene South American fossil floras were notably diverse, even at 47oS in Patagonia, and included lianes, diversity declining only at the end of the Eocene (e.g. Jaramillo et al. 2006, 2010; Herrera et al. 2011; Wilf et al. 2003, 2011); diversity in western North America seems to have been comparable (R. Y. Smith et al. 2012). Overall, latitudinal diversity gradients were flatter or even peaked in temperate regions (e.g. Archibald 2013), as they had since the Triassic; the latitudinal biodiversity gradient, now so pronounced, with diversity decreasing strongly away from the equator, may have become evident only after this time (Mannion et al. 2012, 2013: see below).

A long-term cooling trend began at the beginning of the Oligocene (e.g. Wolfe 1978; Millar 2011; Pagani et al. 2005). Estimates are of a 30o C or more reduction in the MAT since the end of the Eocene (Jahren 2007), temperatures dropping 8.2±3.1oC alone in some 400,000 years at the beginning of the Oligocene some 33.5 m.y.a. in central North America, although apparently with little change in precipitation (Zanazzi et al. 2007). Importantly, seasonality also greatly increased, even if it was to decrease somewhat later in the Tertiary (Wolfe 1978). Seasonality began to develop in extratropical floras in general at the end of the Eocene (e.g. Wing 1987; Eldrett et al. 2009), although marked seasonality in fossil woods is a Neogene (Pliocene and since - the last ca 23 m.y.) phenomenon (Wheeler & Baas 1993); more or less ring porous woods showed a marked increase from the Palaeocene to the Eocene, and again from the Oligocene to the Miocene (Wheeler & Baas 2011). The Antarctic ice sheet appeared ca 33.5 m.y.a. at the Eocene-Oligocene boundary (Coxall et al. 2005; Eldrett et al. 2009 and references), although cooling in the Wilkes Land shelf area and spread of more temperate Nothofagus fusca-type pollen had begun by the middle Eocene (Pross et al. 2102) and there may have been short-lived periods of glaciation from as early as 42 m.y.a. (Tripati et al. 2005).

Finally, there is evidence of increased weathering of rocks at this period and through the later Caenozoic (Pälike et al. 2012)

Overall, tropical floras became less widespread after the Eocene, extra-tropical floras became less diverse and less cosmopolitan (Archibald et al. 2010), and deciduous plants became more widespread. Indeed, few Eocene leaf remains can be assigned to modern genera, and only at the end-Eocene can this commonly be done (e.g. Wing 1987; Dilcher 2000). Fiz-Palacios et al. (2011) suggested that the rate of diversification of angiosperms declined somewhat in the earlier part of the Tertiary, one decline being at about the end of the Eocene.

Temperatures in the Oligocene rebounded slightly and oscillated through the Miocene, and the mid-Miocene ca 16 m.y.a. was quite warm and wet; this was followed by a further temperature decline and aridification, latterly precipitous, to the Pleistocene (e.g. Zachos et al. 2001, 2008; Retallack 2009; Millar 2011; Crisp & Cook 2011). The great ecological importance of grasses, including those that carry out C4 photosynthesis, developed only within the last (10-)5 m.y. (e.g. Edwards et al. 2010), although the origin of this trait goes back 20 m.y. or more. The widespread Cerrado vegetation of Brazil developed at about the same time (Simon et al. 2009; Simon & Pennington 2012), as did many clades with succulent plants, whether terrestrial or epiphytic, and these often have CAM photosynthesis (Arakaki et al. 2011). In the mid-Pliocene some 3.6-6 m.y.a. MATs were 2-3o warmer than they are now and there were novel vegetation assemblages and increased diversity (Willis & MacDonald 2011). Arctic ice started developing ca 7 m.y.a. (Zachos et al. 2001), although it was still not widespread until the early Pleistocene ca 2.2. m.y.b.p. (Brigham-Grette et al. 2013).

Angiosperm groups that include speciose clades that have diversified since the Cretaceous often include many herbaceous and/or shrubby taxa in particular (e.g. Tiffney 1985a, b????). Magallón et al. (1999) noted that major core eudicot clades like Fabaceae (19,000+ species: e.g. Bruneau et al. 2008b; Bello et al. 2009) and (most of) Lamiales that together represent about 45% of core eudicot diversity appear only in the upper Cretaceous (Maastrichtian) and Tertiary. Diversification of Asteraceae (23,000+ species: K.-J. Kim et al. 2005; Funk et al. 2009c for a summary) is also Tertiary in age. Even in far older clades like Myristicaceae, crown group diversification may also be largely a Tertiary phenomenon (J. A. Doyle et al. 2004, 2008; Scharaschkin & Doyle 2005; Richardson et al. 2004; but c.f. in part Couvreur et al. 2011a, c).

What about the diversification of embryophytes other than angiosperms? Podocarps with flattened foliage units are often shade tolerant and their diversification occurred somewhat after the venation density of angiosperm leaves increased - (94-)64(-38) versus 109-60 m.y.a. (Biffin et al. 2011a; Brodribb & Feild 2009; Biffin & Lowe 2011), although overall gymnosperms did not develop the complex of changes that occurred in angiosperm leaves (de Boer et al. 2012). Gymnosperms may also have been at least locally disdvantaged by the conditions after the end-Cretaceous bolide impact and temperature changes happening at about this (Blonder et al. 2014). Indeed, divergence within extant gymnosperm clades (i.e. genera) of both Cycadales and Pinales occurred mostly later, during the mid to later Tertiary (e.g. Oberprieler 2004; Nagalingum et al. 2011; Crisp & Cook 2011; Davis & Schaefer 2011; Leslie et al. 2012; c.f. Salas-Leiva et al. 2013, in part). Extinction may have been higher in gymnosperms than in angiosperms, hence contributing to lower diversity in the former, certainly, gymnosperm clades have longer stems and shallower crowns (Crisp & Cook 2011). Brodribb (2011) and Brodribb et al. (2012) and others have emphasized that some conifers, Pinaceae in particular, are extremely successful in high light but other than high-nutrient conditions, a few species dominating a considerable area of the earth's surface.

One third (ca 3,000 species) of all leptosporangiate ferns are epiphytic (about 10% of all epiphytes, the majority of the non-angiosperm epiphytes) and they may have diversified around the PETM in the early Tertiary (Schneider et al. 2004a, b; Schuettpelz 2007; esp. Schuettpelz & Pryer 2009: Supplemental Tables 2, 3; Watkins et al. 2010). Epiphytic ferns commonly grow on angiosperms and prefer humid conditions (see Watkins & Cardelús 2012 for adaptations of these ferns), an exception, Trichomanes and relatives, had diversified in the early Cretaceous, but they are commonly epiphytic on tree ferns, a very old clade (Schuettpelz 2007; see also Schuettpelz & Pryer 2009; Rothwell & Stockey 2008: early radiations of leptosporangiate ferns). About half - 190/380 species - of clubmosses, Lycopodium s.l., are also epiphytic, and their diversification may have begun in the Late Cretaceous (Wikström & Kenrick 1997, 2001; Wikström 2001).

Mosses and liverworts for the most part seem to have undergone bouts of rapid diversification earlier (see above), but in both there was also extensive diversification in the Tertiary, in liverworts perhaps particularly in the epiphytic Porellales (Cooper et al. 2012; Feldberg et al. 2014; Laenen et al. 2104; c.f. Fiz-Palacios et al. 2011). However, there are perhaps not that many extant bryophytes, and Laenen et al. (2014) suggest that, as in gymnosperms, there may also have been massive extinction events.

Clearly, there was no simple replacement of gymnosperms, or of "bryophytes" and ferns, by angiosperms during the Cretaceous-Tertiary. Pinales in particular are very important players in current biosphere dynamics, as is discussed below. Clades of other groups of embryophytes that lack vascular cambia, such as hornworts, clubmosses, liverworts, mosses, and ferns, also diversified substantially in the post-apocalyptic world, the title of one study, "Ferns diversified in the shadow of the angiosperms" (Schneider et al. 2004), aptly emphasizing this point.

Although ecological conditions may still have been rather different from those of today, any differences are surely less than when comparing Cretaceous and extant angiosperms (Mittelbach et al. 2007).

6B. Animal Groups. An interesting and important question is, is there any relationship between the diversification of animal groups that are now more or less directly dependent on plants for food, etc., and of the plants themselves? The connection between animal and plant can be indirect: That the diversification of orb-weaving spiders, insect-eating bats (vespertilionids), stinging wasps, etc., was more or less contemporaneous with that of angiosperms is because they were eating insects, at least some of which were eating plants (see also Hawkins & Porter 2003; Penney 2004; J. S. Wilson et al. 2012b). Thus Pompilidae, wasps which almost exclusively eat spiders, radiated in the Tertiary after a Mid/Late Cretaceous origin (J. S. Wilson et al. 2012b), the speciose carnivorous Carabidae-Harpalinae (19,800 or so spp.) showing a similar pattern after originating in the Aptian/Albian ca 115 m.y.a. and then doing nothing for ca 32 m.y. (Ober & Heider 2010). Diversification of parasitic and hyperparasitic wasps such as the hyperdiverse Chalcoidea (the chalcid wasps), perhaps half a million species strong and altimately dependent on plants, is most intensive in the Tertiary (Heraty et al. 2013). Similarly, the fleshy fruit "niche" was exploited by particular groups of flies, particularly by Drosophilinae, and the relationships between particular fruits and flies may be very close (Ashburner 1998: alcohol dehdrogenase in flies; Harry et al. 1996, 1998: fig-breeding Lissocephala). In the rest of this section I will focus on animal groups that are particularly important for flowering plants and in which the relationship between animal and plant is direct.

Plant-feeding insects make up at least one quarter of all described species, and over half the beetles (Janz et al. 2006; Farrell 1998; Hunt et al. 2007). There are well over 100,000 species of extant phytophagous beetles in some five clades, particularly the chrysomelids and curculionids, that eat angiosperms, but initial beetle diversification occurred in the Jurassic (Farrell 1998, but c.f. dates; see also Mayhew 2007; Hunt et al. 2007). Since there seems to be no strong association of diversification and the adoption of herbivory, or between shifts from gymnosperms to angiosperms as a food source, and also because over 100 extant beetle lineages had diverged before the beginning of the Cretaceous 140 m.y.a., beetle and angiosperm evolution seem not to be tightly linked (Hunt et al. 2007). Diversification may have begun first on monocots and then moved on to broad-leaved angiosperms (Reid 2000). About two thirds of herbivorous beetles eat only one or a few species of angiosperms, i.e. they are are mono- or oligophagous. Herbivorous beetles and herbivory in particular and insects in general increased with the warming tend of late Palaeocene-Eocene (Farrell 1998; Wilf & Labandeira 1999; Labandeira et al. 2002b; Wilf et al. 2001; Lopez-Vaamonde et al. 2006, Wilf 2008). Kergoat et al. (2005) suggest that diversification of bruchids and Fabaceae may have occurred more or less together; the association between these two is particularly close, some kind of co-evolution.

Species of ants represent only ca 2% of known insect species, but they make up one third of insect biomass, and overwhelmingly dominate in samples collected when rainforest canopies are fogged (Davidson et al. 2003; Pie & Tschá 2009). Unfortunately the relative timing of diversification of ants and angiosperms is unclear. Ants are an old group, and are sister to the Apoidea (spheciform wasps + bees: e.g. B. R. Johnson et al. 2013). Crown-group diversification of ants may have begun 176.4-132.6 m.y.a. (Moreau et al. 2006: depends on calibration used), 143.2-108.6 m.y.a. (Brady et al. 2006), or 158-139 m.y.a. (Moreau & Bell 2013); Grimaldi and Engel (2005) date stem ants to only some 120 m.y.a.. Interestingly, extant members of "basal" ant clades live largely underground (Rabeling et al. 2008). Moreau et al. (2006) thought that ant diversification was dependent on the radiation of angiosperms, which had occurred by around 100 m.y.a., and lineage through time plots showed a dramatic accumulation then. On the other hand, Pie and Tschá (2009) suggested that the rate of divergence of the main clades was constant, but within these clades diversification rates had varied greatly.

Between 100 and 60 m.y. the rise of angiosperm-dominated forests may have been tracked by ant diversification (Moreau et al. 2006), although Moreau and Bell (2013) are less certain about the connection between the two. Certainly, all ant subfamilies are Cretaceous in age (Moreau & Bell 2013); the question is, what kind of forest was around then? Ants may have undergone their early evolution in pretropical forest, moving in to tropical rain forest (they are particularly diverse in New World tropical rain forest) as it developed (Moreau & Bell 2013). Although many ground-dwelling ants are carnivores, the tree-loving Formicinae and Dolichoderinae are canopy-dwellers and eat plant materials (Rico-Gray & Oliveira 2007). Certainly, evidence suggests that the ecological dominance of ants began later in the Eocene, 50-35 m.y.a., ants first becoming common in the fossil amber record then (e.g. Grimaldi & Agosti 2000; Moreau et al. 2006; Dunn et al. 2007; Grimaldi & Engel 2005; LaPolla et al. 2013: over 5% of insects).

Plant-ant associations evolved at about this time (Grimaldi & Agosti 2000; Dunn et al. 2007). Diversification of the ecologically very important herbivores of the New World tropics, the ca 40 species of leaf-cutting attine ants, occurred quite recently - stem group estimates are (16-)13-9(-7) m.y., crown group estimates are (14-)11-8(-6) m.y. (Schultz & Brady 2008). The now widespread associations between ants, plants and sap-sucking hemipterans (e.g. Ueda et al. 2008) are mid-Tertiary in age or later. Here sugar obtained either directly from the extra-floral nectaries of plants, or indirectly, for example by way of their homopteran associates, is an important food/energy source for many arboreal ants (E. O. Wilson & Holldöbler 2005). The homopterans are Auchenorrhyncha, leaf hoppers and spittle bugs, and Sternorhyncha, scale insects and aphids; obligate bacterial endosymbionts are well known from homoptera, and members of Rhizobiales are particularly associated with herbivorous ants (Davidson et al. 2003; Russell et al. 2009). The oldest extra-floral nectaries known are on Populus fossils from the Oligocene (Pemberton 1992), but extra-floral nectaries are not known in extant magnoliids and members of the ANITA grade (Weber & Keeler 2013).

Ants also disperse the seeds of many angiosperms. Elaiosomes, quite commonly found on small seeds or fruits (Beattie 1985; Rico-Gray & Oliveira 2007), vary considerably in their morphological nature and chemistry (e.g. Bresinsky 1963: Kubitzki et al. 2011). They provide food for ants which eat the elaiosomes, but not the seeds themselves (c.f. granivorous ants), and aid in seed dispersal and perhaps in the establishment of the seedling. The fatty acids in the elaiosomes that attract carnivorous ants may mimic those in their animal prey, the elaiosomes being "dead insect analogue[s]" (Carroll & Janzen 1973: p. 235; Hughes et al. 1994). Myrmecochory is particularly common in the ground flora of the east North American and European forests, and some 1,500 species in Australia, a number of which are woody, are also involved (Sernander 1906; Berg 1975; Orians & Milewski 2007; Lengyel et al. 2009, and references), although Türke et al. (2011) suggest that gastropods may also be involved in the distribution of seeds with elaiosomes. It is also common in the Australian and South African floras (Milewski & Bond 1982; Bond et al. 1991). Interestingly, perhaps half the species of stick insects (Phasmatodea) lay eggs that mimic seeds of myrmecochorous plants (Hughes & Westoby 1992).

Conservative estimates are that some 11,500 species of angiosperms are myrmecochorous (Lengyel et al. 2009, 2010) and the trait is highly polyphyletic - caruncles have evolved ca 13 times in Euphorbia alone (Horn et al. 2012). Myrmecochorous clades have about twice as many species as their non-myrmecochorous sister clades (Lengyel et al. 2009). Thus myrmecochory in clades such as Polygalaceae-Polygaleae seems to be linked to their diversification and is a mid-Tertiary phenomenon (Rico-Gray & Oliveira 2007; Forest et al. 2007b; Lengyel et al. 2009, 2010, see also Fokuhl 2008).

The phytophagous beetle sister taxa, weevils (Curculionoidea) and leaf beetles (Chrysomeloidea), include about half of all herbivorous insects. They may have diversified largely in parallel with angiosperms (Farrell 1998), although initially being associated with gymnosperms, diversification beginning there in the Jurassic (e.g. Labandeira et al. 1994; Farrell 1998; McKenna et al. 2009). However, given the evidence already mentioned for quite recent diversification in some gymnosperm clades and the questionable association between phytophagy, gymnosperms or angiosperms and diversification (Hunt et al. 2007), the story need to be rethought. Indeed, Chrysomelidae may diversify rather later than angiosperms, perhaps (86-)79–73(-63) m.y.a. in the Late Cretaceous-Eocene (Gómez-Zurita et al. 2007; also Winkler & Mitter 2008), and especially in the early Tertiary. Crown-group diversification of major angiosperm-associated weevil clades may have been underway by the Aptian 125-112 m.y.a., with a "massive diversification" of Curculionidae - now ca 90% of all weevils - 112-93.5 m.y.a. during the Cretaceous terrestrial revolution (McKenna et al. 2009).

[Paragraph to develop.]Xylocopinae entered the Tertiary as four clades that had diverged about 20 m.y. before, but in the early Tertiary diversification increased considerably; before the Tertiary there is likely to have been extinction in these clades (Rehan et al. 2013). Colletidae, a group of generalist bees, showed no obvious burst of Tetriary diversification (Almeida et al. 2011).

Lepidoptera, with ca 160,000 described and perhaps 500,000 total species, are the biggest insect clade almost exclusively dependent on plants, both as adults and as larvae (Powell et al. 1998; Mutanen et al. 2010). Unfortunately, relationships between the main clades are poorly understood, perhaps reflecting very fast initial evolution (Mutanen et al. 2010). Diversification of lepidoptera may have started on Jurassic gymnosperms (Labandeira et al. 1997), or rather later (Grimaldi 1999). Papilionoidea (butterflies) are well embedded in monotrysian lepidoptera, and Heikkilä et al. (2011) suggested that the main clades, = families, within an expanded Papilionidae diverged quickly in the early Cretaceous, ahile Wahlberg et al. (2009) thought that family clades were largely of late Cretaceous origin. Estimates for diversification within clades representing extant subfamilies are after (e.g. Vane-Wright 2004; Wahlberg et al. 2009; Wheat et al. 2007; Heikkilä et al. 2011), more or less at (Simonsen et al. 2011, or before (Michel et al. 2008; Pohl et al. 2009: 113-84 m.y.a., gene duplications) the K/T boundary. Thus diversification of of Nymphalidae-Nymphalinae seems to be a post K/T boundary phenomenon, occurring 65-33 m.y.a. (Wahlberg 2006), and the same is true of Nymphalidae-Papilioninae (Zakharov et al. 2004). Diversification may have begun before, as in Pieridae which began diversifying the the Late Cretaceous (112-)95(-82) m.y.a. (Braby et al. 2006), but again, much speciation seems to have been in the Tertiary (see Simonsen et al. 2011 for a range of divergence times). Caterpillars of these groups tend to show rather high food-plant specificity. Butterfly (and other herbivore) clades that survived the K/T boundary may initially have eaten several different food plants, but subsequently they diversified on a more restricted set of plants or they shifted their food preferences (Janz et al. 2006; Nylin & Wahlberg 2008; Fordyce 2010; Nylin et al. 2014).

Overall, there seems to be no simple connection between the diversification of plants and the insects associated with them. Some bouts of insect diversification may have occurred (well) after the appropriate angiosperm host clades originated, particularly in herbivores (implicit in Futuyma 1983; see Funk et al. 1995; Percy et al. 2004; Lopez-Vaamonde et al. 2006; leaf-mining Gracillaridae; Winkler & Mitter 2008; McKenna et al. 2009; Janz 2011; Cruaud et al. 2012b). Certainly diversification and overall diversity of phytophagous insect groups may increase after they adopt new hosts (Janz et al. 2006); subsequently the relationship may be reversed. Close co-evolution seems to be the exception (but see Kergoat et al. 2005 below) rather than the rule, and is most evident in shallow rather than deep clades (Berenbaum & Passoa 1999 for references; c.f. Farrell & Mitter 1998); looser co-evolution, with host shifts associated with taxonomy, may be more common (see Futuyma & Mitter 1996). Patterns of relationships between plants and herbivores/gallers may differ from those shown by plants and pollinators. In the latter, diversification of plant clades may occur despite (in the context of some definitions of co-evolution) low diversities and little evolution of their major pollinators (Ramírez et al. 2011; Althoff et al. 2012; Schiestl & Dötterl 2012).

Currently, vertebrates facilitate the wide dispersal of rather large propagules of rain forest trees and the pollination of the rather widely dispersed individuals that produce them (e.g. Regal 1977); mammals in particular are also herbivorous. Mammals have a substantial fossil history before the Cretaceous, but underwent notable diversification in the early Tertiary (Bininda-Emonds et al. 2007; see also Stadler 2011a). Indeed, a recent comprehensive morphological analysis - over 4,500 characters were scored - suggests that crown-group placental mammals are Tertiary in age, age estimates for particular clades being up to 30 m.y. younger than those in earlier studies (O'Leary et al. 2013). For primates, initially diversifying in the arboreal habitat as omnivores, eating plants and their associated insects, see Sussman et al. (2013).

Phyllostomid bat diversification and that of angiosperms is associated, but for different immediate reasons. while fruit-, pollen- and nectar-eating bats (leaf-nosed bats, the phyllostomids) because there was a greater diversity of fruit types and an abundance of flowers (Jones et al. 2005; Teeling et al. 2005). Both frugivory and nectarivory have arisen in parallel, even in New World bats, and some combination of insectivory with these modes of nutrition is common (Datzmann et al. 2010; Rojas et al. 2011). Crown-group diversification of phyllostomid bats is estimated at between 43.1 and 33.4 m.y.a. (probably in the late Eocene), with much diversification 26-16 m.y.a. in the late Oligocene to mid-Miocene (Datzmann et al. 2010; Rojas et al. 2011), indeed, adoption of a plant diet seems to have accelerated bat diversification rates (Datzmann et al. 2010: see also below).

For a phylogeny of all birds, see Jetz et al. (2012). Radiation of important seed-dispersing birds such as Columbiformes (pigeons) occurred some (63.6-)54.4(-46.1) m.y.a. (95% CI), also in the earlier Tertiary (e.g. Tiffney 1986b; Pereira et al. 2007). Bird pollination is also likely to be a Tertiary phenomenon, with three different groups of birds (Trochilidae, Nectariniidae, and Meliphagidae) being most important (Cronk & Ojeda 2008); hummingbirds in particular diversified only in the Pliocene (Bleiweiss 1998a; McGuire et al. 2007, 2014).

Overall, our understanding of the ecological-evolutionary connections between animals, in particular insects, and plants remains unclear (e.g. Futuyma 1983; Janz 2011); there is no simple underlying theory to explain the variety of the interactions. We know little about the details of long-term evolutionary-ecological interactions of plants and the organisms associated with them (see above; Fine et al. 2004 for habitat specialization and herbivore activity in the Amazon, also Janzen 1974a). Furthermore, the sheer complexity of the matrix of defensive compounds inside the plant make simple explanations of the evolutionary dynamics of plant-insect relationships difficult. As Berenbaum and Zangerl (2008: p. 806) note, idiosyncracy is central to the nature of chemical co-evolution, a problem that can only be exacerbated by the difficulty of understanding ecological relationships over time. Yet, as Grimaldi and Engel (2005: p. 625) note, "Despite the fact that the mechanism is obscure as to how insects diversified with angiosperms, the overall patterns are extremely clear that the angiosperm radiations had a profound impact on insects, and vice versa."

6C. Latitudinal Gradients of Diversity. Details of the relationships between groups diversifying in seasonal temperate regions and their tropical relatives have been a matter of speculation for some time (e.g. Bews 1927). Judd et al. (1994) found that the temperate family of temperate-tropical family pairs often arose from within the tropical family, making the latter paraphyletic; the temperate groups tended to be herbaceous, the larger group from within which they arose, woody.

A question is, what global patterns of biodiversity can be discerned, what causes them, and when have they been evident (e.g. Kier et al. 2005)? Broadening the focus to incorporate past climates changes the perspective of such questions. Today, plant (and animal) diversity is indeed broadly correlated with climate, and this is strongly seasonal over much of the globe (Fischer 1960; Francis & Currie 2003: families!, see Qian & Ricklefs 2004 for problems with distribution maps; Hawkins et al. 2011 for a reanalysis). Biodiversity gradients in the past have been most obvious in cooler/glacial periods (Mannion et al. 2013; c.f. Benton et al. 2010). As we have just seen, reduced seasonality characterized the Palaeocene-Eocene, and then there was a much more homogeneous and very diverse flora, with groups like palms being found far to the north and south of their current distributions and considerable diversity at higher latitides (see above). Climates most similar to those of the early Tertiary are now to be found mostly in tropical and to a certain extent south temperate areas (Janzen 1967; Platnick 1992; Chown et al. 2004; Ghalambor et al. 2006). For groups like birds, mammals, insects, and the like, latitudinal gradients of diversity may be a post-Eocene phenomenon (Archibald et al. 2010, 2012; Rose et al. 2011: but temperature gradient similar to that of today; Mannion et al. 2012; also Boyero 2014 for literature); whether or not it is found in prokaryotes is unknown (Timling & Taylor 2012 and references). In soil fungi overall diversity increases towards the equator, although less so in Africa, but the diversity of ECM fungi increases in mid to high northern latitudes and ERM fungi also show a diversity increase towards the poles, in both cases consistent with the distribution of their seed plant associates (Wardle & Lindahl 2014; Tedersoo et al. 2014b: q.v. for details of distributions of functional types and taxonomic groups, whole soil column not sampled). Even today, a few clades like Polygonaceae are most diverse away from the tropics (Kostikova et al 2014b).

Much literature focuses on establishing mechanisms that would cause/explain the current global patterns of diversity, where overall diversity is greatest in the tropics (e.g. Willig et al. 2003; Mittelbach et al. 2007 for a critical summary). Latitudinal gradients have been explained by such things as higher rates of speciation or extinction, differences in the amount of incident energy, differences in habitable areas, and the like. Thus there is perhaps a connection between diversity and environmental energy variously estimated (and this links with latitude), species richness and the rate of molecular evolution, but the connections are independent (Davies et al. 2004b; Moser et al. 2005; Jaramillo et al. 2006). Allen et al. (2002) thought that productive environments could support more individuals, therefore ceteris paribus more mutations and evolution. Attempts to explain current diversity patterns along similar lines continue (e.g. Brown et al. 2004; Condamine et al. 2011; Gillman & Wright 2014; Brown 2014).

Wiens and Donoghue (2004) suggest that phylogenetic niche conservatism might contribute to tropical diversity; groups that are tropical in origin adapt with difficulty to seasonal temperate climates (and vice versa). In general, in North America older plant clades tend to be more southerly in distribution, younger ones are more cold-tolerant and northern, perhaps supporting the idea of niche conservatism. The clades involved are likely to have evolved in the Cretaceous, i.e. before global latitudinal climatic patterns were established (Hawkins et al. 2014 and references: conifers not included). B. T. Smith et al. (2012) refined the niche conservatism hypothesis and proposed that in New World vertebrates, at least, families with southern origins were more likely to show conservatism than those of northern origin. Southern families have not penetrated the highly seasonal Nearctic, perhaps not simply because there is a smaller southern temperate zone, but because that zone is temperate in a different way (more equable) to northern temperate zones, while northern families have experienced greater environmental heterogeneity and are often found in both temperate and tropical areas. Evapo-transpiration, topographical diversity, and related factors are also important (Kreft & Jetz 2007). Linder (2008) linked the timing of diversification in particular areas to whether or not the local environment had been climatically and geologically stable during the Tertiary. Lamanna et al. (2014) looked at the alpha, beta and gamma componants of functional trait space (specific leaf area, seed mass, plant height), noting that trait hypervolume was greater in temperate areas, although it was unclear how species filled this space. However, teasing apart historical and ecological signals in patterns of plant diversity is not at all straightforward (Ricklefs 2005).

Thinking about these patterns in the context of the interactions between angiosperms and their fungal associates which are in turn linked to plant diversity, soil fertility, carbon content, etc., may provide another way of approaching the problem (see below). The geographic distribution of ECM-dominated communities, paricularly pronounced polewards and particularly in the northern hemisphere, may contribute to the obvious but still puzzling (from the causal point of view) current latitudinal gradient in diversity (e.g. Fischer 1960; but c.f. ), in particular, to the hypothesis that diversity is in some way linked with productivity (e.g. Willig et al. 2003). Indeed, communities growing in more extreme and unproductive conditions tend not to be species-rich (Gillman & Wright 2006; Cusens et al. 2012; c.f. Adler et al. 2011: focus on herbaceous communities). Plants in cooler climates have larger ecosystem turnover times for carbon: Figures for tropical, temperate and boreal forests and tundra are ca 14.2, 23.5, 53.3, and 65.2 years respectively (Carvelhais et al. 2014), and its is in boreal forests in particular, but also in many temperate forests, that ECM plants are so abundant. Laliberté et al. (2013) discussed diversity in terms of the youth of the soils; tropical soils were older and more strongly weathered and supported a diverse vegetation, soils at high latitiudes were younger, less weathered, and supported less diversity. However, although they noted that there were different forms of nitrogen, for example, in the soil, the mycorrhizal status of the vegetation also needs to be taken into account in such considerations (see also (see below).

7. Flowers and Pollination.

7A. Flowers, Pollination and Fertilization. Most narratives of angiosperm evolution focus on flowers and fruits and their influence on speciation. Thus the success of angiosperms has been attributed in considerable part to the evolution of flowers (e.g. Eriksson & Bremer 1992; Dilcher 2000), while Burger (1981) saw insect pollination as a key to the diversification of angiosperms, insects being able to find isolated plants in small populations, and angiosperms were able to subdivide the environment effectively. The flower can be considered a key innovation or a group of innovations, thus Frame (2003) emphasized flexibility in construction of the flowers, the speed of the reproductive cycle, the closure of the carpels, and the fact that flowers are edible hence attracting potential pollinators as contributing to the sucess of angiosperms. Monosymmetry in particular has often been thought of as a key innovation (e.g. Donoghue et al. 1998; Neal et al. 1998; Endress 2001; Sargent 2004). Pollination, especially by insects, but also bats and other mammals as well as birds, and seed dispersal, especially by mammals and birds, may interact; both can increase outcrossing, gene flow in general, and speciation (e.g. Kay et al. 2006; Kay & Sargent 2009).

Successful pollination entails that the pollinator follows a more or less complex and specific set of cues. Early angiosperms may have had what we would describe as rather generalized flowers, yet the plesiomorphic condition for pollination specificity in bees seems to be oligolecty, that is, bees pollinated one or a few species, all more or less related; this may have facilitated early angiosperm evolution (Danforth et al. 2006; Sipes et al. 2006; Michez et al. 2008). Floral specialization has increased over evolutionary time, "specialized" monosymmetric flowers in which precise interactions between plant and pollinator are needed for effective pollination becoming more common, yet the bees that pollinate them are likely to be more polylectic (generalist). Thus species of the polylectic Apidae visit over twice as many families of flowering plants as do those of Halictidae and over five times those of Colletidae (Waser et al. 1996). I will return to these issues later. Floral rewards and how they are offered vary: Some plants, probably including most early angiosperms, offer only pollen, various kinds of nectaries are found in other angiosperms, e.g. septal nectaries in many monocots and receptacular nectaries of one sort or another in core eudicots, while oils and fragrances are minor rewards and deceit is surprisingly common.

Adoption of syncarpy seems to be an important evolutionary event (e.g. Friis et al. 2006b). It has evolved seventeen or more times independently, while a compitum, allowing pollen tubes from one stigma to pollinate the ovules in more than one carpel, also evolved in three quarters of these cases (Armbruster et al. 2002). Members of the ANITA grade - perhaps not Cabombaceae - often have an extragynoecial compitum in which pollination of ovules in more than one carpel from pollen landing on a single stigma is possible (e.g. Williams et al. 1993; Lyew et al. 2007; Williams 2009 - see also Igersheim & Endress 1997; Endress & Igersheim 2000; X.-F. Wang et al. 2011). The development of a style allows competition among gametophytes (Mulcahy 1979) and may also be associated with an increase in the size of pollen grains (Roulston 2000 for references). Self pollination is hindered by sporophytic and gametophytic incompatibility (see Ingrouille & Chase 2004), and less effectively by protandry or protygyny (the latter is the basal condition for flowering plants). Closed carpels also protect the ovules and they often become much elaborated as the seeds mature, so promoting dispersal. The evolution of the carpel may have allowed the parental sporophyte to control both fertilization and the allocation of resources to the seed (Lord & Westoby 2012 and references).

Why there should be substantial variation in embryo sac development at the base of the angiosperm tree (and sporadically elsewhere, too) that affects the balance of maternal and paternal genes in the parent sporophyte-endosperm-seedling system, is not well understood. However, a higher ratio of paternal genes in the endosperm may lead to more "selfish" behaviour of individual endosperm tissues as they scavenge nutrients at the expense of other ovules in the carpel (e.g. Friedman et al. 2008; esp. Friedman & Ryerson 2009) - hence perhaps the rather low ovule number (per carpel) of many ANITA-grade angiosperms which have exactly this higher ratio. Endosperm, tissue involved in the nutrition of the embryo and with both maternal and paternal genomes (usually with a diploid maternal and a haploid paternal contribution) is unique to angiosperms, although there is controversy over its origin (c.f. e.g. Friedman & Williams 2004 and Nowack et al. 2007). As Olsen (2004: p S215) noted, "In spite of recent progress in understanding angiosperm phylogeny, all of the main questions regarding the evolutionary history of the nuclear endosperm remain unresolved." - and this is true of endosperm evolution in general.

Angiospermy is also associated with a number of changes in the gametophyte phase of the life cycle, which is usually notably shorter than that of extant gymnosperms. Thus the rate of pollen tube growth in angiosperms is much faster than that of extant gymnosperms - 80-600 µm/hour in ANITA-grade angiosperms (overall 60[Fagaceae]-20,000 µm/hour) versus 10-20 (Gnetum) µm/hour in gymnosperms (Hoekstra 1983; esp. Williams 2008, 2009; also Rudall & Bateman 2008). Fertilization occurs within about 24 hours in angiosperms as compared to seven days - often far more - in most extant gymnosperms (Williams 2008). Speedier pollen tube growth may be helped by the evolution of callose plugs in the tube and a wall made up largely of callose, both apomorphies of angiosperms; gymnosperms lack these plugs and have a cellulose-based pollen tube wall (Williams 2008; Parre & Geitmann 2005: mechanical properties of callose). Much development of the female gametophyte occurs after pollination in gymnosperms, and although less in Gnetum, even there the ovule increases appreciably in size between pollination and fertilization), whereas in angiosperms there is little or no increase (Leslie & Boyce 2012). Conversely, there is little growth of the ovule after fertilization in most gymnosperms, reserves for the developing ovule having already been sequestered in the female gametophyte. Since few reserves are committed to angiosperm ovules with their tiny female gametophytes, when unfertilized ovules abort, little is lost. After fertilization, however, resources are channelled to the developing embryo, a transfer mediated by the evolutionarily novel endosperm tissue; it is as if growth of the ovule had resumed (Sakai 2013).

Overall, angiosperms tend to become mature at a younger age than do gymnosperms (Bond 1989; Verdú 2002). The whole life cycle is speeded up (Stebbins 1965, 1981), the evolution of carpels faciltating maximum seed production, seed dispersal, and seedling survival (Stebbins 1981). Seedlings of angiosperms grow faster than those of gymnosperms; again, time to maturity is reduced (e.g. Bond 1989; Coiffard et al. 2006).

7B. Major Clades With Monosymmetric Flowers. A number of large clades (2,000+ species each) can be characterised by features that seem likely to affect diversification/speciation, although the lack of firm age estimates for these clades remains an obstacle in understanding this. Five of these major clades, Orchidaceae, Zingiberales, Lamiales (at the node [[Calceolariaceae + Gesneriaceae] The Rest]), Fabaceae, and Asteraceae, have a preponderance of members with monosymmetric flowers. Of course, reversion to polysymmetric flowers has occurred, most notably in Fabaceae-Mimosoideae. Together with some rather smaller clades, e.g. Campanulaceae-Lobelioideae, Caprifoliaceae s.l., Lecythidaceae-Lecythidoideae and Iridaceae, these few clades comprise almost one third of all angiosperms. Indeed, diversification in many clades with monosymmetric flowers seems to be greater than that in their sister taxa with polysymmetric flowers (Sargent 2004; Kay & Sargent 2009; c.f. Kay et al. 2006), perhaps because pollinator fidelity is increased.

However, as more is known about floral morphology and development, a clear definition of monosymmetry has become elusive. From a structural point of view, many flowers are monosymmetric at some stage of their development (Endress 2008a, also 1999, 2001b; see also Characters). Melastomataceae are particularly difficult to categorise, some species having strongly monosymmetic flowers, others polysymmetric, and yet others are intermediate; this is why they are not included in the list below. Many highly reduced flowers are also monosymmetric, not only in Poaceae (see below), but also in the speciose Piperaceae, etc.. On the other hand, nany more or less compact inflorescences are functionally polysymmetric flowers, and the monosymmetric peripheral flowers in Asteraceae, some Brassicaceae (e.g. Busch & Zachgo 2007), Adoxaceae and Apiaceae accentuate this functional equivalence of the inflorescence; the often strongly monosymmetric peripheral flowers are the visual equivalent of petals. Inflorescences may be functionally equivalent to a monosymmetric flower, as in Euphorbia-Pedilanthus, some Proteaceae, etc., while polysymmetric flowers of Iridaceae may be functionally monosymmetric (see below). It is unclear what to include in the class "flowers monosymmetric".

There are five large clades with monosymmetric flowers. 1. Orchidaceae (ca 20,000 species) are ground-dwelling or epiphytic and in part myco-heterotrophic herbs of small, sometimes moderate size producing as many as millions of tiny, wind-dispersed seeds per flower. The tepals are more or less free and the flowers, with their distinctive and complex morphologies centred on the gynostemium (stamens and stigma-style all congenitally fused) and labellum (median tepal of the inner whorl), are often inverted. Deceit pollination is particularly common, but pollinators also visit for fragrance and nectar rewards. Although the diversity of floral form in Orchidaceae is great, it is attained by variation on a rather limited basic theme. 2. Zingiberales (2,100 species) are quite large tropical plants, mostly herbs and with large flowers. Their fruits usually have only a moderate number of seeds that are mostly animal dispersed. Flowers in Zingiberales vary considerably in orientation, the parts that are petal-like, number of stamens, etc., and from this point of view are more variable than Orchidaceae. (Note that many taxa in Commelinales, sister to Zingiberales, also have monosymmetric flowers, and it is possible the the common ancestor of the two orders had such flowers.) 3. Core Lamiales (21,000 species) are often more or less herbaceous plants perhaps particularly abundant oustide the tropics, although there are many tropical members; woodiness is more common there. Individual flowers are moderate to quite large in size, each usually producing quite many and small seeds; in general seed dispersal is by wind. Although clades like Lamiaceae have only four seeds per flower, they are still quite small. Most of the monosymmetric 4. Fabaceae (19,400 species, of which 3,300 are in the polysymmetric Mimosoideae) have inverted keel flowers with more or less free petals (Stirton 1981). The plants are either trees, especially common in neotropical forests, or widely distributed herbs. Dispersal is either autochorous (ballistic) or animal-mediated; there are rather few seeds per fruit. Many Fabaceae are nitrogen-fixers, and the family is noted for the diversity of secondary metabolites that it produces, sometimes in association with endophytic fungi.

Of the smaller but still quite large clades in which monosymmetry predominates, 5. Campanulaceae-Lobelioideae include some 1,200 species of laticiferous herbs or shrubs often with slit-monosymmetric flowers that have plunger-type secondary pollen presentation devices. Their dehiscent fruits have many small seeds. 6. Caprifoliaceae comprise some 850 species; the flowers are often rather weakly monosymmetric and the indehiscent fruits have at most few seeds. 7. Some 200 species of Lecythidaceae-Lecythidoideae (Ericales) are trees that are a prominent element of neotropical forests. The polystaminate androecium alone is monosymmetric, the fruit is large, and the seeds are few and large. In 8. Iridaceae, monosymmetry of the flowers of the speciose Gladiolus is obvious. However, from the point of view of the pollinator the flowers of Iris, Moraea, etc., are also monosymmetric; a single Iris flower consists of three strongly monosymmetric meranthia or part-flowers (see also Westerkamp & Claßen-Bockhoff 2007). All told some 750+ species have functionally monosymmetric flowers. The fruits have moderately numerous seeds. 9. Polygalaceae, with some 1,050 species the majority of which are monosymmetric, are phylogenetically close to Fabaceae, although the exact relationships of the two are unclear (see Bello et al. 2009). They have keel flowers that are superficially like those of many Fabaceae, although different parts are involved (Westerkamp & Weber 1999). The fruits usually have few seeds and myrmechory is common.

The final clade to be mentioned here is the insect-pollinated 10. Asteraceae (23,600 species). These are mostly herbaceous to shrubby plants with small flowers that are aggregated into heads or capitulae; in most species at least some flowers of each capitulum are monosymmetric and secondary pollen presentation is widespread. Only a single usually quite small seed per flower is produced, and dispersal is often by wind. Each capitulum is functionally a single polysymmetric or haplomorphic flower which produces quite numerous seeds. Asteraceae are also noteworthy i.a. for the diversity of secondary metabolites they contain.

Diversification as a possible result of the acquisition of monosymmetry can be studied on much finer evolutionary scales. For instance, Stebbins (1974) suggested that monosymmetry had evolved more than 25 times within angiosperm families, Westerkamp and Claßen-Bockhoff (2007) noted that it was found in 38 families; it has in fact evolved hundreds of times (see also Endress & Matthews 2006a; Endress 2008a; Jabbour et al. 2009, esp. 2014), and even within Asteraceae CYC2c different paralogs are involved in the expression of the monosymmetric (ray flower) phenotype (Chapman et al. 2012). Of course, understanding just how many origins there have been depends critically on the evolutionary assumptions we make (e.g. Endress 1997a; Donoghue et al. 1998; Reeves et al. 2003; Cubas 2004; Jabbour et al. 2008) and the definition of monosymmetry that is adopted.

Different pollinator groups have different floral preferences. Adult Lepidoptera prefer to visit radiate flowers, that is, polysymmetric flowers with a definite number signal (e.g. three-merous, five-merous flowers) and that have enclosed nectar (e.g. Leppik 1957). In Apidae, bumble bees (Bombini) in particular appear to have an innate preference for monosymmetric flowers (Leppik 1957; Kalisz et al. 2006; Rodríguez et al. 2004). Honey bees (Apini) frequent polysymmetric (radiate) flowers with relatively accessible nectar (for a review of the cues used, see Horridge 2009). Halictidae-Rophitinae (sister to all other halictids) prefer to visit flowers of asterids, especially those of the lamiids, although other plants are also visited (Patiny et al. 2008).

Polylectic or generalist bees such as bumble bees often visit flowers with complex, monosymmetric corollas which the animal has to learn to work before visits are effective, while more specialist oligolectic bees prefer to visit shallow often polysymmetric flowers with easily accessible rewards (Wcislo & Cane 1996). Thus oligolectic basal megachilids pollinate polysymmetric and sometimes rather large flowers, while more polylectic derived members commonly pollinate monosymmetric Fabaceae and Lamiaceae (for their pollination, see Westerkamp 1997), or polysymmetric Boraginaceae (Litman et al. 2011; Sedivy et al. 2013).

Euglossine bees and bumble bees (see below) in particular pollinate monosymmetric flowers; Westerkamp and Claßen-Bockhoff (2007) consider such flowers to be the "ultimate response" to bees. Birds also visit monosymmetric flowers, and in the gullet-type ornithophilous syndrome stamens in the mouth of the flowers deposit pollen on the head of the pollinator. The development of monosymmetric flowers may be linked to the evolution of dichogamy (separation of the time of pollen dispersal and stigma receptivity), in particular, to that of protandry (Kalisz et al. 2006). However, dichogamy is widespread, and even the polysymmetric or haplomorphic flowers of ANITA grade angiosperms are dichogamous, being protogynous.

Most of the plant clades just mentioned are more or less herbaceous. There are long-standing suggestions of a correlation between the rate of molecular evolution and plant habit: Molecular evolution is faster in herbs/annuals (e.g. M. A. Wilson et al. 1990; Bousquet et al. 1992: esp. chloroplast genes; Gaut et al. 1992: chloroplast rbcL gene, grasses evolve notably faster even than other monocot herbs, 1996; Barraclough et al. 1996: rbcL gene; Andreasen & Baldwin 2001; Soria-Hernanz et al. 2008: ITS, correlation not very strong; Rydin et al. 2009b; Barker et al. 2009; Korall et al. 2010 [ferns]; Müller & Albach 2010; Yue et al. 2010; Frajman & Schönswetter 2011; c.f. Whittle & Johnson 2003: comparisons of branch lengths of species pairs, ?sampling; Gaut et al. 2011: summary). Both chloroplast and nuclear genes show an increased rate of molecular evolution (Gaut et al. 2011), but not all genes are equally affected (Yue et al. 2010).

In a series of extensive analyses of both monocots and eudicots, Smith and Donoghue (2008) confirmed that there are usually substantial increases in the rate of molecular evolution in herbs as compared to trees, shrubs, or simply to plants with long life cycles. For instance, within commelinids the clades Arecaceae, Bromeliaceae and Rapateaceae, all with long life cycles, showed a low rate of molecular evolution - and none is very diverse, at least using sister-group comparisons.

The cause of the correlation between the rate of molecular evolution and life history is unclear, but it is perhaps connected with mutation rate or population size and hence to speciation rate (Gaut et al. 2011 and references). Taller plants, i.e. trees, etc., tend to have lower rates of molecular evolution, at least, perhaps because growth/mitotic rates slow down in meristems a long way from the ground (Lanfear et al. 2013). The evolution of herbs, with small seeds, from trees has been linked with a rise in the speciation rate of the former (Dodd et al. 1999), although Verdú (2002) suggested that is was not so much the herbaceous habit per se that was important, but the associated condition, length of time to maturity (see also Baker et al. 2014: Amazonian trees). Herbs also show an increased rate of climatic niche evolution (Smith & Beaulieu 2009). In general, rates of molecular evolution (substitution rates) may be correlated with the rate of speciation, with more molecular evolution occurring in speciose clades (Webster et al. 2003, see also Barraclough & Savolainen 2001), although this is not always the case (Müller & Albach 2010: Veronica).

To summarize: Much angiosperm diversity, but not biomass production or net primary productivity (see below), is concentrated in groups that are annuals or herbaceous or shrubby perennials and that have animal pollinated flowers; disseminules are small, rarely fleshy (Eriksson & Bremer 1991, 1992), any animal dispersal often being by hooks and the like. Several of the large groups with monosymmetric flowers mentioned above (core Lamiales, Asteraceae) include many such plants. Overall diversification rates/species numbers are high in these clades, particularly in Asterales and Lamiales (Magallón & Sanderson 2001; Magallón & Castillo 2009), although these rates are best attached to particular clades within those orders (see the euasterids).

7C. Major Clades With Wind-Pollinated Flowers. In wind-pollinated angiosperms there has been selection for small carpellate flowers and a reduction in ovule number per flower, most wind-pollinated taxa having few to a single ovule per flower and single-seeded fruits (Friedman & Barrett 2008, 2011). D. W. Taylor et al. (2012) suggested that in Fagales, at least, the evolution of monospermous fruits occurred before the evolution of wind pollination, and some fossil Fagales are reported to have perfect flowers and nectaries.

Clades in which wind pollination predominates are usually not notably speciose, the adoption of abiotic pollination often being associated with a decrease in speciation rate (e.g. Dodd et al. 1999). A clear exception is Poaceae, 10,050 or so species of largely herbaceous wind-pollinated plants with single-seeded fruits (in most species the flowers can be categorized as being reduced-monosymmetric). Cyperaceae-Juncaceae, another clade of herbaceous, wind-pollinated plants with more or less reduced flowers and usually with single-seeded fruits, contains about 4,800 species. Fagales include about 1055 species, nearly all trees, monoecious, the flowers are much reduced, the staminate flowers being catkinate, the ovary is usually inferior, and the fruits are often quite large and always one-seeded. For the wind pollination syndrome, see Linder (1998).

For the evolution of dioecy, see Dufay et al. (2014) and Renner (2014) and references; monoecy and dioecy (in the latter, slightly over 3/10ths of the ca 15,600 species), woodiness, and the wind pollination syndrome are associated features here. Kay and Sargent (2009) noted that Poaceae and Cyperaceae/Juncaceae (Thurniaceae should be added to the latter clade) were exceptions to the rule that animal pollination led to an increase in speciation rate, being about seven times more diverse than their animal-pollinated sister clades. Clades immediately below Poaceae are small, and their flowers are small, but are probably pollinated by insects; note that the relationships of the [Thurniaceae [Cyperaceae + Juncaceae]] remain unclear. The mostly animal-pollinated Cucurbitales, probably sister to Fagales, have ca 2,300 species, i.e. about twice as many species as in Fagales. However, clades in which dioecy predominates are not notably speciose (Heilbuth 2000; Vamosi & Otto 2002; Kay et al. 2006, etc., but c.f. Käfer & Mousset 2014, and in part Leslie et al. 2013).If insect pollinated, the floral displays tend to be dimorphic, those of the staminate plants being showier and so more visited; extinction is thus perhaps more likely, but perhaps c.f. Amborella.

7D. A Cautionary Note. But what is known about the relationships of such features just mentioned to the diversification of the clades that posess them? Using Poaceae as an example, we can see how complex and difficult a question like "Are Poaceae diverse, and why?" can be. A series of points:

1. The first three clades of Poaceae that are successively sister to the remainder contain some 26 species out of the 11,000+, and these three "basal" clades are forest plants (e.g. Givnish et al. 2010b).

2. Many bamboos are woody (ca 2,000/2,125 spp.) and have a distinctive, synchronized monocarpic flowering habit; they are arguably ecologically distinct from the rest of the family.

3. Poaceae-Poöideae (ca 3,850 spp) are noted for their association with endophytes, an association that could be ca 40 m.y. old (Schardl et al. 2004). The presence of these endophytes affects the palatability of foliage to herbivorous mammals and of seeds to granivorous birds, and animals eating the infected material may not thrive. The level of aphid infestation and that of their parasites and parasitoids, and even the pattern and rate of decomposition of dead grass, are also affected (e.g. Madej & Clay 1991 - birds; Omacini et al. 2001 - aphids; Lemmons et al. 2005 - decomposition). A variety of alkaloids, including loliine (pyrrolizidine) and ergot alkaloids, are produced by the fungi; the distinctive loliine alkaloid is primarily active against insects (Schardl et al. 2007). Various aspects of root growth may also be affected (Sasan & Bidochka 2012).

4. Grasses are well known for the diversity of silica bodies in their leaves, and these play a role in protection against herbivory, while silicon concentration itself is correlated with the rate of breakdown of plant tissues, and so with nutrient cycling (see silica).

5. About 75% of the PACMAD clade, some 4,500 species, has C4 photosynthesis (Sage et al. 1999; Grass Phylogeny Working Group II 2011), and are ecologically very distinctive (see below). C4 plants tend to be less attractive to herbivorous animals because of their lower nitrogen concentration and greater amount of fibrous tissue (Caswell et al. 1973). The rise and spread of C4 grasses with their silica-rich tissues in the early Miocene may have been followed by the radiation of grazing mammals such as horses with hypsodont teeth that could deal with such refactory plant material (Thomasson & Voorhies 1990; Retallack 2001; Keeley & Rundel 2003). However, the relation of tooth morphology and silica content of grasses is questionable (Sanson & Heraud 2010), and although prairie grasses expanded in Nebraska in the Early Miocene ca 23 m.y.a., hypsodont ungulates were already around by then (Strömberg 2004).

To conclude. There are two sometimes overlooked issues. First, determining exactly which clades are speciose/diversifying rapidly is critical. Second, we often think of the evolution of angiosperms as being largely the consequence of the evolution of flowers (and fruits), diverse floral and fruit form representing adaptations to pollination and fruit dispersal, ensuring reproductive isolation, etc.; flowers allowed greater speciation rates (e.g. Hickey & Doyle 1977). This may well be true - there are indeed many angiosperms, and floral differences are often involved in species barriers - but there have also been more physiological changes that have profoundly affected the ecology and evolution of angiosperms and indeed the climate of the whole earth. It is not simply species numbers and flowers alone that matters, but also what species "do", their roles in the ecosystem (e.g. Bengtsson 1998). Some clades seem to have ecosystem effects far beyond the numbers of species they include; see also "The Eco-Physiological Context of Angiosperm Evolution" and especially "Asymmetries in Evolution".

[The rest of this section not integrated] In extant plants, seed size is more or less correlated with genome size (Beaulieu et al. 2007a; Linkies et al. 2010: for a possible negative correlation of genome size and plant size, see Beaulieu et al. 2007b) and more so with plant habit. Genome duplication (polyploidy) has ocurred many times and at all levels of the tree (see de Martins et al. 2006; Soltis et al. 2009; Duarte et al. 2010; Chalhoub et al. 2014: Brassica napus is 72x), and it may faciltate diversification by allowing the subfunctionalisation and neofunctionalisation of genes, the evolution of novel regulatory pathways, and other changes (e.g. Guo et al. 2013). However, the exact role it plays is unclear (e.g. Mayrose et al. 2011); certainly, duplication occurs in gymnosperms, too, even if the chromosome numbers there are low, and also in other land plants. Species-rich clades and genome duplications have been associated, Soltis et al. (2009: p. 336) linking "a dramatic increase in species richness" in Poaceae, Fabaceae, Brassicaceae and Solanaceae with genome duplications there. However, as van de Peer et al. (2009a), Schranz et al. (2012) and others have pointed out, duplication and diversification may not be particularly closely linked in time. Fawcett et al. (2009) dated a series of genome duplications within angiosperms to about 70-57 m.y.a., around about the time of the bolide impact, suggesting that palaeopolyploids forming then were at a selective advantage because of their hybrid vigour, also having extra genes/alleles available for selection (see also Crow & Wagner 2006 and references; van de Peer 2009a; Franzke et al. 2011). Genome duplications could reduce the probablity of extinction by increasing environmental tolerance and genetic variation, while individual mutations would be less likely to have an immediate effect. Note that Wood et al. (2009) suggest that polyploidy affects primarily cladogenesis, less the diversification rate of those clades; polyploidy may usually be an evolutionary dead end, with recently-formed polyploid plants speciating less and in particular showing higher extinction rates than diploids (Mayrose et al. 2011). Lomax et al. (2013) did not find any signal of increased genome size in increased guard cell length (the two are correlated) in the early Tertiary. Indeed, immediate connections between gene and/or genome duplication and diversification of angiosperms remaintob be established.

It has been suggested that trees have a distinctive evolutionary rhythm, speciating rather slowly. In any one species the number of individuals may be quite large, and although they may be rather dispersed they are long-lived, the species themselves also being rather long-lived (Petit & Hampe 2006). However, in the fire-prone Mediterranean ecosystem neither diversification nor molecular evolution differed between seeders and resprouters, two "strategies" allowing plants to survive fires, although seeders under some scenarios should have shown more diversification (Verdú et al. 2007).

Chanderbali et al. (2009, esp. 2010 and references), promote a fading borders/sliding boundaries model of floral evolution (see also Thiessen & Melzer 2007), and find that the expression of genes that are quite tightly linked to particular floral whorls in eudicots show much less specificity in expression in more basal angiosperms (they studied Lauraceae and Nymphaeaceae). As gene expression is canalized, distinctions between different kinds of floral organs become sharper. Colouring of the corolla in particular, in terms of pigment type, amount, and pattern of deposition, seems to be under the control of a small family of regulatory genes in a diverse set of angiosperms (Schwinn et al. 2006).

8. The Eco-Physiological Context of Angiosperm Evolution.

Although our understanding of the eco-physiological dimension of angiosperm evolution was for some time rather poor, the situation is now fast improving (Feild & Arens 2007 for a good introduction, see also Internat. J. Plant Sci. 173(6). 2012. for useful articles). Thus some of the differences in the leaves of early angiosperms when compared with those of other vascular plants (e.g. Hickey and Doyle 1977), as well as other vegetative changes, can be linked with eco-physiological changes (Sack & Scoffoni 2013 for a summary). These in turn may have facilitated the spread of the l.t.r.f. habitat in which much angiosperm diversity is now to be found, and they are also implicated in the long-term decline in atmospheric CO2 concentration that characterises the Tertiary. These changes affect the rate of photosynthesis, nutrient cycling and acquisition, silcate breakdown and rock weathering, and the like (e.g. Knoll & James 1987; Volk 1989: emphasis on deciduous ecosystems). There are a number of feedback loops, many positive, implicated in changing climates and CO2 concentration (e.g. Berner 1999; Beerling 2005a; Beerling & Berner 2005). These eco-physiological changes have had far-reaching effects, allowing angiosperms to grow in a great diversity of environments, including large areas of ever-wet forests, and they provide the basic ecological space for features associated with pollination and seed dispersal to interact with aspects of the biotic and abiotic environment (see also Boyce et al. 2010; Marazzi & Sanderson 2010). Seed plants in particular, and plants with secondary thickening in general, have changed the global environment (e.g. Beerling et al. 200[1?]; Feild & Edwards 2012).

But this is just the beginning. A plant is best thought of as some kind of a composite or metaorganism or chimaera (e.g. Herre et al 2005; Beerling 2005a; L. L. Taylor et al. 2009; Bragina et al. 2014), so we have to add to this the interaction of plants with their fungal associates, whether ecto- or endomycorrhizal or various kinds of endophytes, the bacteria associated with them, the evolution of lignin-decomposing fungi, and the effect of all these on mineral weathering in rocks, soil structure, carbon sequestration, and nutrient cycling. The physiological-ecological context of angiosperm evolution is very complex.

As background, remember that the climate in the Late Jurassic-Early Cretaceous was dry - certainly Pangea had a notably dry interior - but continents were drifting apart, and sea levels were rising. CO2 concentrations were still high, perhaps 3,500-5,000 p.p.m. in the early Cretaceous 135-100 m.y.a., since when they have declined - with the odd hiccup (Beerling & Franks 2010). There may have been a particularly abrupt decrease in the middle of the Cretacous (Feild et al. 2011b; Barclay et al. 2010), while concentrations briefly spiked at a high of over 1,200 p.p.m. at the PETM (see above). During the recent glaciations they dropped to 180-190 p.p.m., as low as any time during the whole period of land plant evolution (e.g. Zachos et al. 2008; Gerhart & Ward 2010; Boyce et al. 2010).

Below I discuss several of these more ecophysiological aspects of flowering plant evolution.

8A. Venation Density, Photosynthesis, and Climate.

8B. Vascular Evolution.

8C. Wood and Litter Decay.

8D. Ectomycorrhizae and Their Associates.

8E. C4 Photosynthesis, Grass, and Grasslands.

8F. Other.

8G. Summary.

8A. Venation Density, Photosynthesis, and Climate. During the 200+ million years prior to the diversification of flowering plants, the venation density of the leaves of vascular plants held largely constant despite considerable fluctuations in atmospheric carbon dioxide concentrations (e.g. Boyce et al. 2010; Lee & Boyce 2010; Boyce & Leslie 2012 for a summary), although stomatal density is negatively correlated and size is positively correlated with atmospheric CO2 concentrations (e.g. Franks & Beerling 2012). There seem to have been no major changes in plant productivity despite major changes in CO2 concentration (Boyce & Zwieniecki 2012), certainly, there is no simple positive correlation. Venation density in non-flowering plants continued to hold steady through the Cretaceous (Feild et al. 2011b), and importantly, both extant members of the ANITA grade and Chloranthaceae as well as fossils from the first ca 30 m.y. of the angiosperm record have similar low venation densities of around 2.4mm mm-2 (Feild et al. 2011b: post Hauterivian), and they also show lower CO2 exchange than most magnoliids and basal eudicots (Feild et al. 2011a). These ancestral angiosperms may have had chloranthoid teeth and guttated, but they are likely to have had low drought tolerance (Feild et al. 2011a, c); the leaves also had large and distant stomata, often lacked any palisade mesophyll tissue, and the abaxial surface of the blade reflected light back inside (Feild & Arens 2007).

The venation density of angiosperms other than the ANITA grade and Chloranthaceae (and other shade-tolerant plants, succulent plants, etc.), doubled at around 108-94 million years ago (Feild et al. 2011b), and only with the increase in density did productivity increase (Boyce & Zwieniecki 2012). This density increase greatly reduced the main element in the resistance to water flow through the plant, that is, passage through the mesophyll (Sack & Holbrook 2006; Sack & Scoffoni 2013), and further increase in density at the end-Cretaceous made the evolution of leaves with dense, small stomata advantageous (better stomatal control, higher stomatal conductance), so carbon assimilation per unit water loss increased (e.g. Franks & Beerling 2009; de Boer et al. 2012). Increased vein density came at a cost of increased carbon allocation to the veins, although this was partially offset by vein tapering and the high density of minor veins (McKown et al. 2010; Beerling & Franks 2010). These narrowed veinlets allowed an easy flow of water, perhaps because the proto- and metaxylem in then have vessels with simple perforation plates (Feild & Brdoribb 2013). Overall, with a three-fold increase in venation density, there is a 178% increase in maximum photosynthetic CO2 uptake (e.g. Brodribb et al. 2007; Brodribb & Feild 2010; Feild et al. 2011a; Roth-Nebelsick et al. 2001: vein architecture; McKown et al. 2010: leaf hydraulics). Despite the decline in atmospheric CO2 concentration, the efficiency of CO2 diffusion into the leaf improved; stomatal size decreased but their density increased so allowing stomatal conductance to increase (e.g. Franks & Beerling 2009; Haworth et al. 2011; de Boer et al. 2012; Franks et al. 2012); overall, trees may have small, dense stomata when compared with shrubs and herbs (Beaulieu et al. 2008: n = 101). Limited data suggest that root diameter has decreased, allowing for more efficient exploration of soil space to satisfy the increased water demands of the plant (Comas et al. 2012). Furthermore, the water potential of angiosperm leaves can decrease 50% before stomatal closure occurs, so maximum leaf hydraulic conductivity can persist in dry conditions, whereas in ferns, for example, closure occurs before there is any decrease (Brodribb & Holbrook 2004; see also Haworth et al. 2011, 2013 for stomatal opening in land plants). Increased transpiration that results from increased stomatal conductance will also promote evaporative leaf cooling (Hetherington & Woodward 2003; Boyce & Lee 2010), perhaps particularly important at times like the PETM when temperatures globally were very high.

Areas with ever-wet tropical humid climates seem to have been rather restricted in the Cretaceous (e.g. Boyce et al. 2010; Boyce & Lee 2010; Feild et al. 2009a). However, the increased transpiration from angiosperm leaves may have helped to drive the spread of widespread tropical forest with reliably high rainfall (e.g. Boyce et al. 2008, 2009, 2010). Thus simulations in which the Amazon rain forest is replaced with non-angiosperm vegetation decreased the extent of ever-wet rainforest there by about 80% (Boyce & Lee 2010; Lee & Boyce 2010). As Boyce et al. (2010) note, the extent of rain forest in other parts of the tropics shows less change in such simulations, but this might have been different under conditions earlier in the Tertiary; the elevation of large areas of continental Africa had not yet occurred, continents were in different positions, etc.. The spread of perhumid conditions in which large angiosperms dominated may have selected against drier, rather small stature angiosperm forest subject to frequent fires; fires were widespread in the Cretaceous, but decreased notably in many parts of the world from the mid Palaeocene to the Pliocene (Bond & Scott 2010; Belcher et al. 2010b; Bond & Midgley 2012), although Australia may be an exception (e.g. Crisp et al. 2011). Much woody angiosperm diversification has been in rainforests, and epiphytes, an appreciable component of diversity in general and often herbaceous, are abundant there, somewhat under 25,000 species of flowering plants being epiphytic (Feild et al. 2009a; Boyce et al. 2009, 2010; Schuettpelz & Pryer 2009; Boyce & Lee 2010; Boyce & Leslie 2012). Menispermaceae are today common in l.t.r.f., and they showed a burst of diversification close to the K/T boundary (Wang et al. 2012).

Finally, Boyce and Leslie (2012) suggest that the high assimilation rates facilitated by high venation density may also, in conjunction with a shortening of the life cycle, etc. (e.g. Williams 2012), have enabled the evolution of annual herbs, a life form exceedingly uncommon in vascular plants, fossil or extant, other than angiosperms.

8B. Vascular Evolution. Early angiosperms were probably smallish, sympodial trees that were rather tolerant of shaded and disturbed conditions and that grew in humid, more or less tropical conditions (Feild & Arens 2005). The ecological context for the early evolution of vessels is provided by living members of the ANITA grade (Feild 2005), other than the aquatic Nymphaeales. Thus vessels may have evolved in plants growing in humid conditions (Feild 2005), and Amborella, Gnetales (well, Gnetaceae), Austrobaileyales, and fossil groups with vessels grow/may have grown in such conditions.

Bannan (1934) and Mauseth (2009) describe the major features of angiosperm and gymnosperm wood. Although individual vessels in both magnoliids and ANITA-grade angiosperms may be more effective in transmitting water than individual tracheids, on a xylem cross-sectional area basis plants with such vessels may have a hydraulic efficiency similar to that of tracheid-bearing gymnosperms (Sperry et al. 2006; Feild & Holbrook 2001; Hudson et al. 2010). Tracheids in conifers may be short and have end walls, yet their overall hydraulic efficiency is higher than might be expected because of the low resistance to water flow of the margo-torus pits. The central torus can block the pit, so localizing embolisms, yet the fibrils in the margo are widely spaced compared with those in angiosperm pits and so allow water to flow quite readily (Pittermann et al. 2005; Sperry et al. 2007; Hacke et al. 2007; Hudson et al. 2010). Margo-torus pits are largely restricted to Pinales. Some palaeozoic medullosan seed ferns, especially taxa like Medullosa, had long, wide tracheids that probably had high water conductivities like those of some angiosperms with vessels (J. P. Wilson & Knoll 2010). Ferns in general have wide and long tracheids with surprisingly high transport rates (Pittermann et al. 2011).

Vessels in magnoliids and ANITA-grade angiosperms, so-called "basal vessels", are rather different from those in core eudicots (Hacke et al. 2007; Sperry et al. 2007), being short, not very dense, with scalariform perforations, having little difference between the pitting of the end and lateral walls, there is incomplete break-down of the pit membranes, intertracheidal pit resistance is lower than that of intervessel pits, etc.. Furthermore, the resistance to water flow of the scalariform perforation plates of early-evolving xylem is higher than had been estimated (e.g. Christman & Sperry 2010).

Vessels may have been of functional value initially because heteroxylic wood allows the specialization of cells in the xylem for support, storage, etc., the heteroxylly [sic] hypothesis (e.g. Sperry et al. 2007; Hudson et al. 2010; J. P. Wilson & Knoll 2010). Despite lacking vessels (or almost so), as in most gymnosperms, the wood of Amborella has a small amount of parenchyma (Carlquist & Schneider 2001; Feild et al. 200b; c.f. Carlquist 2012). Indeed, the avoidance of cavitation, air bubbles developing in the cells, may have driven the early evolution of vessels (Sperry et al. 2007; Hacke et al. 2007; Philippe et al. 2008; Brodribb et al. 2012: angiosperm:gymnosperm comparisons). Vessel conductance increases substantially when the peforation plates become simple and vessels themselves become long (see e.g. Christman & Sperry 2010; Hudson et al. 2010; Feild et al. 2011c). There were also changes in the Specific Root Length index, a measure of root length/unit biomass. This seems to have increased, i.e. roots became thinner and their hydraulic capacity increased (Comas et al. 2012). Evolution of the whole vascular system, from root to stem to leaf, was slow, but eventually wide vessel elements with simple perforations, the vessels being well over 10 cm long, became an integral part of an efficient water transport system. Vessels cannot be interpreted as a simple key innovation, and their evolution may have been a rather protracted process (Feild & Arens 2007; Feild & Wilson 2012).

Less is known about the functional/ecological significance of variation in the phloem of angiosperms and gymnosperms (see Jensen et al. 2012 and references for flow across the sieve plates of seed plants). Even if some differences between sieve tubes (angiosperms) and sieve cells (gymnosperms) may be somewhat over-emphasised - the nucleus in both may be non-functional, although they differ in how they become non-functional - they have different sieve plate morphologies, occlusion mechanisms, and ontogenetic/functional associations with neighbouring cells (e.g. see Behnke 1986; Schulz 1992).

There is also substantial variation in phloem pressure and phloem loading in angiosperms, and active phloem loading seems to be most common in the predominantly herbaceous euasterids; a variety of selective advantages for active loading can be suggested (Turgeon 2010b; Fu et al. 2011: see Garryales). Passive loading, with associated high sugar concentrations in leaf cells, may be correlated with the woody habit, and one kind of active loading involving the synthesis of raffinose family oligosaccharides is not connected with plant habit, but perhaps rather with climate (warmer: see Davidson et al. 2010). Interestingly, woody plants that have active phloem loading are usually asterids (e.g. Buddleja, Catalpa, Ilex, Syringa), while herbs with passive transport are members of the predominantly woody rosids (e.g. Rosaceae, Paeonia, Lythrum) - although Saxifraga, an herbaceous rosid, has active phloem transport, while the woody Cercis and Styrax also have active loading (Rennie & Turgeon 2009; Fu et al. 2011). However, the situation is a little confusing since the classifications of phloem transport types in Davison et al. (2011) and Fu et al. (2011) are somewhat different; I have not yet integrated them; see also Batashev et al. (2013) for minor-vein phloem anatomy and physiology.

Other variation in plumbing includes that in the water supply to the flower. The large flowers of at least some magnoliids may obtain their water through the xylem, whereas smaller flowers, as in the core eudicots, may be hydrated primarily via the phloem (Feild et al. 2009a, b, but sampling).

8C. Wood and Litter Decay. Another element to consider is litter and wood breakdown, as well as their loss by burning (Cornwell et al. 2009). About 30% of the organic carbon in the biosphere is currently locked up in lignin (Boerjan et al. 2003). Factors like leaf mass per area (MA, the inverse of specific leaf area [SLA], the relation leaf area to dry mass, cm2 g-1) and primary and secondary venation type have been linked with features like the rate of photosynthesis, plant growth, litter decay, nitrogen content, and nutrient cycling. However, there is much within-community variation in such features in angiosperms and any phylogenetic signal in such correlations is not well understood (e.g. Cornwell et al. 2008; Wieder et al. 2009; Walls 2011).

Both low MA and high amounts of nutrients in litter, features of angiosperms, are implicated in speedy litter breakdown. Angiosperm floras in the Cretaceous (Potomac, 110-105 m.y.a.: Royer et al. 2007) and Eocene (49-47 m.y.a.: Royer et al. 2010) had a low leaf MA, under 100g/m2; the three gymnosperm plants examined in the former flora had a mean of 291 g/m2. Even contemporary tropical non-riparian lowland rainforest may have only a moderate MA, e.g. ca 198 g/m2, as on Barro Colorado Island (Royer et al. 2010), and extant gymnosperms, like the extinct gymnosperms just mentioned, have a lower SLA than do angiosperms (Berendse & Scheffer 2009 and references). However, MA per se is unlikely to have been the only factor speeding breakdown of angiosperm remains. Although angiosperm woods are on the whole denser than gymnosperm woods, they, too, decompose faster (Weedon et al. 2009); brown rot fungi, which can barely degrade lignin, are more common in conifer forests than lignin-decaying white rot fungi (Boddy & Watkinson 1995).

Decay is affected by the composition of plant parts. The lignin content of angiosperms is about 20% lower than that of gymnosperms (Robinson 1990), and denser gymnosperm woods have proportionally still more lignin and less nitrogen, while the reverse relationship holds in angiosperm woods (Weedon et al. 2009). In general, both lignin and polysaccharide content are negatively correlated with the rate of litter breakdown (Cornwell et al. 2008); Martínz et al. 2005: decomposition of lignocellulosic compounds). Furthermore, the syringyl-rich lignins that characterise many angiosperms are more easily decomposed by fungi than the guaiacyl-rich lignins of other seed plants (Ziegler et al. 1985), and angiosperm leaves, litter and wood all have more nitrogen and phosphorus (on a %age basis) than do those of gymnosperms (Cornwell et al. 2008; Weedon et al. 2009); the polyphenol concentration of pines (Pinus muricata was the species studied) also affects nitrogen mobilization (Northup et al. 1995). Overall patterns of wood decomposition vary in detail, and heterogeneity in decay rates depends on the local decay organisms and tree species present, and even on the age of the tree (Weedon et al. 2009). The factors affecting decay are not well understood (Weedon et al. 2009) and the chemistry of woods is complex (e.g. Kögel-Knaber 2002).

Litter from extant ferns and fern allies and bryophytes is slow to decompose compared to that of gymnosperms and especially angiosperms (Cornwell et al. 2008; Lang et al. 2009). The litter of deciduous angiosperm trees decomposes faster than that of evergreens, angiosperm wood faster than gymnosperm wood, and the litter of angiosperm forbs in particular decomposes faster than that of any other group of land plants (Cornwell et al. 2008; Weedon et al. 2009) - note that more easily decomposable leaves are likely to be more palatable to insects, too (see below). However, Liu et al. (2014) pointed out that leaves of most magnoliids have a high SLA and decompose relatively slowly (see also Cornwell et al. 2014). UV light also decomposes lignin (Austin & Ballaré 2010). Of course, mean annual precipitation, which, as we have seen, can be affected by angiosperm transpiration, and temperature are positively correlated with litter and wood turnover and so with the release of the nutrients they contain (Yin 1999; Weedon et al. 2009; Wieder et al. 2009).

Graminoid litter - presumably mostly Poaceae and Cyperaceae - decomposes more slowly than that of forbs, and the litter of ectomycorrhizal trees tends to decompose more slowly - although not as slowly as that of Sphagnum (Pérez-Harguindeguy et al. 2000; Cornelissen et al. 2001; Cornwell et al. 2008; Lang et al. 2011). Graminoid lignin is somewhat different in composition from other lignins, having an appreciable amount of p-hydroxyphenyl units and being low in nitrogen which is removed before the leaf dies (e.g. Cornelissen et al. 2001; Wedin 1995). Tissues of C4 grasses have a particularly low N content which negatively affects its decomposability (Forrestal et al. 2014). Roots of Poaceae also decompose more slowly than those of other plants (Birouste et al. 2012: sample small, Mediterranean). There is also a negative correlation between litter longevity and silicon concentration in tissues; Poales, and especially Poaceae, have a high silcon concentration, and this is especially high in the annual species (Cooke & Leishman 2011b).

Ferns, gymnosperms and lycophytes tolerate nutrient-poor conditions, perhaps the ancestral conditions for many of them (Page 2004). The high photosynthetic rates of most angiosperms allow high growth rates and the nutrients that they need are released by the fast decay of their litter, and eudicot angiosperms in particular may utilize any flushes of nutrients produced by litter and wood breakdown, they scavenge nutrients effectively (Berendse & Scheffer 2009). In addition, the disturbed habitats that angiosperms may early have favoured are likely to have had elevated levels of nutrients (Berendse & Scheffer 2009). If early angiosperms were pioneer plants, they might be able to tolerate high herbivory because they had metabolically cheap, rather thin, rapidly expanding leaves with a low amount of fibre and low concentrations of secondary metabolites like terpenoids, phenols, and tannins; their high quality habitat allowed rapid growth and low defence (see e.g. Bond & Scott 2010), nutrient cycling was fast and their whole reproductive cycle was relatively short (e.g. Verdú 2002; Williams 2008, 2009). Extant angiosperms with the highest leaf venation densities are woody pioneers (Feild et al. 2011b), but members of the basal angiosperm clades, including magnoliids, have relatively slowly decomposing ("slow return") leaves, and magnoliid taxa like Piperales with more quickly decomposing leaves are smaller plants (Liu et al. 2014). Ectomycorrhizal plants have a lower rate of litter decay than endomycorrhizal (see below).

It is not only the amount and rate of decay that matters, but its seasonality. In evergreen plants, whether angiosperm or gymnosperm, nutrient cycling is gradual, nutrients being released throughout the year and tending to be taken up by the plants again. In deciduous species, however, nutrients tend to become available in flushes, and some are lost to the ecosystem, and this will increase weathering (Knoll & James 1987).

Litter decay results in the release of large amounts of CO2, angiosperm growth removes CO2. CO2 in the soil increases biotic weathering and removes carbon from the terrestrial system (see below). Fire is also very important (Bond et al. 2010). Brener (2003) noted that rocks rich in organic matter derived from plants are particularly prominent in the mid Cretaceous 120-90 m.y.a. to the Palaeocene. Substantial amounts of organic matter may be converted to inertinite, charcoal from fires in mire systems, and this is found through the Cretaceous, but less since (Scott & Glasspool 2006). Indeed, the life history characteristics of early angiosperms may have encouraged fires, which, however, were unable to burn closed angiosperm forests when these finally developed (Bond & Midgley 2012). Fires were common through the Cretaceous, but then dropped precipitously, there was a small peak in the Oligocene but considerable increases in the last 10 m.y. (Bond & Scott 2010; Belcher et al. 2010b). Fires cause the release of CO2 into the atmosphere, on the other hand, substances like inertinite are highly resistant to decay, so sequestering carbon. Fires also effect the nitrogen cycle, volatilizing N (Forrestal et al. 2014 and refs.).

8D. Ectomycorrhizae and Their Associates. There are perhaps 2,500-3,000 species of ectomycorrhizal (ECM) seed plants, while ericoid mycorrhizae (ERM) are found in 4,000 species and orchid mycorrhizae (ORM) over 22,000 more (Brundrett 2009; see also Smith & Read 2008), although Rinaldi et al. (2008) estimate that there are 8,000 species of ECM plants. Ca 7,750 described species of fungi, but probably many more (20-25,000?), are involved (Blackwell 2011; esp. Rinaldi et al. 2008; see also Pickles & Pither 2013); impressive single-site diversity of such fungi has been documented (Horton & Bruns 2001: examples mostly Pinaceae-dominated forests). Thus there are many more species of ECM fungi than of ECM plants, although the relationship may be reversed in Ericaceae and Orchidaceae (Rinaldi 2008).

ECM/ERM forests

Here the focus is on ECM and ERM plants, the ecological distinction between ECM and ERM fungi not being that great (e.g. Villareal et al. 2004 for references; Brundrett 2004; see also above); orchids and orchid fungi represent a very different kind of associated (see below). Many ECM-dominated communities are not notably diverse, in part perhaps because of the dearth of readily available nutrients (L. L. Taylor et al. 2009; Reich 2014 for literature; see below). Furthermore, ECM plants are clumped phylogenetically (e.g. Alexander & Lee 2005; L. L. Taylor et al. 2011), the ecologically most important ECM species being found in four main clades, Dipterocarpaceae/Sarcolaenaceae/Cistaceae, Fabaceae-Detarieae, Fagales, and Pinaceae. Members of these clades, along with those of the ERM Ericaceae, can all dominate the communities in which they grow, especially in boreal forests and tundra and (cool) temperate and tropical montane habitats. ECM trees also dominate in the tropical West Malesian dipterocarp forests, African Miombo and Sudanian forests, and parts of the Guineo-Congolian rainforest (e.g. Hart et al. 1989; Malloch et al. 1980; White 1983; Safer 1987; Sanford & Cuevas 1996).

ERM Ericaceae (including Epacridaceae, Prionotaceae, Empetraceae and Vacciniaceae; Grubbiaceae and Diapensiaceae were the only other families listed) are characteristic and often very common in heathlands world-wide (Specht 1979a; Read 1996), including those in alpine and arctic tundra (Specht 1979a; Chapin & Körner 1995; Jonasson & Michelsen 1996; Michelsen et al. 1998), in montane shrubberies especially in the northern Andes, parts of the eastern Himalayan-Yunnan region, and Malesia, and in heathlands of southern Africa and Australia (see also articles in Specht 1979b). Tundra alone occupies ca 8% of the earth's surface and five of the seven most important biomass accumulators there are ECM or ERM Ericaceae, Salicaceae and Rosaceae, the other two are Cyperaceae (Chapin & Körner 1995; Gardes & Dahlberg 1996). Boreal forests occupy ca 17% of the land surface (Lindahl et al. 2002), and the trees there, mostly Pinaceae and some Salicaceae and Betulaceae, are all ECM, while ERM Ericaceae often dominate in the understory (e.g. Read 1991; Villareal-Ruiz et al. 2004; Vrålstad et al. 2002; Vrålstad 2004; Kranabetter & MacKenzie 2010). Detarieae-dominated forests occupy millions of square kilometres in Africa. The map show areas where ERM Ericaceae (olive), ECM Pinaceae (red), and Fabaceae-Detarieae communities (green) are particularly common (from Specht 1979a; White 1983; White et al. 2000; Andersson 2005 - in progress). Biomass estimates for some of these communities are given below.

Many ECM plants have a distinctive ecological syndrome: They are trees, often locally dominant; they are mast fruiters, i.e., they fruit more or less simultaneously yet intermittently over large areas, and they have large seeds; and the soils they grow on are poor in inorganic nutrients, often with humus accumulating (e.g. Connell & Dawson 1989; Richards 1996; Torti et al. 2001; Newbery 2005; Peh et al. 2011: see also Koenig & Knops 2000, 2005; Norden et al. 2007 for mast fruiting). Fabaceae-Detarieae also have most of these features, but not all are mast fruiters, and not all Fabaceae that do are ECM plants. However, ECM/ERM plants from cooler areas like Pinaceae, Salicaceae, and some Betulaceae, and perhaps ERM Ericaceae, have a somewhat different ecological syndrome. Although they are trees or shrubs, they have much smaller seeds and do not often show mast fruiting, however, like other ECM plants, they can dominate the communities in which they are found, they grow on acidic and peaty soils, and they can tolerate soils with toxic metals (e.g. Read & Perez-Moreno 2003; Nara et al. 2003; Cairney & Meharg 2003). (Note that mast fruiting has recently been described from a number of trees and lianes from tropical French Guiana in South America, and these are neither known to be ECM plants nor to be particularly dominant in the communities where they grow [Norden et al. 2007].)

ECM fungi and their seed-plant associates together form the soil conditions that both prefer. Eenzymes, etc., produced by the ERM plant-fungus association contribute to the formation of acidic mor humus that ERM plants like and VAM plants do not (Read 1991). Stable protein-tannin complexes formed by Rhododendron maximum are more easily accessed by its own fungus associates than by fungi from ECM and and VAM plants growing with it (Wurzburger & Hendrick (2009). Similarly, Newbery et al. (1997) found that in some forests on poor soil in Cameroon the phosphorus in soil and litter was preferentially accessed by ECM Dialeae (= Fabaceae-Detarieae) that dominated there, the plants effectively making the kind of soil to suit themselves. Although Näsholm et al. (2013) interpret ECM fungal activities in conifer forests somewhat differently, with nitrogen in some circumstances being retained in the mycelium, the consequences are similar; non-ECM plants will be at a disadvantage in the nitrogen-poor conditions that result.

The leaves of ECM taxa like oaks and pines are well defended, often long-lived, the plants are efficient at removing N and P from them when they die, and the result is persistent, nutrient-poor humus unsuitable for VAM plants which are often faster-growing . ECM and ERM plants can also utilize N as complex organic compounds (Cornelissen et al. 2001: see also above), and this is affected by pH and litter polyphenols, which also vary in tandem at the infraspecific level (Northup et al. 1995). Indeed, Averill et al. (2014) noted that there was about 70% more carbon per unit nitrogen in the soils of ecosystems dominated by ECM plants; the nitrogen remained accessible to the fungi, but not to their microbial competitors. However, Averill et al. (2014) also thought that litter with a higher C:N ratio would lead to less overall C storage in the soil because microbes would respire relatively more C to obtain N. Low rates of litter decay (often accompanied by high MA - leaf mass per area - values) are particular features of both gymnosperms and angiosperms that are able to grow in stressful, nutrient-poor environments (Berendse & Scheffer 2009). The litter of some ECM trees tends to decompose more slowly than that of other vascular plants (Pérez-Harguindeguy et al. 2000; Cornelissen et al. 2001; Alexander & Lee 2005; Cornwell et al. 2008; Lang et al. 2011), and ERM Ericaceae are also noted for producing nitrogen-poor litter that is slow to decompose (e.g. Read 1991). Although aspects of this story, particularly the generality of any distinctive foliar traits of ECM plants (Koele et al. 2012; Liu et al. 2014 for Fagaceae), are questionable, the result of leaf decay in ECM plants is soil with acid conditions and persistent litter with a high C:N ratio; this will tend to constrain mineralization, as will the seasonal/cold climates that many ECM/ERM plants favour (Read 1991).

ECM/ERM communities are often found on rather extreme soils, including serpentines (Branco & Ree 2010), that are either poor in nutrients (e.g. Michelsen et al. 1998), and/or rich in organic materials and/or without much other vegetation (e.g. Read 1993). In such communities soil pH is, or becomes, low, and sometimes massive amounts of mor humus commonly accumulates, especially in cooler climates; podzolization may also occur (van Schöll et al. 2008). Even in the l.t.r.f. of West Malesia there are huge peat lenses on which ECM dipterocarps dominate some communities (Richards 1996). In general, the acid, nutrient-poor conditions and high water tables that develop are not conducive to the activity of potential decomposers of humus - a self-reinforcing cycle - and there is CO2 sequestration.

Siderophores and low molecular weight organic chelators like oxalic acid produced by the bacterial associates of ECM fungi and the ECM themselves all increase the breakdown of silicate minerals and weathering of rocks, both basaltic and granitic (e.g. Knoll & James 1987; Frey-Klett et al. 2007; L. L. Taylor et al. 2009, 2011, 2012; Comas et al. 2012). CO2 produced by the respiration of the fungus-plant association is used up in this weathering as it reacts with water CaCO3 and silicate minerals, and carbon is ultimately carried out to sea (e.g. Berner 1997; Beerling 2005a; L. L. Taylor et al. 2009). The low molecular weight organic acids can mobilize cations such as Ca++ and Mg++, increase phosphorus availability, etc.; siderophores chelate iron and oxalate forms complexes with aluminium ions, detoxifying the aluminium but also increasing the weathering of aluminium-containing minerals in rocks (Landeweert et al. 2001; Hoffland et al. 2001; van Schöll et al. 2008). It is not for nothing that ECM fungi have been dubbed "rock-eating fungi" (Jongmans et al. 1997). There have also been increases in the Root Length Density index, an estimate of root length/unit soil volume (this would be much increased if the mycorrhizal hyphae were factored in), so all in all, foraging for nutrients became more efficient (Comas et al. 2012); the very fine ericoid roots of Ericaceae must have the highest density index.

Whether or not the establishment of conspecific seedlings is less affected than might be expected in such ECM forests needs more study, but some evidence points in that direction. In some temperate forests the regeneration of the more abundant species (not necessarily ECM) show weaker negative density dependence that that of the less common species (D. J. Johnson et al. 2012a, b, but c.f. Dickie et al. 2012), perhaps enhancing their dominance, although this is not a general latitudinal effect (Comita et al. 2014). However, whether the common species in ECM-dominated communities behave similarly is unknown. In more species-rich areas of South American forests there are stronger negative density dependence effects, fungal pathogens and insect herbivores driving up diversity (Mangan et al. 2010: Panama; Terborgh 2012: review, esp. Peru; Johnson et al. 2012a, b: Bagchi et al. 2014; Comita et al. 2014; see also Kulmatiski et al. 2008 and Schnitzer et al. 2011: grasslands).

Overall, ECM/ERM comminities may not be notably productive, but some dipterocarp communities, which can also be very diverse (e.g. Lee et al. 2002), are exceptions. Bornean Dipterocarps show very high levels of above-ground wood production when compared with other species in the same community, and they also show higher productivity (as half as much again) when compared with forests in the western Amazon (Ecuador, Peru) that are similar in soils, precipitation, etc.; dipterocarps were more productive than their non-dipterocarp counterparts (Banin et al. 2014). This high productivity was despite a much lower amount of phosphorus in the soil in the dipterocarp forests and a C:N ratio about 50% higher (Banin et al. 2014). How these figures might relate to underground carbon storage and to the activities of ECM is unclear.

The importance of ECM fungi for angiosperm evolution is not just because they facilitate the nutrient and water supply of their associates and make life difficult for non-ECM plants and for free-living microbes, but also because of their direct and indirect effects on the biosphere - on soil, on weathering, on carbon sequestration, and hence on the earth's climate. ECM plants increase mineral weathering, and rainfall, in part from transpiration, also allows more silicate weathering, and weathering is a principal sink for atmospheric carbon dioxide (Boyce et al. 2010; Berner 1997); an increase in atmospheric CO2 removed by the weathering of rock has been linked to the decrease in atmospheric CO2 concentration during the Tertiary (Pagani et al. 2009; L. L. Taylor et al. 2009). In drier years, there may even be competition between ECM and lignin-decomposing fungi for water, leading to a reduction in the rate of wood decomposition (Koide & Wu 2003). Finally, carbon in non-decomposing biomass may become buried in sediments much more easily than in VAM forests, particularly those in the tropics where carbon turnover is very fast (Tedersoo et al. 2012). All these biogeochemical effects of ECM plants are as much immediately caused by the activity of fungi and bacteria associated with the plant as by any activities of the plant itself (e.g. Landeweert et al. 2001; Taylor et al 2009; Bonfante & Anca 2009).

For information on the dating of associations between woody plants and ECM fungi, see Clade Asymmetries below.

8E. C4 Photosynthesis, Grass, and Grasslands. The global distribution of C4 vegetation, especially grasslands and savannas, has been estimated at ca 18.8 x 106 km2, somewhat over 15% of the total area (Still et al. 2003: C4 crops factored in). All told C4 photosynthesis accounts for about 23-28% of terrestrial gross primary productivity, although the biomass of C4 plants is only ca 5% of the global total (Still et al. 2003: GPP = 35.3 vs 114.7 Pg C yr-1, simulated biomass, leaf, wood, root = 18.6 vs 389.3 Pg C; see also Lloyd & Farquhar 1994; Ehleringer et al. 1997; Retallack 2001). Other estimates of total biomass are similar: 15.6 vs 488.5 Pg C (Ito & Oikawa 2004). Most of the biomass difference suggested by Still et al. (2003) is in the woody part of the biomass, that of C3 plants being 352.7 PgC and that of C4 plants zero (obviously Caryophyllales not factored in here); in both cases root and leaf biomass were about equal, the total in C3 plants being about twice as much that in C4 plants, 36.6 vs 18.6 PgC.

For summaries of C4 photosynthesis, see Kellogg (2013), also Williams et al. (2013), Heckmann et al. (2013), Christin and Osborne (2014), etc.. It is especially common in Poaceae (R. Sage et al. 2011), being found in about three quarters of the almost 6,000 species of the PACMAD clade of Poaceae alone. The C4 photosynthesic syndrome has evolved 22-24 times there, and 66-68 times in angiosperms as a whole (R. Sage et al. 1999, 2011, 2012; Ludwig 2011b), as in many species of Cyperaceae (ca 1,500 species), Amaranthaceae (ca 500 species) and other core Caryophyllales, Euphorbiaceae (Euphorbia subg. Chamaesyce), etc. (Arakaki et al. 2011; R. Sage et al. 2012). Origins in monocots and eudicots are roughly contemporaneous, mostly occuring within the last 30 m.y. or so (Christin et al. 2011b, q.v. for a number of dates; Kadereit et al. 2012); Cowling (2013) has a rather different take on the evolution of C4 photosynthesis, suggesting perhaps much more ancient origins.

The great expansion of C4 grassland has occurred only within the last 10 m.y., and within the last 2-3 m.y. in particular (e.g. Strömberg & McInerney 2011; McInerney et al. 2011; R. Sage et al. 2012). Similarly, the extensive and very speciose Brazilian Cerrado savanna vegetation with flammable C4 grasses and also those in Africa, also developed within the last (10-)5 m.y. (Simon et al. 2009; Simon & Pennington 2012; Maurin et al. 2014). One estimate of the global extent of grassland, including savanna, is 52.5x106 km2 (Gibson 2009).

Root systems in mature grasslands are dense, and the soils are up to 1 m deep with good crumb structure and much organic matter (mollisols: Retallack 2001, 2009). The total carbon sequestration in grasslands is greater than that of the forests they replaced, and in particular the proportion of the biomass sequestered in the soil increases. Grassland soils are notably moister than corresponding woodland soils because woodlands have a lower albedo and transpire more, so somewhat paradoxically grasslands support a cooler, drier climate, yet one that allows increased weathering, which consumes carbon (Retallack 2009). Overall, grasslands can be considered a long-term carbon sink so contributing to long-term global cooling (Volk 1989; Retallack 2001); as Retallack (2009: p. 100) noted, "grasslands did not merely adapt to climate change, but were a biological force for global change". In general, erosion from grasslands leads to a loss of organic carbon in sediment that is an order of magnitude larger than the corresponding loss from forests. Nutrients are also rapidly mobilized and ultimately lost in run-off; the lost nutrients support ocean productivity (Volk 1989). See also also below; for more details on the evolution of grasslands, see Poaceae.

Although only some 7,500 species, somewhat over 2% of angiosperms, are C4 plants, they account for about 23% of terrestrial gross primary productivity (Lloyd & Farquhar 1994; Ehleringer et al. 1997; R. Sage et al. 2012). C4 photosynthesis is very efficient, especially in monocots (Braütigam et al. 2008); C4 monocots do better in warmer environments, C4 eudicots also in colder, drier and saline climates. Thus in the rather cold Gobi deserts 15-17% of the species are C4 plants and they contribute 30-90% of the biomass there (Vostokova et al. 1995; Pyankov et al. 2000). Overall, C4 photosynthesis is efficient, it arose many times, it is of great importance ecologically, yet this importance is geologically very recent, C4 grasslands at low latitudes finally coming to dominate only 3-2 m.y.a. (R. Sage et al. 2012 for references).

The adoption of fructans as storage polysaccharide in Poaceae-Poöideae, many Asparagales and Asterales, etc., may also be linked with the ability of the plants involved to grow in seasonally dry or frost-prone climates outside the tropics (Hendry 1993; Hendry & Wallace 1993; Vijn & Smeekens 1999).

8F. Other. There are a number of other eco-physiological groups of angiosperms that are also dominated by a few main clades. The first three groups, succulents, plants with CAM photosynthesis, and the epiphytic habitat, overlap.

1. Succulence of some form, whether of root, stem or leaf, occurs in some 690 genera and 12,500 species (Nyffeler & Eggli 2010b; see also von Willert et al. 1990; Eggli & Nyffeler 2009). Succulents include species which either avoid drought, although they are rarely found in the driest conditions, or are salt tolerant - usually mutually exclusive strategies (Ogburn & Edwards 2010). They include many of the C4 chenopods mentioned above, Cactaceae, Crassulaceae, and a number of epiphytes, perhaps particularly orchids. The venation density of the leaves of succulent plants tends to be low (Sack & Scoffoni 2013).

2. CAM-type photosynthesis is particularly prevalent in clades that either grow in arid terrestrial environments or are epiphytes; succulent epiphytes are quite often CAM-type plants. All told, some 17,000 or more species in Crassulaceae, Bromeliaceae, Cactaceae and Orchidaceae-Epidendroideae in particular have CAM or its variants (Winter & Smith 1996b; Sayed 2001). The origin of CAM clades seems to be largely contemporaneous with that of C4 clades, being largely Miocene and younger, indeed, there seems to have been a "global surge" of succulent CAM plant diversification within the last 10 m.y. like that of C4 grasslands (Edwards & Ogburn 2012: p. 726).

3. Ca 24,440 species of angiosperms are epiphytic (Schuettpelz & Pryer 2009; Zotz 2013), about half being members of Orchidaceae-Epidendroideae (Ramírez et al. 2007; Gustafsson et al. 2010; Conran et al. 2009) and Bromeliaceae (Givnish et al. 2008a, 2014a). Both of these groups diversified in the Tertiary, along, perhaps, with epiphytic ferns (Dubuisson et al. 2009). One third of all leptosporangiate ferns are epiphytic - ca 3,000 species, about 10% of all epiphytes - and they may have diversified around the PETM in the early Tertiary (Schneider et al. 2004a, b; Schuettpelz 2007; esp. Schuettpelz & Pryer 2009; Watkins et al. 2010). Seedless vascular plants are particularly important components of the epiphytic vegetation in the rainforests of the Antipodes and Oceania (Dubuisson et al. 2009).

4. Lianes may make up some 25% (10-44%) of both stem density and species richness of woody plants in tropical forests, and they are especially prominent in disturbed forests; stem-twining vines seem to be commoner in old forests, tendril vines in younger forests (Schnitzer & Bongers 2002). Ca 8,700 species of scandent plants are recorded from the New World alone (Gentry 1991). Major clades of lianes include Menispermaceae, Bignoniaceae-Bignonieae, and Sapindaceae-Sapindoideae-Paullinieae.

8G. Summary. We can now return to the issue of when l.t.r.f. as we know it appeared (see above). As with flowers, is not the evolution of angiosperms per se that marks major changes; these occurred later (Feild & Arens 2007). Thus the venation density of ANITA-grade angiosperms is rather similar to that of non-angiosperm lignophytes and their xylem is in several respects functionally not that different. Early angiosperms may be perhaps distinguished from gymnosperms by their fast seedling growth and overall short reproductive cycles (e.g. Bond 1989; Coiffard et al. 2006). but, as Feild and Arens (2007: 21) noted, "Among basal angiosperms, the initial transitions to higher-light environments are characterized by a high degree of lineage-dependent, functional experimentation, in which fine-tuned performances were assembled piece-by-piece."

Venation density showed two marked increases in the Cretaceous, one around the Middle to Late Albian ca 108-94 m.y.a., early in the Cretaceous Terrestrial Revolution, and one around the K/T boundary, when values reached 12-16 mm mm-2 (Feild et al. 2011b). Quickly-decomposing leaves are found mostly in the eudicots (?and some monocots?) (Liu et al. 2014). Large trees first appear in the fossil record in the Middle to Late Albian less than 110 m.y.a., and wood with scalariform perforation plates was particularly common in the Cretaceous (Wheeler & Baas 1993). Features like vessel length and perforation plate morphology - scalariform perforation plates became less common - that would favour xylem conductance, and wood parenchyma, but not ray morphology, changed across the K/T boundary (Wheeler & Baas 1991). Such changes may be connected with changes in venation density and water conductance needs, but, as Wheeler and Baas (1993) noted, there is conflict between features of Cretaceous fossil woods and paleoclimatic indicators, indicators that are based on our understanding of how wood of extant plants functions (see also Philippe et al. 2008), so interpretation of these changes is not easy. Increased plant productivity and diversity would also allow animals that ate pollinated or dispersed angiosperms to diversify (see also Boyce et al. 2010).

Light conditions in the closed forest habitat pose a particular challenge. The PHYA/C gene pair duplicated before the origin of crown group angiosperms, and PHYA in particular may have been very important in angiosoperm evolution. PHYA is intimately involved in germination and in etiolation responses of the seedling, especially in shady conditions such as occur on the forest floor, for example, preventing seedling etiolation in response the the far-red light that dominates the spectrum there. Furthermore, it is involved in the germination response of hydrated seeds to very brief pulses of light (the very low fluence response - VLFR) such as sunflecks (Mathews et al. 2003). Unfortunately, how ANITA grade angiosperms might respond to manipulation of their PHY genes is unknown.

9. Clade Asymmetries.

When thinking of overall patterns of seed plant diversity and evolution, there are a number of striking examples of what may be called clade asymmetries. There are two rather different kinds of these asymmetries. One includes small (in terms of species numbers) clades of animals that are of particular importance across whole communities or ecosystems and are more or less involved in the pollination and seed dispersal of relatively very large numbers of plants. As we will see, these are quite well known, especially on a fairly local scale, but here the scale is global. The other kind of asymmetry is that in more physiological-ecological relationships, where relatively small clades of plants have major effects on aspects of biome functioning, particularly through their effects on carbon cycling.

Both kinds of asymmetries have major implications for species persistence, the ecological structuring of communities and ecosystems, and the way one thinks about diversity and evolution in general. Specifically, we now have the tools to begin to identify and think about the disproportional ecological impact of a few and not notably speciose clades of plants and animals that are either restricted to particular biomes or provide comparable services across biomes (see below for supergeneralists, keystone clades and ecosystem engineers).

9A. Plant-Animal interactions.

9A1. Pollination.





9A2. Seed Dispersal.

As Ollerton et al. (2011: p. 321) noted, "if a policy-maker or conservation planner were to ask an ecologist the straightforward question, 'How many species of flowering plants are pollinated by animals?' the answer would be: 'We do not know'.", but they provided an estimate - around 308,000. However, for more specific questions like "How many species of plants are dispersed by [such and such group of] bats?", and "How many species are pollinated by [such and such group of] of bees?", it is still very difficult to obtain reliable estimates.

Estimates of the numbers of species of bees, birds or bats may be fairly accurate, but the same certainly cannot be said of the numbers of species of plants that they service, although the focus here is less on the details of how a plant gets pollinated, but the numbers of plants and of their major pollinators. Unfortunately, many observations in the literature do not allow one to distinguish between a visit of an animal to a plant that is casual or one that results in pollination. Furthermore, the study of plant-animal relationships in general still often focus on only one of the partners. Thus pollinating bees were initially categorized as such based largely on observations on plants visited for pollen, but pollination also occurs when bees are nectaring; add variation in time - from season to season, within a season, as well as time of day that the stigma is receptive - and space, and characterizing pollination relationships becomes difficult (e.g. Fishbein & Venable 1996; Waser et al. 1996; Kandori 2002; Ollerton et al. 2003; Thompson 2009; Crone 2013). Some bees classified as being oligolectic, i.e. pollen specialists, may not even be sffective pollinators at all, being robbers or irrelevant to the pollination process (Linsley 1958; Michener 1979).

In the estimates below, I have necessarily had to rely on extrapolation, numbers being based on very scanty observations extrapolated to flowers with a similar floral morphology. Hence floral syndromes have necessarily had to be used, despite the problems mentioned earlier. Indeed, Grant (1966) noted that flowers with ornithophilous syndromes were particularly prominent in North America where the humming birds that pollinated them were migratory; in tropical America such syndromes were less evident. Similarly, only 2-3% of the species in Neotropical cerrado vegetation have ornithophilous flowers, but humming birds take nectar about the same number of species that do not have ornithophilous flowers, and some of these are pollinated (Muruyama et al. 2013). Humming birds are often observed to visit flowers that do not have an ornithophilous syndrome, and sometimes ignore flowers that do! Furthermore, relationships between plant and pollinator are by no means constant (e.g. Aizen et al. 2012; Natalis & Wesselingh 2013). Even if they are constant locally, this may not be true across the range of the species (Newman et al. 2014; van der Niet et al. 2014 and references: pollinator ecotypes). The estimates of numbers of pollinators below in part rely on floral syndromes, anecdotal evidence, and other suspect data.


Plant groups with species pollinated by euglossines include Araceae (visited for fragrances, e.g. the very speciose Anthurium and Spathiphyllum), Bignoniaceae, Gesneriaceae-Gesnerioideae (ca 300 spp., both male and female bees involved - Wiehler 1978), Lecythidaceae-Lecythidoideae, 700 to perhaps 2,000 species of Orchidaceae-Epidendroideae (fragrances), and Zingiberales, especially Costaceae and Marantaceae, also Apocynaceae, Convolvulaceae, Euphorbiaceae (perhaps 70 species in Dalechampia alone - Armbruster 1993; Armbruster et al. 2009), Fabaceae (including the nectarless Swartzia), Solanaceae, and Rubiaceae (see Dressler 1968; Cameron 2004; Roubik & Hanson 2004; Ramírez et al. 2011; Schiestl 2012, and references).

In any one community there may be up to 50 species of bees, and bee populations are often notably stable (Roubik 1989; Roubik & Hanson 2004; Zimmermann et al. 2009). Hentrich recorded ca 23 species of bees visiting ca 48 species of plants in Nouragues, French Guiana, while Ramírez (2009) noted that just one species of Euglossa might visit 74 species of plants from 41 families - and that at a single locality.

It is estimated that crown group euglossine diversification occurred only 42-27 m.y.a., montane clades diverging only in the last 8-4 m.y. (Ramírez et al. 2010); another estimate of crown group age is slightly younger, some (35-)28(-21) m.y.a. (Cardinal & Danforth 2011).

Overall, these 200 or so species of euglossine bees are likely to be the major pollinators of well over 4,000 species of Neotropical plants (Wiehler 1976; Williams 1982; Ramírez et al. 2002 for a summary of the literature; Ramírez pers. comm.).

Bumble bee pollination is common in temperate and in arctic-alpine floras in particular, almost irrespective of the morphologies of the flowers visited. Ericaceae, perhaps most notably the large genera Rhododendron and Vaccinium, are particularly common in such communities, but practically all other genera in these habitats are visited by the bees, and again, the morphology of the flowers of the taxa involved is very diverse (e.g. Ranta & Lunberg 1981; Tomono & Sota 1997; Kudo et al. 2011 and references). Although I have not found estimates for the numbers of species involved, the number of Ericaceae alone pollinated by these bees is likely to be appreciable. Bumble bees are also prominent in alpine environments, where hundreds of species in large genera like Gentiana, Rhododendron (Corlett 2004 and references) and Pedicularis (perhaps 600 species here alone - Macior 1994; Williams et al. 2009; Eaton et al. 2012) largely depend on them for pollination (e.g. Eaton et al. 2012). Members of Lamiaceae and many other Lamiales, Fabaceae, particularly Faboideae, and Impatiens (Balsaminaceae) are also often visited (Williams et al. 2009). In Ranunculaceae the overwhelming majority of the 600-700 species of Delphinieae are bumble bee-pollinated (Jabbour & Renner 2012b), this having long been recognised in Aconitum in particular (see map in Kronfeld 1890). In South America bunble bees pollinate genera like Rubus, Scutellaria, Lathyrus and Lupinus, all of which have diversified substantially there (Asmussen & Liston 1998; Hines 2008). Bumble bees in Europe visit a variety of flowers (Raine & Chittka 2007a, b; Goulson & Darvill 2004), and this is true more generally. They can also handle polysymmetric flowers quite easily (Laverty 1994; Sedivy et al. 2013), and that bees in general are typically more specialized when pollen collection is compared with nectar foraging; learning to handle pollen flowers is quite difficult even for bumble bees (Strickler 1979; Goulson & Darvill 2004; Benton 2006; Raine & Chittka 2007b; Ghoulson 2010).

Local diversity of bumble bees can be quite high, with 4-12 species occuring in one community (Hines 2008 and references); while one fifth or more of the world's bumble bee species are found in the Sichuan-Chongqing region of China alone (Williams et al. 2009). In the Front Range of the Colorado Rockies ca 18 species of bumble bees pollinate ca 43 species of plants (Macior 1974).

Bumble bees diversified over a similar time frame as did the euglossine bees, i.e. about 47-25 m.y.a., although their stem group (they split from meliponines) age is considerably more, 100-80 m.y.a. (Hines 2008); Cardinal and Danforth (2011) suggest a somewhat more recent age for crown-group bumble bees of (31-)21(-12) m.y.. The Eocene-Oligocene boundary of ca 34 m.y.a. was a time of sharp cooling and increase of seasonality, and bumble bees flourish in cooler climates, being facultatively endothermic (Hines 2008 and references). The bees moved into South America about 8-6 m.y.a., perhaps along with the plant genera of northern origins that they now pollinate (Asmussen & Liston 1998; Hines 2008).

Estimates of the numbers of species of plants pollinated by bumble bees are hard to make, but upwards of 3,000 is a plausible number. Bumble bees are effective buzz pollinators (Goulson 2010), and the buzz pollination floral syndrome has evolved many times, perhaps some 4,000 species of angiosperms, mostly core eudicots, being involved (Buchmann & Hurley 1978; Buchmann 1983). ?Other bees doing this.

The origin of the Apis clade is late Eocene/earliest Oligocene, with the diversification of extant species beginning a mere ca 13.5 m.y.a.; it is unclear if diversification began in Europe (fossils) or Asia (Kotthoff et al. 2013 - they favour the first hypothesis - and references).

The evolution of flowers which have oils as their primary reward may have begun in the Eocene (Renner & Schaefer 2010). However, Cardinal and Danforth (2013) estimated that Centradini and Tetrapedia, which take oil from Malpighiaceae in particular, evolved in the Late Cretaceous (87-52 and 92-66 m.y.a. respectively); see also Neff and Simpson (1981) for the bees. Martins et al. (2014) found Centradini to be paraphyletic, Epicharis diverging (102-)91(-79) m.y.a. and Centris (95-)84(-72) m.y.a., about contemporaneous with Xi et al.'s (2012b) estimate of the stem-group age of Malpighiaceae of (100-)86(-73) m.y. ago. This is also broadly consistent with some kind of co-evolutionary story, Martins et al. (2014) suggesting that the evolution of oil collection in the bee clade was in the common ancestor of Epicharis and other bees (corbiculate bees later lost the ability to collect oils). However, crown ages of the two genera are (39-)28(-18) m.y.a. (Epicharis) and (58-)44(-36) m.y.a. (Centris), while those of Malpighiaceae range quite widely, 75-60(-32) m.y.a. (Wikström et al. 2001; Davis & Anderson 2010; Renner & Schaefer 2010; Xi et al. 2012b), i.e., all generally (much) younger than stem ages. Details of the evolution of the association between the bees and malpigs are currently unclear.

Some 2,000 species of oil flowers in 11 families are pollinated by 447 species of bees (Alves-dos Santos et al. 2007; Martins et al. 2013 for general statistics).

Iridaceae figure particularly prominently, and around 34 species of the family are known to be pollinated by Nemestrinidae, with around 100 more species thought to be fly-pollinated (Manning & Goldblatt 1996, 1997; Goldblatt & Manning 2000). Here the plant:pollinator ratio is anywhere from 6:1 (highly conservative) to much in excess of 30:1.


As with attempts to estimate numbers in other plant-pollinator interactions, it is difficult to work out which relationships between a species of plant and pollinating bird are more or less obligate for the former (they never are for the latter). Many humming birds and honey eaters, for instance, also eat insects they find on flowers, although this may be irrelevant when thinking about pollination relationships. Nectarivorous birds may also visit quite a variety of flowers usually pollinated by other animals (e.g. Muruyama et al. 2013), while other animals may pollinate flowers visited by humming birds (e.g. Snow & Snow 1980; Brown & Hopkins 1995; Fleming et al. 2005).

In the estimates below of numbers of plants visited I have focussed mostly on larger clades of plants and on literature covering flower visitation in particular regions. The result is that taxa like Brachychiton are probably included (in the general figures for bird visitation in Australia), some of the 40 or more Old World bird-pollinated species of Erythrina (Bruneau et al. 1997) are, while species like Holmskiodia sanguinea are probably not (see also Porsch 1936 and references for early literature). I also focus on just some of the major groups of birds that pollinate plants. Not mentioned, for example, is the role played by New World orioles (Icterus), tanagers, and other more or less casual flower visitors (e.g. Stiles 1981) in pollination, although they may be responsible for a few of the records of "bird-pollinated flowers". Orioles may be particularly important in pollination in drier forests (Stiles 1985). For a recent summary of many aspects of bird pollination, see Fleming and Kress (2013).

Some 1,000 or more species of Ericaceae-Vaccinioideae-Vaccinieae and Gesneriaceae-Gesnerioideae (some 600 species of the latter alone - Wiehler 1978), also with their centres of diversity in the Colombian-Ecuadorean region, may be pollinated by humming birds (Luteyn 2002; Weber 2010). To these plants can be aded some 250 species of Salvia (Wester & Claßen-Bockhoff 2011), 225 species of Heliconia (Pedersen & Kress 1999), 500-600 species of Acanthaceae (E. A. Tripp & L. McDade, pers. comm.; Tripp & Manos 2006), about 360 species of the Centropogon alliance of the Campanulaceae-Lobelioideae (L. Lagomarsino, pers. comm.), some 55 species of Erythrina (Bruneau 1997), over 40 species of Penstemon (P. Wilson et al. 2006, 2007), hundreds of species (perhaps 1,060-1,300 species) of Bromeliaceae, mostly at higher altitudes in the Andes, not in drier habitats or in terrestrial lowland forest habitats (e.g. Benzing et al. 2000a; Kessler & Krömer 2000; Givnish et al. 2014), about 125 species of Loranthaceae, perhaps 100 species of Fuchsia, 138/555 species of Passiflora (K. Porter-Utley & J. MacDougal, pers. comm.), and so on - other families visited include just about all sizeable sympetalous families in the humming birds' ranges, including Rubiaceae (especially important see also Snow & Snow 1980), Rosaceae, Melastomataceae, and Symplocaceae, etc. (see e.g. Snow & Snow 1980; Sazima et al. 1996 for other examples). Seven species of migratory humming birds pollinate ca 130 species of plants (including some species of Penstemon) in the western United States alone, particularly at high elevations (Grant 1994; Grant & Grant 1968; Brown & Kodric-Brown 1979).

Humming birds as a whole, and particularly the Andean species, have notably small mean ranges when compared with those of other birds (McGuire et al. 2014), but there are still usually several species of birds in any one locality, up to 25-30 species being recorded from a single local assemblage (Graham et al. 2009, 2012). Figures in Fleming et al. (2005) are 3-28 species per site, pollinating 14-51 species of flowers from herbs (commonest), whether epiphytic or not, to trees. In an Andean rainforest at around 2000 m, 79 species of flowering plants (in twelve families and 29 genera) were visited by 26 species of humming birds, of which the eight commonest visited 74% of these plants (Dziedzioch et al. 2003), while in the Monteverde forest, Costa Rica, 23 species of humming birds (this excludes uncommon and rare species) visited 181 species of plants in 60 genera and 28 families, 8.8% of the total flora (Murray et al. 2000). Even in southeastern Brazil, home to relatively few humming birds, four species of birds visited 23 species of plant belonging to 21 genera and 14 families, individual species of birds visiting between three and eighteen species of plants (Sazima et al. 1996: species visited only once excluded), while Buzato et al. (2000) recorded 86 species of plants (23 families, 44 genera) being visited by 15 species of humming birds, although at any one site there were 28-33 species of plants being visited by four main species of birds. Some 37 species of Andean Passiflora supersection Tacsonia alone and a few other species are visited by the long-billed hummingbird Ensifera ensifera (Abrahamczyk et al. 2014). Trap-lining birds may visit fewer species of plants than do territorial birds (Snow & Snow 1980).

Humming birds and swifts are sister clades and probably diverged in the Palaeocene 47.4-36.9 m.y. (McGuire et al. 2014). Rather surprisingly, the earliest humming birds known are from Oligocene Europe in deposits 34.3 m.y. old (Mayr 2004; McGuire et al. 2014). Crown-group humming bird diversification seems to have begun much later in lowland South America (24.7-)22.4(-20.3) m.y., much speciation occurring about 13-12 m.y.a. along with the uplift of the Andes (Bleiweiss 1998a; McGuire et al. 2007, 2014; Tripp & McDade 2014: crown-group diversification began (29.9-)28.8(-28.4) m.y.a.).

The overall imbalance of species numbers of pollinator/plants pollinated is probably similar to that of the euglossine bees just mentioned, with around 330 species of birds pollinating over 5,000 species of plants (4,040 species above, but this is still a considerable underestimate).

There are other, more general, estimates. Thus Muruyama et al. (2013) estimated that perhaps 20% of the species in Amazonian rainforest were pollinated by humming birds, compared to 2-3% in Cerrado vegetation; if the number of flowering plants in Amazonia is around 60,000, that would suggest 12,000 species were pollinated by birds there alone. Kress and Beach (1994) estimated that humming birds pollinated 14.9% of the 276 species of plants they examined at La Selva, Costa Rica, and when extrapolated to Amazonia this would yield a broadly comparable number of 8,940 species. However, these 274 species are not a random sample of the whole flora there, and Stiles (1985) estimated that there were 56 bird-pollinated species at La Selva (Kress & Beach 1994 recorded 41 species), only 3.8% of a total flora of 1650 species (Hartshorn & Hammel (994 estimate 1,280 species of flowering plants). If the estimate offered by Stiles (1985) were extrapolated to the whole of Amazonia it would give a figure of 2,625 humming bird-pollinated species there.

Sunbirds and spider hunters are both members of Nectariniidae-Nectariniini while flower peckers are the related Nectariniidae-Dicaeini, and they began diversifying in the middle Eocene around 45 m.y.a.; the stem group is perhaps Palaeocene in origin (Barker et al. 2004; Fleming & Muchhala 2008). Lorikeets, Psittacidae, probably date from the early Cenozoic (see Fleming & Muchhala 2008). For a phylogeny of Meliphagidae, see Driskell and Christidis (2004). The group is mid-Tertiary in age, and Barker et al. (2004) suggested that diversification occurred 50-45 m.y.a. in the Eocene. The Hawaiian-Oceanic Drepanidae are derived from an ancestor like a rose finch, and so are members of Carduelinae. Much diversification of clades representing extant species took place 5.8-2.4 m.y.a., especially after the formation of Oahu ca 4 m.y.a. (Lerner et al. 2011). Givnish et al. (1995) estimated that the age of the common ancestor of Cyanea was of the order of 17.4-8.7 m.y.a., about three times estimates of the age of diversification of Drepanidae, their pollinators.

The plants visited by Old World nectarivorous birds are mostly woody, in part at least because the birds need perches when feeding (Stiles 1981; Fleming & Muchhala 2008). Compared with humming birds, the relationships between bird and flower sometimes seem rather indiscriminate (see also Stiles 1981). From Africa to Australia, the birds often fly in mixed flocks (c.f. in part Brown & Hopkins 1995), any one species of bird may visit many species of plants, and any one species of plant may be visited by many species of birds, although bird-plant relationships are not totally promiscuous (Gill & Wolf 1975; Ford et al. 1979; Rebelo 1987; Brown & Hopkins 1995; Franklin & Noske 2000). Below I discuss bird pollination in Australia, South East Asia-Malesia, New Zealand, Hawaii, and Africa.

In Australia there are about 70 species of honeyeaters, a number of lorikeets, and a few species of other bird groups, for a total of about 111 species that pollinate flowers; Stiles (1981) estimated that there were ca 310 nectar feeding birds in the whole Australasian region, a figure that he thought was very definitely an upper estimate, while estimates in Fleming & Muchhala (2008) are 56 genera and 242 species, of which over 60% are honeyeaters. In other estimates, about half the honey eaters, ca 80 species, may be nectarivorous, individual species varying considerably in their diet (see also Recher 1981). Cheke and Mann (2008) suggested that honey eaters visited about 450 species of flowering plants from 100 families.

>p>Much literature does not distinguish between the type of pollinator. Keighery (1980, 1982) recorded about 21 species of birds visiting about 750 species of flowers in Western Australia alone (estimaes lower in Brown et al. 1997, but pollinators listed); Western Australia may be the epicentre of bird pollination in that region. In monsoonal northwestern Australia, some 24 species of birds visited 116 species of plants in twenty eight families (Franklin & Noske 2000). Ford et al. (1979) thought that in Australia some 300 species of Proteaceae and Myrtaceae were pollinated by about 100 species of birds, the brush flowers of Myrtaceae in particular being pollinated by lorikeets. There are about 1,100 Australian species of Proteaceae, and many species, including members of the large genera Grevillea and Banksia, are likely to be pollinated by birds (Maynard 1995) - an estimate of bird pollinated species, and Myrtaceae are also extremely diverse there. In addition, there are about 70 species of bird-pollinated Loranthaceae in Australia (Barlow 1984), while Toon et al. (2014) discuss the evolution of bird pollination (ca 37 spp.) in Fabaceae-Mirbelieae/Bossiaeeae some time between over 25 m.y.a. (stem age) to ca 17 m.y.a. (crown age).

A (gu)estimate is that around 120 species of birds pollinate 1,000< species of plants in Australia. The proportion of ornithophilous flowers may be relatively high on that continent since the copious nectar produced incurs very litle cost to the plant, an advantage given the nutrient-poor soils so common there. There is less ornithophily in the more nutrient-rich east coast forests (Orians & Milewski 2007).

It is more difficult to estimate numbers of bird-pollinated plants outside Australia, although in the area China and India to New Zealand the same groups of birds are involved. Here I do little more than list groups of plants where bird pollination may be expected to preponderate.

In the area from South East Asia to Malesia, there are a few groups of plants that are likely to be visited by birds. These include Ericaceae like Rhododendron, where 80 species from the island of Papua alone may be bird-pollinated (Stevens 1976; see also Corlett 2004), Paphia and Dimorphanthera, also largely Papuan and with around 75 species with red, tubular flowers, and about 95 species in the old genus Agapetes, with its centre of diversity in southwest China and adjacent Myanmar and India and also oftebn with red, tubular flowers. In addition, the widespread Aeschynanthus (Gesneriaceae) has around 185 species which have red flowers with the gullet syndrome. There may be some 36 species of bird-pollinated Loranthaceae in China (Qiu & Gilbert 2003) and 165 in Malesia (Barlow 1998). However, Brown and Hopkins (1995) note the apparently unspecialised morphologies of many of the flowers visited by birds in a site they studied in southeastern Papua New Guinea. They describe "knob" flowers from Schefflera and "fluffy cups" from Syzygium, etc.; apart from one species of Loranthaceae, none of the 17 species of flowers they list as being pollinated by birds are in groups that have been mentioned so far, although they do include both Myrtaceae and Proteaceae, important nectar sources in Australia. The 17 species of plants pollinated by three nectarinids in a locality in Sarawak included Malvaceae-Bombacoideae, Musaceae, Sapotaceae, Myrsinaceae and Zingiberaceae (Momose et al. 1998); two spiderhunters pollinated 8 species of Zingiberaceae in four genera (Sakai et al. 1999b) as well as three species of Loranthaceae (Yumoto et al. 1997) at localities in Borneo.

New Zealand has a mere 12 species of pollinating birds, of which only three were recorded as making almost 90% of the visits to flowers (Kelly et al. 2010). They are probably major visitors to 29 species of plants, and all told 85 species - or perhaps double that number - may be visited by the birds (Kelly et al. 2010; Lee et al. 2013). However, understanding plant/flower interactions in the islands in difficult, since one of the commonly pollinators arrived from Australia a mere years ago, and three of the other species have suffered serious recent declines. One of the pollinators, the stitchbird, is in a monotypic family and is unrelated to any of the other bird groups so far mentioned (Kelly et al. 2010).

Hawaii is noted for the remarkable radiation of Drepanidae, of which Drepanidinae in particular were/are (some species are extinct) both nectarivorous and insectivorous. All told, about 7 species of Drepanidinae seem to take/have taken nectar, to which can be added the 5 extinct species of Mohoidae (look-alikes of Meliphagidae) that were endemic to the islands. These few species of birds are/were probably pollinators of some 178 species of plants, of which around 125 species are Campanulaceae-Lobelioideae (Brighamia and Cyanea), but the main nectar source is probably Metrosideros, especially the protean M. polymorpha (Carlquist 1970; Lammers & Freeman 1986; Givnish et al. 1995; T. J. Givnish pers. comm. x.2013). Pender et al. (2013) date the diversification of both birds and plants to within the last 17 m. years.

Rebelo et al. (1984) suggested that ca 86 species of Proteaceae in the South African Fynbos were pollinated by the sugarbird, Promerops caffra, although sunbirds also visit them (Rebelo 1987). There are about 200 species of probably bird-pollinated Loranthaceae in all of Africa (Polhill & Wiens 1998), while 64 bird-pollinated species of Iridaceae (Goldblatt & Manning 2006) and 13 species of Cyrtanthus alone (Amaryllidaceae) are found in southern Africa (Snijman & Meerow 2010). Most of the species of Aloe in southern Africa are bird pollinated (Rebelo 1997), and there are probably over 400 species in the genus, nearly all African, although bees are also involved in pollination in a number of species (Symes et al. 2009; Hargreaves et al. 2012). Perhaps another 287 species of bird-pollinated plants can be added from southern Africa (Rebelo 1987: 424 species, from which Proteaceae, etc., have been removed). At a more local scale, Rebelo (1987) estimated that perhaps 318 species of plants were pollinated by six species of birds (including Promerops caffra) in the Cape region alone of South Africa.

Perhaps 950 species are pollinated by birds, which, apart from the sugar birds, are mostly members . As in Australia, the relatively high frequency of ornithophily in the Cape flora may be connected with the prevalence of nutrient-poor soils there (Rebelo 1987; Orians & Milewski 2007).

To summarize differences between Old and New World nectarivous birds and the plants that they pollinate. Humming birds tend to pollinate herbs and epiphytic plants, while in the Old World nectar-feeing birds more frequently pollinate larger trees (e.g. Stiles 1981; Kress & Beach 1994; Fleming & Muchhala 2008). Both humming birds and phyllostomid bats, restricted to the New World, are more specialized than their Old World ecological counterparts, although African sunbirds show a moderate degree of specialization, similarly, bird-pollinated flowers, at least, in the New World seem to be more specialized (Stiles 1981; Fleming & Muchhala 2008). Papuan plant-pollinator relationship may be less specialised that those in Australia (Brown & Hopkins 1995). Assemblages of humming birds and phyllostomid bats in any one site in the New World are more diverse than their Old-World counterparts (Fleming & Muchhala 2008). Overall, the general diversity of plants pollinated by birds and bats is lower in the Oriental region than in the New World or the Australo-Papuan region (e.g. Corlett 2004).


For good introductions to bat pollination, see Dobat and Peikert-Holle (1985) and Fleming and Kress (2013).

Phyllostomid bats are relatively small and often hover when they feed, and the plants they pollinate are trees as well as vines and epiphytes; they are active in the l.t.r.f. as well as in deserts (Fleming et al. 2005, 2009). In any one site there may be 1-6 species of bats, and these pollinate 4-19 species of flowering plants (Fleming et al. 2005). In the Monteverde forest, Costa Rica, 7 species of bats visited 33 species of plants, only 1.6% of the total flora (Murray et al. 2000). Phyllostomines are important pollinators of columnar cacti, Aagave, and Malvaceae-Bombacoideae, with 16 species recorded as pollinating 90 species of plants including some of these cacti (Arizmendi et al. 2002). Clairmont et al. (2014) found pollen of 11-14 species of plants (2.4-3.9/night) in the excreta of three phyllostomines in Cuba, although the figure was 17-21 species (3.5-5.3 species/night) in two species of fruit-eating bats; the study was carried out in the wet season.

Diversification of the bats has occurred within the last 30-12 m.y. (Datzmann et al. 2010), and bat-pollinated flowers may have begun evolving in the Miocene (Fleming et al. 2009), ca 20 m.y.a..

Estimates are that at least 500 species of plants in 27 families are pollinated by bats (Vogel 1969). Figures in Dobat and Peikert-Holle (1985) are 590 New World species of plants in 43 families, although some other estimates are substantially lower - 364 species in 44 families (Fleming et al. 2009). However, the latter figures in particular need to be revised substantially upwards. Thus Fleming et al. (2009) list 20 bat-pollinated species in the Centropogon alliance (Campanulaceae-Lobelioideae), although L. Lagomarsino (pers. comm.) estimates that about 180 species of that group may be pollinated by bats, while 110 species is the estimate in Dobat and Peikert-Holle (1985). Similarly, 5 bat-pollinated species of Passiflora are listed by Fleming et al. (2009), while Jørgensen et al. (2012) suggest a figure of 17 species (8 known pollinators, 9 likely).

In the Old World there are only 6 genera and 15 species of nectar-feeding bats (again, some species visit flowers on a more opportunistic basis), the macroglossine Pteropodidae (e.g. Fleming et al. 2009). They are found from Africa to Australasia and the Pacific (Fleming & Muchhala 2008). Pteropodid bats are on average larger than phyllostomid bats, they tend to hold on to the plant when feeding, and the flowers they pollinate are robust and are usually borne on trees (Fleming et al. 2009). Estimates are that there are under 200 species of bat-pollinated flowers in the Old World (Dobat & Peikert-Holle 1985); 168 species in 41 families is the figure in Fleming et al. (2009).


Van der Niet and Johnson (2012) estimated that one quarter of plant speciation events might involve pollinator differences. However, details of con- and heterospecific pollen movement and related topics like the establishment and efficacy of barriers to crossing between species are not at issue here (see e.g. Armbruster 2014 for a recent review). The focus is on numbers of species of plants and animals involved in particular sets of pollination relationships, since this is one way of allowing us to think about ideas of co-evolution, mutualism, and the like. The idea of co-evolution promoted by Ehrlich and Raven (1964) has been used to describe many different kinds of evolutionary relationships, and so the term has to be defined precisely when used (e.g. Hembry et al. 2014).

Floral variation and plant-pollinator interactions have long been of central interest to biologists. Thus Stebbins (1970: p. 308) noted that in animals major categories might differ in characters related to survival, while in plants the "flower must become a highly integrated stucture, with all of its parts precisely adjusted to each other" for cross pollination by animals with specialised habits to be successful. Fifty years or so ago plant-pollinator relationships were often thought of in terms of mutual co-evolution, with an emphasis on lock and key relations between particular flowers and their pollinators implying 1:1 relationships between the two (e.g. Grant & Grant 1965). Stebbins (1970), although cautious, conveyed this general idea when he noted that euglossine bees obtained fragrances from orchids, extensive speciation in both being the result, and also when he discussed intermediates between different pollination syndromes.

Ollerton et al. (2011) estimated that the number of animal-pollinated plants as 308,006, 87.5% of an estimated 352,000 species of flowering plants (see Paton et al. 2008). Sekercioglu (2006) had suggested that some 600 species of birds visited plants for nectar, 350 more being casual visitors, and that they visited 500 of a total of 13,500 plant genera (his estimate), i.e. about 3.7%. Assuming that there are around 300,000 species of flowering plants, this might suggest that all told some 11,000 species are bird-pollinated. Estimates of plant:pollinator relatinships have been made for the flora of New Caledonia where there are 43 species of native bees and a flora of over 3,050 species of flowering plants; Donovan et al. (2013) estimated a plant:bee ratio of 71:1, while in New Zealand the ratio was 57:1. Whatever their limitations, we can start off with such figures as rough estimates, and they suggest major asymmetries in the flower-bird relationship since estimates of the numbers of birds that pollinate flowers are less than 1/10th the number of species of plants they pollinate.

A single species of bee may visit over a hundred species of flowers (ref.?).

A single species of pollinator may visit many species of plants, so there are often marked asymmetries in the specificity of relationships (Bronstein 1994), e.g. S. D. Johnson and Steiner (2000), Mello et al. (2012). Overall ratios of 10 species of plant to 1 species of pollinator are at the low end of the spectrum. Thus in Costa Rica, Stiles (1981) estimated that 55 species of humming birds pollinated mostly or exclusively around 300 species of plants. In the Cape region of South Africa, Rebelo (1997) estimated that perhaps 318 species of plants were pollinated by five species of sunbird and the Cape sugarbird, Promerops caffra, the 15:1 plant:bird ratio he noted as being particularly high. Promerops is particularly attracted to 80 or more Cape Proteaceae, while perhaps 37 species depend for their pollination on the malachite sunbird, Nectarinia famosa (Geerts & Pauw 2009). Long-tongued dipteran flies in southern Africa, a small-scale example of species number imbalance, have similar plant:pollinator ratios, anywhere from 6:1 (highly conservative) to much in excess of 30:1; thus Prosoeca ganglbaueri pollinates 20 or more species (van der Niet & Johnson 2012). Also in southern Africa, the satyrid butterfly Meneris/Aeropetes tulbaghia pollinates 19 species of plants belonging to 8 genera and 4 families (S. D. Johnson & Bond 1994). In Western Australia, the New Holland honeyeater, Phylidonyris novaehollandiae, has been recorded as visiting flowers of 142 species of plants from 32 genera and ten families (Brown et al. 1997). In the Andes, 37 species of Passiflora supersection Tacsonia (and some other plants) are pollinated by the long-billed hummingbird Ensifera ensifera (Abrahamczyk et al. 2014). Interestingly, many of these examples are from the southern hemisphere (Johnson & Steiner 2000).

From the point of view of the plant this promiscuity may be more apparent than real. Members of a single polylectic (generalist) bee species, or colony, or even an individual bee, may visit many species of plants, but a single bee may be much more selective on any one trip, or even throughout its lifetime (e.g. Heinrich 1976; Chittka & Thomson 1997; Heard 1999; Hagbery & Nieh 2012 for general pollen/nectar constancy). Thus the bees may visit only one or a few species in any one trip, so being functionally mono- or oligolectic (specialist). Along the same lines, since many humming birds, honey eaters, bumble bees and the like are widely distributed, at any one place the plant:pollinator ratio is rather lower (e.g. Rebelo 1987).

Understanding the relative timing of plant and pollinator diversification is important when thinking about the evolution of such plant:pollinator relationships. There are suggestions that in general plants diversified earlier that their bird or bat pollinators (Fleming & Muchhala 2008: ages of families used; Fleming & Kress 2013: esp. table 5:3). More or less strict co-evolution would suggest that the plants and pollinators diversified together, however, some text-book examples of floral co-evolution are breaking down. Examples are the yucca/yucca moth and orchid/orchid bee associations. Thus, crown-group euglossine bees can be dated to 42-27 or 38-34 m.y.a., especially rapid diversification going on 20-15 m.y.a. (Ramírez et al. 2010) or (35-)28(-21) m.y.a. (Cardinal & Danforth 2011). Orchids that these bees pollinate speciated up to 12 m.y. later, (31-)27-18(-14) m.y.a. (Ramírez et al. 2011); these are dates of three immediately unrelated clades of orchids that are involved. On the other hand, much of the divergence in Yucca seems to have occurred before that of its main pollinator, Tegeticula, but only a mere 6-4 m.y.a., and given the vagility of the moth, it is difficult to imagine how co-evolution might work. Initial diversification in Yucca may have been in association with Parategeticula, a poor flier and now rather uncommon (Althoff et al. 2012). Other examples of such temporal asynchronies include diversification of two groups of bird-pollinated New World Acanthaceae was more recent than that of their humming bird pollinators (Tripp et al. 2013c; Tripp & McDade 2014; McGuire et al. 2014), and in the apparently less tight association of aroids with scarab beetles, the beetles diversified well before the plants (Schiestl & Dötterl 2012). Although the sword-billed hummingbird split from other humming birds ca 11.6 m.y.a. (McGuire et al. 2014) and the stem age of the clade of Passiflora whose species it largely pollinates is ca 8.4 m.y. (Abrahamczyk et al. 2014: many support values rather low, the crown age is ca 7.1 m.y.), we lack information as to when the sword bill itself evolved. The pollinator/plant asymmetries discussed here are driven by the evolution of groups of polylectic pollinators like bumble bees and humming birds, and many of these relationships are of relatively recent origin, plant diversification being (substantially) later than pollinator diversification.

In much floral evolution there is little evidence of co-speciation; f There is little evidence for a co-evolution defined as reciprocal (mutual) evolution and speciation in plant-pollinator interactions (Jordano 1987; Waser et al. 1996; Sazima et al. 1996; Chittka et al. 1999; Fenster et al. 2004; Waser & Ollerton 2006; Raguso 2008; Ollerton et al. 2009a; Fleming & Kress 2012: pp. 182-188). Still less is there evidence for plant:pollinator relationships resulting in reciprocal bursts of speciation (Hembry et al. 2014). Figs may be an exception (Cruaud et al. 2012a, b and literature), but even here there may be selection on the pollinator without corresponding changes in the plant (Moe & Weiblen 2012; Hembry et al. 2014; see also ).

Corbiculate bees are estimated to be (89-)77(-66) m.y.o., within which the crown-group stingless meliponines are (61-)58, 51(-48) m.y., euglossine orchid bees (35-)28, 26(-17) m.y., bumble bees (48-)26, 21(-12) m.y., while honey bees are only (30-)22(-16) m.y.o. (Cardinal & Danforth 2011; Martins et al. 2014).

Ideas of hyperdominance may be applicable here. Hyperdominance favours the evolution of character complementarity, where features of plant (e.g. flower colour, tube length, pollen quantity, nectar composition) and pollinator (e.g. sensitivity to particular wavelengths of light, dietary needs) match (Guimarães et al. 2011). Similarly, the sucrose-rich nectars that characterise humming bird-pollinated flowers are associated with the ability of humming birds, but not starlings, thrushes, swifts, mocking birds, etc., to digest sucrose (Baker et al. 1999) and the very ability to taste sweetness (Baldwin et al. 2014).

The asymmetry in numbers between pollinator and plant suggests that any co-evolutionary relationships are at most diffuse (see also Placentini & Varassin 2007). These asymmetries represent groups of plants that converge on morphologies accessible to super-generalist pollinators; the plants may evolve, but their pollinators are less likely to (Guimarães et al. 2007, 2011; Thompson 2009). This is compatible with the ideas of Wiens et al. (1983) who included such relationships in their idea of unilateral evolution, in which plants evolve profoundly altered floral features to attract non-specialised (from the point of view of the plants visited) pollinators, although in many cases these pollinators are very specialised when compared with their own relatives in terms of features like behaviour, the ability to learn, and the like. At the level of species, relationships between plant and pollinator may be quite specific, the reverse is less likely to be true. In some plant-pollinator interactions plants may exploit pre-existing perceptual/sensory biases of the pollinator, effectivly manipulating their behaviour. This can happen in pollination by deception (e.g. Schaefer & Ruxton 2009; Moré et al. 2013), and there benefits are one-sided, and it also occurs commonly in cases like those under discussion when both plant and pollinator are benefited (e.g. Chittka 1996; Schaefer & Ruxton 2009, 2010; Ramírez et al. 2011; Schiestl 2010; Schiestl et al. 2010; Ramírez et al. 2011; Schiestl & Dötterl 2012; Shresthra et al. 2013; Hembry et al 2014; c.f. Strong et al. 1984). Similarly, Stiles (1981) had contrasted the behavioural flexibility of the pollinator (humming birds in this case) with the evolutionary flexibility of the plant. [[; see also Dyer et al. 2012; Wright et al. 2013]].

Wiens et al. (1983) expected to find similar relationships in plants with wind or water pollination, also in those with pollination by social bees, passerine birds, most flies, and perhaps beetles; they themselves looked at pollination of South African Protea species by small mammals. Thus it is less that long-tongued euglossine bees that pollinate a variety of Zingiberales, for example, have specialized on flowers with long tubes, but rather, the plants have specialized on long-tongued pollinators (Borrell 2005; see also S. D. Johnson 2010). Such imbalances have been noted before (e.g. Weins et al. 1983), even if their sigificance has not percolated down to textbooks. The asynchrony in timing of the evolution of the two partners in pollination relationships that may now seem to represent an obligate association for at least one of the two (e.g. Fleming 2004; Ramirez et al. 2011; Schiestl & Dötterl 2012) also suggests the nature of such relationships.

That there have been pervasive - if not very tightly linked and usually very asymmetric - interactions between plants and their pollinators is incontestable (Thompson 2009; Guimarães et al. 2011). Despite the apparent promiscuity of polylectic pollinators, individual plant:pollinator interactions may be exquisitely precise, witness the deposition of pollinaria by the orchid Catasetum on a visiting euglossine bee, and the complex morphologies of the staminate and carpellate flowers of this orchid (for which, see e.g. Darwin 1862a). Of course, if the effects on the insect in such interactions are independent of other interactions in which it is involved, there could be evolutionary specificity in the response of the animal (see in part Bawa 1990). Features of the pollinator may also evolve along with features of a plant guild that it pollinates (Newman et al. 2014; van der Niet et al. 2014). In southern Africa a number of species of plants belonging to unrelated families depend on the services of a small group of pollinators (S. D. Johnson 2010; see also Huang & Shi 2013). Thus Pauw et al. (2009) described rather diffuse co-evolution between individual species of flies with long probosces and and a group of species with long-tubed flowers. There may be more or less reciprocal evolution between a single species of fly and plant or group of plants, not necessarily related, and there are also other plants, not necessarily with rewards for the pollinator, in which evolution is one-sided; the interactions take place in a complex geographical mosaic, with some of the flies having great variation in proboscis length, and a variety of pollination ecotypes developing (e.g. Pauw et al. 2008; Newman et al. 2014; Anderson et al. 2014; see also Bascompte & Jordano 2007).

In hummingbirds, at least, along with other iconic "New World" bird groups, initial evolution may have been in Europe (Mayr 2004; Mayr & de Pietri 2014), so further complicating the issue. Indeed, the earliest direct evidence of birds visiting flowers comes from the Middle Eocene of Germany ca 47 m.y.a. where eudicot (tricolpate) pollen was found in the gut of Pumiliornis tesselatus. Pumiliornis, although of uncertain relationships, is not close to any of today's major flower pollinators, such as parrots, honeyeaters and humming birds (Mayr & Wilde 2014). The challenge when thinking about floral evolution and pollinator preferences is to understand the evolutionary changes - which may well be more mutually co-evolutionary - that initially resulted in morphological, etc., changes in the animal partner that we now see as the features of a supergeneralist pollinator (Guimarães et al. 2011); whether any clade of bird-pollinated plants dates back to 47 m.y.a. when there is first evidence of pollination by birds is debatable (c.f. Mayr & Wilde 2014). The currently highly asymmetrical plant:pollinator relationships are now superposed, as it were, on an earlier and probably rather different set of relationships.

Here I turn to look more generally at aspects of the evolution of plant-pollinator relationships. Thinking about asymmetries in pollinator:plant relationships leads to a set of apparent paradoxes (see also Johnson & Steiner 2000). Snow and Snow (1980) noted that although a highly specialized flower might have but a single humming bird pollinator, a very specialized bird might pollinate several species of plants, i.e. it was a generalist. Some small groups of animals are polylectic or generalist pollinators that service a disproportionately large number of plants. However, we often think of both plant and pollinator as being specialists (for pollination/dispersal syndromes and guilds, see also characters). Indeed, the morphology and behaviour of polylectic pollinators is by no means generalist. For example, the southwest African nemestrinid fly Moegistorhynchus longirostris has a tongue 40-90 mm long (S. D. Johnson 2010). Polylectic bees such as Apidae have large brains and a well developed sensory system, enabling individuals to learn how to pollinate diverse flower morphologies ranging from simple to complex (e.g. Heinrich 1976; Laverty 1994; Raine & Chittka 2007a, b), while the literature on bird and bat pollination is full of the remarkable adaptations of these animals that are involved in pollination. Similarly, the flowers visited by polylectic pollinators like humming birds and bumble bees are specialized, often being monosymmetric, with concealed nectar, etc.. Such specialized monosymmetric flowers may indeed be visited by rather few species of polylectic pollinators, be they bees, flies, or humming birds, although several species of bee may visit the one species of Pedicularis (Macior 1982). Indeed, Rebelo [1987] suggested that both plants and pollinating birds in the South African fynbos were generalists, while Cameron (2004) thought that most species of orchids attracted many species of euglossine bees, while most species of bees were attracted to several different species of plants.

Oligolectic bees are bees that visit relatively few species of flowers, and/or a group of rather closely related plants, i.e. within a single family, so they are specialized from that point of view; oligolecty refers to pollen-collecting behaviour, not nectaring, where bees tend to be more catholic (Waser et al. 1996). Oligolectic bees may have fewer obvious morphological adaptations for pollination (Michez et al. 2012), and the flowers such bees visit are often what would be described as unspecialized, with radial symmetry, poorly concealed nectar, etc., although oligolectic bees may also pollinate monosymmetric flowers (e.g. Bawa 1990; Sedivy et al. 2008). Plants with generalist-type flowers are apparently accessible to a wide variety of pollinators (e.g. Bawa 1990). Solitary bees are often oligolectic, and oligolectic bees are in general most diverse in desert and arid often extratropical regions, and they tend to be short-lived and the flowering times of the plants they pollinate are also often rather short (Linsley 1958; Michener 1979). Thus in arid and semi-arid areas (deserts, the Great Basin, parts of California; Chile) there are numerous species of oligolectic bees (e.g. Waser et al. 1996). Such specialist/oligolectic bees are common and at least sometimes compete for the same resource (see in part Moldenke 1976, 1979a, b; Petanidou & Ellis 1996; Lindberg & Olesen 2001; Stang et al. 2007). For example, the creosote bush, Larrea tridentata (Zygophyllaceae), with an open and "unspecialized" floral morphology, is common in the American southwest. It is the focus of visits by 22 species of oligolectic bees and regularly visited by another 22 species of polylectic bees, not to mention other more transient visitors (Hurd & Linsley 1975); 12 species of oligolectic Andrena bees are major visitors to Camissonia campestris (Onagraceae: Linsley et al. 1973: see also Cruden 1971: Nemophila; Ehrenfeld 1979: Euphorbia; Waser et al. 1996: Ranunculaceae). Plant species with unspecialized flowers may be visited by several species of oligolectic bees, but such specialist pollinators may be no more effective in or necessary for pollination than are generalists (e.g. Ehrenfeld 1979; Olesen 1997 and references).

Overall, there are many species of plants with specialized flowers and many species of bees that visit a relatively few species of plants. The two groups interact relatively little, and pollinator-plant relationships are not nested in any simple fashion: Specialist flowers interact more with generalist pollinators, while generalist flowers interact with specialist, and often also generalist, pollinators (e.g. James et al. 2012; c.f. Bascompte et al. 2003; Pawar 2014). In floral evolution, unspecialised flowers probably pollinated by several species of oligolectic bees and other pollinators precede specialised flowers pollinated by one or a few species of polylectic pollinators just as the polylectic habit in bees tends to be derived. Of course, there are young, very speciose clades of plants that are commonly pollinated by oligolectic bees, Asteraceae being a prime example (see Waser et al. 1996 for the large numbers of pollinators visiting a single asteraceous species). Incidentally, it has been suggested that oligolecty permits the evolution of large numbers of sympatric species of plants because each is pollinated by different species of pollinators (e.g. Linsley & MacSwain 1958), the behaviour of at least some polylectic pollinators will have the same effect.

Monosymmetric flowers in which precise interactions between plant and pollinator are needed for effective pollination have become more common over evolutionary time, and simultaneously bees, for example, have tended to pollinate a greater variety of hosts; polylectic behaviour in bees is often derived (e.g. Müller 1996; Michener 2007; Sedivy et al. 2008; Litman et al. 2011; Danforth et al. 2013; c.f. Moldenke 1979b). In the humid tropics polylectic bees, which often live longer, are proportionally commoner than oligolectic bees (Michener 1979). Although in Venezuelan forests, at least, fruit set in specialized (monosymmetric, gullet types) flowers may be less than that in generalized flowers (Ramírez 2003), this cannot be linked to the particular pollinators involved.

For a polylectic pollinator that serves as a hub (when diagramming out plant-pollinator relationships) the effect of the extinction of a single species of plant may be slight, but the extinction of such a pollinator may affect some of the plants it pollinates more seriously. Of course, such consequences will depend on the overall patterns of modularity and connectedness of the plant-animal relationships, connectance being notably higher in polylectic bumblebees or humming birds, less in agaonid wasps and oligolectic bees - and in the examples given by Jordano (1987) also euglossine bees (see also Waser et al. 1996; Lindberg & Olesen 2001; Rezende et al. 2007; Stang et al. 2007; Olesen at al. 2007; Vamosi & Vamosi 2012; also Vásquez & Simberloff 2002: disturbance and pollination; Colles et al. 2009; Armbruster 2012). For oligolectic pollinators, the relationship will tend in the reverse direction; plant specialists or species with low numbers of interactions are more likely to go extinct than species with more diverse sets of interactions (Aizen et al. 2012; James et al 2012). The high degree of asymmetry in pollinator/plant interactions is compatible with recent work demonstrating the apparent inevitability of the development of such asymmetries (Suweis et al. 2013; Fontaine 2013). In an experimental study, communities in which generalist species, more highly nested, developed as the population of the whole system increased, even as the whole became less resilient to perturbations, unstructured systems being more resilient (Fontaine 2012; esp. Suweis et al. 2013). In general, removal of single polylectic pollinators from pollination networks may not have much effect, although the removal of a single species of bumble bee from a subalpine community in the Rockies perturbed general pollination relationships there (Brosi & Briggs 2013). [elaborate or delete: Rezende et al. (2007) suggested that extinctions might have some phylogenetic signal, but this is certainly not always true (Ramírez et al. 2011).]

When thinking about such asymmetric relationships the idea of pollinators/fruit dispersers being keystone clades that show phylogenetic niche conservatism (e.g. Fleming et al. 2005; S. D. Johnson 2010: see below) readily spring to mind. Out of place: the numbers of plants involved in pollination asymmetries is not that large, in the estimates above only ca 5% of the total, although such figures are likely to be considerable underestimates.

9A2. Seed Dispersal.

Major diversification of fruit-eating phyllostomid bats began (27-)22(-18) m.y.a. in the late Oligocene to mid-Miocene (Datzmann et al. 2010; see also Rojas et al. 2011). This is a long time after the beginning of diversification of Piper, at least, raising the question of how what now seems to be close to an obligate relationship of both sides has evolved (Fleming 2004). Old World fruit-eating bats (pteropodids) tend to disperse seeds of later-successional trees, and they prefer fruits of families like Sapotaceae, Meliaceae, Arecaceae and Rubiaceae (Muscarella & Fleming 2008). Bats can be very abundant, and New World phyllostomids are wide-ranging compared to Old World pteropodids (Muscarella & Fleming 2008). The ecological importance of these bats in terms of the services they provide plants is considerable (Freeman 2000; Muscarella & Fleming 2008).

Kattan and Valenzuela (2013) summarize the information pro and con the importance of Ficus as a food resource, noting that in some places the local species, although at times producing large amounts of food for frugivores, nevertheless do not do so throughout the year.

New World phyllostomid fruit bats have networks that are more highly nested and have higher connectance than fruit-bird networks, but were less robust to extinctions (see also Guimarães et al. 2011; Suweis et al. 2013 for this phenomenon); at the same time, there was low complementary specialization within a network (Mello et al. 2011a, b). Fruit-eating phyllostomid bats that are ecologically specialised may be generalists when looking at bat/plant networks (Mello et al. 2011a). Note that fruit bats have a monophyletic origin while fruit-eating birds are polyphyletic.

9B. Carbon Sequestration.


Major Players.

C4 photosynthesis, and Grasses and Grasslands.

Ectomycorrhizal Plants.

Seagrasses, Mangroves, and Tidal Saltmarshes.



Bengtsson (1998) and others have emphasized that species numbers are only one metric of evolutionary importance or success, however, numbers are quite easy to come by and they are usually the metric of choice. Estimates of biomass, productivity, even area occupied, whether for clades or for species, are much harder to obtain, but are other possible metrics, and from the point of view of global ecosystem functioning are of great importance. Here the focus is on particular clades of seed plants, sometimes quite small in size, that have a disproportionately large effect on communities, ecosystems, even the global environment. In particular, they dominate the communities in which they occur and fix and/or sequester large amounts of carbon.

It has been noted in a rather general way that in just about all communities there are common species; one can almost expect 25% of the species to contribute 50% of the biomass or over 80% of the individuals, and the slope of biomass accumulation is less than that of species number accumulation (Gaston 2011; see also Gaston 2010; M. D. Smith & Knapp 2003), but the asymmetries discussed here are more extreme. If around 60% or more of the canopy individuals and/or basal area are represented by a single species, that species is commonly described as being monodominant (Connell & Lowman 1989; see also Peh et al. 2011), and this is the monodominance that is the focus here, although it is sometimes extended to include members of a particular clade that grow together. Species that are dominant only in early successional phases (Type II transitional dominance, including Shorea albida!: Connell & Lowman 1989) are usually not considered further, although Newbery et al. (2013) described the long-lived Microberlinia bisulcata (see below), in the Cameroons as a "transient dominant". Indeed, a factor to take into account is the extent to which some of the vegetation types discussed reflect human activities, even if they are not successional, and this is discussed below.

Pitman et al. (2001, 2013) noted a surprisingly large number of common (>1 individual/ha) and widespread species of trees at least 10 cm across in the terra firme forests of western Amazonia. Some 83 of these oligarchic species (there were 150 of these species altogether) from several different families occurred per hectare in Peru, and although they represented over 50% of the individuals, individual species were not close to being monodominants, even by the somewhat relaxed definition sometimes adopted below. Ter Steege et al. (2013) found that half the individuals with stems at least 10 cm across in Amazonian rainforests as a whole were accounted for by a mere 227 species in 41 families in 11 orders; they called these 227 species "hyperdominants" (they would be hypodominants following classical ideas of dominance). In any one plot 32 of these species represented 40.7% of the individuals (medians; ranges 0-78, 0-93%: ter Steege et al. 2013). One or two of these common species may be dominants as defined here (see Arecaceae, Fabaceae below), but few biomass estimates are available; the rest are not considered further.

The estimates of area, biomass, carbon accumulation, primary productivity, etc., given below should be taken with more than a grain of salt, and they can vary very widely from author to author (e.g. Brown & Lugo 1984; Botkin & Simpson 1990; Dixon et al. 1994; Chmura 2011). Not only do different countries have different definitions of "woodland", "grassland", "peat soils", and the like, but the distinction between communities such as sea-grass, marine salt-marsh and mangrove communities are not always clear. It is also easy to forget that there are three different kinds of tons, and which is being used is not always mentioned. Ideally, biomass estimates for both above and below ground are needed, and the latter in particular should include dead biomass, but frequently estimates of only one are given, and any estimation of the one from figures of the other should be undertaken with caution (e.g. Cairns et al. 1997; Pan et al. 2013); here the focus is on below-ground carbon accumulation.

Major Players.

C4 photosynthesis and Grasses and Grasslands.

C4 photosynthesis, grass, and grasslands together make up a major component of global ecology. Overall only somewhat over 2% of angiosperms - perhaps some 7,500 species - are C4 plants (R. Sage et al. 2012). They can be divided into three main groups: grasses, sedges, about which little is known ecologically, and core eudicots, particularly chenopods; in none is the origin of C4 photosynthesis monophyletic. For an entry into the literature, see R. Sage et al. (2012); drivers of the evolution of this distinctive syndrome are probably the decrease of CO2 in the atmosphere at the beginning and again towards the end of the Oligocene, and increasing temperature, which together would lead to an increase in photorespiration, perhaps the immediate driver in the evolution of the syndrome - but it will be clear that we understand little about details of its origin and spread (see also Cowling 2013). For details of the evolution of C4 photosynthesis, see e.g. Kellogg (2013), Heckmann et al. (2013), Williams et al. (2013), Christin and Osborne (2014) and references.

The global distribution of C4 vegetation is ca 18.8 x 106 km2 and that of C3 vegetation, ca 87.4 x 106 km2 (Still et al. 2003, q.v. for map). All told C4 photosynthesis accounts for about 23-28% of terrestrial gross primary productivity (35.3 Pg C yr-1, vs 114.7 Pg C yr-1), although the biomass of C4 plants is less than 5% of the global total, 18.6 vs 407.9 Pg C yr-1 (figures from Still et al. 2003: see also Lloyd & Farquhar 1994; Ehleringer et al. 1997; Retallack 2001). Most of the difference is in the woody biomass, that of C3 plants being 352.7 PgC and that of C4 plants zero (obviously Caryophyllales not factored in); in both cases root and leaf biomass was estimated to be about equal, that of C3 plants being about twice as much as C4 plants, 36.6 vs 18.6 PgC (Still et al. 2003). Other estimates of total biomass are similar: 15.6 vs 488.5 Pg C (Ito & Oikawa 2004).


For good summaries of the ecology of grasses and grasslands, see Coupland (1993a, b), White et al. (2000) and Gibson (2009). Factors like fire, increased temperature, rainfall seasonality, and low CO2 all interacted in the spread of C4 grasses, grasslands and savanna, C4 photosynthesis minimizing photorespiration and grasses being particularly flammable because of the litter they produce (e.g. Lehmann et al. 2011; Scheiter et al. 2012; R. Sage et al. 2012; Kellogg 2013), although how these variables interact may differ according to the continent (Lehmann et al. 2014). Decreasing CO2 concentration 8-5 m.y.a. is evident in the marine coccolithophore record (Bolton & Stoll 2013); decreasing precipitation is unlikely to have been involved (Retallack 2013, but c.f. in part Hoffmann et al. 2012).

Grasses also have a great effect on soils and weathering (see above). Grassland grasses have dense root systems, and savanna trees allocate relatively more carbon to below-ground biomass than do forest trees, and there has been the recent evolution of woody plants with massive stem and root systems underground, but with little permanent above-ground biomass (Scheiter et al. 2012; Pennington & Hughes 2014, see also above). Only some 600 species of grass dominate ecologically worldwide, and most of these are C4 photosynthesizers (Edwards et al. 2010). Andropogoneae, with some 1,200 species and 90 genera, are notable here in their positive response to annual burning (Forrestel et al. 2014 and references), while in African, Australian and North American grasslands and savannas in particular members of the ASH clade (Andropogon, Hyparrhenia, Schizachyrum), with some species, are prominent among the dominants (Estep et al. 2014).

Productivity estimates for grasslands in particular, including both C3 and C4 species - are that they currently account for 11-19% of net primary productivity on land and 10-30% of soil C storage (Hall et al. 2000); soil C storage estimates in Averill et al. (2014) are (12.3-)14.5(-17.7) kg C m-2, NPP figures being (477-)576(-675) kg C m-2 yr-1. Gibson (2009) suggests that grasslands store 650-810 GtC, ca 33% of the global total, and 55-95% of that is stored underground, the higher values being in higher-latitude (probably = Arctic) areas. More general figures for tropical savannas and grasslands together - the grasses are likely to be C4 grasses - in Carvalhais et al. (2014: Tables S1 + S2) are ca 338 Pg total C, a carbon density of around 17.7 kgC m-2, and a mean turnover time of (12.2-)16(-22.1) years; the last set of figures is only slightly higher than those for l.t.r.f.. Comparable figures for temperate grasslands and shrublands are (145-)187(-249) Pg total C, a carbon density (13-)16.7(-22.2) kgC m-2, and a mean turnover time of (32.8-)41.3(-54.6) years; there are much longer residence time for the carbon, largely because of the cooler temperatures.

Chenopods. C4 eudicots are often found in some combination of arid, ephemeral, warm to cold (at least in the winter), disturbed and/or saline conditions (Ehleringer et al. 1997; Kadereit et al. 2012). In the rather cold Gobi deserts of Mongolia 15-17% of the species are C4 plants, and over 50% of these are chenopods; chenopods contribute 30-90% of the biomass there, although overall C4 plants are only 3.5% of the total Mongolian flora (Vostokova et al. 1995; Pyankov et al. 2000). In such areas Amaranthaceae-Chenopodioideae make up over half the C4 species (Pyankov et al. 2000). Similar fast-growing C4 Chenopodioideae (and some Polygonaceae), some of which like Haloxylon aphyllum are arborescent - it can reach 10 m in height with a trunk 1 m across (Winter 1981) - also dominate the halophytic vegetation of the somewhat warmer Central Asian Turanian deserts (Winter 1981). Succulent C3 chenopods are common in the Gobi in true desert conditions, and also in moist, saline soils (Pyankov et al. 2000).

Aridification in Australia began early in the Miocene ca 22 m.y. ago. C4 taxa like Atriplex also diversified there; the genus was probably a major item in the food of the extinct giant (ca 230 kg) kangaroo Procoptodon goliah (Prideaux et al. 2009; Kadereit et al. 2010).

Ectomycorrhizal Plants.

ECM/ERM forests

The almost 4,000 species of Ericaceae with ERM (ectendomycorrhizae) are not included in the totals above. However, Vrålstad (2004), Tedersoo et al. (2010b) and others have suggested that ECM and ERM form a single ecological guild, one of whose characteristics is that the fungi are intermediaries in the uptake of organic nitrogen by the plant (e.g. Rad 1991, 1996; c.f. Persson & Näsholm 2001), and they are included in the discussion here. Orchid mycorrhizae, also often considered to be modified ECM, are not discussed further.

ECM/ERM plants are especially common in subarctic to (cool) temperate/montane habitats, but also in West Malesian dipterocarp forests, Australian Eucalyptus woodlands (the mycorrhizal ecology of which is little known), the African Miombo and Sudanian woodlands, and also considerable areas of the Guineo-Congolian coastal and Ituri rainforests (e.g. Malloch et al. 1980; White 1983; Safer 1987; Connell & Lowman 1989; Hart et al. 1989; Read 1991; Sanford & Cuevas 1996; Torti et al. 2001; Peh et al. 2011); Sudanian and Miombo woodlands are biogeographically close (Linder et al. 2012).

ECM/ERM plants tend to dominate the communities in which they grow, and a very approximate estimate of the number of dominant ECM species is 1,000. This includes ca 160/388 species of Dipterocarpaceae, 11/13 Nothofagaceae, and 50/165 Fagaceae from Malesia alone (data from Ashton 1981; Soepadmo 1972), however, Ashton (pers. comm. vii.2012) noted that only ca 13 species of dipterocarps were major dominants. Ca 20 species of Ericaceae are widespread in boreal forest and tundra habitats, although a number of species of Vaccinium can be very abundant locally in montane forests in Malesia and Rhododendron species can dominate locally in the Himalayas-Yunnan region. Five of the seven genera that are important elements of tundra biomass are ECM plants: Salix, Betula, Dryas, Vaccinium and Empetrum; two Cyperaceae (Eriophorum, Carex) are the others (Chapin & Körner 1995).

Many vegetation types dominated by one or a few ECM species also include other ECM/ERM plants. Thus in the Mediterranean Maquis, ECM Cistaceae, Fagaceae and Pinaceae are all important components of the vegetation. There are extensive oak-pine ECM forests in the eastern United States, Mexico, and the Mediterranean, while forests with ECM Fabaceae, Dipterocarpaceae and Phyllanthaceae are common in tropical Africa. Boreal forests are dominated by ECM Pinaceae with some ECM Betulaceae and Salicaceae, but the understory often includes several ERM Ericaceae (Read 1993). In western North America the oak-pine forests include a substantial element of Arbutus menziesii (Waddell & Barrett 2005), an ericaceous tree with arbutoid mycorrhizae.

However, ECM plants do not simply dominate communities, many are large individuals, each representing a substantial amount of standing biomass, and, very importantly, large amounts of carbon in standing plants, the soil and litter commonly accumulates in ECM-dominated communities (see also above). Thus peat deposition is often associated with ECM/ERM plants, indeed, Buffam et al. (2014) emphasized the importance of both peat-containing wetlands and lakes in long-term carbon storage in rather mixed Wisconsin-Michigan forests of the Northern Highlands Lake District; at 33% of the area, they represented over 80% of the fixed carbon storage, so being major players in long-term carbon sequestration there. For summaries of global peat deposition, see Yu et al. (2010) and Page et al. (2011).

ECM and their seed-plant associates together form soil conditions that both prefer (see also Read 1993). Thus enzymes, etc., produced by the ERM plant/fungus association contribute to the formation of acidic mor humus that ERM plant like and VAM plants do not (Read 1991). In Rhododendron, at least, stable protein-tannin complexes formed by the plant are more easily accessed by its own fungus associates than by fungi from plants with other kinds of mycorrhizal associations (Wurzburger & Hendrick 2009). Nitrogen mobilization is also affected by the polyphenols in the litter (e.g. Northup et al. 1995). Although Näsholm et al. (2013) interpret ECM fungal activities in conifer forests somewhat differently, with nitrogen in some circumstances being retained in fungal mycelium, the consequences are similar; non-ECM plants will be at a disadvantage in the nitrogen-poor conditions that result. Similarly, Newbery et al. (1997) found that in some forests on poor soil in Cameroon the phosphorus in soil and litter was preferentially accessed by the dominants, ECM Dialeae (= Fabaceae-Detarieae), again, ECM plants effectively making the kind of soil to suit themselves.

Leaves of ECM plants may decompose more slowly than those of other seed plants, irrespective of whether they are deciduous or evergreen (Pérez-Harguindeguy et al. 2000; Cornelissen et al. 2001; Cornwell et al. 2008; Lang et al. 2011), although this story may have to be revised (see Koele et al. 2012). ERM Ericaceae are also noted for producing nitrogen-poor litter that is slow to decompose (e.g. Read 1991); litter from ERM plants may be the most recalcitrant (Read 1991; Cornelissen et al. 2001; Alexander & Lee 2005). Litter accumulation is also notable in tropical ECM communities (Torti et al. 2001). The leaves are well defended, often long-lived, and the plants are efficient at removing N and P from them when they die, and the result is persistent, nutrient-poor humus unsuitable for often faster-growing VAM plants; in addition, ECM and ERM plants can utilize N as complex organic compounds (Cornelissen et al. 2001: see also above). Low rates of litter decay (often accompanied by high MA - leaf mass per area - values) are particular features of both gymnosperms and angiosperms that are able to grow in stressful, nutrient-poor environments (Berendse & Scheffer 2009). The result is acid conditions and persistent litter with a high C:N ratio; this will tend to constrain mineralization, as will the seasonal/cold climates that many ECM plants favour (Read 1991). However, while Averill et al. (2014) noted that there was about 70% more carbon per unit nitrogen in soils of ecosystems dominated by ECM plants, the nitrogen remaining accessible to the fungi, but not to their microbial competitors, they also thought that litter with a higher C:N ratio would lead to less C storage in the soil because microbes would respire relatively more C in their total growth activities.

Dipterocarps largely dominate Southeast Asian tropical peatlands (most are Malesian, and in particular Bornean). It has been estimated that Dipterocarpaceae occupy about 56% of the total tropical peatland area, close to 250,000 km2, and about 6.2% of the global peatland area (Page et al. 2011, 2012). This peat contains about 68.5 Gt carbon, a figure that is some 77% of the tropical and 11-19% of the global totals for peatlands; these figures do not include estimates of above-ground biomass (Page et al. 2011). These figures are over twice the total carbon storage in all other forests in Malaysia and Indonesia (Brown et al. 1993; Page et al. 2012), which include a substantial component of other ECM trees. Carbon in waters draining from disturbed dipterocarp peat swamps may be as much as ca 4,180 years old (Moore et al. 2013), indicating that carbon storage there can be quite long term, and the beginning of the formation of some peat deposits has been dated to the late Pleistocene 40,000 y.a., and the peat may be 25 m deep (Page et al. 2004, 2012). Amazonian peatlands, which sequester perhaps 9.7 Gt carbon, are poorly known, but on a per area basis their carbon accumulation is only a little over half that in Malesia; unfortunately, the mycorrhizal status of the plants in these peatlands seems to be unknown (Lähteenoja 2011; Lähteenoja et al. 2011). Note that these figures are very approximate: other estimates are 84 Gt C in tropical peat, 16 Gt C in southern peats, and as much as 621 Gt C in northern peats (Rydin & Jeglum 2013 and references; see also Immirizi & Maltby 1992; Rieley et al. 1997 for other estimates, including pre-human peatland areas).

Dipterocarpaceae in Malesia are also abundant away from peatlands, and again, the soil is often rather humus-rich, as in Lambir forest, Sarawak. There dipterocarps make up only 7.4% of the species but 41.6% of the basal area (918.41 m2); the figures for Shorea alone are 4.7%, 21%, and 467.8 m2, Dryobalanops aromatica and Dipterocarpus globosus between them accounted for 13.2% of the basal area, and seven dipterocarps (out of the ten most dominant species) accounted for 23.1% (Davies et al. 2005). Dipterocarps are also important elements in drier and more open woodlands. Shorea robusta (sal) is a gregarious tree that grows in monsoon areas from Pakistan to China, especially in the India-Assam-Myanmar area. Sal forests occupy 115,000 to 120,000 km2 (11.5x106 ha) and make up ca 15% of Indian forests (Tewari 1995). In Africa Monotes is a significant component of the rather dry forests and woodland otherwise dominated by Fabaceae-Detarieae (see below).

Malesian dipterocarp forests are noted for their high diversity on a global scale (e.g. Lee et al. 2002). They also have high above-ground wood productivity, even when compared with generally similar west Amazonian forests (Banin et al. 2014). From these points of view, dipterocarp forests represent an extreme in the ecological spectrum represented by ECM plants.

Fabaceae are not generally thought of as being ECM plants, but a number of species, especially Old World Detarieae, are mycorrhizal (e.g. Read 1991; Onguene & Kuyper 2001). Species in some 36 of the ca 82 genera included in Detarieae are reported to be at least locally dominant (e.g. Letouzey 1968; Mackinder 2005), and 11 of these dominants are in a rather small clade (Macrolobieae/the Berlinia clade) with 16 genera, of which 10 are known to be ECM (see also Wieringa & Gervais 2003). A few species of these Fabaceae-Detarieae dominate ca 3.27-3.75x106 km2 of Miombo forests in the Zambezian region (estimates from White 1983; see also Newbery et al. 2006). The ECM detarioid Isoberlinia is a major component of Sudanian Woodland (White 1983) which forms an interrupted band south of the Sahara from Mali to Uganda (White 1983; upper band of blue in the map above). This forest is biogeographically closest to Miombo woodlands among other African vegetation (Linder et al. 2012). Some Detarieae like Cynometra are endomycorrhizal (VAM) (but this can also be a dominant tree: Eggeling 1947; Makan et al. 2011), while a few other Fabaceae, both ECM and VAM (e.g. Mora), may also dominate locally (see also Peh et al. 2011).

In Miombo forests Detarieae represent 20-90% of the trees, 30-96% of the basal area, and with biomass estimates in the range of 35-97 Mg ha-1 (Högberg & Piearce 1986; Frost 1996). Figures for the carbon dynamics of tropical savannas and grasslands together in Carvalhais et al. (2014: Tables S1 + S2) are around 328 Pg total C, a carbon density of ca 17.7 kgC m-2, and a mean turnover time of (12.2-)16(-22.1) years.

Detarieae are ecologically important elsewhere in Africa. Gilbertiodendron dominates large areas of the eastern Congo Ituri rainforest (Torti et al. 2001; Makana et al. 2011). Microberlinia dominates Guineo-Congolian forests in Cameroon, and other Detarieae dominate parts of the forest that grows somewhat inland from the coast from Sierra Leone to western Gabon, and again in the periphery of the Zaire basin (White 1983). Indeed, a caesalpinioid Biafran forest subtype has been recognised that includes this sub-coastal forest, and of the 34 important genera recorded from it, 28 are Detarieae, and 11 of these are described as being characteristically gregarious (Letouzey 1968). Other ECM plants in the woodlands and savannas of Africa and Madagascar include Monotes (Dipterocarpaceae), Uapaca (Phyllanthaceae), Asteropeiaceae and Sarcolaeanaceae (Tedersoo et al. 2011 and references)

In the New World, the Aldina (Faboideae) and the coppicing Dicymbe (Detarieae), both ECM plants, dominate forests in the Pakaraima Mountains in the central Guiana Shield region (McGuire 2007b; M. E. Smith et al. 2011). The latter in particular has a remarkably high basal area of 38.4-52.5 m2 per hectare, around 25(-40) m2 being more normal figures (Henkel 2003). Peltogyne (Detarieae: ?mycorrhizal status) is one of the rare monodominants of the Amazon, where it occupies ca 53% of the basal area of trees 10 cm or more in d.b.h. on Maraca Island, Roraima, a figure that increases in proportion in larger trees (Nascimento et al. 1997).

The Amazonian rainforest is not noted for monodominance, and none of the 42 common Amazonian species mentioned by Pitman et al. (2001) is known to be an ECM plant. However, of the 20 most abundant Amazonian trees, plants 10 cm d.b.h. or more, recently listed by ter Steege et al. (2013) as being "hyperdominants", the ECM Eperua falcata (see Peh et al. 2011), along with E. leucantha (mycorrhizae?), Fabaceae-Detarieae, are notable as being 50% more abundant (usually far more) than any other non-palm on the list. However, how this hyperdominance might convert to the modified (clade, as well as single species) more classical idea of monodominance is unclear, and biomass figures for Eperua forests are not known.

Fagaceae, Nothofagaceae, and many other Fagales are common in forests of temperate areas in eastern and western Eurasia and North America, in southern temperate regions, and on hills and mountains in Central America and Malesia. They often grow in association with ECM Pinaceae, as in eastern north America (e.g. Abrams 1996).

Fagaceae frequently dominate north temperate vegetation. White oak (Quercus alba) alone represents (12-)19-26(-49)% of witness trees, i.e. trees that were probably present before Europeans arrived, in the oak-dominated forests of eastern North America (81% in some southern Illinois forests). White oak, which grows with up to three more ectomycorrhizal species, two of which are usually other Fagaceae, makes up anything from (36-)50-80(-± 100)% of all trees (Abrams 2003). Six of the 30 species of Quercus growing in those forests are notable dominants (Abrams 1996). Fagaceae, again mostly Quercus, are abundant in western North America, and in California the black oak, Quercus kelloggii, is particularly widespread and has the greatest timber volume of any oak (Waddell & Barrett 2005). Oak trunks may get buried in sediment in flood plains, and the mean age of carbon storage in such conditions is ca 1,960 years, individual trunks being up to 14,000 years old (Guyette et al. 2008); along the same lines, in mixed ECM temperate forests where the half-life of conifer wood was about 20 years, buried wood persisted for up to 1,400 years (Hyatt & Namian 2001).

The ECM American chestnut, Castanea dentata, was previously the dominant large tree in some 800,000 km2 of forest in eastern North America, but it now persists largely as suckers after its devastation by chestnut blight in the first half of last century (Thompson 2012: see below). It has since been replaced by mixed oak or oak-hickory forests (Abrams 1996; see e.g. van der Gevel et al. 2012 for the future), so the forests remain dominated by ectomycorrhizal trees.

Pinaceae are the major component of boreal/subarctic forests. Estimates of the area occupied by these forests range from 12 x 106 km2, or ca 17% of the land surface of the earth (Moore 1996; Lindahl et al. 2002), to 9.2 x 106 km2, a figure that is 73% of the conifer forests of the world (Kuusela 1992). However, () suggested that the core area of boreal forests in Eurasia alone was 12x106 km2, so the global total may be as much as 17.1 x 106 km2 (see also Melillo et al. 1993: estimates for boreal woodland + forest are 18.5 x 106 km2). ECM Pinaceae, along with some Salicaceae and Betulaceae, also ECM, make up the bulk of these forests, while ERM Ericaceae are often common in the understory (e.g. Villareal et al. 2004; Vrålstad et al. 2002; Vrålstad 2004; Kranabetter & MacKenzie 2010).

Botkin and Simpson (1990) estimated above-ground biomass and carbon for boreal forests in North America to be 4.2±1.0 kg/m2 and 1.9±0.4 kg/m2 respectively which, when extrapolated to a total forest area of 5,172,427 km2 gave biomass and carbon figures of 22.5±5x1015 g and 9.7±2x1015 g respectively. Moore (1996) estimated living above-ground biomass ("phytomass") in North American boreal forests as 12 x 1015 g, to which could be added 76 x 1015 g in soils (including dead and fallen trees) and 135 x 1015 g in peatlands. Extrapolating to a total area of 10.6 x 106 km2 (the average of the first two figures in the preceding paragraph), this would then give a figure of some 420 x 1015 g of carbon in soils and peatland combined. Carbon burial figures are estimated at 49.3 Tg C y-1 (Chmura et al. 2011: area 13.7 x 106 km2), while soil C storage estimates in Averill et al. (2014) are (49.7-)61.4(-73.1) kg C m-2, NPP figures in the latter being (292-)319(-346) kg C m-2 yr-1. Estimates of the current carbon pool for forests in Russia, Canada, and Alaska, roughly boreal forest, are 88x1015 g (vegetation) plus 471 x 1015 g (soils), the area under forest cover being 13.7 x 106 km2 (Dixon et al. 1994). Figures for the carbon in boreal forests in Carvalhais et al. (2014: tables S1 and S2) are some 505 PgC, ca 34.2 kgC m-2, and a mean turnover time of (45.4-)53.3(-73.4) years. Clemmensen et al. (2013), working on Swedish conifer forests, emphasized that in older, less disturbed forests much carbon came from roots and in particular from their fungal associates, and the latter also contributed substantially to total respiration, which affects rock weathering (see also Högberg et al. 2010; Tedersoo et al. 2012, also below).

Ericaceae are important components of the extensive tundra vegetation which occupies some 8% of the global land surface (Read 1991; Chapin & Körner 1995; Gardes & Dahlberg 1996; Camill et al. 2001; Kranabetter & MacKenzie 2010), or around 9.7 x 106 km2 (Melillo et al. 1993: alpine tundra included). Such habitats are dominated by ericoid plants, nearly all Ericaceae, but one species of Diapensiaceae (e.g. Bliss 1979; Sistla et al. 2013; Timling & Taylor 2012 for mycorrhizal diversity), indeed, Read (1993) characterized the tundra by its ericoid mycorrhizae. The mycorrhizal status of Diapensiaceae needs clarification, and although belonging to Ericales, the family is not immediately related to Ericaceae; only a single species, Diapensia lapponica, with a circumpolar distribution (see Diapensiaceae), is involved. All other ericoid plants in these habitats are Ericaceae, Vaccinium and Empetrum in particular being two of the seven prominent biomass accumulators there (Chapin & Körner 1995; Kranabetter & MacKenzie 2010); most others are ECM plants.

Ericoid plants represent 30-87% of the above-ground biomass and 40-83% of the net annual above ground primary productivity in tundra (figures from Bliss 1979), and ECM and ERM plants together made up more than 95% of the vascular plant biomass in some heath tundra sites (Michelsen et al. 1998; see also Sistla et al. (2013: 6/10 species listed in Table 2). Peat is formed both by heathland vegetation and in the boreal forests. Estimates in MacDonald et al. (2006) are that northern peatlands stored 188-455 Pg carbon, while Yu et al. (2010) thought that 547 gigatons of carbon were stored there, with an additional 15 gt in Patagonian peatlands.


In this context, another area on which to focus is the permafrost region. The northern polar permafrost encompasses the tundra region and also much of the boreal conifer forest above 60o N if areas of patchy permafrost are included, although permafrost is widespread only above 70o N in western Asia and even further north in much of Europe. The map here is based on that by Brown et al. (1997, q.v. for detail; c.f. Tarnocai et al. 2009); areas with some, but less than 50%, permafrost are extensive, but are not included. Tarnocai et al. (2009) estimated permafrost to occupy about 18 x 106 km2, about 16% of the global soil area. Figures for the tundra in Carvalhais et al. (2014: tables S1 and S2) are about 158 PgC, a carbon density of 20.2 kgC m-2, and a mean turnover time of (44.7-)65.2(-78) years, although above 75o N the mean turnover time is ca 255 years.

The total amount of organic carbon in the permafrost area, which includes extensive bogs dominated by Sphagnum and Cyperaceae (e.g. Gorham 1991; Camill et al. 2001) and deltaic deposits, is estimated to be 1672 Pg, about 50% of the global below-ground organic carbon pool, and of this, 88% is in permanently frozen soils (Tarnocai et al. 2009: estimates of carbon in peatlands are broken out separately). Much of this carbon is stored below 200 cm (Tarnocai et al. 2009). Ping et al. (2008) estimated that around 98.2Gt of carbon was stored in the 3.04 x 106 km2 of the treeless North American Arctic alone. This figure is about twice as high as in previous estimates, in part because Ping et al. (2008) emphasized the importance of sampling to 1 m deep and so including carbon stores that had been buried by cryoturbation. Extrapolating to the 5.05 x 106 km2 of the Arctic as a whole (see Walker 2005), around 172 Gt carbon may be stored there.

Mosses are very important components of the tundra and boreal forests. A few species of feather mosses, pleurocarpous Hypnales, form close associations with Nostoc, nitrogen moving from the latter into the former (Bay et al. 2013), although further movement in the ecosystem is unclear (Rousk et al. 2013; Lindo et al. 2013). Mosses represent a substantial proportion of the biomass (Gorham 1991; Chapin & Körner 1995). Spagnum, particularly in more boggy areas, is the main moss, and it decomposes more slowly than other bryophytes and vascular plants in these communities (Verhoeven & Liefveld 1997: secondary metabolites; Lang et al. 2009; Lindo et al. 2013; Sistla et al. 2013; Rydin & Jeglum 2013); it is also associated with numerous bacteria which affect its own functioning and that of the ecosystem to which it belongs (Bragina et al. 2104).

The ecological role of Cyperaceae is poorly understood (Barrett 2013). Members of the family are often particularly common in wet tundra habitats in the Arctic (ca 8% of the land surface), and include Eriophorum and Carex, two of the seven major contributors to the biomass there (Chapin & Körner 1995), the other five genera being ECM or ERM core eudicots, and Carex itself is the biggest genus in the Arctic (Elven et al. 2011. Roots of cyperaceous plants may penetrate into the mineral soil below the shallow layer of soil dominated by roots of ECM plants (Read 1993). Cyperaceae-dominated communities were notably extensive during the last glacial maximum north of 550 N (Bigelow et al. 2003). Even today about 13% of all species growing in Quebec and Labrador north of 54o N belong to Carex, and 16% are Cyperaceae (Poaceae are next at 11%), and they can be major components of plant cover there, especially in wetter habitats (Cayouette 2008; Escudero et al. 2012).

Habitats in alpine and other extreme conditions may be dominated by Cyperaceae. Thus there are some 450,000 km2 between 3,000 and 5960 m altitude on the Tibetan plateau dominated by the ECM Kobresia pygmaea (Miehe et al. 2008, see also Zhou 2001). ECM species of Kobresia are widespread and sometimes dominant in alpine, Arctic and tundra habitats (e.g. Gardes & Dahlberg 1996; Muhlmann & Peintner 2008; Newsham et al. 2009; Gao & Yang 2010). Polygonum (Bistorta) viviparum is another perennial herbaceous ECM plant of the tundra, growing both as a pioneer and as a prominent component of established vegatation (e.g. Gardes & Dahlberg 1996; Michelsen et al. 1998; Brevik et al. 2010).

There is a final aspect of ECM activities which affects global carbon balances that has not yet been mentioned. In ECM roots the fungus forms the interface between the plant and the soil, rather than the root epidermis with its root hairs as in non-ECM plants (e.g. L. L. Taylor et al. 2009). ECM fungi have been called "rock-eating fungi" (Jongmans et al. 1997), highlighting the fact that ECM fungi in particular - VAM fungi less so, although they, too, are active - facilitate subsurface weathering of rocks, especially when basaltic, so sequestering additional CO2 in the process (e.g. Landeweert et al. 2001; van Schöll et al. 2008: Al moves from the rock to the humus layer?; Taylor et al. 2009, 2011, 2012; Comas et al. 2012; Quirk et al. 2012). Chelating agents and oxalic acid and other low molecular weight organic acids are secreted by the fungi, facilitating this weathering; overall, the amount of weathering can be linked to carbon fixation in photosynthesis and how much is allocated both directly to the roots and indirectly to the fungus (Taylor et al. 2009). Indeed, it has been suggested that the evolution of the ECM habit "represents the most profound alteration in root functioning to occur in plant history..." (Taylor et al. 2011: p. 369; c.f. in part Boyce & Lee 2011). Many eudicot angiosperms, but not magnoliids, have narrow roots compared with those of other vascular plants, allowing more efficient scavenging in the high latitude/nutrient poor soils where ECM plants are so prominent (Comas et al. 2102), although there seem to be no comparisons specifically between ECM and VAM plants; here ericoid roots, at as little as 40µm across, represent an extreme. However, ECM increase Ca and Mg fluxes caused by weathering particularly in communities with lower NPP and that are weathering silcate rocks; these fluxes are highest when NPP is high and forests are growing on basaltic rocks, i.e. which would include much l.t.r.f. (Taylor et al. 2012).

Seagrasses, Mangroves, and Tidal Saltmarshes.

The following three communities, sea-grasses, mangroves and tidal salt marshes, all have carbon burial rates well over 100 g C M2 y-1, which is considerably more than twenty times that in tropical, boreal or temperate forests (usually substantially less than 10 g C M2 y-1: Mcleod et al. 2011; Chmura 2011). All three systems are accretionary, in that they also capture much sediment in which the carbon they produce, but also allochthonous carbon, is stored; sediments can reach 10 m or more thick (Chapman 1974; McKee et al. 2007; Mcleod et al. 2011; Chmura 2011; Fourqueran et al. 2012). Storage may be for thousands of years, well over ten times as long as that in tropical rain forest, for example (Chambers et al. 2001; Mcleod et al. 2011).


The gross primary productivity of sea-grasses has been estimated at 1903 g C m2y-1, rather like that of mangroves, their global primary productivity is 628 Tg C y-1, while their net ecosystem production (1211 g C m2 y-1 and globally 400 Tg C y-1) is substantially higher than that of mangroves because of their relatively low respiration rates. Sea-grasses are responsible for about 1.13% of all marine primary productivity, yet they bury as much as an estimated 27-44 Tg C y-1, some 12% of the total C storage in the marine ecosystem (Duarte et al. 2005: area 30x106 ha; Duarte 2011), although they occupy less than 0.2% of the area of the oceans. Indeed, this burial estimate may be only half the actual amount (Fourqueran et al. 2012). Although the ammout of carbon in the sea-grass plant itself is small, that stored in the soil, which can form mats up to 11 m thick in the Mediterranean, is very great (Fourqueran et al. 2012), larger than that of most forests and comparable with mangrove storage. 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: highest areal estimate below).

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 60 x 106 ha (); although the last is an old estimate, it is relevant here where the emphasis is on conditions immediately before human activities became transformative. A substantial amount of sea-grass carbon moves into other marine ecosystems, including the deep sea (Suchanek et al. 1985). Not surprisingly, estimates in Mcleod et al. (2011) vary - they 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. Other 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; see Charpy-Roubaud & Soumia 1990 for estimates of benthic algal productivity). This carbon may be sequestered for 4,000 years or more in the anoxic soils of sea-grass beds (Orem et al. 1999; Serrano et al. 2011, 2013).

To summarize. 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, both autochthonous and allochthonous (Orth et al. 2006; Kennedy et al. 2010 for summaries). Sea-grasses often form monodominant stands, individual clones of some species being very long-lived.


Mangroves can be divided into two groups, the much more speciose eastern group, from east Africa to the western Pacific, which includes ca 40 species, ca 14 of which are Rhizophoraceae, and the western group, from west Africa to the Americas, with only eight species, three of which are Rhizophoraceae (for their evolution, see Ricklefs et al. 2006). Plaziat et al. (2001) suggested that the separation of the two groups occurred ca 20 m.y.a.. Depending on how species limits are drawn, no dominant mangrove species is common in both areas (Tomlinson 1986).

The mangrove ecosystem is very productive and also has high carbon flux rates. Mangroves occupy 13.7-15.2 million hectares, and they store 4-20 PgC globally (Bouillon et al. 2008; Donato et al. 2011 and references; 16.7 m ha in Valiela et al. 2001), although towards the beginning of the last century there may have been 22.0-25.5x106 hectares (figures estimated from Valiela et al 2001, correction of current figures by changes in those multiyear records that exist, also with the lower current estimate of Spalding et al. 2010). Other estimates are that they bury 17.0-23.6 Tg C y-1, their gross primary productivity is 2087 gCm2y-1, global primary productivity is 417 Tg C y-1, but with a rather lower net ecosystem production (221 g C m2 y-1 and globally 44 Tg C y-1) because of a relatively high respiration rate, at least when compared with the sea grass community (Duarte et al. 2005: area 0.2 x 1012 m2). Spalding et al. (2010) estimated net primary productivity to be 140-168 tg y-1, of which 10(-30)% was incorporated into sediments, which makes up 15% of the organic carbon accumulating in marine sediments globally. 10% of refractory organic carbon in marine sediments may come from mangroves, which equals the amount of carbon in atmospheric CO2 (Spalding et al. 2010). Estimates in Mcleod et al. (2011) are a carbon burial rate of (187-)226(-265) g C m-2 y-1 (range 20-949), total carbon burial of 25.7-40.3 Tg C y-1), area 13.8-15.2x106 ha).

Their overall floristic composition is sometimes not that dissimilar to that of inland salt vegetation; indeed, some European inland salt vegetation may have connections with vegetation that bordered the Tethys Sea (Chapman 1974; see also above). C4 and some C3 Poaceae (Flowers & Colmer 2008; Bennett et al. 2013) and chenopod Amaranthaceae, also often C4 plants, are notably common in salt marshes and inland salt vegetation, but Plumbaginaceae, Caryophyllaceae, Aizoaceae, Frankeniaceae, Nyctaginaceae, Tamaricacaceae (all Caryophyllales), Cyperaceae and Juncaceae, also Restionaceae (all Poales), Juncaginaceae (Alismatales), as well as Primulaceae and some Asteraceae (sometimes prominent in degraded saltmarshes) may also be appreciable elements of the vegetation (Chmura 2011; esp. Chapman 1974). All told there are some 350 species of halophytes (Flowers et al. 2010).

For the reasons just mentioned, estuarine productivity is difficult to estimate. Like vegetation dominated by sea-grasses, salt marshes actively trap sediments (Marani et al. 2013 and references). Estimates of carbon burial in salt marshes are given by Mcleod et al. (2011), which, they estimate, occupy 2.2-40x106 ha: the rate of burial is (194-)218(-242) g C m-2 y-1 (range 18-1713) and total carbon burial is 4.3-96.8 Tg C y-1. Duarte et al. (2005) estimated that salt marshes occupied ca 40x106 ha with a gross primary productivity of some 3595 gCm2y-1 and global primary productivity of 1438 Tg C y-1, while their net ecosystem production was 1585 g C m2y-1 and globally 634 Tg C y-1, substantially higher than either mangrove or seagrasses. They estimated C burial to be 60.4-70.0 Tg C y-1.


In the more ecophysiological interactions under discussion, one or a few clades largely dominate important aspects of community/ecosystem functioning; relatively few groups of ECM plants occupy perhaps 50% of the earth's forested areas (L. L. Taylor et al. 2011). Although there are suggestions that the total standing biomass of the trees in forests is invariant with respect to species number and composition or latitude (Enquist & Niklas 2001; Enquist et al. 2007; but c.f. e.g. Dixon et al. 1994), above- and below-ground biomass, nutrient cycling and productivity all vary considerably. The ecosystem functions emphasized here are carbon sequestration and to a lesser extent primary productivity, but the two are of course not necessarily linked (Lähteenoja 2011). In general, carbon estimates are of above-ground biomass, or that in soils and peats, and in peats in particular below ground C can represent over half the total forest carbon pool (Dixon et al. 1994), with sequestration times being relatively long term. On the other hand, in many speciose tropical lowland rainforests productivity is high, standing carbon biomass is high, but below ground biomass is relatively low, carbon sequestration times are short, and biomass turnover is relatively fast (e.g. Dixon et al. 1994).

There are several immediate issues that arise when thinking of the importance of particular vegetation types for carbon sequestration. One is that the definitions of these vegetation types are imprecise. Thus the area of grassland mentioned above depends on how "grassland" is defined, similarly, there is no consensus over the definition of vegetation types in the forest/savanna transition (Torello-Raventos et al. 2013). Although I have separated mangrove- and sea grass-dominated communities, members of both are halophytes, that is, plants tolerating at least 200mM salt, and both intergrade with both estuarine and inland halophytic vegetation, the former including abundant Poales, especially Poaceae, the latter often dominated by Caryophyllales; in both these other vegetation types C4 plants are common (Flowers et al. 2010).

The second is that estimates of the amount of above- and below-ground carbon and similar measures for current ecosystems are estimates for ecosystems that have often been more or less profoundly modified by the activities of humans. The areas occupied by different vegetation types have changed greatly over the last 10,000 years, hence, in part, the differences in some of the areas estimated (Dixon et al. 1994). Longleaf pine savanna has decreased from ca 90 million to less than 2 million acres, and the area occupied by mangroves has also decreased greatly because of cutting (e.g. Spalding et al. 2010). Salt marshes, however, may have increased in extent because of land clearance and the resultant increase in sediment in rivers that facilitated the development of salt marshes in their estuaries (e.g. Kirwan et al. 2011; Chmura 2011), and agricultural nutrients in runoff have also affected subaquatic estuarine vegetation (e.g. Brush & Hilgartner 2000). Stands of thermophilous Abies alba in the Mediterranean have disappeared because of human activities (Tinner et al. 2013). Even in "primary" forests, human activities also have an impact on biomass estimates. Thus there was ca 1/3 loss in biomass in primary - but obviously not untouched - forests in Peninsula Malaysia over a single decade late last century (Kerridge et al. 1987; Dixon et al. 1994 and references), and the actual above-ground carbon in forest throughout the whole Indo-East Malesian area is very substantially below its potential value because of human activities (Brown et al. 1993). However, depending on the nature and intensity of human activities, not all ECM plants will be negatively affected. Oak has increased in eastern North America since Europeans arrived there (Abrams 1996), while the widespread ECM Kobresia pygmaea-dominated community of Tibet may be of quite recent origin, grazing pressure facilitating its current wide extent which it has reached since the spread of the Tibetan empire in the seventh century CE (Miehe et al. 2008, see also Zhou 2001).

The focus here is as far as possible on pre-agricultural vegetation, although one could well argue that as soon as humans started using fire, they began to cause major vegetational changes. Indeed, the Late Quaternary megafaunal extinctions, whether caused by human hunting or climate change or some combination of the two (Lorenzen et al. 2013), have had substantial effects on community composition and biome limits (Gill 2013).

The third is that the situation gets far more difficult as one thinks about vegetation types earlier in the Holocene and in the Tertiary. How have the ecosystems with these small groups of species with a disproportionately great influence on current global ecology behaved over time? Grasslands, mangrove vegetation, and the like, are not fixed and invariant elements of the biosphere; their extents, and the roles that individual species play in them, can change over even quite a short period, and as we think about the longer term, change is ubiquitous.

In the short term, i.e. over the last few hundred years, some of the human activities just mentioned may have had little effect on mycorrhizal activity, at least, and there may be ecological complementarity and stasis if such ecosystems include members of different clades of ECM plants (c.f. Cadotte et al. 2012); perhaps Salicaceae, Betulaceae and Pinaceae, all ECM plants, interact in this way in Boreal forests. The ecological death of the dominant Castanea dentata, an ECM plant, in the eastern U.S.A. seems to have had little overall effect on the ecosystems there, chestnut being replaced by ECM oak-hickory forests (Abrams 1996). Although the species of trees growing in eastern deciduous forests in the eastern North America have changed considerably - and continue to change - in response to logging pressure, changing fire regimes, etc., since the advent of Europeans, the dominant species have remained ECM plants, even if their relative abundance has changed (Abrams 1996, 2003). However, with the suppression of fires in the last three hundred years or so replacement of oak-pine forests by largely non-ECM species does seem to be under way (Abrams 1996, 2003). The extent to which the ECM-dominated Mediterrananean Maquis vegetation reflects human activity is unclear, but again, the major components of the different successional stages are all ECM plants (Comandini et al. 2006).

As mentioned above, the floristic composition of vegetation became much more "modern" in the latter part of the Tertiary, and in North America forest composition may be little changed over the last 15 million years or so (Graham 1999; Hawkins et al. 2014). However, although biomes may seem to be fairly stable over the medium term, this is partly the result of how they are delimited, and individual species and their abundance may vary substantially within the one biome (Williams et al. 2004); communities have certainly not been stable over this period.

Indeed, since the beginning of the Pleistocene ca 2.6 m.y.a., there have been great changes in community composition and location; many plant communities are quite novel and recent, even evanescent phenomena. Mapping of post-glaciation forest changes in North America shows that some species have been fairly constant in abundance, if not in location, but they are mixed with other species that as it were appear from nowhere and come to be abundant over wide areas (e.g. Webb 1988; Williams et al. 2004; see also Jahn 1991). The various forest communities currently found in North America are largely Holocene phenomena, communities coming and going even in recent times (Curtis 1959; Williams et al. 2004 and references), and the same is true elsewhere in the world (Torres et al. 2013). Williams and Jackson (2007; see also Donoghue & Edwards 2014) discuss these "no-analog communities", communities with species combinations unlike those of any current communities, in the context of species that are assumed to have the same fundamental niches as those of their living descendents, but of course their realised niches may also differ, further complicating attempts to understand how past vegetation functionaed.

Prior to 3.3 m.y.a., boreal forests with ECM taxa like pine, spruce, larch and birch grew in the east Siberian-North American-Greenland area from 60-80o N, although especially since 2.7 m.y.a. the conifers, etc., have been replaced by tundra (Brigham-Grette et al. 2013). The association of Picea, Betula and Alnus, characteristic of Recent boreal forest, was first recorded in North America a mere 7,000 years ago (Williams et al. 2004). Boreal peatlands are post-Pleistocene in age (MacDonald et al. 2006), even if some tropical peatlands are somewhat older (Page et al. 2004). The composition of tundra vegetation has changed considerably from glacial to interglacial periods, and more carbon accumulated in the latter (Brubaker et al. 1995). As permafrost thaws, peat accumulation, especially by Sphagnum, but also by spruce, etc., may increase along with above-ground primary productivity (Camill et al. 2001). Changes were complex (Lindo et al. 2013), and mosses were in places replaced by angiosperms with their rather more labile leaf litter, plant biomass showing an overall increase (Sistla et al. 2013). The changing relative proportions of forbs and graminoids in Arctic tundra and steppe over the last 50,000 years are detailed in Willerslev et al. (2014).

Stepping back a little further in time, differences become dramatic. The grassland and savanna biomes that are now such a prominent feature of global vegetation can be dated to the Pliocene, within the last 10 m.y. or so, and especially within the last 3 m.y., even if the grass clades now growing there had begun to evolve considerably earlier in the Tertiary (e.g. R. Sage et al. 2012; Pennington et al. 2006b; Simon et al. 2009; Simon & Pennington 2012). Diversification of Sphagnum, now such a prominent component of boreal forest and tundra vegetation, is dated to about the middle of the Miocene (Shaw et al. 2010a; Shaw & Devos 2014). Although the discovery of Sphagnum-like fossils in Ordovician rocks 455-460 m.y.o. suggests that peatlands have been around for a rather long time (Graham et al. 2013), evidence for this is wanting. Betula, now conspicuous in northern forests, has probably diversified within the last 10 m.y. (Xing et al. 2014).

Associations of species unlike any extant are found in western North America during the warmest part of the Miocene 17-15 m.y.a. (Millar 2011). Furthermore, in the Mesozoic and early Tertiary latitudinal diversity curves were almost flat or even peaking in more temperate areas, and it seems that current curves, with diversity peaking near the Equator, are more a phenomenon of a post-Eocene globe with more extreme and seasonal N-S temperature gradients (e.g. Wolfe 1987; Mannion et al. 2012, 2013; Archibald et al. 2012). In the Palaeocene and Eocene in particular plants that today have different climatic preferences tended to grow together, but as temperatures dropped, particularly in the Oligocene, vegetation with more local facies developed. Tall trees (80+ m tall: Tng et al. 2012 for records) today tend to grow in thermally equable climates, so it would be interesting to know the distribution of such trees in the early Tertiary (Larjavaara 2013); a single tall tree can sequester a considerable amount of carbon. Even today, estimates of both living carbon biomass and dead and below-ground biomass are highest for some temperate and warm temperate forests, as well as mangroves and peat swamps, not l.t.r.f. (Keith et al. 2009; Pan et al. 2013: living biomass; c.f. in part Carvelhais et al. 2014). Interestingly, the proportion of wind-pollinated trees and shrubs are higher in humid areas away from the tropics (Regal 1982; Ollerton et al. 2011); temperate wind-pollinated trees and shrubs tend to be ECM plants, as in about half the examples mentioned by Regal (1982).

ECM Pinus seems to have been a mid-latitude (30-50o N) plant in the Cretaceous, but in the warm Palaeocene and Eocene it retreated to higher latitudes, although also persisting near the equator. In high latitude Eocene floras Pinaceae could be quite common, and with other ECM plants they made up about 2/5ths of the species on Canadian islands 75-80o N. (McIver & Basinger 1999). With the climatic deterioration of the Late Eocene-Oligocene, it moved back to mid latitudes while persisting at higher latitudes (Miller 1993). In the Oligocene Pinus moved into western Malesia (e.g. Muller 1972). In the late Eocene mixed deciduous broad-leaved and evergreen and deciduous conifer forests grew within both the Arctic and Antarctic circles (e.g. Collinson 1990; Jahren 2007; Harrington et al. 2011; Collinson et al. 2012; Pross et al. 2012), and a unique biome in which angiosperm and VAM gymnosperm trees were mixed developed in Eocene South America below 24oS (Jaramillo & Cárdenas 2013). However, Bouchal et al. (2014) suggest that vegetation similar to that of the modern chaparral and nemoral conifer forest of the Coastal Ranges was to be found in the Late Eocene Front Range.

Plants with distinctive pollen assignable to the Normapolles complex and comparable with that of extant Fagales (but probably not Nothofagaceae or Fagaceae) were both diverse and ecologically prominent in rocks from east North America to western Asia from the Late Cenomanian/Early Turonian ca 93.5 m.y.a. (but c.f. Batten 1989; Clarke et al. 2011 for cautionary comments). Of the other pollen provinces, the southernmost was also characterized by Nothofagites pollen probably also from Fagales (e.g. Pacltová 1981 for a review; Kedves & Diniz 1983; Friis et al. 2006b, 2010b; Nichols & Johnson 2008). I have seen no discussion about any ECM-associated activities of these plants, and in general understanding ecophysiological relationships earlier in the Tertiary, let alone in the Mesozoic, presents major challenges.

As noted above, sea-grass, salt-marsh and mangrove and to a somewhat lesser extent grassland vegetation are all very productive and all sequester considerable amounts of carbon. Communities dominated by ECM trees, particularly those in the boreal zone (Dixon et al. 1994), all sequester considerable amounts of carbon in their soils; the accumulation of raw humus on the forest floor in tropical ECM forests has long been noted (e.g. Alexander 1989). However, the rate of nutrient turnover in mono- or oligo-dominant ECM vegetation types varies. It can be very high, particularly in the tropics (Torti et al. 2001), and the mono- or oligo-dominant woody vegetation there is not always species-poor, as White (1983) noted for Miombo vegetation and Beard (1946) for the Mora-dominated forests of Trinidad; the dipterocarp-dominated forests at Bukit Lambir, Sarawak, are among the most species-rich tropical forests anywhere (Lee et al. 2002). Interestingly, Mora in particular behaves like some conifers (Enright & Ogden 1995; Aiba et al. 2007) and is almost an add-on to the vegetation, communities with and without Mora being otherwise similar; similarly, emergent dipterocarps may form a separate stratum above the rest of the forest (see Ashton & Hall 1992).

In many cases, communities in which ECM clades dominate grow under quite extreme environmental conditions, whether of substrate or climate (Read 1991). Thus Brodribb et al. (2012) noted that the ECM Pinaceae (as well as other Pinales, which are endomycorrhizal), successfully competed with angiosperms, but not in the most productive environments, while the marine and estuarine environments inhabited by mangroves and sea-grasses are physiologically extreme for angiosperms. The dominance of a relatively few groups of plants in often rather unproductive environments, particularly marked as one proceeds polewards, may reflect the relative rarity of successful adaptations to more extreme conditions; that is certainly true of the adaptation of angiosperms to the submerged marine environment. However, as with just about all features of angiosperms, the physiological/ecological traits under discussion have evolved several times, although all have a strong phylogenetic signal.

Understanding the paleoecology of these traits is difficult; here I summarize information about their evolution. As with other features of plants, when traits such as plant-fungal associations first appeared does not convert in any simple fashion to immediate major ecological effects of comparable antiquity. However, answering questions like, "How many times did ECM associations develop?, When did they evolve?, When did they become common?", is central (see also Eastwood et al. 2011). The clusters of origins of C4 photosynthesis in the PACMAD clade of Poaceae, and again in Cyperaceae and in Amaranthaceae (e.g. Kadereit et al. 2012), and the separate origins of adaptations to life growing completely submerged in the sea in Alismatales, suggest further complexities underlying the evolution of some of the traits. Similarly, ECM clades have originated several times in the N-fixing clade, even if exactly which caesalpinioid legumes in and around Detarieae are ECM plants is unclear.

Some of these questions need to be answered separately for seed plants, ECM fungi, and dispersed pollen of a type now associated with ECM plants, however, continuing uncertainty in angiosperm dates in particular rather confuses the issue. ECM associations have formed perhaps 78-82 times in fungi, especially in ascomycetes and basiodiomycetes, but also Zygomycota, and over 40 families of seed plants, most notably in rosids and in the N-fixing clade in particular, are involved (Hibbett et al. 2000; Hibbett & Matheny 2009; Bruns & Schefferson 2004, Wang & Qiu 2006; Smith & Read 2008; Tedersoo et al. 2010b, 2014a; Koele et al. 2012 in part), with more to be discovered especially in tropical and south temperate areas (Tedersoo & Smith 2013). Dates of fungal ECM clades, including those associated with Pinaceae, are split about equally between Late Cretaceous (e.g. Amanita) and Eocene (e.g. Hebelomateae) in age (Ryberg & Matheny 2012; Tedersoo et al. 2014a and references). Bonito et al. (2014) in the course of looking at the evolution of truffles (ascomycetes) suggested that the age of the clade that included Helvellaceae and Tuberaceae, all ECM fungi, was (184.7-)160.8(-137.4) m.y.a.; the m.r.c.a. of Tuberaceae themselves was dated to some (179.1-)156.9(-134.5) m.y.a., and they thought that its host was likely to have been an angiosperm.

Relatively few major seed plant clades have species that dominate in ECM communities. Estimates of the age of Fagales, in which ECM-formation may be an apomorphy, are a little more than 100 m.y. (e.g. Cook & Crisp 2005; Friis et al. 2006a; Wang et al. 2009; Magallón & Castillo 2009). Pinaceae, also commonly ECM, may be some 200-350 m.y. old (see Eckert & Hall 2006), although the earliest fossils identified as Pinaceae are from Upper Jurassic deposits ca 150 m.y. old (Rothwell et al. 2012). Crown-group Pinaceae are around (271-)153(-136) m.y.o. by some estimates (Gernandt et al. 2008; Magallón et al. 2013), but other ages are late Cretaceous or even younger (Willyard et al. 2007; Crisp & Cook 2011). Suggestions that ECM associations in Dipterocarpaceae and Fabaceae-Amherstieae (= Detarieae) developed before the break-up of Gondwana over 130 m.y.a. (Henkel et al. 2002; Moyersoen 2006) are overly optimistic. Although there is dipterocarp resin in India in the Early Eocene around 52-50 m.y.a. (Rust et al. 2010), there is considerable spread for the age of clades in this part of the tree. Diversification in Fabaceae is very largely Tertiary.

Normapolles-type pollen and macrofossils associated with it have been linked with Fagales other than Fagaceae and Nothofagaceae (Batten 1981, 1989). This pollen was abundant and diverse in the Turonian-Campanian of the Cretaceous, some 94-80 m.y. before present, peaking in the Coniacian-Santonian ca 88 m.y.a. and occurring in much of the Northern Hemisphere in the area 20-45oN Cretaceous palaeolatitudes from eastern North America to west central Asia (Kedves 1989; Sims et al. 1999; Friis et al. 2003a, esp. 2006a, 2010b and references). Elsewhere in the Northern hemisphere Aquilapollenites and Wodehouseia pollen - affinities uncertain (for the former, variously linked with Santalales, Apiaceae and Caprifoliaceae-Morinoideae, see Farabee 1993) - predominated, in tropical Gondwanan areas pollen of Arecaceae was common. However, Nothofagites pollen, linked to Nothofagus, also Fagales, characterized southern temperate Gondwanan areas during the later Cretaceous (Nichols & Johnson 2008) and Nothofagus is thought to have dominated in mid-Eocene forest on Wilkes Land ca 660 S. (Contreras et al. 2013).

It has been suggested that the decline of atmospheric CO2 over the last 120 m.y. is at least in part connected with the origin of clades of ECM plants (L. L. Taylor 2009, 2011). If the present and past are connected, Normapolles and Nothofagites plants, along with most Fagales, were ECM; if these plants were abundant in the Late Cretaceous, they may have had a transformative effect on the environment. Given the ages of Fagales and Pinaceae, ECM seed plants "may have [been found] over a larger area and for a much longer time period in northern temperate zones than in the tropics" (Tedersoo et al. 2012: p. 4167). It has even been suggested that overall, ECM plants may have progressively supplanted VAM plants at weathering hotspots from some time in the Cretaceous (L. L. Taylor et al. 2011), indeed, ECM associations may be "the most profound alteration in root functioning to occur in plant evolutionary history" (ibid., p. 369). However, age uncertainties make life particularly difficult here; from the ages given above, the fungal ECM habit is at least sometimes likely to have originated rather later than the ECM seed plant clades on which the fungi are now found (see also Ryberg & Matheny 2012; Bruns et al. 1998; Horton & Bruns 2001).

To integrate: Pseudolarix was widely distributed in the northern hemisphere at latitudes above 400 in the Early Cretaceous (Barremian, 115 m.y.a.), but the post-Oligocene cooling trend and Late Miocene-Pliocene mountain building would favour Pinaceae (LePage 2003). However, there are massive amounts of dipterocarp resin in India in the Early Eocene, some 52-50 m.y.a. (Rust et al. 2010).

The divergence of the two main sea-grass clades, one including Hydrocharitaceae and the other Posidoniacaeae, etc., has been put at ca 107 m.y.a., while within the latter group the first split can be dated to ca 73 m.y. (Janssen & Bremer 2004). It is unclear how many times adaptation to the marine habitat has evolved, since individual species in sea-grass families and other families of Alismatales may tolerate a range of salinities (e.g. Barbour 1970).

There are a number of independent adaptations to the mangrove habitat (Tomlinson 1986; Spalding et al. 2010), although Rhizophoraceae-Rhizophoreae and Arecaceae-Nypa are particularly important there. By the Eocene, ca 50 m.y.a., many mangrove genera are known from the fossil record, and several, including Pelliciera, are known from both the Old and the New World (but see Martínez-Millán 2010). Pelliciera is now Central American, although it grew in Europe in the past (Plaziat et al. 2001; Ricklefs et al. 2006 for some dates). Nypa, today found only in the Indo-Malesian area, appeared in the Upper Cretaceous ca 70 m.y.a. and by the early Palaeocene ca 55 m.y.a. was found in both the Old and New Worlds (Arecaceae, q.v. for fossils). Fossil hypocotyls identified as Ceriops and preserved with good anatomical detail have been found in the Lower Eocene London Clay (Wilkinson 1981; but c.f. Collinson & van Bergen 2004). Rhizophora is known from the Caribbean in the late Eocene (Graham 2006) and Rhizophoreae from the Early Eocene 55-48.5 m.y.a. in western Tasmania, Australia (Pole 2007).

C4 photosynthesis may have originated in the Oligocene ca 33 m.y.a., but C4 grasses became diverse - and made a corresponding major contribution to overall vegetation biomass - only in the late Miocene 9-8 m.y.a., the process being complete as recently as the late Pliocene 3-2 m.y.a. (e.g. Edwards et al. 2010; Strömberg & McInerney 2011; McInerney et al. 2011; Strömberg et al. 2011; Arakaki et al. 2011; R. Sage et al. 2012). The great expansion of C4 grassland began in the Miocene, a mere nine million years ago, and was completed only 3-2 m.y.a. (e.g. Strömberg & McInerney 2011; McInerney et al. 2011 for North America; Bouchenak-Khelladi et al. 2014; etc.); for further details, see Poaceae. C4 grass-rich and fire-prone savannas in Africa and the Cerrado in South America developed at about the same time (Simon et al. 2009; Simon & Pennington 2012; Maurin et al. 2014; Pennington & Hughes 2014).

An analogy with the related ideas of keystone species and ecosystem engineers, species that directly or indirecty disproportionately control the resources needed by other organisms (Wright & Jones 2006), may be helpful here (e.g. Leighton & Leighton 1983; Terborgh 1986; Watson 2001; Watson & Herring 2012; Mouquet et al. 2012b). The clades we are talking about have a disproportionate effect on the community, ecosystem or even biosphere relative to their species numbers (see Power et al. 1996). Thus Brodribb et al. (2012; see also Coomes & Bellingham 2011) thought of conifers in general as being ecosystem engineers because of their major effect on the environnment. However, whether keystone clades or ecosystem engineers, the clades being discussed are not sharply distinguishable from all other clades in terms of their effects on the environment (for demolition of the simple idea that there are keystone species - species "important for something", see Hurlbert 1997), nevertheless, they have major effects at ecological scales from the local community up to the global ecosystem.

The clades under discussion are associated with major biomes or ecosystems (Pennington et al. 2004; see other papers in Proc. Roy. Soc. B, 359(1450). 2004), and it is at this level that the ecological interactions under discussion play out. It is increasingly a matter of comment that a number of clades seem to be more or less restricted to biomes (e.g. Schrire et al. 2004; Pennington et al. 2009; Dick & Pennington 2011; de Nova et al. 2012). In such cases ideas of phylogenetic biome or niche conservatism are invoked: Clades retain niche-related traits or, more generally, have conserved ecological roles (e.g. Wiens & Donoghue 2004; Crisp et al. 2009; Crisp & Cook 2012; B. T. Smith et al. 2012). The ages of the ECM clades mentioned above are usually much more than 10 m.y., and so their evident ecological conservatism is relatively ancient (Tedersoo et al. 2014a). However, as Mouquet et al. (2012a) note, the term "phylogenetic conservatism" has been used in various ways in the literature on phylogenetic community ecology, so, as with keystone species, its use may generate more heat than light; niche conservatism seems to be little more than the recognition that some ecological features are associated with clades more than might have been expected, but this is true of subsets of many groups of characters.

[Next three paragraphs: out of place.]General diversity and community/ecosystem stability may be connected. Petchey and Gaston (2002a, b) suggested that if functional diversity/functional traits in the community are to be conserved, a large proportion of species in that community will also have to be preserved; there is little redundancy in functional diversity. Isbell et al. (2011) found that 84% of the grassland species studied promoted ecosystem functioning at least under some conditions even in the limited periods during which their experiments were carried out.

Even if dominant species can maintain ecosystem functioning in the face of the loss of rare species, at least for a time (e.g. Smith & Knapp 2003), phylogenetic diversity may still improve ecosystem functioning, although this may also depend on rainfall, temperature, levels of soil nutrients and CO2, etc. (see e.g. Chapin et al. 1997; Zavaleta et al. 2003; Maestre et al. 2012; Cadotte et al. 2012). Experiments measuring biomass production find that productivity and diversity become more closely linked over time (Reich et al. 2012); as conditions change, different species may assume importance - and the history of the Tertiary is one in which conditions have never been fixed for long. Some species may even be quite flexibile in the the ecological roles they play (Aizen et al. 2012), although other studies suggest more conservatism (Maherali & Klironomos 2007; Stouffer et al. 2012). However, little of the work on community/ecosystem functioning, other than some on grasslands, has emphasized the kinds of communities that are the focus here.

Estimates are that tropical ecosystems store 47% terrestrial carbon and have 59% terrestrial primary productivity (10% of both in the Amazon Basin alone: Tian et al. 2010). Similarly, of global terrestrial net primary production, that in l.t.r.f. is around 36% (19.1/53.2 x 1015 gC) of the total, that of grassland + savanna ca 19% (9.7/53.2 x 1015 gC, of which over half comes from tropical savanna), contributions of boreal forest, temperate coniferous forest, etc., being less than 6% each (Melillo et al. 1993). On a per area basis the inequalities between biomes are clearer, thus soil carbon storage, at ca 11.7 kg C m-2 and NPP, at ca 956 kg C m-2 yr1 in tropical forests, compares with figures of 14.5 and 576 respectively for grassland and ca 61.4 and ca 319 for boreal forests (Averill et al. 2014). Ca and Mg fluxes from rock weathering are highest in forests - tropical - with very high NPP and where there is weathering of basalt (L. L. Taylor et al. 2012). [Last sentence out of place.]

Overall, the implications of these asymmetries in relationships between animals, plants, and the environment, are complex, but we can see that species numbers per se are but one way of thinking about seed plant evolution. By focusing on the construction and maintenance of the ecological scaffolding of community structure over evolutionary time and in a phylogenetic context, angiosperms with dense venation, C4 grasses and ectomycorrhizal plants represent pillars, and ants, bumble bees, fruit bats and the like, arches and spandrels. These groups appear to have had a major role in constructing and maintaining the environment, while the bulk of the tens of thousands of euasterid species make up the paintings in the spandrels (apologies to Gould & Lewontin 1979). These paintings are forever changing as individual species go extinct, for instance because of the breakdown of plant/pollinator relationships, while other relationships are evolving. Plant communities come and go, and the relation between present, past and future is unclear (e.g. Torres et al. 2012). Over time the whole biosphere has changed as groups of plants with different eco-physiological capabilities assume prominence, and this helps provide the context for the diversification of seed-plants, and of their associated animals, at all levels.

10. In Conclusion.

Gorelick (2001) summarized some twenty hypotheses that have been advanced to explain diversification/success of the angiosperms (see also Crepet & Niklas 2009), many having to do with flowers, and all told some 120 or more hypotheses have been advanced to explain the patterns of species richness that are such a distinctive feature of the environment (Palmer 1994). Work has tended to focus on understanding speciation within individual very speciose clades (e.g. Davies et al. 2004c), and much literature emphasizes the acquisition of "key innovations", apomorphic features of often assumed functional and ecological advantage whose development allowed a subsequent increase in the overall speciation/diversification rate of the clade in which it arose (e.g. Marazzi & Sanderson 2010). Thus clades in which latex (Farrell et al. 1991; see also Powell et al. 1999; Agrawal & Konno 2009: survey of laticiferous plants and latex; Konno 2011: chemistry), nectar spurs (Hodges & Arnold 1995; Hodges 1997; Kay et al. 2006), monosymmetric flowers (Donoghue et al. 1998; Neal et al. 1998; Endress 2001; Sargent 2004; Kay & Sargent 2009; c.f. in part Kay et al. 2006), humming bird pollination (Schmidt-Lebuhn et al. 2007), animal pollination (Eriksson & Bremer 1992; Kay et al. 2006b), self sterility (Ferrer & Good 2012), or the climbing habit (Gianoli 2004) have evolved, are often more diverse in terms of extant species than their sister clades lacking these distinctive features. Interestingly, although Malpighiales and Ericales appear to be disproportionately common among the small trees of the understory of tropical rain forests (Davis et al. 2005a), they include taxa with many kinds of flowers and fruits, and monosymmetric flowers of a variety of morphologies are scattered in both clades. Neither clade can be well characterised either morphologically or chemically, and key innovations for them are hard to identify, although they may become evident if the focus is turned to smaller clades within these two major groups.

Key innovations that cause the more or less immediate diversification of the clade in which they arise may be individually less important than we might like to think, and identifying key innovations is far more than simply linking a feature to a named node (e.g. Sims & McConway 2003; Davies et al. 2004a; Donoghue 2005; Erkens 2007; Crepet & Niklas 2009; Marazzi & Sanderson 2010; c.f. Endress 2011a). Indeed, understanding the not-so-simple idea of persistence is also important (Leslie et al. 2013). Overall, determining that an innovation might be a key innovation is a difficult process (e.g. Cracraft 1990; Sanderson 1998; Ree 2005b; Maddison et al. 2007). There are several related issues.

1. The increase in speciation that results from the acquisition of a key innovation has to be distinguished from simple radiation of a clade when it moves into in a new area, even if allowing the plant with an innovation to move into new ecological space may be part of the definition of a key innovation (Sargent 2004; Marazzi & Sanderson 2010). Thus in Guatteria much speciation may have occurred only subsequent to its entry into South America (Erkens et al. 2007). Although Howarth and Donoghue (2004, esp. 2005) note possible connections between changes in CYC-like genes and changes in floral form in Dipsacales (CYC-like genes are widely involved in symmetry changes, especially in core eudicots (X. Yang et al. 2012; Preston & Hileman 2012, direct links remain to be established - and linking these changes with diversification is yet another issue. Thus crown-group Valerianaceae may be 60-55 m.y. old (Bell & Donoghue 2005a), but diversification in the Andean paramo, which resulted in ca 1/7th of the species currently recognized in the family, happened less than 5 m.y.a. on the arrival of Valerianaceae in South America (Bell & Donoghue 2005b; Moore & Donoghue 2007, see also Viburnum). It is not obviously associated with the evolution of particular floral (or other) key innovations (see also Richardson et al. 2001). Similarly, rapid diversification of Andean species of Lupinus - where most species of the genus are now found - began only some 1.76-1.19 m.y.a. and probably was driven by the ecological opportunities available in the high altitude habitats there (Hughes & Eastwood 2006; Drummond 2008; Drummond et al. 2012); bumble bees, also immigrants to Andean South America, may have been an important factor in the diversification of these plants (Hines 2008). Finally, in Halenia (Gentianaceae) with its "key innovation" of five nectar spurs, diversification and acquisition of these spurs are not simply linked (von Hagen & Kadereit 2003, see also Gentianella, etc.).

2. Key innovations are rarely simple features, rather, they may involve a complex suite of changes, as with the evolution of vessels and leaf venation discussed above. Thus Edwards and Donoghue (2006) suggest that several key elements of the cactus ecological niche were established before the evolution of the cactus life form and subsequent diversification of Cactaceae (Ogburn 2007; Ogburn & Edwards 2009; Nyffeler & Eggli 2010 for information), partly because the resolution of paraphyletic groups helped spread what appeared to be phylogenetically linked characters through the tree (Donoghue 2005). Moreover, the importance of some changes may be less in the changes themselves, but subsequent changes that they make possible and/or their importance in ecological conditions developing long after their origin. It may also be the combination of traits or the culmination in the development of traits that is important, rather than any one trait itself (Ogburn & Edwards 2008; Horn et al. 2012: Euphorbia subgenus Chamaesyce; Schranz et al. 2012; see also Stebbins 1951). The evolution of flowers, vessels, the effects of genome duplications, C4 photosynthesis, etc., all seem to fit this model.

3. Just as most angiosperm characters are highly homoplastic, arising in parallel, being lost many times, and characterising both large and small clades, so are individual features rarely consistently key innovations. Thus even if the evolution extra-floral nectaries may be deemed a key innovation, as in some Senna (Fabaceae), this does not mean that it always is; the loss of such nectaries may equally be a key innovation in related taxa (Marazzi & Sanderson 2010). Similarly, as has already been noted, some wind-pollinated clades are very speciose, most are not.

4. Returning to an issue raised above, in many very speciose clades, including angiosperms as a whole, patterns of clade numbers do not suggest any immediate diversification after acquisition of the putative key innovation. Characters that seem to facilitate diversification but that evolve well before the diversification they are supposed to facilitate are best thought of as exaptions (de Queiroz 2002), and at one level it is clear that this interpretation is appropriate for most of the characters considered to be key innovations of angiosperms or of major clades within it - whether flowers, vessels, or C4 photosynthesis. Flowers may become important in facilitating diversification only with the evolution of bees (Cappellari et al. 2013). Pollen is one reward for bees, nectar is another, and the distribution and morphology of nectaries also needs to be factored in to the equation. Nevertheless, although bees are quite a diverse group, with some 17,500 species (Michener 2007), it is particular groups of bees, not notably speciose, that play a disproportionately important role in current bee-plant interactions (see above; c.f. Cappellari et al. 2013).

Certainly, simply listing clades or, worse, families, orders, etc., and characters may not be very helpful (e.g. S. A. Smith et al. 2011). Thus almost three quarters of Asteraceae are members of the chemically very distinct Asteroideae. Over four out of five Orchidaceae are Epidendroideae (ca 18,000 species), and much diversification occurred in the "higher epidendroids" some (64-)59-42(-36)/(49-)39-34(-22) m.y.a. (Ramírez et al. 2007; Gustafsson et al. 2010). Exactly where monosymmetry is an apomorphy in Asterales as a whole is unclear - and so on.

Parallelism and convergence, homoplasy, are everywhere one looks, even in early land plant evolution (e.g. Boyce 2010). As more becomes known about details of molecular evolution, widespread homoplasy is appearing at this level, too. Understanding developmental/regulatory pathways is important. The frequent reaquisition of woodiness in clades that have become herbaceous may be because elements of the cambial regulatory program remain untouched (Groover 2005; see also Blein et al. 2010: vegetative development). There are elements of common developmental mechanisms involved in independent acquisitions of monosymmetry (e.g. Feng et al. 2006: Fabaceae and Plantaginaceae; Zhang et al. 2010, Malpighiaceae), duplication of CYC genes being involved (see also Damerval & Manuel 2003; Rosin & Kramer 2009; Preston et al. 2011b). Irish (2009) suggests that petals may have evolved several times because of the independent cooption of underlying gene regulatory networks. Parallelisms also occur at the amino acid level as in C4 photosynthesis (e.g. Bläsing et al. 2000; Christin et al. 2007b, 2008b, 2009a; Brown et al. 2011).

It is a challenge to think about the evolution of the morphological and other novelties that are the focus here. Heterochrony (the male gametophyte of flowering plants is a good case in point - e.g. see Takhtajan 1976), heterotopy (e.g. Baum & Donoghue 2002), and homeosis (e.g. Mathews & Kramer 2012) are all part of this mix. As Preston et al. (2011b) put it as they summarized aspects of the developmental evolution of angiosperm flowers, "reduce, reuse, and recycle" has been the order of the day, and it seems that old dogs can indeed be taught new tricks (Rosin & Kraemer 2009; Mathews & Kramer 2012). We have tended to think of evolution as the modification of pre-existing form: "Are petals in x really modified stamens?". Now we have the tools to think more about the evolution of novelty, elements of developmental pathways that merge and form new regulatory combinations; Mathews and Kramer (2012) review floral and in particular ovule development across seed plants from this point of view.

In this context, the often rather sporadic distributions of secondary metabolites has long been difficult to understand. But as with cambia, the ability to synthesise a particular secondary metabolite having been acquired, it may be switched off easily, but not lost, and so the metabolite can be "reacquired" (e.g. Grayer et al. 1999; Wink 2003, 2008, 2013; Liscombe et al. 2005; Albach et al. 2005c; Agrawal et al. 2012). However, in other situations pathways may degenerate and change is irreversible (Zufall & Rauscher 2004). Associations between plant and fungus/microbe in both mycorrhizal and endophytic associations, and/or lateral transfer of genes, may also go some way towards understanding the rather unpredictable pattern of distribution of many secondary metabolites (Wink 2008; Lamit et al. 2009); endophytes may synthesize metabolites normally ascribed to the plant partner.

The idea of evolutionary "tendencies" persists (e.g. Endress & Matthews 2012), similar discussions recurring periodically in the phylogenetic literature (e.g. Cantino 1985; Sanderson 1991). Indeed, some phenotypes may be the result of parallel mutations that occur only because of a previous change in the larger clade (see Shubin et al. 2009 on deep homology) and Marazzi et al. (2012) attempt to locate such evolutionary precursors - in this case, extrafloral nectaries in Fabaceae - on the tree. The ability of a plant to form an association with nitrogen-fixing bacteria is a good example (see Fabales: e.g. Soltis et al. 1995b), the clustered origins of C4 photosynthesis in grasses and elsewhere invite a similar explanation (see e.g. McKown et al. 2004; Christin et al. 2011a, 2013; Grass Phylogeny Working Group II 2011), as do the origins of various symmetries in angiosperm flowers (Irish 2009; Preston et al. 2009). Genes can be transferred via grafts in host-parasite connections, chloroplasts can move via grafts between different free-living organisms - and perhaps genes may be transferred from live pollen that lands on the stigma, germinates, but does little else (Christin et al. 2012: confirmation needed!), and such phenomena may explain clustering of apparently independent origins of features.

The rise to dominance of the angiosperms and the diversification of particular angiosperm clades also involves other organisms - plants, animals, fungi, bacteria - as well as changes in the environment itself, and it is a thoroughly ecological process (e.g. Thompson 1998; Harmon et al. 2009). One has to take into account both intrinsic and extrinsic traits of plants. Along these lines, Lavin et al. (2004) and Schrire et al. (2005) suggest that it is more profitable to think of diversification and distribution of Fabaceae in terms of vicariance of biomes rather than of the classic geographical areas. The area a clade inhabits, especially if it is non-contiguous, may affect diversification (Vamosi & Vamosi 2010, 2011; see also Marazzi & Sanderson 2010 above). Under such circumstances diversity may be limited by ecological factors (e.g. Vamosi & Vamosi 2010), although if the assumption that clades increase steadily in diversity with time is unreasonable (Rabosky 2009; Vamosi & Vamosi 2010), so is the implicit assumption that the environment does not change.

Initial angiosperm evolution took place under ecological conditions rather different from those under which they prospered later; then continents were drifting apart, there was increasing carbon dioxide concentration and rising sea levels, and ever-wet tropical humid climates, initially rather restricted, were becoming more extensive. Even if "basal" clades that are now species poor were much more diverse in their early history (Magallón & Castillo 2009 and references), they may have been responding to conditions that are not found today. Angiosperm-dominated vegetation is largely of Tertiary age, so the early Tertiary environment - warmer, less seasonal, few fires - may provide another context for thinking about its evolution. Subsequent Tertiary diversification occurred as temperatures and atmospheric carbon dioxide concentration were dropping, seasonality increasing, and, especially towards the end, fires increasing. Climate has been changing dramatically throughout the history of crown-group angiosperms, spurred by angiosperms themselves and their associated fungi (e.g. Knoll & James 1987; Volk 1989; Boyce et al. 2010); see above.

In general, the evolution of flowers, vascular systems, and just about all aspects of plants seems a complex, protracted, and clade-dependent process (e.g. Feild & Arens 2007). Flowers and vessels may not have been of immediate evolutionary importance, at least if judged in terms of numbers of extant taxa in early-branching clades with these features. The initial branches of the angiosperm tree are highly asymmetric in terms of species number in extant clades (see e.g. Sanderson & Donoghue 1994; Magallón & Sanderson 2001). Friis et al. (2006b) emphasized that such clades have long fossil records yet include only a few extant species, and they also differ from other angiosperms in ecophysiological features. Thus ANITA grade angiosperms have low veinlet densities rather like those of gymnosperms and ferns, so transpiration rates and hence photosynthetic capacities (Pc) are rather low (Brodribb et al. 2007; Boyce et al. 2009; Feild et al. 2009a; Brodribb & Feild 2010); their vascular anatomy is also unlike that of many other angiosperms (e.g. Sperry et al. 2007; Feild & Thomas 2012). Similarly, distinctions between the nature and arrangement of floral parts that are obvious in say, core eudicots are less evident in members of the ANITA grade, endosperm formation is variable, etc. (e.g. Buzgo et al. 2004; Endress 2005c; M. L. Taylor et al. 2008; Friedman 2008b).

As Feild and Arens (2005: p. 402) observed, diversification may well depend "on the fortuitous combinations of a large repertoire of traits" rather than on any particular key innovation (see also Crepet & Niklas 2009 and references; Magallón & Castillo 2009). Overall angiosperm success seems to be in considerable part the result of diversification of individual angiosperm clades with various combinations of characters and responding to various ecological/environmental contexts, and establishing an immediate connection between acquisition of an apomorphy or group of apomorphies and diversification is difficult. Angiosperms show bursts of diversification in separate clades, especially in a number of asterids and monocots (e.g. Magallón & Sanderson 2001; Sims & McConway 2003; Crepet & Niklas 2009), and parallelisms from the molecular level up are pervasive (e.g. Endress & Matthews 2012; Mathews & Kramer 2012 and references). Phylogenetic niche conservatism of adaptations to "major ecological niches" mean that some groups will follow these niches when there is an opportunity (Donoghue 2008; especially Lavin et al. 2004; Schrire et al 2005; Marazzi & Sanderson 2010); adaptation to such niches may not occur very frequently. We have to factor in the major climatic changes in the Tertiary, while extinction, although difficult to document, plays an important role. Thus as recently as ca 30 m.y.a. there were humming birds in Europe (Mayr 2004), and Cyclanthaceae are known from European Eocene deposits (Smith et al. 2008). Both groups are now iconically New World, and humming birds are involved in the pollination of over 2,000 species of flowering plants there.

Species number is only one estimate of "success" in evolution, and there is a weak negative correlation between diversity and biomass produced (Wing & Boucher 1998). Biomass production, primary productivity, etc., provide more ecological estimates of success, and the possible evolutionary importance of the features just mentioned are to be seen in the context of the eco-physiological evolution of angiosperms and the environmental changes that resulted. Venation density and vascular evolution, in association with other ecological features, have helped shape the evolution of biomes within which diversification has occurred. Biome change continues, the evolution of grasslands dominated by C4 grasses within the last 10 m.y. being just one example. We have to accept the evolutionary implications of the clade size:ecological importance asymmetries; at various levels and contexts, species asymmetries seem the rule.