EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans, also lignins], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; 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; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte 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]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium with 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; shoot meristem patterning gene families expressed; 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, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; 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, plant endohydrous; endodermis +; 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; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; root apex multicellular, root cap +, lateral roots +, endogenous; endomycorrhizal associations + [with Glomeromycota]; 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; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; 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, sporophylls spiral; 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; apical cell 0, rhizoids 0; 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; 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], 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, hypodermis suberised and with Casparian strip [= 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; protogynous; 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], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, 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 lamellate only in the apertural regions, thin, compact; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], 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, pollen tube elongated, unbranched, 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, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; 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]; nuclear genome size <1.4 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; Magallón et al. 2015: 139.4 m.y.a.). 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. (2014) 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). (152-)144(-133) m.y.a. is the estimate in Silvestro et al. (2015). It would be amusing to graph these ages against their publication dates...
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. Chloranthoid laminar teeth - three veins converging at or below the apical gland - may be a feature of all angiosperms (Doyle & Upchurch 2014).
Protogyny is very common in "basal" angiosperms (Routley et al. 2004: Amborellaceae are ± dioecious), while protandry is common in eudicots, and above Alismatales in monocots (see also Bertin & Newman 1993; Endress 1994b). For connections between protogyny and protandry and self compatability and self incompatability, see Routley et al. (2004 and references). 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.
Different topologies of basal angiosperms (see below) may have little effect when thinking about angiosperm evolution, certainly for characters like the evolution of habit/habitat (c.f. Drew et al. 2014). Whether or not an 8-nucleate embryo sac and triploid endosperm are synapomorphies for all angiosperms or only for those angiosperms above the ANITA grade 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 Friedman and Ryerson (2009). If Nymphaeales are sister to Amborellales, then diploid endosperm may be the ancestral condition, with triploid endosperm evolving in parallel in Amborella and in the [[magnoliid + Chloranthaceae] [other angiosperms]] clade (see also Williams & Friedman 2004 and references; Xi et al. 2014). For more on endosperm evolution, see below.
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 (see also Wortey et al. 2015; Lu et al. 2015). Tryphine of many angiosperms, but not gymnosperms, includes hydroxycinamic acid (HCAA) and flavonol α-1,2-linked diglycosides (3-O-sophorosides) that may be antioxidants protecting against UV radiation (Fellenberg & Vogt 2015; see alsobelow ). 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) two 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), where higher up on the tree changes in these features occurs is unclear.
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 stigma type, Thien et al. (2009), for the evolution of placentation types, see Ickert-Bond et al. (2014c), 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 trees used, 2008), Taylor and Osborn (2006) and especially Wortley et al. (2015: note sampling, treatment of variation, and optimization) and Lu et al. (2015). For various other aspects of early angiosperm evolution, see below.
Ecology & Physiology. 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).
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 the common ancestor of all seed plants, if not still deeper in the tree.
Genes & Genomes. For 1C values (converted to 2C values here, see Plant DNA C-values Database, consulted vi.2013 (also Bennett & Leitch 2005, 2010). Genome size in many angiosperms is small, 1-1.4 picograms being the estimated ancestral nuclear C value for angiosperms (Masterson 1994; Leitch & Bennett 2005; Leitch et al. 2005). However some Proteaceae, Liliales and Asparagales have very large genomes. Extant gymnosperms have quite large genomes, although those of 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 are not connected (see also below). 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. (2012). 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) - synonymy: AP3 and PI with DEF and GLO respectively.
Chemistry, Morphology, etc. Some taxa in the ANITA grade have been surprisingly little studied. Thus root morphology, cork development, etc., are unknown in Amborellaceae, an absence of knowledge complicated by the very distinctive and derived "aquatic" morphology and anatomy of Nymphaeales.
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. Compared with conifer lignin, primarily made up of guaiacyl units, the S-rich lignins of angiosperms is less dense and less highly condensed, the polymer units are smaller and have more β-ether interunit linkages; wood fibres are rich in S units, while in vessel elements G lignin predominates (Wagner et al. 2015). I do not know if this has implications for fungal-mediated breakdown of lignin. 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 monocots 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.
For programmed cell death in flowering plants, particularly evident in ovule, embryo sac and embryo development, see van Hautegem et al. (2015). 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. In plants that have rhizomes the hypodermis is more or less suberized and has a Casparian strip (e.g. Perumalla et al. 1990b). 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).
Phylogeny. The balance of evidence is tilting towards the hypothesis that angiosperms are sister to a clade that includes all extant gymnosperms. For convenience, direct links to Cycadales and Pinales are provided here; for a general discussion on the relationships of the major extant seed plant clades, see seed plant phylogeny.
Within early-diverging angiosperms, Donoghue and Mathews (1998) listed 16 different hypotheses of relationships that involved the first three nodes. However, Amborellaceae alone have often been found to be sister to other angiosperms (not an hypothesis that Donoghue and Mathews included!), Nymphaeales are sister to the rest, and then Austrobaileyales - the ANITA grade (the acronym varies) (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; E. K. Lee et al. 2011; 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).
On the other hand, 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 Poaceae alone. 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) the relationships [Ceratophyllum [[Amborella + Nymphaeales] other angiosperms]] were recovered.
There have been suggestions that there is an [Amborellales + Nymphaeales] clade. This topology was perhaps particularly prominent in some analyses of mitochondrial genes, as in Qiu et al. (2006b), although there were several unexpected if poorly supported relationships elsewhere in their preferred tree (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. 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.
Sampling and analytical strategies may well be critical here, particularly when there are relatively few taxa each with very large amounts of data (e.g. Jarvis et al. 2014). 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 result in the gradual stabilization of support values, rather, these continued to fluctuate even when there was quite a lot of data and relatively small 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). Thus 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 now 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, and euasterids. The discussions focus on the usually rather conservative topologies of the trees in this site, but the bottom line is that in places there is still substantial uncertainty about relationships.
Classification. For full bibliographic information on all names above genus in angiosperms used here see Reveal and Chase (2011), Reveal (2012) and especially Reveal (2000 onwards); it is to be hoped that the latter resource is kept up-to-date.
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
EVOLUTION AND DIVERSIFICATION OF THE ANGIOSPERMS (This section remains under construction)
The first three sections below are more introductory, while the others attempt to summarise particular aspects of angiosperm evolution and diversification. In sections 2 and 3 aspects of the evolution of insects and fungi respectively are summarized; their associations with angiosperms has been of great importance for both parties. Some of the issues raised here are taken up more specifically later and more from the point of view of the plant. Our knowledge of the evolution of stem-group angiosperms remains very poor (section 4). The evolution of flowers and fruits figure prominently (see sections 4 and 5 in particular) in the mythology of angiosperm evolution and success, and they are indeed important (section 7), although not in any simple sense. Certainly, numbers of species are but one measure of success or importance, and in sections 5D, 6D and 8B in particular 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. In section 8 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 9 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.below
1. Important Caveats.
2. Angiosperms and Insects.
2A. Insects, Plants and Herbivory.
2B. Diversification of Phytophagous Insects.
2C. Diversification of Pollinating Insects.
3. Angiosperms and Fungi.
Early Plant-Fungal Relationships.
4. Angiosperm History I: Evolution in Stem Group Angiosperms.
4B. Pollination and Seed Dispersal.
5. Angiosperm History II: Cretaceous Origins.
5B. Early Cretaceous Evolution.
5C. Later Cretaceous Evolution.
5D. Venation Density, Stomatal Size, and Vascular Evolution.
6. Angiosperm History III: Caenozoic Diversification.
6A. Flowering Plants.
6B. C4 Photosynthesis, Grasses, and Grasslands; also, some other Ecological Groups.
6C. Latitudinal Gradients of Diversity.
6D. Gene and Genome Duplication and Genome Size.
6E. Diversification of other Plant and Animal Groups Associated with Flowering Plants.
7. Flowers and Pollination.
7A. Flowers, Pollination and Fertilization.
7B. Major Clades With Monosymmetric Flowers.
7C. Major Clades With Wind-Pollinated Flowers.
7D. A Cautionary Note.
8C. Wood and Litter Decay. (in the process of being modified)
8. Asymmetries in Evolution.
8A. Plant-Animal interactions.
9. 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 as well as of many ordinal trees where we know less than we would like. Indeed, the huge data sets being developed both demand critical attention to analytical methods and are likely to yield unexpected topologies. But 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; Hengchang Wang et al. 2009; Smith et al. 2010; Magallón 2009; Milne 2009: sampling; Burleigh 2012; Sauquet et al. 2012; Magallón et al. 2013; Magallón 2014; Sytsma et al. 2014; Warnock et al. 2014; Clarke & Boyd 2014; Bell 2015). 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. some Nymphaeales. In all too many cases there are wildly different estimates for the same event. For instance, compare Wikström et al. (2001, 2004), Clarke et al. (2011) and Z. Wu et al. (2014) for angiosperm ages, Wikström et al. suggest a crown-group age in the Cretaceous, Clarke et al. an age in the Jurassic or earlier, and Wu et al. an age in the mid-Permian. 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. ago. See also Sauquet et al. (2012) for Nothofagus, Crisp and Cook (2011) and Martínez et al. (2012) for cycads, Barreda et al. (2010b, 2012) and Heads (2012) for Asteraceae (Waters et al. 2013 for a critique of the latter), and Crisp et al. (2014) for Xanthorrhoeaceae-Xanthorrhoeoideae. Although many ages for clades are given on these pages (many dates for older literature, not all mentioned here, are conveniently assembled in Hedges & Kumar 2009), all dates should be treated with extreme caution. The original papers should be consulted for details of methodology, the actual node to which the date refers (I have tried to be accurate), the range of dates, and the topology of the tree that is being dated.
Although it might seem that a clade living on a volcanic island must be younger than that island, several examples suggesting the contrary are to be found in these pages (see also Heads 2011). Island ages cannot be used as age constraints without there being other evidence.
Fossil evidence is central to dating. However, fossils are usually 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; fragmentary fossils may be assignable to more than one node. 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 morphological 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). 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; Parham et al. 2011; Warnock et al. 2014; etc.), but carefully-evaluated fossils have a major role to play in checking molecular dates (Wilf & Escapa 2014: sobering). Good, well-identified fossils give a minimum age (Donoghue & Benton 2007). The fossil record is sure to have surprises.
Poaceae present particular problems. Amber fossils of Poaceae-Poöideae (Poinar 2004, 2011) from the Cretaceous of Myanmar/Burma are dated to ca 98.8 m.y. (Shi et al. 2012). Such dates would imply that many many other dates for flowering plant clades are much too young and would cause a general rethinking of angiosperm evolution. Core eudicot angiosperm fossils have also been found in this amber (e.g. Poinar 2011, Poinar et al. 2007, 2008). Even the ca 66 m.y. age of grass phytoliths from India will have a substantial effect on other age estimates, and hence on diversification rates (Christin et al. 2014).
2. Distributions are not easy to interpret. There is abundant evidence that the present and past distributions of many plant and animal groups are very different. Thus early in the Caenozoic 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 hoatzins, humming birds and parrots were flying around in Europe (Mayr 2002, 2004). Genera and families continue to be added to the list of groups in which past and present distributions are very different (e.g. Friis et al. 2011: numerous examples; Stull et al. 2012; Manchester et al. 2012; Grímsson et al. 2013; Hofmann et al. 2015; Sadowski et al. 2015), and many taxa now restricted to Southeast Asia grew in Europe and North America in the Caenozoic (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, esp. 2014, 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). However, Wilf and Escapa (2014) question young ages of a number of Patagonian fossils and so question dispersal-type explanations based on these ages. Smedmark et al. (2014) rightly emphasized how difficult it was to reconstruct biogeographical events if more than one resolution was allowed for nodes whose support was weak, however, using a single tree for such reconstructions was inadvisable (and this would be true of some attempts at optimisation, etc.). 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 straightforwar 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; Igea et al. 2015 - 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 particularly diverse, and if so, why?", are not that straightforward. 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). In some groups uncertainty over species numbers is particularly great, thus estimates for Ophrys range from 16 to 252 (e.g. Bateman et al. 2011a; Vereecken et al. 2011).
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, 2011; Frohlich & Chase 2007; Pennisi 2009; Lee et al. 2011). Here we need to 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-group angiosperms, i.e. extant flowering plants and their immediate common ancestor ("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-group angiosperms are as much as 270 to 182 m.y.o. (Smith et al. 2010), they will still have a substantial stem history. For the bulk of this some 100 m.y.+ time plants along the angiosperm stem probably had naked seeds, lacked flowers, etc.. 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 over the last fifty years or more in identifiying plants that can be placed somewhere between origin 1 and 3 (Taylor & Taylor 2009; Doyle 2012), the reports of Jurassic flowers by Z.-J. Liu et al. (2015 and references) needing confirmation.
5. Many characters seem to come and go on the tree almost willy-nilly, and this makes character optimisation a distinctly hazardous undertaking. Thus using either parsimony or maximum likelihood, making apparently reasonable assumptions about the relative weighting of gains versus losses, 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; Wortley et al. 2015), 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; Kriebel et al. 2014). 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 (see Introduction).
Endosperm evolution, particularly in monocots, is a good example. Tobe and Kadokawa (2010) discuss endosperm morphology in terms of cellular and helobial types. However, this 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). Initial 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 asymmetry (Buell 1938). Add 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 also unclear (Olsen 2004), and there is 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 above the ANITA grade - and a supporting argument here might be that Amborella has an embryo sac unique in the angiosperms. Simple parsimony, whether ACCTRAN or DELTRAN, helps little here since there are no outgroups (e.g. Friedman & Floyd 2001; Ronse De Craene et al. 2003).
6. Understanding the palaeoecological context of the evolution of angiosperms is a challenge; the present is an imperfect key to the past. Ecological contexts change over time, and that of the early Caenozoic diversification of angiosperms is likely to be quite different from those of the origins of stem- and crown-group angiosperms. The Caenozoic context is initially connected with the bolide impact at the K/P boundary and the eruptions that produced the massive Deccan Traps, although much of angiosperm diversity - and that of the animals associated with it - as we now appreciate it seems to be a phenomenon of the later Caenozoic, and again the ecological context has changed; Meseguer et al. (2014b) attempt to deal with the problem. Seed plant ecophysiology has helped drive biosphere evolution and shape stem- and crown-angiosperm diversification since the Permian and before.
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), and 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).
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 they can be difficult both to estimate and to 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 (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 can key innovations be linked to particular nodes? Having worked out changes in clade sizes over time, associating environmental/extrinsic and organismal/intrinsic features to these changes is not easy, although Bouchenak-Khelladi et al. (2015; see also Donoghue & Sanderson 2015) make the attempt. But diversity/species numbers is but one way to measure success, and other measures such as dominance, biomass production and net primary productivity are discussed in below
8. Finally, most angiosperms and the organisms with which they associate are symbiotic systems at a variety of levels. Features ascribed to plants may 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. Organisms other than fungi are endophytes, most notably, plants may have a variety of endophytic bacteria, 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 (Kembel et al. 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). Bacteria also flourish in the rhizosphere, where they can facilitate the uptake of oragnic nirogen (J. F. White et al. 2015). An individual plant is a microcosm or some kind of complex chimaera, as Herre et al. (2005) noted, referring to tropical plants and their endophytic fungi in particular. Angiosperm physiology is mediated by fungi and bacteria both in the soil and in the plant, and this has shaped and continues to shape both the local and the global environments.
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 e.g. Janzen 1980; Schemske 1983; Brouat et al. 2001; Futuyma & Agrawal 2009; Kato et al. 2010; Fordyce 2010; Janz 2011; de Vienne 2013). The term "co-evolution" has come to 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 radiation of a clade when it changes its food source. 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 a herbivore on a new host, "escape and radiate" (e.g. Ehrlich & Raven 1964; Fordyce 2010), and is quite common (de Vienne et al. 2013). We have to ask, to what extent is/was the evolution of the plant and insect connected? Dating the diversification of the two partners is critical here (see above). Complicating our understanding of the interactions of insects and plants are the symbiotic bacteria and other organisms associated with both partners (Frago et al. 2012; Zhu et al. 2014).
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 for the most part rather nutrient-poor, and plant cell walls are made up of the rather indigestible cellulose and still more indigestible lignin. Lignin and cellulose digestion in termites occurs via their association with protozoa or the fungi they cultivate (Ni & Tokuda 2013), while some other insects and 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 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 have more similar animals eating them (Weiblen et al. 2006; Futuyma & Agrawal 2009 for literature), simply because they will tend to taste similarly, having similar secondary metabolites. However, related plants may show greater than expected diversity of traits involved in defence as they try to escape the herbivores eating their congeners growing in the same area (e.g. Becerra 2007; Becerra et al. 2009; Kursar et al. 2009).
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).
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 (Brower & Brower 1964 on butterflies; Nishida 2002 for a review).
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), while Novotny et al. (2010: around 24 guilds listed) found specialisation greatest in four guilds, leaf suckers, larval leaf chewers, leaf miners, and fruit chewers, guilds like root and phloem chewers showing less specificty. 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).
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.
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; Endara & Coley 2010). (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 like polyphenolics are more generalised, and butterflies such as Lycaenidae are the herbivores, while "qualitative" defences are highly toxic and butterflies like Nymphalidae are specialized herbivores (Fiedler 1996).
However, the nature and amount of the defensive compounds produced can also be explained, and perhaps more satisfactorily, 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. Fast-growing plants need 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). When there are low concentrations of available nutrients, growth is slow, the leaves are long lived, and defences are laid down (Coley et al. 1985; Endara & Coley 2010). Along the same line, 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, and some geographical dimensions of these correlations are discussed later. 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, while external feeders tended to be larger, show less host specificity, and formed more speciose clades. Nylin et al. (2014) thought that transient polyphagy in nymphalid butterflies facilitated diversification and subsequent host-plant shift (see also Ehrlich & Raven 1964), however, recent work suggests that in some butterflies, at least, there is no simple connection between host-plant shift abnd diversification (Hamm & Fordyce 2015). The plesiomorphic condition in lepidoptera is small size and internal feeding such as burrowing, features of the basal clades, which have jaws, and the basal Glossata, with probosces, such as Eriocraniidae (Menken et al. 2009; Imada et al. 2011), and overall the change in host plant preferences has been from specialist to generalist (Menken et al. 2009).
To summarize: 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 can be uncertainty in both areas; this is discussed further below.
2B. Diversification of 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). Species estimates for various insect groups are given below, but there is considerable uncertainty in overall arthropod numbers. The total number is likely to be substantially below the 20,000,000 or so once suggested, but estimates still vary between 1.6 and 6.1 million (e.g. Hamilton et al. 2013 and references).
Weevils include some 62,000 described species and 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). 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); for Scolytinae, see under Pinaceae.
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). Basal clades, in which adults have jaws, include Micropterigoidea (their larvae often eat hepatics), Agathiphagoideae (Agathis), and Heterobathmioidea (Nothofagus), and they may have diverged as early as the end-Triassic (Wahlberg et al. 2013). Glossata, which make up other Lepidoptera, have probosces, and relationships among major groups of ditrysian Glossata (the female has separate openings for mating and laying eggs), which include the majority of macro- (butterflies and large moths) and microlepidoptera (mostly smaller moths), have been unclear (Mutanen et al. 2010). However, Kawahara and Breinholt (2014) link large moths with much smaller pyraloid and gelechioid moths, the combined clade being sister to butterflies. Cho et al. (2011 and literature; see also Regier et al. 2009; Mutanen et al. 201; Wahlberg et al. 2013) also suggested that butterflies and large moths were are not sister groups. Within the butterfly clade, with a crown-group age of perhaps 104 m.y.o. (Wahlberg et al. 2013) is a small clade made up of the mostly night-flying Hedylidae, the American moth-butterflies, and relationships 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). For Grimaldi (1999) and Grimaldi and Engel (2005) diversification of Glossata began in the mid- to upper Jurassic, while Labandeira et al. (1997) and Wahlberg et al. (2013) suggested somewhat older dates.
There are over 4,000 species of aphids (Hemiptera-Aphididae) feeding on plant sap, and they tend to be monophagous. Diversification may be Late Cretaceous/early Caenozoic (von Dohlen & Moran 2000). Hemiptera-Sternorrhyncha (with around 2,000 species) and Psyllidae (jumping plant lice) tend to be very host-specific.
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). Initial divergence within butterflies s.l. (Papilionoidea) may also have been around 110-95 m.y.a. (Heikkilä et al. 2011).
Lizards, snakes, and perhaps modern mammal orders, all diversified more during the KTR (Benton 2010), although dinosaurs seem to have been unaffected (Lloyd et al. 2008). Wilson et al. (2012) note that multituberculate mammals in particular were quite diverse after 90 m.y.a., and dentition suggests that some had become herbivorous, although they also occupied other niches. Wilson et al. (2012) thought this might reflect the increasing ecological importance of angiosperms, many being commonly herbaceous and with with poor defences against herbivores. Diversification of mosses, beetles and hemipterans occurred along with that of rosid angiosperms 108-83 m.y.a. (Hengchang Wang et al. 2009; Moreau et al. 2008).
Galls, often with very distinctive morphologies, result from close associations between plant and insect (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 are based on extrapolation and so partly depend on the numbers of flowering plants 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 and make up perhaps 25% of all 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; Csóka et al. 2005). 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). Some other insects, including 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.
[Work Needed on these next paragraphs]. 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, here 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 estimates of ages for the origin of angiosperms, with crown-group Megachilidae, a major clade including the leaf-cutting bees, dated at (154-)126(-100) m.y.a. (Litman et al. 2011). Crown-group bees [??] are some (132-)123(-113) m.y.o. (Cardinal & Danforth 2013), all families having diverged by the K/P boundary. 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).
Crown-group Apidae are dated to (95-)87(-78) m.y. (Cardinal & Danforth 2011). Within Apidae, the somewhat over 1,000 species of primitively eusocial corbiculate bees have the relationships [[Euglossina + Apina] [Meliponina + Bombina]] (e.g. Cardinal et al. 2010; Cardinal & Danforth 2011; Danforth et al. 2013; Martins et al. 2014a), although morphology-based trees suggest relationships [Euglossina [Bombina [Apina + Meliponina]]] (Canevazzi & Noll 2015 and references). Corbiculate bees are estimated to be (89-)77(-66) m.y.o. (Martins et al. 2014a, 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 the euglossine orchid bees to (35-)28(-21) m.y. and (38-)26(-17) m.y., of bumble bees (Bombina/i) to (31-)21(-12) m.y. and (48-)26(-14) m.y., and of honey bees (Apina/i) to (30-)22(-16) m.y. and (29-)22(-17) m.y. (estimates from Cardinal & Danforth 2011 and Martins et al. 2014a respectively); another estimate of the age of crown group euglossines is 42-27 m.y. (Ramírez et al. 2010).
These general relationships are consistent with the appearance of bees in the fossil record. Both Apidae and Megachilidae, derived long-tongued bees, are known from Baltic amber of Eocene age (Danforth et al. 2006 and references). An early fossil, 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 may rather be a 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 placed in Cretotrigona, a stem meliponine) have been re-evaluated (Engel 2000).
3. Angiosperms and Fungi.
Early Plant-Fungal Relationships.
Early Plant-Fungal Relationships. Embryophytes and fungi established associations very early in the Silurian/Devonian (Selosse & Tacon 1998; Nebel et al. 2004). In some extant basal embryophyte clades mucoromycetes are associated with the gametophytes, Endogone-like fungi (Mucoromycotina) forming mycorrhizae with liverworts like Treubia and Haplomitrium (Field et al. 2012, 2014) and with hornworts (e.g. Bidartondo et al. 2011; Desirò et al. 2013). In liverworts, mucoromycete fungi are found in the thallus, and the relationship between plant and fungus seems to be one of mutualism (Field et al. 2014). Mosses - 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; Rimington et al. 2014). Interestingly, the genome of the glomeromycote Rhizophagus irregularis has a number of similarities with those of Mucoromycotina (Tisserant et al. 2013), and both groups have Mollicutes-related endobacteria (Desirò et al. 2014).
Early vascular plants of the 407 m.y.o. Rhynie Chert formed associations with both Mucoromycotina and Glomeromycota (Strullu-Derrien et al. 2014). Since 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, these early plant-fungus relationships are perhaps best called paramycorrhizal associations (Kenrick & Strullu-Derrien 2014).
3A. Mycorrhizae. 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). For the general 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). For comprehensive surveys of mycorrhizal associations, see Brundrett (2008: updated online resource, 2009) and Akhmetzhanova et al. (2012) 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 (see below). 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 monilophytes, but with the sporophytic generation in seed plants (Desiró et al. 2013), however, in some lycophytes and monilophytes the same fungus is found in both generations (Winther & Friedman 2008; Field et al. (2015).
Aquatic flowering plants, hardly surprisingly, often lack mycorrhizae (see Safir 1987 and Radhika & Rodrigues 2007 and references for records; de Marins et al. 2009), and mycorrhizae are also often absent in Caryophyllales, Proteales, etc.. 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). Orchid mycorrhizae (q.v.) will not be discussed further; van der Heijden et al. (2015) suggest that 25,000 species of fungi may be associated with them alone. However, ericoid mycorrhizae are part of the story; at least some fungi associated with both families have fairly extensive saporotrophic machinery (Kohler et al. 2015).
Endomycorrhizae or vesicular-arbuscular mycorrhizae (VAM) are very widespread, being found in about 70% of seed plants, 80% of all land plants, and 92% of plant families (Blackwell 2011), perhaps 200,000 species or so of plants being involved (Rinaldi et al. 2008). VAM associations are of long standing, if not of the common ancestor of all land plants (see above, also Parniske 2008), at least of a major subset of vascular plants. Just how many times VAM associations evolved in land plants is unclear; in part, it depends in part on the very definition of mycorrhizae. Mycorrhizae of any kind are not often found in fossil gymnosperms, although VAM have been described in 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. Sexual reproduction in Glomeromycota seems to be very uncommon. The spores are multinucleate, the nuclei in any one spore not having an 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).
Morphological details of the fungus-plant association vary, Paris-type associations lacking arbuscules and the commoner Arum-type with coils and arbuscules (e.g. Smith & Smith 1997; Torti et al. 1997; Peterson & Massicotte 2004). The proportion of fungal biomass inside and outside the plant depends on the group of Glomeromycota involved (Maherali & Klironomos 2007). 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; see also Fabales). 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 invasion of plant tissue by the fungus may be similar to the establishment of parasitism (Bonfante & Genre 2010), something similar occurring in Fabaceae, too.
Some 290 species of Glomeromycota have been described (Öpik et al. 2010; Merckx et al. 2012), and all form VAM. Recent surveys suggest 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 hence that the diversity of Glomeromycota has been considerably underestimated. In a recent survey in a VAM forest in New Zealand, Martínez-García et al. (2014) could associate only 8 out of the 113 glomeromycote OTUs found there with names. However, even if there are 1,000 or even many more species of glomeromycotes (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 (e.g. Gosling et al. 2013; Martínez-García et al. 2014), and Wenner et al. (2014) found that fungi in related species (= same genus, subfamily) of Asteraceae tended to be most similar (here Glomeromycota were in a minority). In Distichlis spicata there is preferential VAM infection of female plants (Reuss-Schmidt et al. 2015). Overall, the diversity of VAM fungi was not correlated with that of its hosts (Tedersoo et al. 2014b). Many plants form associations with several species of fungus, and ecological specialists and generalists may form 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). 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). As a result, the estimation of the costs and benefits accruing to the parties involved is very difficult (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).
In VAM associations, nutrient uptake by the plant - especially of phosphorus, and 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 phosporus. Root hairs or a VAM association may be alternative ways for a plant to obtain phosphorus when it is in short supply (Schweiger et al. 1995 and references). Glomeromycetes are unable to break down and utilize complex biopolymers (Tisserant et al. 2013), and they obtain at least carbohydrates from the plant (Helber et al. 2011; see also Walder et al. 2012; Kaiser et al. 2014), 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). VAM also have substantial beneficial effects improving soil structure (Taylor et al. 2009), drainage and hence weathering, and also 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.
Ectomycorrhizae (ECM)/plant relations are surveyed by Itoo and Reshi (2013); ericoid mycorrhizae (ERM) are also included in this section (see below). ECM fungi are asociated with relatively few 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). Most ERM are ascomycetes, and hypogeous fungi are derived from ascomycete ECM fungi (Read 1996; Tedersoo et al. 2006). Leotiomycetes, ascomycetes that are commonly ERM, become more diverse towards the poles and their ericaceous associates are also common there (Wardle & Lindahl 2014; Tedersoo et al. 2014b). Basidiomycetes of the Sebacinales-B group can form associations with both Ericaceae and Orchidaceae, but different species are involved (Setaro et al. 2012). There is a strong phylogenetic signal in the plants that form ECM associations (e.g. Alexander & Lee 2005; L. L. Taylor et al. 2009, 2011), and this is discussed below.
ECM associations with Pinaceae, perhaps 200 m.y.o. or more, are probably the oldest; crown-group Fagales, an ECM clade, have been dated to 120-62 m.y.a., which is not very helpful. Mycorrhizal associations in Ericaceae have been dated to ca 90 m.y.o. (van der Heijen et al. 2015 and references), but the fossil Paleoenkianthus, on which this age is based, may not even be stem Ericaceae (see elsewhere), and even if it were to be linked with Enkianthus, that genus has VAM fungi. Ericoid mycorrhizae can be dated to somewhat over 65 m.y. (see elsewhere).
Many species of fungi are involved in ECM associations. Basidiomycetes are frequent ECM associates, but Pezizales and other ascomycetes like the widespread Geococcum are also quite common and Zygomycota are also involved. Conservative estimates are 7,750 species of fungi (including Ericaceae but excluding Orchidaceae), 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 fungal richness. Pickles and Pither (2013) discuss the need to sample throughout the soil column for ECM fungi, but Anderson et al. (2013) found that mycelium frequency decreased with depth. 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).
Species of ECM fungi are often quite widespread, some tropical lowland ECM associations being as diverse as those in more temperate climates (Henkel et al. 2012: Dicymbe-Fabaceae; Brearley 2012: Dipterocarpaceae). However, 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). Indeed, there is in general 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, also sometimes VAM) found that phylogenetic relationships of the host had a strong effect on ECM richness and community composition (see also Pölme et al. 2013).
Other ECM variants include tuberculate mycorrhizae, clusters of roots surrounded by hyphae (Smith & Pfister 2009). Ericaceae also form mycorrhizal associations - ericoid mycorrhizae (ERM). 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; Clemmensen et al. 2014: ECM and ERM of different importance in forests of different ages; Talbot et al. 2008: VAM; Inselbacher et al. 2012). ECM fungi have few enzymes involved in lignin and cellulose breakdown, while ERM fungi may have quite a number of them (Kohler et al. 2015).
ECM/ERM seed plants are generally woody, although there are some herbaceous ECM taxa, particularly in Arctic-Alpine environments (e.g. Newsham et al. 2009). ECM help the plant acquire nitrogen and phosporus 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). The 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/ERM plants (Näsholm et al. 2013).
There is probably an evolutionary sequence, white rot fungi → brown rot fungi → ECM (e.g. Kohler et al. 2015), although too much should not be made of these decomposition types. Hibbett et al. (2000) suggested that white-rot fungi might also be derived from within ECM clades. White rot and brown rot fungi are both wood decomposers, utilizing the cellulose, but only the former, widely scattered through Agaricomycetes, can mineralize the lignin so removing it from the ecosystem (Eastwood et al. 2011; Floudas et al. 2012; Kohler et al. 2015). Development of ECM associations in Boletales, at least, may be favoured by low nitrogen and high organic material (= mostly lignin), ecological conditions that result from the activities of brown rot fungi. ECM fungi may also also be Boletales (and other groups: Eastwood et al. 2011; see also Floudas et al. 2012). ECM hyphae form a complete sheath investing the rootlets, the Hartig net, and hyphae penetrate between the exodermal/cortical cells; this sheath, not the root/root hair system, forms the interface between the plant and the soil (e.g. L. L. Taylor et al. 2009). Usually the Hartig net involves simply the outermost layer of cells, but sometimes, as in Pinaceae, the hyphae penetrate more deeply (Brundrett 2004). The fungal hyphae are septate and are not intracellular except in ERM, which lack a Hartig net. ECM in particular are not saprotrophic, i.e. they do not obtain their metabolic carbon from dead organic matter, rather, this comes from the plant (e.g. Michelsen et al. 1996; Jonasson & Michelsen 1996; Hashimoto et al. 2012; Lindahl & Tunlid 2014). ERM fungi may retain saprotrophic genes from their ancestors, unlike ECM fungi which have few enzymes involved in cellulose and lignin breakdown (Kohler et al. 2015). Interestingly, fungal isolates from ECM and ERM plants, and also from those with dark septate endophytes, sometimes more or less interdigitate on phylogenetic trees and show little phylogenetic divergence (e.g. Vrålstad et al. 2002; Walker et al. 2011; Perotto et al. 2012).
>ECM, ERM and VAM in general. ECM networks, as in Dicymbe forests in Guyana, can be complex, the network being established as the seed germinates (McGuire 2007b). A single species of plant can form more than one kind of mycorrhiza, and individual mycorrhizal fungi may form simultaneous associations with more than one plant, and quite commonly with more than one species of plant; the result is the formation of very complex mycorrhizal networks (e.g. Villareal-Ruiz et al. 2004; Simard & Durall 2004; Selosse et al. 2007b; Kennedy et al. 2012; van der Heijden et al. 2015 and references). 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 also occur on other angiosperms growing in the same area, and in particular as ECM on Pseudotsuga (Pinaceae) (Kennedy et al. 2012). There is similar lability in the ascomycete Rhizoscyphus ericae, often growing as an ERM on the hair roots of north temperate Ericaceae and as an ECM on Pinus in the same community (Grelet et al. 2010; see also Villarreal-Ruiz et al. 2004); the fungus also forms mycorrhizal associations with Jungermanniales-Schistochilaceae, leafy liverworts (Pressel et al. 2008). Salix may harbour ECM and/or VAM, not to mention dark septate endophytes (see below: e.g. Van der Heijden 2000; Becerra et al. 2009; see also Poole & Sylvia 1990; Molina et al. 1992 for VAM/ECM associations). ECM fungi in woodlands and savannas of Africa and Madagascar are relatively uniform, but 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). Liverwort gametophytes can form associations with fungi that are also ECM on the flowering plant on which the liverwort is epiphytic. Examples include Marchantia/mycorrhizal fungus/Podocarpus and the myco-heterotrophic chlorophyll-less liverwort Cryptothallus/the basidiomycete Tulasnella/Pinus-Betula (Read et al. 2000; Bidartondo et al. 2003; Kottke & Nebel 2005 and references).
Mycorrhizae 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). Other distinctive root morphologies like dauciform roots, roots appearing carrot-shaped because they are densely covered by long root hairs, are particular responses of the plant to nutrient-poor conditions (e.g. Schweiger et al. 1995; Playsted et al. 2006; Gao & Yang 2010).
Extant forests made up of VAM trees are overall more diverse than forests with ECM trees (Malloch et al. 1980; McGuire 2007a). There are rather few species of 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).
Overall, temperate and boreal areas have the highest ECM fungal diversity, and ECM-associated plants often dominate there (Wardle & Lindahl 2014; Tedersoo et al. 2014b). 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). VAM are found to 82o N while ECM and ERM are found to only 79o N, being limited by the ranges of their mostly woody hosts (Newsham et al. 2009). However, VAM fungal species 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, and this contrasted strongly with the diversity of other ecological groupings of fungi, although the disparity in terms of numbers of clones was somewhat less (D. L. Taylor et al. 2013). Overall, 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).
Associations between plant and fungus can be very close. In myco-heterotrophic associations the plants lack chlorophyll entirely and are nutritionally dependent on the activities of their associated fungi. Glomeromycotes are the associates in some myco-heterotrophic plants including the gametophytes of lycophytes and ferns to the sporophytes of some monocots, Gentianeae (Merckx et al. 2012). Myco-heterotrophic Ericaceae (and Orchidaceae) have modified ECM associations where the plant gets carbon indirectly from other angiosperms also associated with the fungus (e.g. Perotto et al. 2012).
3B. Endophytic Fungi. In addition to mycorrhizal associations, there are numbers of other non-parasitic (at least initially) fungi growing inside plants. These 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). Transmission is via the seed (vertical transmission). In other endophytes, transmission is usually via fungal spores (horizontal transmission) (Arnold 2008). 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). (The "fine endophytes" described as growing in the roots of some Arctic plants [Newsham et al. 2009] are considered to be VAM.)
All seed plants, but perhaps particularly Poaceae and Ericaceae (e.g. Petrini 1986, other papers in Fokkema & van den Heuvel 1986; Saikkonen et al. 2004), harbour endophytic fungi (Rodriguez et al. 2009; Hoffman & Arnold 2010; Friesen et al. 2011). The number of species of fungi involved is probably very large. 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. 2007). Most endophytes are Ascomycota, and a new order of ascomycete fungi, Phaemoniellales, has recently been described, initially being based on endophytes growing in the sapwood of Peruvian Hevea (K.-H. Chen et al. 2015; see also Gazis et al. 2012). Xylariaceae and Clavicipitaceae are notably common endophytic groups (Rogers 2000). However, Martin et al. (2015) found 118 basidioomycete taxa (from a mere 12% of all isolates, still no real handle on total diversity there!) in leaves and sapwood from 192 collections of two species of Hevea; many appear to be wood decaying white rot fungi (brown rot fungi are at most uncommon as endophytes), and some have very wide distributions.
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 facilitate stress tolerance in the host (Rodriguez & Redman 2008). 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). Beetles fed high-endophyte Merremia umbellata (Convolvulaceae) leaves seemed to do fine, but their chances of getting captured by predatory ants increased nine times (Hammer & Vanbael 2015). 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 (dark because of fungal melanin?) endophytes may facilitate the uptake of nitrogen (Newsham et al. 2009; Newsham 2011), while nitrogen has been found to move 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 (Behie et al. 2012). Ligninases have been detected in a number of ascomycetes endophytic in Uruguayan Myrtaceae (Bettucci & Tiscornia 2013), while subtstances synthesized by endophytic fungi in Carapa guianensis may be antibacterial, antiviral, or trypanocidal (Ferreira et al. 2015).
The life style of the immediate fungal relatives of endophytes are various. Endolichenic fungi, fungi living inside lichens (but not the mycobionts whose association with algae constitutes the lichen thallus), and endophytic fungi may be phylogenetically close, while lichenising and endophyte clades tend to be exclusive (Arnold et al. 2009b; U'Ren et al. 2012; K.-H. Chen et al. 2015). Grass endophytes (related to ergot, also ascomycetes) 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). In general, endophytic fungi are often more related to pathogens and other endophytes than to saprotrophic fungi (U'Ren et al. 2009) and they are sometimes derived from necrotrophic fungi, parasitic fungi that first kill the host cell before digesting it (Delaye et al. 2013; García-Guzmán & Heil 2013; see also K.-H. Chen et al. 2015). Sebacinales (basidiomycetes) are particularly diverse ecologically, and they are common endophytes (Weiß et al. 2009) as well as being involved in the distinctive modified ECM of Ericaceae and Orchidaceae. Trichoderma (Hypocreales, an ascomycete) also has different kinds of associations with plants, and endophytes may become saprotrophic or mycoparasitic on the death of the host plant (Chaverri & Samuels 2013; see also K.-H. Chen et al. 2015 and references).
3C. Further Complexities. 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; Kusari et al. 2012; 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 Archaeplastida dates to around 1.5 billion years ago (Wink 2008).
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 (Rogers 2000; Eaton et al. 2010 and references). 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. A single species or even plant may have a variety of associations with fungi, as mentioned above. 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. 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 fungal genome itself (Bianciotto et al. 2003; Hoffman & Arnold 2009). Numerous bacteria (mostly Proteobacteria) and a diversity of fungi have such relationships, although they sometimes seem rather casual (Hoffman & Arnold 2010). Bacteria can be integral to ECM associations, whether facilitating the establishment of the association (mycorrhiza helpers) or being 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).
Bacteria are other common endophytes. Obvious examples here are nitrogen-fixing bacteria (see the N-fixing clade), but a great 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 some 11,615 bacterial OTUs may be found on that island alone (Kembel et al. 2014: use of current phylogenetic ideas does not affect results - S. W. Kembel pers. comm. xi.2014) and also in the rhizosphere. Some of these bacteria are known to affect the growth of the plant, whether by fixing nitrogen, deterring pathogens, or the like (Kembel et al. 2014 for references), or, in the case of the rhizosphere, facilitating the uptake of organic nitrogen (J. F. White et al. 2015).
4. Angiosperm History I - Evolution in stem group angiosperms.
4A. Relationships. If crown-group angiosperms are 270 to 175 m.y.o. (e.g. Zeng et al. 2014), so certainly Jurassic, if not mid-Permian (see above), rather than Cretaceous in origin and only some 140-130 m.y.o., we have a series of problems. We may need to think about a different sets of gymnosperms/pteridosperms as being involved in the evolution of the angiosperm flower and we may need to rethink the ecological context of the evolution of angiosperms and of the insects associated with them. How angiosperms persisted as a presumably not very diverse clade for 50 m.y. or much, much more also becomes a question (Z. Wu et al. 2014). Of course, given the extensive variation in the divergence estimates of both plants and the animals associated with them, one can tell almost any story one wants.
That being said, the angiosperm stem group probably diverged from other seed plants by the late Palaeozoic (Moldowan et al. 1994; E. L. Taylor et al. 2006). So how might the heterosporangiate strobilus with short internodes that is the angiosperm flower have evolved from the separate male and female strobili of most gymnosperms, living or fossil? Is the flower a monoaxial structure, as in most cycad strobili, or is it polyaxial, as in a pine cone, or are the flowers of some groups of plants monoaxial and those of other groups polyaxial? The latter idea might suggest that that flowering plants are polyphyletic (Friis et al. 2011: pp. 141-144 for a summary of such ideas). Indeed, X. Wang and Wang (2010) and Z.-J. Liu and Wang (2015) have suggested that angiospermy may have arisen more than once.
Candidates for stem-group angiosperms include Corystospermales (Pteruchus, Ktalenia, etc.: Frohlich & Parker 2000), Bennettitales (especially common in the Jurassic), and Caytoniales (poorly known in the younger Mesozoic). In the much-discussed Caytonia the ovule is borne inside an inverted cupule, the cupule wall being equated with an outer integument - with interesting implications for pollination (e.g. Doyle 2006, 2008b; Doyle & Donoghue 1986a, b, 1992; Doyle & Endress 2010; Friis 2011). Other pteridosperm groups that have been linked with angiosperms include Pentoxylon and glossopterids, the latter a poorly known group in which ovules are borne on the leaf (Friis et al. 2011 for a summary), the diminutive Petriellales, and Peltaspermales (Taylor & Taylor 2009).
A phylogenetic association between Cycadeoids or Bennettitales, so-called "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 (the BEG group), and Caytonia may also be part of this group (Friis et al. 2007, 2009a: four new genera in this complex, 2013; 2011: especially useful, see chapter 5; Mendes et al. 2010). Bennettitales were especially common in the Jurassic, Erdmanithecales persisted into the Late Cretaceous, while Gnetales are still extant.
However, 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). Gnetales themselves are far from having a flower, although many morphological studies have associated then with the angiosperms, the anthophyte hypothesis (see elsewhere), although they may be best placed sister to or even inside Pinales (see below). Overall, the BEG clade seems to have little immediately to do with angiosperm origins.
The envelopment of the seed to produce a fruit-like structure is likely to have happened independently in the Bennettitales and angiosperms (Rothwell & Stockey 2010; see also Friis et al. 2011; Tomlinson 2012 and angio-ovuly). Pollen tubes in Pinaceae and in angiosperms probably evolved independently since at least some glossopterids had multiciliate male gametes (Nishida et al. 2004; c.f. Lee et al. 2011: cilia regained).
There are 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 found in a variety of habitats, so it is a little difficult to explain the absence of Jurassic angiosperm megafossils 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). Some of these angiosperm-like pollen types are associated with macrofossils, for instance, the late Triassic Sanmiguelia, although whether any can be linked to the angiosperm line is uncertain (c.f. Cornet 1986; Friis et al. 2011: pp. 158-162). If columellate pollen is ancestral in angiosperms, there may be connections with the Triassic reticular-columellar Crinopolles pollen type (Doyle 2001; Zavada 2007).
There are a series of reports of possible pre-Cretaceous angiosperms from China. X. Wang (2010a) described such plants, and he thought that carpels consisted of an axis (= placentae) subtended by bracts (= carpel walls: see also Guo et al. 2103; Liu & Ni 2013). The early to mid Jurassic Schmeissneria, previously placed in Ginkgoales, was considered to be angiospermous, having closed carpels (X. Wang et al. 2007; X. Wang 2009, 2010b; Z.-J. liu & Wang 2015 for discussion), while another mid-Jurassic fossil, Xingxueanthus, had closed carpels as well as a style, and (Wang & Wang 2010); these were stem-group angiosperms. Euanthus panii, also from the same locality, was described as having 5 sepals and petals, probably 5 tetrasporangiate stamens, a semisuperior ovary with quite a long hairy style, and ovules, although details of ovules and anther contents in particular are hard to make out (Z.-J. Liu & Wang 2015) and the authors were not sure whether these are fossils of stem- or crown-group angiosperms. All these identifications need confirmation.
Rudall and Bateman (2010) reasonably thought 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 fifty 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). Indeed, although the ovule-bearing structures of Caytonia can be linked with the carpels of extant angiosperms by invoking appropriate morphological gymnastics, 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) concluded that our understanding of the fossil record was insufficient to help much in understanding angiosperm origins. Taylor and Taylor (2009) reached much the same conclusion, and as they noted, timing is important - for instance, glossopterids are not known after the Permian-Triassic boundary, i.e. some 100 m.y. before the earliest angiosperms - at least, by some estimates.
Thinking about morphology and development together 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) had suggested that the heterosporangiate strobilus had 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 evolve, and 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 (see also Harrison et al. 2005b; Pires & Dolan 2012; Almeida et al. 2014).
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; see also above). Only morphology can allow us to infer what the immediate ancestors of crown-group angiosperms might be, yet morphological features can be difficult to detect in fossils, even if sampling of fossils can be quite extensive (e.g. Rudall et al. 2013). How credible are morphology-based trees of fossils?
Pollination & Seed Dispersal. Early seed plants are likely to have been wind pollinated. A number of gymnosperms, both living and extinct, have saccate pollen, and there is a general correlation between saccate pollen, erect cones, inverted or downwards-facing ovules, and the presence of a pollination droplet - although perhaps not in Cordaitales. The sacci are a device to help float the pollen onto the micropyle rather than to facilitate wind dispersal, and they may also reduce the settling velocity of the pollen, a low settling velocity being characteristic of pollen involved in wind pollination (Schwendemann et al. 2007; Bolinder et al. 2015; c.f. Hall & Walter 2011 in part). Saccate pollen has evolved more than once (e.g. Stützel & Röwekamp 1999b; Leslie 2008, 2010b).
Insects first appeared in the Middle Silurian (Misof et al. 2014: molecular dates to Late Devonian; Garrouste et al. 2012: fossils), and may well have pollinated some pre-Cretaceous gymnosperms; beetles, neuroptera, mecopterids (scorpion flies, Mecoptera, perhaps) and true flies (bee flies may be early Jurassic - see Wiegmann et al. 2011), thrips, as well as other groups were probably involved (Labandeira 1998, 2006, 2010; Grimaldi 1999; Labandeira et al. 2007; Ren et al. 2009; Peñalver et al. 2012), and crown-group ages of all thes clades are dated to the Carboniferous (Misof et al. 2014). Bennettitales flourished from the Triassic to the Cretaceous, and they had large, rather flower-like reproductive structures, in Cycadeoideaceae in particular producing both pollen and ovules, but details of their pollination are unclear (Friis et al. 2011).
Thrip-, beetle-, fly- and moth-pollination are all known in extant gymnosperms (Kato & Inoue 1994; Schneider et al. 2002; Oberprieler 2004; Labandeira 2005). There are a number of old but not very speciose clades of weevils (Curculionoidea) and leaf beetles (Chrysomeloidea) that are found on gymnosperms, including cycads, an association that has been dated to the Jurassic or earlier, and initial diversification of these insects may have been on gymnosperms in the Jurassic (e.g. Labandeira et al. 1994; Farrell 1998; McKenna et al. 2009), but this story may need to be rethought (Hunt 2007). Some species in all three extant genera of Gnetales (perhaps related to Bennettitales) are pollinated by insects, and features of fossil "ephedroid" pollen frequently fit the insect pollination syndrome, the pollen tending to clump (Bolinder et al. 2015).
Frame (2003) suggested that florivory by insects - extant angiosperms being for the most part notably palatable to insects - might have been the route by which angiosperm-pollinator relationships became established. See also below for possible pre-Cretaceous insect pollination of angiosperms.
Tomlinson (2012) discussed the difference between angio- and gymnospermy and angio- and gymno-ovuly, Robert Brown emphasizing the latter rather than the former. In extant gymnosperms unfertilised ovules are relatively large compared to the seed, since they keep on growing until the time of fertilization, which may be long after pollination. In angiosperms, however, ovules are small and the seeds are often relatively much larger. Angiosperm ovules can be aborted with little loss to the plant if pollination does not occur, but in gymnosperms the loss is more substantial (Haig & Westoby 1989).
Sims (2012) suggested that during the middle Mississippian to Pennsylvanian average seed size increased to about 8 mm3, a value that held largely steady until the evolution of flowering plants, when it decreased; cycads (large) and pines (small) are the two ends of the size spectrum in extant gymnosperms. Angiosperm seeds are very variable in size and range from 10-7 to 104 grams, i.e. smaller than megaspores to massively larger than them, while gymnosperm seeds, at 10-3 to 103 grams, are rather larger than those of the basal clades of extant angiopserms (Haig & Westoby 1991; Moles et al. 2005a). Seeds of Mesozoic seed plants are diverse morphologically (e.g. Anderson & Anderson 2004), and animal dispersal is likely to have been quite common (Friis et al. 2011). Lovisetto et al. (2012) discuss the evolution of fleshiness in disseminules of seed plants in general; similar genes are involved, even if the location of fleshiness may be very different morphologically.
Plant-Animal Interactions. For plant-arthropod associations, see Labandeira (2006), who noted that medullosan pteridosperms showed a particularly high level of herbivory in the Carboniferous compared to that of other plants of that time. Galls, often thought to have diversified along with early angiosperms, are known on Glossopteridales and Peltaspermales in particular from the Lower Permian (Schachat & Labandeira 2015). Lepidopteran diversification may have begun on Jurassic or even Late Triassic gymnosperms (Labandeira et al. 1997; Wahlberg et al. 2013), although this has been questioned (Grimaldi 1999; Grimaldi & Engel 2005).
5. Angiosperm History II: Cretaceous Origins.
5A. Introduction. In addition to the wide spread of dates suggested for crown group angiosperms (see above), there are 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 Caenozoic successors. As to events at the Cretaceous-Palaeocene (K/P) boundary, some suggest that these had a major effect only on North American plants, any more global effect being more muted, others suggest there were major global changes in vegetation structure and composition. Similar tensions are evident in the literature on the evolution of animals like mammals and insects.
Angiosperm diversification is often discussed in terms of the consequence of the evolution of flowers (and fruits), the diversity of flowers and fruits representing adaptations to pollination and fruit dispersal, ensuring reproductive isolation, etc.; flowers allowed greater speciation rates (e.g. Hickey & Doyle 1977; Niklas et al. 1983). This may well be true - floral differences are often involved in species barriers - and there are other important changes in the life cycle like increased efficiency in producing seeds and shorter gametophyte phase (see below), but there have also been 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, flowers and fruits that matter, but also what clades "do", their roles in the ecosystem, are very important in understanding angiosperm evolution (e.g. Bengtsson 1998).
Our understanding of the eco-physiological dimension of angiosperm evolution is improving fast (e.g. Feild & Arens 2007; Internat. J. Plant Sci. 173(6). 2012; etc.). Some of the differences between the leaves of early angiosperms and those of other vascular plants have long been evident (e.g. Hickey and Doyle 1977), these, and other vegetative changes, can be linked with changes in the rate of photosynthesis, nutrient cycling and acquisition, silicate breakdown and rock weathering, and the like (e.g. Knoll & James 1987; Volk 1989: emphasis on deciduous ecosystems; Sack & Scoffoni 2013; also below). But this is just the beginning. All metazoan organisms are some kind of metaorganism or chimaera (e.g. Herre et al 2005; Beerling 2005a; L. L. Taylor et al. 2009; Bragina et al. 2014). The interactions of plants with their fungal associates, whether ecto- or endomycorrhizal or various kinds of endophytes, the bacteria associated with them, and their effect on the weathering rocks, soil structure, carbon sequestration, and nutrient cycling are all part of the story. All these changes may have facilitated the spread of the l.t.r.f. habitat in which so much biotic diversity is now to be found, and they are also implicated in the long-term decline in atmospheric CO2 concentration that characterises the Caenozoic. Interactions of plants with their pollinators and seed dispersers have taken place in the context of this changing biosphere (see also Boyce et al. 2010; Marazzi & Sanderson 2010). In what follows, I initially focus on angiosperm evolution, but later I will attempt to integrate angiosperm diversification with that of some of their more important plant and animal associates.
5B. Early Cretaceous Evolution. 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. Atmospheric CO2 concentrations were about 1,600 p.p.m. around the Jurassic-Cretaceous boundary, possibly the highest concentrations since their decline in the late Devonian ca 360 m.y.a., but then they declined; oxygen concentrations were also high (Shi & Waterhouse 2010; He et al. 2012; Franks et al. 2013). CO2 concentrations were still high, perhaps 3,500-5,000 p.p.m. [check figures] in the early Cretaceous 135-100 m.y.a., since when they have declined, if with the odd hiccup (e.g. Beerling & Franks 2010). There may have been a particularly abrupt decrease in the middle of the Cretaceous (Feild et al. 2011b; Barclay et al. 2010).
The most comprehensive reviews of Cretaceous angiosperm history are those of Friis and collaborators, and this whole section draws heavily on Friis et al. (2011); see also Krassilov (1997), Dilcher (2010), Taylor (2010: focus on genes possibly involved), and Doyle and Upchurch (2014). 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.
The pollen of early angiosperms was more or less globose, monosulcate, with a continuous tectum, columellate infratectum, and thin endexine (e.g. Doyle 2005; Friis et al. 2011; see also Hughes 1994 and references). Fossil pollen from the Cretaceous Valanginian-Hauterivian 141-132 m.y.a. has been attributed to angiosperms, and their diversification 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 are magnoliid-type or somewhat monocot-like plants (e.g. Friis et al. 1997a, 1999, 2001, 2010a, 2011; Heimhofer et al. 2007 - see also Doyle et al. 2008 for an evaluation of early putatively monocot fossils). Doyle (2001) noted the abundance of fossils with ascidiate carpels and exotestal seeds in these floras - and in extant members of the ANITA grade and Chloranthaceae. Doyle and Endress (2010: note tree [Chloranthaceae [[magnoliids + monocots] eudicots]]]) and Friis et al. (2011) should be consulted for possible phylogenetic placements of a number of mostly magnoliid and ANITA-grade Cretaceous fossils.
Many older plant fossils have remarkable character combinations (e.g. Feild & Arens 2005; Fries et al. 2011 and references). For example, Archaefructus, probably an aquatic herb from 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 in their entirety (see also Z. Zhou et al. 2003; Friis et al. 2003b, 2011; Ji et al. 2004; Doyle & Endress 2007; Crepet et al. 2004 for analyses of this and other early fossil angiosperms). Whatever the interpretation, even if Archaefructus is sister to all extant angiosperms (Sun et al. 2001; Crepet et al. 2004), given that we don't know other plants from that part of the tree, the significance of this position is unclear. Recent morphological work suggests 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.
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, but see Z. Zhou 2014: eudicots). 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, and it is a relief to know that they are really.
Thinking about the morphology of extant magnoliids and ANITA grade angiosperms may help here. Distinguishing between perianth and prophylls and bracts can be difficult in these plants, there can be intermediates between perianth and stamens, the numbers of parts and their arrangement vary, embryo sac development varies, etc. (e.g. Buzgo et al. 2004; Taylor et al. 2008; Endress 2008a; Doyle & Endress 2011; Abercrombie et al. 2011). Taxa in which DEF-like and GLO-like proteins can form homodimers predominate in the ANITA grade and magnoliids (DEF-like proteins cannot do this above the latter node, and GLO-like proteins in eudicots); heterodimers are formed throughout flowering plants, although the situation in gymosperms is less clear (Melzer et al. 2014). This ability to form both homo- and heterodimers may contribute to the diversity of floral morphologies in these basal clades (Melzer et al. 2014), and perhaps in their extinct relatives. Chanderbali et al. (2009, esp. 2010 and references), promoted a fading borders/sliding boundaries model of floral evolution (see also Thiessen & Melzer 2007). 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). Such factors may contribute to the the difficulty in assigning early angiosperm fossils to extant clades.
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), however, 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) while 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 fossils assignable to Chloranthaceae from the late Barremian ca 130 m.y.a. onwards, some being very like extant Hedyosmum (e.g. Crepet & Nixon 1996; Friis et al. 2006b, 2011). Magnoliids diversified somewhat later for the most part as did Lauraceae (Friis et al. 1997a, 2006b for reviews). 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. For a critical re-evaluation of the North American Potomac floras, large Aptian to Albian in age (125-100 m.y.o.), see Doyle and Upchurch (2014).
The flowers of early angiosperms are rather generalized and small to very small, quite often less than 1 mm across - there are very small fossil waterlilies, very small Hedyosmum-like flowers (Chloranthaceae), etc. (see e.g. Crane et al. 1995; Doyle & Donoghue 1986a; Friis & Crepet 1987; Friis & Endress 1990; Friis et al. 2000, 2006b, 2010b, 2011; Endress 2001a; Weberling 2007; Doyle 2008b; Doyle & Endress 2000, 2010, 2011). The stamens are often wedge-shaped, with a massive apex, stout filaments and connectives, and anthers opening by laterally-hinged valves (e.g. Crepet & Nixon 1996; Endress 2008c and references; Endress 2011a) - although perhaps not in the earliest angiosperms. Styles were at most short, and dry stigmas and protogyny were probably the common conditions (e.g. Sage et al. 2009; Endress 2010a). There was often only a single carpel per ovule, perhaps the ancestral state for angiosperms (e.g. Doyle 2012), the stamens produced only a few pollen grains, and there is no evidence of nectaries (e.g. Crepet et al. 1991; Dilcher 2000; Friis et al. 2006b, 2011). However, quite "derived" features are early apparent. Thus Sinocarpus, from the Barremian-Aptian 139-122 m.y.a., had carpels that were apparently connate at the base (Leng & Friis 2003), and flowers with inferior ovaries were surprisingly common early on (e.g. Crane et al. 1995; Friis et al. 1999, 2011).
As to what pollinated early angiosperms, little is known. Their tiny flowers were probably aggregated into inflorescences to attract pollinators (Friis et al. 2006b, 2011), but how pollinators handled these flowers is unknown, although extant members of early-branching clades of Lepidoptera (monotrysian "microlepidoptera"), at least, are usually very small. Insect pollination is likely (Hu et al. 2008), although Hu et al. (2012 and references) suggest that pollination may have been by both insects and wind, ambophily (see also Friis et al. 2011). B. Wang et al. (2013) reviewed the possible role of beetles in the pollination of early angiosperms, noting that potential pollinators such as Scarabaeoidea and Chrysomeloidea had evolved by or at the early Cretaceous. Labandeira (2010 and references) suggested that many pollinating clades of Hymenoptera, Diptera, and Lepidoptera originated around Late the Barremian/end Albian some 125-100 m.y.a., and although Misof et al. (2014: p. 767) note, "we dated the spectacular diversifications within Hymenoptera, Diptera and Lepidoptera to the early Cretaceous, contemporary with the radiation of flowering plants", the connections between insects and plants then are unclear. Pollination in early angiosperms may have occurred during florivory, angiosperms being notably palatable to insects (Frame 2003).
Pollen was initially produced in rather low quantities, but it is found in insect coprolites and may have been eaten by the pollinator (Friis et al. 1999); the paucity of dispersed pollen morphs and the diversity of pollen morphs associated with plant remains also suggest some kind of insect pollination (Friis et al. 1999). There is no signal from fossil pollen that unambiguously suggests particular pollinators, and although pollen size and style length are correlated in a general way, there are no plots of pollen size over time (Roulston et al. 2000). Bees are unlikely to have pollinated early flowers, and certainly, their diversity then was low (e.g. Grimaldi & Engel 2005). Pollenkitt, produced by tapetal degeneration and rich in plastid-derived lipids that are used by bees, helps pollen grains stick together and to the pollinator, although the pollen of cycads, for example, may clump in the absence of pollenkit (e.g. Hall & Walter 2011; Bolinder et al. 2015); pollen of early flowers is not often clumped (Doyle et al. 1975; Hu et al. 2008).
Nectar is unlikely to have been a common reward. Septal nectaries may be an apomorphy for monocots, being scattered throughout that clade and found in some Alismatales (not in Araceae); they may have appeared by 120 m.y.a. or earlier. Many Laurales have paired glandular bodies at the base of the stamens that may provide some reward to the pollinator, and the clade with these nectaries is dated to around 127-89 m.y.a. (see Laurales). "Food bodies" have been reported in 115-100 million year old flowers from Lower Cretaceous Burmese amber, i.e. towards the end of this period (Santiago-Blay et al. 2005). On the other hand, Ren (1998) though that brachyceran diptera were involved in the pollination of early angiosperms. A number of these flies are known from the late Jurassic and early Cretaceous (Ren 1998; c.f. Z. Zhou et al. 2003 for dates). They can have quite long probosces over 5 mm long "especially suitable for visiting long tubular flowers" (Ren 1998: p. 86) and visited flowers for nectar, he thought. Given both the age and the size of these brachyceran flies, it is unclear what they might have been doing; there is no real evidence that they were pollinating then.
A diversity of insect groups visit the flowers of extant basal angiosperms (Thien et al. 2000). 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. Thermogenic (beetle) pollination occurs in some extant members of many "basal" lineages, including the ANITA grade and some magnoliid angiosperms, Araceae, etc., although it is not known from most Laurales, Amborella, or Acorus (Thien et al. 2000; Seymour et al. 2003; Seymour 2010); beetles are attracted to haplomorphic flowers lacking definite symmetry signals (Leppik 1957). Of course, other factors such as scent are also involved.
The seeds of early angiosperms were mostly dry and rather small compared with those of both extant gymnosperms and angiosperms (Tiffney 1986a; Eriksson et al. 2000a, esp. b, also Haig & Westoby 1991; Moles et al. 2005a; Linkies et al. 2010); Eriksson et al. (2000b) estimate an average volume of less than 1 mm3 for seeds in the Famalicão flora. A small size is perhaps to be expected since plant and seed size are quite strongly linked (e.g. Harper et al. 1980; Eriksson et al. 2000b; Moles et al. 2005b) and these early angiosperms were not large plants. In another study, seed size was estimated to be 2-3 mm3; seed contents were probably mostly endosperm, and given the small to minute size of the embryo with respect to the endosperm, a period of morphological dormancy was likely before a plantlet developed and germination could occur (Forbis et al. 2002; Linkies et al. 2010). Seeds of extant members of the ANITA grade are mostly notably smaller than those of extant gymnosperms (e.g. Moles et al. 2005a), and the embryo is small.
Dispersal of disseminules of many early plants likely to have been by wind (Wing & Boucher 1998). However, in a sample of some 100 taxa from the Barremian-Aptian (132-112 m.y.a.), ca 25% were probably fleshy and animal dispersed (Eriksson et al. 2000b; c.f. Tiffney 1984). The fruits were small and mostly single seeded, although they may have been aggregated (see Eriksson et al. 2000b; Eriksson 2008; Dilcher 2010, in part; Sussman et al. 2013). It is unclear what animals ate these fruits. Eriksson et al. (2000b) suggest reptiles and multituberculate mammals, and perhaps other mammals and birds, but the dentition of multituberculates from that period does not suggest herbivory (Wilson et al. 2012), while many early birds are likely to have been carnivorous and/or aquatic (Jarvis et al. 2014) although gut contents with seeds have on occasion been recovered.
Growth rates of early angiosperms may have been high and reproduction rapid compared with gymnosperms (Doyle & Hickey 1976; Bond 1989; Wing & Boucher 1998; Verdú 2002), The reproductive cycle was relatively short, with a short time between pollination and fertilization (see below), seeds were small, 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; Abercrombie et al. 2011).
Vegetative changes have been very important in angiosperm evolution. Angiosperm leaves are very different from those of most other vascular plants (Hickey & Doyle 1977). Fossils show more regular venation in several orders developing, teeth were early evident, and compound leaves became more common. The ecological consequences of such changes in the later Cretaceous in particular are discussed elsewhere.
Tricolpate pollen, the signature of eudicots, is 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). Monocot pollen 120-110 m.y.o. 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 monocots are largely herbaceous and may have fossilized less well.
Whatever habitats the very first angiosperms prefered, there is a consensus that they were soon components of disturbed, well lit or open and mesic communities (e.g. Doyle & Hickey 1976; Hickey & Doyle 1977; Tiffney 1984; Eriksson et al. 2000b; Heimhofer et al. 2005; Bond & Scott 2010; Boyce et al. 2010), and mention of flood-plain, swamp and riparian habitats is common (see also Wing & Boucher 1998; Coiffard et al. 2008, 2012) - Aethophyllum, a small (but hardly herbaceous), fast-growing conifer (?Voltziales), had occupied similar habitats in the lower middle Triassic (Rothwell et al. 2000). However, how fast nutrient turnover in the litter of these angiosperms might be is debatale (Berendse & Scheffer 2009; Royer et al. 2010; c.f. G. Liu et al. 2014). In the Portugese Late Barremian-Aptian 124-112 m.y.a. climate and environment were unstable, which might favour angiosperms adapted to disturbed habitats (Heimhofer et al. 2005).
Arguing by analogy with extant angiosperms, early angiosperms may have been fairly small (Friis et al. 2010b) tropical trees with sympodial growth that tolerated shady, humid and disturbed ("dark and disturbed") conditions (e.g. Feild 2005; Feild & Arens 2005, 2007; Coiffard et al. 2006; Berendse & Scheffer 2009 for a summary). Leaves of plants growing in such conditions are likely to have had relatively low venation density (e.g. de Boer et al. 2012), and a vascular system with vessels, etc., is not likely to have been at a premium. Later angiosperms moved into more open conditions (e.g. Feild & Arens 2007; Bond & Scott 2010). There are also 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, see also 2011: pp. 46-47).
Coiffard et al. (2012) perhaps inadvertently give the impression that around 130-125 m.y.a. angiosperms were largely a clade of aquatics, noting that 5/11 genera that grew in the first stage of the rise to dominance of angiosperms "competed with charophytes" (p. 20955). They did not say that the ancestral angiosperm was aquatic, but Goremykin et al. (2012) do think that this is likely. Early herbaceous nymphaealean-type plants are indeed likely to have grown in aquatic or marsh-like habitats (G. Sun et al. et al. 2008, see also Friis et al. 1999, 2011). (Whether Nymphaeales are sister to Amborellaceae or not will have little effect on ancestral reconstructions of habitat preferences). But how woody the early angiosperms were is unclear. Seed size of the 132-112 m.y.o. Famalicão flora is similar to that modern, tree-dominated floras, but Eriksson et al. (2000b) thought the plants were herbaceous or shrubby (see also Hickey & Doyle 1977). 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). Philippe et al. (2008) suggested that earliest angiosperms might have had cambium, but its wood lacked thick-walled fibres and in general cell walls were thin (see also Amborella). Others have suggested that the angiosperm progenitor was a "diminutive, rhizomatous to scrambling herb" (Taylor & Hickey 1992: p. 137, c.f. the palaeoherb hypothesis). However, both very xeromorphic and aquatic plants are likely to be derived; loss of cambial activity in aquatics may be difficult to reverse (). In any event, early climatic niche (habitat) evolution is likely to have been slow (Smith & Beaulieu 2009).
5C. Later Cretaceous Evolution. The Late Cretaceous began ca 99.6 m.y.a. with the Cenomanian, but I also include the period from 110-80 m.y.a., basically beginning in the Albian, that encompasses the so-called Cretaceous Terrestrial Revolution (KTR: Lloyd et al. 2008; Benton 2010; Meredith et al. 2011). The sea was initially about one hundred and fifty meters above its present level. 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: Coiffard et al. 2007, 2007).
During this period major changes in the terrestrial vegetation continued (e.g. Crepet 2008; Coiffard & Gomez 2011; Coiffard et al. 2012). Angiosperms continued to spread latitudinally from the more tropical areas they initially inhabited (Axelrod 1959; Hickey & Doyle 1977; Wing & Boucher 1998; Hemihofer et al. 2005 for further references). Some low latitude floras were dominated by angiosperms even in the Cenomanian-Turonian ca 94 m.y.a. (Coiffard et al. 2012 for references). Mid-latitude floras were also changing considerably, large trees first appearing in the fossil record in the Middle to Late Albian less than 110 m.y.a., and fossil woods became notably more common (Philippe et al. 2008; Wheeler & Lehman 2009). There were a significant number of eudicots in mid-latitude North America in the Albian-Turonian, ca 100 m.y.a., and again they appeared slightly earlier at lower latitudes, S of palaeolatitude 30o N (e.g. Crane & Lidgard 1989, 2000; Lupia et al. 1999). Platanoid fossils were found along river channels ca 110 m.y.a. in the Late Albian of northern Alaska (Spicer & Herman 2010; Pott et al. 2012 and references), and angiosperm abundance increased there, although diversity in the high Arctic was low and there was at most little endemism (Spicer & Herman 2010).
Fossils from the Aptian/Albian ca 112 m.y.a. still had odd assemblages of characters (see also Friis et al. 1995), but fossils referable to extant angiosperm families begin to appear in east North America around 115-90 m.y.a., and by some 85 m.y.a. their diversity had increased considerably (Crane & Herendeen 1996; also Lidgard & Crane 1988; Friis & Crepet 1987; Friis & Endress 1990; Crepet et al. 2004, etc.). Many major euasterid, rosid and monocot clades seem 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 Saxifragales (ovary inferior, crowned by a nectary, styles more or less separate, i.e. they look very like the old woody Saxifragaceae) were especially common, as were ericalean flowers with a variety of morphologies (Friis et al. 2006b, 2011). Indeed, Saxifragales, although now not very speciose, may represent an ancient and rapid radiation (Fishbein et al. 2001; Fishbein & Soltis 2004; Jian et al. 2008). Groups like Laurales had become common by around 112 m.y.a. (Doyle & Upchurch 2014).
Diversification in Pentapetalae, with their "typical dicot" flowers, was probably underway by (121-)115-109(-101) m.y.a. (molecular estimates), and their distinctive tricolporate pollen suggests that they may have been around since the Albian 125-112 m.y. ago. Thus Magallón et al. (2015) date this clade to around 123.7 m.y. ago. 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). Initial malpighialean diversification was rapid, and relationships have been hard to disentangle (Wurdack & Davis 2009; but c.f. Xi et al. 2012).The origins of several clades within Malpighiales and Ericales that 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). Crown group Menispermaceae, prominent lianes in current l.t.r.f., are dated to around 109.1-106.3 m.y.o. (W. Wang et al. 2012); l.t.r.f. is probably its ancestral habitat (W. Wang et al. 2012). Burnham (2009) noted that there were few lianes through most of of the Mesozoic, but liane woods from the Cretaceous-Palaeogene were dominated by Menispermaceae (Smith et al. 2013).
Nectar is a major pollinator reward in extant angiosperms. With the diversification in Pentapetalae nectar produced by receptacular nectaries is likely to have become a common 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. A flower, the Rose Creek fossil from the earliest Cenomanian some 99 m.y.a., is the earliest known pentapetalan fossil, although not identifiable to an extant family, and it has a nectary (Basinger & Dilcher 1984). 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). Nectaries are conspicuous in floral diagrams of Late Cretaceous flowers in particular (Friis et al. 2011: fig. 16.6, 17.10). However, as mentioned above, nectaries may have appeared earlier, and extant angiosperms other than monocots and eudicots have quite a diversity of nectaries. By the mid-Cretaceous pollen was more abundant and is quite often found in clumps, suggesting that pollenkitt had evolved and that pollinators were becoming more specialized (Hu et al. 2008; Leslie & Boyce 2012). Citerne et al. (2010) thought that 93.5-89 m.y.a. in the Turonian was a period of floral innovation and evolution of pollinators.
At ca 2.5 cm across, the Rose Creek flower is relatively large compared to the flowers of other Cretaceous angiosperms, it has five stamens that are somewhat unexpectedly opposite the petals and styluli that are shorter than the ovary. Flowers from this period commonly have spreading petals and stamens with the anthers distinct from the filaments and short styluli or single styles; they are still mostly quite small, although there are a few quite large flowers, mostly terminal in position (Friis et al. 2011). Rather suprisingly, ca 50% of end-Cretaceous mesofossil flowers had inferior ovaries, a higher proportion than in the present flora (Crepet & Friis 1987; Friis et al. 2011: fig. 16.8). Sympetaly (Actinocalyx bohrii had flowers ca 3 mm long with connate petals) and monosymmetry (evidence for the latter is indirect, seeds and other fossils 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).
Seeds/diaspores in the later Cretaceous remained small (Tiffney 1984, 1986b), although a gradual increase in size was evident (Eriksson et al. 2000a). Although Tiffney (1984, 1986a, b) thought that abiotic dispersal was prevalent, Eriksson et al. (2000a) noted that biotic dispersal was probably appreciable. For Tiffney, ants, fish, reptiles and archaic mammals were possible dispersers, but not birds, for Eriksson et al. birds and mammals (multituberculates) were likely candidates. Eriksson et al. (2000a) distinguished between the "disperser" and "recruitment" hypotheses for changes in fruit size; in the former, the evolution of animals that could handle large fruits drove the evolution of plants with large diaspores, while in the latter the increasing size of angiosperms was associated with larger seeds/diaspores that were initially dispersed by rather generalist dispersers, only later did more specialist frugivores evolve. Eriksson et al. (2000a, see also Moles et al. 2005a; c.f. Tiffney 1984) incline to the latter hypothesis, and from what is known about mammal and bird evolution (see below), this seems most likely.
Around 108-94 m.y.a. (Late Albian), and again at the end of the Cretaceous, the venation density of angiosperms increased and became markedly greater than that of non-flowering plants and ANITA-grade angiosperms (Feild et al. 2011b; c.f. Bond & Scott 2010 in part), and l.t.r.f. of sorts may have begum to spread, see below. 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 in 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 quite high even close to the Arctic Circle (Hofmann et al. 2011; see Spicer & Herman 2010 for the high Arctic), and angiosperms may have achieved at least some measure of ecological dominance (Friis et al. 2006b). Towards the end of the Cretaceous there were changes in atmospheric CO2 concentration, etc., and some taxa in the Aquilapollenites flora went extinct, perhaps because of the loss of their pollinators (Spicer & Collinson 2014). Similarly, floristic changes and the demise of the dinosaurs in India are Late Cretaceous (Samant & Mohabey 2014).
Eudicots 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 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). The deciduous habit was relatively common in these flood plain habitats (Wolfe 1987). 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, pollen of free sporing plants dropping from 80% to 45% over the same period. However, not all fern families behaved the same, and there are differences between Australia and North America (Nagalingum et al. 2002). There was an end-Cretaceous rise to dominance of angiosperms in Patagonia (Iglesias et al. 2011).
In the Late Cenomanian/Early Turonian ca 93.5 m.y.a. there were four main pollen provinces. The tropical province was dominated by pollen that may have come from Areccaceae,, while plants with distinctive pollen assignable to the Normapolles complex and comparable with that of some extant Fagales, an order that is largely ectomycorrhizal (ECM), were both diverse and ecologically prominent in rocks from east North America to western Asia; interestingly, fossil flowers with such pollen are usually perfect, while flowers of extant Normapolles Fagales are generally imperfect. 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, 2011). Given that Pinaceae, also ECM, were also part of the vegetational mix then, it suggests that ECM plants were a notable component of the vegetation, at least locally, and this may have implications for carbon sequestration (see also below). The tropical zone between these two pollen floras was characterised by palm pollen, but conditions may commonly have been dry (Burnham & Johnson 2004).
Extant Normapolles plants and Nothofagaceae are trees, although some are shrubs. Trends like increasing seed size were already evident about 85-75 m.y.a., probably reflecting the increasing size of angiosperm plants (e.g. Eriksson et al. 2000a; Moles et al. 2005a, b), and fleshy fruits had appeared in monocots 120 m.y.a., perhaps reflecting closing of the canopy (see also Dunn et al. 2007). 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 diameter, may have produced Normapolles pollen (Lehman & Wheeler 2001), so a diverse forest might not be expected, however, identifications suggested for these woods rarely include Fagales (Wheeler & Lehman 2009). Trees up to 2 m in diameter have been found in Late-Cretaceous riparian swamps (Parrott et al. 2013).
By ca 80 m.y.a. angiosperms had come to make up ca 40% of both floristic diversity and abundance even at higher latitudes (e.g. Axelrod 1959; Crane & Lidgard 1989; Lupia et al. 1999; see also Nagalingum et al. 2002), with monocots and magnoliids predominating in the area 50oN and 20oS.
The Late Cretaceous may have been the "dawn of modern angiosperm forests" (Coiffard & Gomez 2011: p. 164; also Coiffard et al. 2012), but their Turonian forests of ca 90 m.y.a. still grew primarily in disturbed and/or riparian-type habitats (see also Jud & Wing 2013; Spicer & Herman 2010: Late Cretaceous in northern Alaska; Miller 2013: 105 m.y.a. Albian); Platanaceae, found along channel margins in the Cenomanian, had spread onto flood plains in the Turonian. Until the Mid or even Late Cretaceous angiosperms were mostly small herbs to small trees of the understory growing in dryish conditions (Bond & Scott 2010), perhaps rather weedy plants (Feild et al. 2011b). 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). Royer et al (2010) estimated the SLA of fossil angiosperms 110-105 m.y.a. was low, implying fast nutrient turnover (see also Berendse & Scheffer 2009), however, most extant magnoliids show a "slow" leaf spectrum with a higher SLA, etc. (G. Liu et al. 2014).
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; He et al. 2012; Bond & Midgley 2012); Cretaceous mesofossils are often charcoalified (Friis et al. 2011). Berner (2003) noted that rocks rich in charcoal derived from plants are particularly prominent in the mid Cretaceous 120-90 m.y.a. to the Palaeocene, and fires may have been encouraged by the relatively high atmospheric oxygen concentrations of 21-25% then (Brown et al. 2012). Substantial amounts of inertinite, charcoal from fires in mire systems, are found through the Cretaceous, but less since (Scott & Glasspool 2006). Fires were unable to burn closed angiosperm forests when these finally developed (Bond & Midgley 2012). Frequent fires were likely to have been accompanied by increased runoff/erosion and loss of phosphorus to the ocean (S. Brown et al. 2013), while nitrogen is lost by volatilization (Forrestal et al. 2014 and references).
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). 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). After 100 m.y.a. there was little change in pteridophyte diversity or a moderate decrease, the beginnings of a decrease in gymnosperm and cyccad diversity, and a dramatic increase in angiosperm diversity (Niklas et al. 1983; S. Brown et al. 2012).
Although Strömberg et al. (2013a) suggested that in the Late Cretaceous (ca 73 m.y.a.: Wyoming) angiosperms were not notably abundant compared with other co-occurring vascular plants, she noted that they did vary considerably in niche optimum and niche breadth. (Similarly, non-polypodiaceous ferns dominated Late Campanian (73 m.y.a.) 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, and Wing and Boucher (1998: p. 379) concluded that diversification of flowering plants then was "the evolution of a highly speciose clade of weeds but not necessarily a major change in global vegetation", while Eriksson et al. (2000a) suggest that Late Cretaceous vegetation was open, rather dry (leaf size was relatively small - Upchurch & Wolf 1987), and disturbed by herbivores such as herds of large dinosaurs. In the New World there is no evidence for l.t.r.f. in the Cretaceous (Burnham & Johnson 2004), however, there may have been l.t.r.f.-like forests in the increasingly moist climates that were developing then (see also Schönenberger 2005; Wing et al. 2012; etc.).
5D. Venation Density, Stomatal Size, and Vascular Evolution. Atmospheric CO2 concentration gradually declined from the late Jurassic-early Cretaceous to the later Oligocene ca 40 m.y.a., bottoming out in the Pleistocene (Shi & Waterhouse 2010; Franks et al. 2013). This provides the background for thinking about changes in CO2 uptake and water loss, both associated with increased photosynthetic efficiency. A combination of features unique to many, but not all, angiosperms - xylem dominated by vessels, high venation density, precise positioning of the veins in the blade, and dense, small stomata - allowed productivity to increase and more carbon to be sequestered (e.g. Boyce & Zwieniecki 2012; Zwieniecki & Boyce 2014).
The ecological context for the evolution of venation density and vasculature can perhaps be provided by living members of the ANITA grade (Feild 2005; Feild & Arens 2005), other than the aquatic Nymphaeales; Doyle and Upchurch (2014) also noted the similarity between leaves of early angiosperms and those of the ANITA grade. Vessels in magnoliids and ANITA-grade angiosperms, so-called "basal vessels", are rather different from those in core eudicots, and water conductivity was not high (Hacke et al. 2007; Sperry et al. 2007). Venation density of the leaves is low, and spacing of the veins is suboptimal (Zwieniecki & Boyce 2015), as in non-angiosperm vascular plants. Ancestral angiosperms are likely to have had low drought tolerance (Feild et al. 2011a, c); their leaves 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).
Venation. Most extant angiosperms have distinctive hierarchical-reticulate and very dense venation. However, during the 200+ million years prior to the diversification of flowering plants, the venation density of the leaves of vascular plants had held largely constant at below ca 3 mm/mm2, and this despite considerable fluctuations in atmospheric carbon dioxide concentrations (e.g. Boyce et al. 2010; Lee & Boyce 2010; Boyce & Zwieniecki 2012; Boyce & Leslie 2012 for a summary). Venation density in non-flowering plants held steady through the Cretaceous (Feild et al. 2011b).
Extant members of the ANITA grade, Chloranthaceae, shade tolerant and succulent plants, etc., and also fossils from the first ca 30 m.y. of the angiosperm record have similar low venation densities of around 2.4 mm/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). In the pre-Albian before ca 113 m.y.a. about half the fossils still had leaf blades with a low venation density ca 3 mm/mm2 (e.g. Feild et al. 2011b; Boyce & Zwieniecki 2012). However, the venation density of many angiosperms doubled at around 108-94 million years ago, a change occurring independently in monocots, magnoliids and eudicots (Boyce et al. 2009; Feild et al. 2011b), and the veins became much more ordered hierarchical-reticulate. This density increase greatly reduced the main element in the resistance to water flow through the plant, that is, its passage through the mesophyll (Sack & Holbrook 2006; Sack & Scoffoni 2013). When venation density surpassed 6 mm/mm2 the path length for water transport inside the leaf (from vein to stomatal pore) equalled and then became shorter than the internal diffusion path of CO2 (from stomatal pore to chloroplast), ans stomata could become small and dense, facilitating the movement of CO2 into the leaf despite its falling atmospheric concentrations (e.g. de Boer et al. 2012).
The venation density of angiosperm leaves increased again around the Campanian-Maastrichtian boundary ca 70 m.y.a., and plants whose leaf blades had a venation density of ca 3 mm/mm2 were then a mere 4% of the total (Brodribb & Feild 2009; Feild et al. 2011b; Boyce & Zwieniecki 2012). Only after this did tropical forests assume a more "modern" physiology, and only then did trees have a venation density around 10 mm/mm2 or more like to that of plants in the most productive l.t.r.f. today (Brodribb & Feild 2009; Feild et al. 2011a, b). Furthermore, angiosperms alone have leaves in which veins are the same distance from each other as from the lower surface of the leaf, an arrangement found even in shade angiosperms, perhaps because they maximize photosynthesis in sunflecks (c.f. monilophytes); this allows optimal uniform delivery of water to the stomata (Zwieniecki & Boyce 2014). Both these sets of changes seem to have occurred independently in monocots, magnoliids and eudicots
Venation density increase was accompanied by a decrease in stomatal size and an increase in stomatal density, which together increased stomatal gas exchange capacity. For any given stomatal area, smaller stomata allow more water to be lost, but, importantly, more CO2 to be taken up; pore depth is shallower in small than in large stomata (Franks & Beerling 2009a; de Boer et al. 2012: Fick's and Stefan's laws are relevant here). Overall, carbon assimilation per unit water loss increased (e.g. Franks & Beerling 2009; Haworth et al. 2011; de Boer et al. 2012; Franks et al. 2012). Water could be supplied to the leaf by the efficient vascular system even if humidity decreased, whether because of drying climates or the emergence of the tree into the canopy (e.g. de Boer et al. 2012; see also Boyce & Zwieniecki 2012). Small stomata also have a faster relative response time than large stomata as do grass stomata compared with those from other vascular plants (Franks & Farquhar 2006; Franks & Beerling 2009a), however, little is known about the stomatal size/response time connection (Raven 2014). Details of guard cell shape are also important (Hetherington & Woodward 2003), and the great range of relative stomatal pore area (pore area/guard cell + pore area) in vascular plants as a whole, but even when comparing Tradescantia with Triticum, is also pertinent (Franks & Farquhar 2006), although there seems to be little information about this. Drake et al. (2013) compared five species of Banksia and found that leaves with smaller stomata indeed had a higher rate of gas exchange, maximum operating stomatal conductance, and overall high productivity. Trees have small, dense stomata when compared with shrubs and herbs (Beaulieu et al. 2008: n = 101). Small stomata may also allow areas of the epidermis to be freed up for other functions (Franks & Beerling 2009a), although this seems somewhat notional.
Increased vein density comes at a cost of increased carbon allocation to the veins, partly offset by vein tapering (McKown et al. 2010; Beerling & Franks 2010). The veinlets allowed an easy flow of water into the mesophyll, their proto- and metaxylem having vessels with simple perforation plates (Feild & Brodribb 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). 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 earlier (Brodribb & Holbrook 2004; see also Haworth et al. 2011, 2013 for stomatal opening in land plants). Increased transpiration resulting from increased stomatal conductance will promote evaporative leaf cooling (Hetherington & Woodward 2003; Boyce & Lee 2010), perhaps particularly important at times like the Palaeocene-Eocene Thermal Maximum (see below) 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; maps at the end of Willis & McElwain 2014). However, the increased transpiration from angiosperm leaves may have helped to drive the spread of l.t.r.f. with reliably high rainfall (e.g. Boyce et al. 2008, 2009, 2010), conditions of the Late Cretaceous becoming more humid (Eriksson et al. 2000a). 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; see also Feild et al. 2011b; Boyce & Leslie 2012; Feild & Brodribb 2013). There was less change in the extent of rain forest in other parts of the tropics in such simulations, but this might have been different under conditions earlier in the Caenozoic; large areas of continental Africa had not yet become elevated, continents were in different positions, etc. (Boyce et al. 2010).
Vascular Anatomy. Vessels in ANITA-grade plants are short, not very dense, with scalariform perforations, little difference between the pitting of the end and lateral walls, incomplete break-down of the pit membranes, and intertracheidal pit resistance lower than that of intervessel pits, etc. (Hacke et al. 2007; Sperry et al. 2007). The resistance to water flow of the scalariform perforation plates in such xylem is higher than had been estimated (e.g. Christman & Sperry 2010), and even if individual vessels may be more effective in transmitting water than individual tracheids, when comparing xylem cross-sectional area plants with such vessels may have a hydraulic efficiency little different from that of tracheid-bearing gymnosperms (Sperry et al. 2006; Feild & Holbrook 2001; Hudson et al. 2010).
Tracheids in Pinales in particular 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 air bubbles developing in the cells during embolism, 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). Some palaeozoic medullosan seed ferns, especially taxa like Medullosa, had long, wide tracheids that probably had high water conductivities like those of some angiosperms vessels (J. P. Wilson & Knoll 2010), and ferns in general have wide and long tracheids with surprisingly high transport rates (Pittermann et al. 2011).
The acquisition of vessels cannot be interpreted as a single key innovation, and their evolution was likely a rather protracted process (Feild & Arens 2007; Feild & Wilson 2012). They may have been of functional value initially because heteroxylic wood, i.e. wood with vessels and tracheids, 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 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). Wood with scalariform perforation plates was particularly common in the Cretaceous (Wheeler & Baas 1993), but as they 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 functional interpretation is not easy. 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).
Eventually wide vessel elements with simple perforations, the vessels themselves being well over 10 cm long, became an integral part of an efficient water transport system. However, vessel elements with long, oblique, many-barred scalariform perforation plates occur throught the angiosperm phylogeny, for instance, in the common ancestor of euasterids.
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. 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 Icacinales), although 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). Passive loading, with associated high sugar concentrations in leaf cells, may be correlated with the woody habit. Woody plants with 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). However, Saxifraga, herbaceous, and Cercis and Styrax, both woody, have active loading (Rennie & Turgeon 2009; Fu et al. 2011). 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).
5E. Discussion. The "museum" hypothesis is that current 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). Many clades seem to have been little affected by events at the K/P boundary, or initial rapid diversification slowed down as global cooling occurred ("ancient cradle"), or diversification rates increased towards the present, the "recent cradle" theory (see Couvreur et al. 2011c for references). Thus the diversification 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/P boundary. Palms are iconic plants of l.t.r.f. today, so either 1) the rainforest of 100 m.y.a. was rather different from that of today (see e.g. Feild et al. 2011b), or 2) l.t.r.f. of "modern" aspect remained very restricted in extent for millions of years, or 3) there are methodological problems with the analyses (see e.g. Quental & Marshall 2010). Coiffard and Gomez (2009) thought that early palms may have been swamp plants plants like living basal Arecales (their examples were Calamus, Nypa, and Mauritia), while in the New World most of the palm fossils may have been from seasonally dry tropical forest (Burnham & Johnson 2004). 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) also show similar constant rates of diversification. Meredith et al. (2011: p. 523; c.f. O'Leary et al. 2013) observed that the KTR of 125-80 m.y.a., during which angiosperms increased from 0 to 80% of the vegetation in many parts of the world, was "a key event in the diversification of mammals and birds". I return to the question of the appearance of l.t.r.f. with a "modern" aspect and its associated animals below.
6. Angiosperm History III: Caenozoic Diversification.
Background. For a summary of global climate during the Caenoxzoic, see Zachos et al. (2001). Atmospheric CO2 concentrations briefly spiked at a high of over 1,200 p.p.m. at the Palaeocene/Eocene Thermal Maximum, but they continued to fall throught the Caenozoic (Arakaki et al. 2011). Global temperatures were high at the beginning of the Caenozoic, and then declined, although with pronounced if sometimes short-term increases. During the recent glaciations CO2 concentrations 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). Continental drift was active, India and the Deccan plate colliding with Asia, Australia approaching Southeast Asia, and the Atlantic Ocean widening (interestingly, a 52-50 m.y.o. amber fauna from India showed little evidence of Indian insularity: Rust et al. 2010). Land connections around the southern end of the world were broken. Major mountain ranges such as the Andes and the Himalayas-Tibetan plateau were elevated, and with the latter came the development of monsoonal climate in Southeast Asia.
6A. Flowering Plants. The end-Cretaceous bolide impact in the northern Yucatan region of Mexico occurred ca 65.5 m.y.a. and there were massive volcanic outpourings visible today as the Deccan Traps in India at about this time or a little earlier (Schoene et al. 2015; see also Keller 2014) that injected very large amounts of carbon dioxide and other gases into the atmosphere. Together, they contributed to the world-wide changes in the biota that were evident at the Cretaceous/Palaeogene (K/P) boundary (Cretaceous/Tertiary [K/T or C/T] boundary in older literature). Indeed, changes may have begun a little earlier in the Late Cretaceous (references in Schoene et al. 2015).
There was up to 80% loss of plant species in some places in North America at the K/P boundary (Upchurch & Wolf 1987), although other estimates are around 25-33% (Nichols & Johnson 2008; c.f. Salas-Leiva et al. 2013). There seem not to have been widespread fires (Belcher 2010). Diet-specific herbivorous insects were seriously affected (Labandeira et al. 2002a, b; Wilf 2008 - surveys of leaf damage types). However, the severity of the effects seems to have depended in part on physical location (K. R. Johnson & Ellis 2002); nothing much at all happened in the high Arctic (Spicer & Herman 2010). 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/eruptions (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). In Patagonia in particular, and perhaps elsewhere the Southern Hemisphere, changes at the K/P boundary were rather muted (Wilf et al. 2013). In Colombia, there were more changes in ecological structure rather than extinction (De la Parra et al. 2007).
"Sudden ecosystem collapse" occured at least locally in North America, even some common plants not transgressing the K/P 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 Caenozoic forests in North America differs 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/P boundary, even if species did not (Tschudy & Tschudy 1986). Insect-pollinated and/or evergreen taxa of seed plants suffered more than wind-pollinated and/or deciduous taxa (Collinson 1990; McElwain & Punyasena 2007). Complicating the interpretation of the data, an imbalance between macrofossils (high extinction) and sporomorphs (low extinction) is commonly noted, the macrofossil record being more and the microfossil record less local (Mander et al. 2010).
Groups like Annonaceae, Arecaceae, and Araceae seem to have constant diversification rates across the K/P boundary (literature summarized by Couvreur et al. 2011a). Menispermaceae, today often lianes of the l.t.r.f., showed a burst of diversification close to the K/P boundary (Wang et al. 2012). Seed ferns survived until well into the Palaeocene in Tasmania (McLoughlin et al. 2008). Several clades of Cretaceous heterosporous water ferns are not known from the Cainozoic, although some extant clades are known from the Cretaceous (Collinson et al. 2013).
Animal groups other than dinosaurs also suffered more or less severely. Thus there are estimates of about 60% loss of butterfly diversity at the K/P boundary (Wahlberg et al. 2009) and a mass extinction of birds, lizards and snakes in western North America, but perhaps elsewhere, too (Longrich et al. 2011, 2012). Rather surprisingly, given text-book accounts, mammal diversification may have been little affected (Bininda-Emonds et al. 2007; Meredith et al. 2011; G. P. Wilson et al. 2012; c.f. O'Leary et al. 2013: dating there probably an underestimate, see dos Reis et al. 2014). Indeed, the diversity of multituberculate mammals was at a peak across the K/P boundary and seems unaffected by events then (Wilson et al. 2012), while in India Intertrappean floras show little evidence of animal extinctions (Spicer & Collinson 2014). Marine extinctions were quite common (Schulte et al. 2010; Ohno et al. 2014).
A mixed and rather confusing record, but overall the affect of the end-Cretaceous bolide impact/Deccan Traps eruptions on angiosperms seems rather muted, even if some animal groups were severely affected. Even in places with much devastation plants may have been unable to grow for a mere one or two years (Spicer & Collinson 2014), and plant propagules in the soil are likely to have survived the possibly relatively transient atmospheric changes at the K/P boundary better than many animals which largely lack resting stages in their life cycles (Cascales-Miñana & Cleal 2013). Indeed, no major adverse effects on land plants were detected in recent analyses (Cascales-Miñana & Cleal 2013; Magallón et al. 2015: level of family origination was high then). There may have been decreases in the diversification rates of ferns and low diversification and high extinction of gymnospermous seed plants, and diversification rates at the level of genus increased, with overall net diversity for vascular plants being high as a result (Silvestro et al. 2015: mostly leaf fossils; see also Niklas et al. 1983). Estimates of the time that vegetation took to fully recover 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), mire vegetation being least affected by the impact (Nichols & Johnson 2008). The bolide impact in North Dakota adversely affected species gowing along river channels more 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), a small change given the average difference between nonangiosperms and eudicots, ca 8 mm/mm2), and any long-term effects of these changes are unclear. A fast-growth strategy might allow the plants to deal better with changing light regimes (see the "impact winter": Ohno et al. 2014 and refs.) and heterogeneities in resource availability (Blonder et al. 2014).
There were major changes in angiosperm ecology and diversity in the early Caenozoic. For angiosperm clades that crossed the K/P boundary, the average seed mass, initially rather low, increased markedly (e.g. Tiffney 1986b; Eriksson et al. 2000a; Collinson & van Bergen 2004; Sims 2010). This trend can be seen within Juglandaceae, with many winged disseminules (Eriksson et al. 2000a; Friis et al. 2011), as well as in Fagaceae, which lack such disseminules (Tiffney 1986a). Xiang et al. (2014) thought that relatively open habitats after the K/P boundary may have favoured the diversification of fagalean clades with winged disseminules, although such habitats are unlikely to have persisted. Around the end of the Cretaceous flower size must have increased, flowers even in the later Cretaceous usually being only a few millimetres in size (Friis et al. 2011).
The increase in seed size that began at the end of the Cretaceous may be linked primarily to a change in forest type, closed, more humid forests made up of tall trees becoming more common (e.g. Eriksson et al. 2000a, b; Tiffney 2004; 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 early growth of the seedling, although they may also be favoured by dry conditions, soils with low mineral nutrients, etc. (Leishman et al. 2000; Bolmgren & Eriksson 2005), although within individual forest communities there is great variation in seed size, in part connected with the successional status of the species, early successional species tending to have smaller seeds (e.g. Westoby et al. 1996; Eriksson et al. 2000b). Euasterids, many of which are herbaceous or shrubby, tend to have small seeds (Eriksson & Kainulainen 2011), and they diversified greatly in the Cainozoic; seed volume decreases somewhat from the end-Eocene onwards (e.g. Tiffney 1984; Eriksson et al. 2000a; Friis et al. 2011).
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, often animal dispersed seeds while ectomycorrhizal Pinaceae and in particular Salix and Betulaceae-Betuloideae have small, wind-dispersed seeds.
In general angiosperm diversity in the tropics and warm temperate areas was rather low during the Palaeocene (Wilf 2008). However, by around 64.5 m.y.a. the Castle Rock flora is described as "an excellent example of early modern tropical rainforest in North America" (Burnham & Johnson 2004: p. 1607). In 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). There are no particular changes in diversification rates at around this time (Silvestro et al 2015; Magallón et al. 2015). A Late Palaeocene flora from Colombia ca 59 m.y.o. had a familial composition similar to that of current neotropical rainforest, with Arecaceae, Araceae, Fabaceae, Malvaceae, MenispermaceaeLauraceae and Zingiberales all being represented, even if overall both plant (esp. beta diversity) and herbivore diversity were rather low (Jaramillo et al. 2006; Graham 2010: vegetational history of Latin America), and 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). Plants in this flora (Wing et al. 2009; see also Burnham & Johnson 2004) has a very high venation density and the flora is the first fossil evidence of functional equatorial neotropical megathermal rainforest (= l.t.r.f.: Feild et al. 2011b; see also Jud & Wing 2013). Early Eocene paratropical forest is described as being common in the eastern part of the Northern Hemisphere (Mayr 2009). Interestingly, however, taxa with wild-dispersed fruits are not commom in Palaeocene Colombian floras, still less in the Late Cretaceous-Maastrichtian (Herrera et al. 2014). 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 short-lived Palaeocene-Eocene thermal maximum (PETM) of about 55 m.y.a. temperatures increased 3-8o 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).
In South America plant diversity and origination rates increased at about the time of the PETM, and there is no evidence of thermal damage to the leaves (Jaramillo et al. 2010) despite temperatures 5-70 above current values (Jaramillo & Cárdenas 2013). In North America (Wyoming area) mesophytic plants, especially conifers, were temporarily replaced by species that could tolerate both increased temperature and decreased precipitation, and plant and herbivore diversity and activity were high, perhaps correlated with the high temperature (Currano et al. 2008). Movement of floras and replacement of Cupressaceae and Podocarpaceae occurred elsewhere, too (Wing & Currano 2013). Diversity was also very high in Late Palaeocene Gulf Coast floras, pollen diversity increasing ca 15% (Harrington & Jaramillo 2007). Although Citerne et al. (2010) suggest that this was a period of floral innovation, overall increases of diversification were not detected (Magallón et al. 2015; Silvestro et al. 2015). There may have been major diversification of herbivorous beetles in particular and insects in general (Farrell 1998; Wilf & Labandeira 1999; Wilf et al. 2001; Lopez-Vaamonde et al. 2006).
The PETM may be associated with some marine extinctions, and there were shifts in the distributions of both terrestrial plants and animals, reowking of sediments and increased sediment flux (and more clay moving to the sea), overall there seems to have been little extinction (Wing et al. 2005; Willis & MacDonald 2011; McInerney & Wing 2011; Foreman et al. 2012; Wing & Currano 2013; c.f. Mander et al. 2010). However, 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), which Mander et al. (2010) consider to be a significant decline - sporomorphs are a more reliable indicator of presence than are meso- or macrofossils.
Fires decreased notably in many parts of the world from the mid Palaeocene to the Pliocene (Bond et al. 2005; Bond & Scott 2010; Belcher et al. 2010b; He et al. 2012; Bond & Midgley 2012), Australia perhaps being an exception (e.g. He et al. 2011; Crisp et al. 2011; Crisp & Cook 2013). Perhumid conditions had spread and large angiosperms dominated; litter decayed quickly and there were few shrubs to support fire (c.f. the Cretaceous). However, in parts of Europe there is evidence for episodic fires in a vegetation dominated by ferns and perhaps Fagales (Collinson et al. 2007). There was a small peak of fire activity in the Oligocene, but considerable increases in the last 10 m.y. associated with the spread of grassland and savanna (Bond et al. 2010; 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 resulting in the sequestration of carbon. Fires also affect the nitrogen cycle, volatilizing N (Forrestal et al. 2014 and refs.).
Although temperatures soon moderated after the PETM, they then became gradually warmer, peaking again at similar high values during the Early Eocene Climatic Optimum of 52-50 m.y.a., a much warmer, wetter and more temperate period than now (e.g. Greenwood & Wing 1995; Upchurch et al. 2007; Zachos et al. 2001, 2008; Sluijs et al. 2009; Kroeger & Funnell 2011). Species diversity of both animals and plants was probably at a maximum in later Eocene forests, partly because of these flatter global temperature gradients and an overall 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). 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 British Colombia in North America and Primorye, eastern Russia, in deposits of about this age (Archibald et al. 2014). Some angiosperms grew at the then-north pole ca 60 m.y.a. (Daly et al. 2011 for how plants could grow at such high latitiudes). 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; see also Spicer & Herman 2010); there seems to have been some local endemicity (Harrington et al. 2011).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). Rich forests ca 45 m.y.o. have been described from palaeolatitude 78.6o N in Canada (Jahren 2007). 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 precipitation seasonality (Schubert et al. 2012). Palm trees also grew well inside the Antarctic 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).
At this time, extratropical climates showed little seasonality, and plants which would seem to have mutually exclusive climatic preferences grew together. Overall, latitudinal diversity gradients were flatter or even peaked in temperate regions (e.g. Archibald 2013), as they had since the Triassic (see also below). Wing (1987) emphasized the uniformity and homogeneity of Palaeocene 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. Taxa whose ranges are now tropical had much wider distributions in the Eocene (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). A number of plant taxa now restricted to Southeast Asia grew in Europe and North America at various times in the Palaeocene and Eocene - and on 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, and both are notably speciose (Archibald et al. 2010).
A long-term cooling trend was accentuated 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 in the far north since the end of the Eocene (Jahren 2007), temperatures dropping 8.2±3.1oC in just 400,000 years at the beginning of the Oligocene some 33.5 m.y.a. in central North America, apparently with little change in precipitation (Zanazzi et al. 2007), although in parts of North America woodlands became more open and arid in the Late Eocene/Oligocene (Mayr 2009). The Antarctic ice sheet appeared ca 33.5 m.y.a. at the Eocene-Oligocene boundary and persisted through much of the Oligocene (Zachos et al. 2001; 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).
Importantly, seasonality also greatly increased, even if it was to decrease somewhat later in the Caenozoic (Wolfe 1978). Seasonality is evident in extratropical floras in general at the end of the Eocene or somewhat earlier (e.g. Wing 1987; Eldrett et al. 2009), but 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).
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. Although few Eocene leaf remains can be assigned to modern genera, by the end-Eocene this can commonly be done (e.g. Wing 1987; Dilcher 2000). Although ecological conditions may have differed somewhat from those of today, any differences are surely less than when comparing Cretaceous and extant angiosperms (Mittelbach et al. 2007).
Temperatures in the later Oligocene rebounded slightly and oscillated through the Miocene, and the mid-Miocene ca 16 m.y.a. was quite warm and wet. However, this warmer period was followed by a further long-term temperature decline, latterly precipitous, to the Pleistocene when full-blown ice sheets first appeared in the North Hemisphere - they had been preceded by 10 m.y. by ice sheets in the Southern Hemisphere (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 in which such grasses are also prominent 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 6-3.6 m.y.a. MATs were 2-3o C 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).
In South America the tropical flora did not shift south when temperatures were high during the Early Eocene Climatic Optimum, rather, a new kind of vegetation whose ecophysiology is unknown developed in paratropical areas below 24oS, and the dissimilarity between tropical and extratropical floras increased (Jaramillo & Cárdenas 2013; see also Romero 1993 and references). Aspects of the subsequent evolution of the extra-tropical flora there are rather distinctive (see below).
6B. C4 Photosynthesis, Grass, and Grasslands; also, some other Ecophysiological Groups. Overall, C4 photosynthesis is efficient, it has arisen many times, and it is of great importance ecologically. 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 land area (Still et al. 2003: C4 crops factored in). Another estimate of the global extent of grassland, including savanna, is 52.5 x 106 km2 (Gibson 2009). Although a mere 7,500 species, somewhat over 2% of angiosperms, are C4 plants and their biomass is only ca 5% of the global total, they account for about 23-28% of terrestrial gross primary productivity (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; R. Sage et al. 2012). 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 were not factored in); 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.
C4 photosynthesis 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. The C4 photosynthetic 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 C4 species), Amaranthaceae (ca 500 C4 species) and other core Caryophyllales, Euphorbiaceae (Euphorbia subg. Chamaesyce section Anisophyllum: ca 340 C4 spp.), etc. (Arakaki et al. 2011; R. Sage et al. 2012: see e.g. Kellogg 2013a; Williams et al. 2013; Heckmann et al. 2013; Christin & Osborne 2014; etc., for summaries of C4 photosynthesis).
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).
Origins of C4 photosynthesis in monocots and eudicots are roughly contemporaneous, mostly occuring within the last 30 m.y. or so (Christin et al. 2011b: a number of dates; Kadereit et al. 2012); Cowling (2013) has a rather different take on the evolution of C4 photosynthesis, suggesting much more ancient origins of the syndrome. The great expansion of C4 grassland is geologically very recent, occuring only within the last 10 m.y., and within the last 3-2 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 savannas in Africa, also developed within the last (10-)5 m.y. (Simon et al. 2009; Simon & Pennington 2012; Maurin et al. 2014). Associated with the spread of grasslands is a pronounced increase in fires ca 10 m.y.a. (e.g. Bond & Midgley 2000; Keeley & Rundel 2005; Bond & Scott 2010).
Grasslands often have distinctive soils. 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, so they reflect incoming radiation less, and are warmer and so transpire more. Somewhat paradoxically grasslands support a cooler, drier climate, yet one that allows increased weathering, which consumes carbon (Retallack 2009). 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 and ultimately support ocean productivity (Volk 1989). Nitrogen is volatilized in fires, but C4 grasses have low nitrogen requirements. See also below.
For more on the evolution of grasslands, see Poaceae. Overall, grasslands can be considered a long-term carbon sink and they contribute 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".
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).
There are other important eco-physiological groups of angiosperms whose members are concentrated in only a few main clades. The first three groups mentioned below, 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 also quite often CAM-type plants. All told, some 17,000 or more species in Crassulaceae, Bromeliaceae, Cactaceae and Orchidaceae-Epidendroideae, all succulents of one sort or another, have CAM or its variants (Winter & Smith 1996b; Sayed 2001). The origin of CAM clades is largely contemporaneous with that of C4 clades, being 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 Caenozoic. 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.
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). Some questions are, what global patterns of biodiversity can be discerned, what causes them, and when have they been evident (e.g. Kier et al. 2005)? Knowing the number of taxa involved, the ages of the clades, and the ecological attributes that can be linked with these clades are all important, and the perspective changes when the focus broadens to incorporate past climate changes.
Today, plant (and animal) diversity is 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). Diversity usually declines away from the tropics. 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 Carex, Polygonaceae and Ranunculaceae are most diverse away from the tropics (e.g. Escudero et al. 2012b; Kostikova et al 2014b). Whether or not such gradients are found in prokaryotes is unknown (Timling & Taylor 2012 and references).
Herbivore diversity is often thought to be greater in tropical than in temperate forests, and so 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). Two 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). Overall, specialized insect herbivores are more frequent in tropical regions, and this is connected with the greater lineage diversity of their hosts there; the numbers of generalist herbivores showed no latitudinal correlations (Forister et al. 2015; see above for herbivore specialization). It would be interesting to know how this might relate to amount of herbivory.
These gradients have been most obvious in cooler/glacial periods in the past (Mannion et al. 2013; c.f. Benton et al. 2010), and for groups like birds, mammals, insects, and the like, they may be a post-Eocene phenomenon (Archibald et al. 2010, 2012; Rose et al. 2011: temperature gradient similar to that of today; Mannion et al. 2012; also Boyero 2014 for literature). Reduced seasonality characterized the Palaeocene-Eocene, and the flora was much more homogeneous with considerable diversity even at higher latitides, although not at the very highest. Now-tropical groups like palms were found far both to the north and south of their current distributions in the Palaeocene/Eocene (see above).
Much literature focuses on establishing mechanisms that would cause/explain current global patterns of diversity (e.g. Willig et al. 2003; Mittelbach et al. 2007 for a critical summary). Latitudinal gradients can perhaps be explained by differences in rates of speciation or extinction, differences in the amount of incident energy, differences in habitable areas, longer time of stable climate, 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. Evapo-transpiration, topographical diversity, and related factors are also important (Kreft & Jetz 2007). Lamanna et al. (2014) looked at the alpha, beta and gamma components 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. Attempts to explain 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). Thus older plant clades tend to be more tropical/southerly in distribution, younger ones are more cold-tolerant and northern, in line with the ages of temperate and tropical climates. The tropical clades probably evolved in the Cretaceous, i.e. long before the current latitudinal climatic patterns were established, the temperate clades are mostly (but not all) post-Eocene in age (see also Kerkhoff et al. 2014: New World; Hawkins et al. 2014 and references: conifers not included). Along these lines, 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. The older a clade, the more time it will have to speciate, and amount of speciation may also be linked with the area of biomes (Fine & Ree 2006). However, separating historical and ecological signals in patterns of plant diversity is not at all straightforward (Ricklefs 2005).
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 origins. Southern families have not penetrated the highly seasonal Nearctic, perhaps not simply because there is a smaller southern temperate zone where they diversified less/were exposed to less competition, 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. 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 Caenozoic.
There are differences between the two hemispheres, high latitude southern floras being less diverse but older than northern floras (Kerkhoff et al. 2014). Compared with the tropics, the southern flora had an only somewhat lower phylogenetic diversity, while in northern latitudes the phylogenetic diversity was notably lower (Kerkhoff et al. 2014). In the equatorial Andes, as minimum temperatures decrease with increasing elevation, the ages of the clades of the woody plants, at least, increases (Qian 2014: focus on families). To Segovia and Armesto (2015), this was because the woody Andean plants were representatives of an old, temperate, Gondwanan flora, and there is further evidence for this flora in the Patagonian fossils ca 52.2 m.y.o. (e.g. Wilf & Escapa 2014 and references; see also Segovia & Armesto 2015). Similarly, Leslie et al. (2012) found that most southern hemisphere clades of Pinales are older than northern clades, the latter having been more subject to major climate swings beginning in the Oligocene. Equable climates most similar to those of the early Caenozoic 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; Leslie et al. 2012).
Thinking about these patterns in the context of the interactions between angiosperms and their fungal associates, interactions 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, particularly pronounced polewards and especially in the northern hemisphere, may contribute to the current latitudinal gradient in diversity, in particular, to the hypothesis that diversity is in some way linked with productivity (e.g. Willig et al. 2003). ECM-dominated communities are common in more extreme and unproductive environments and they are species-poor (Gillman & Wright 2006; Cusens et al. 2012; c.f. Adler et al. 2011: focus on herbaceous communities). It 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.
6D. Gene and Genome Duplication and Genome Size. Within angiosperms alone nuclear genome size varies 2000-fold (Greilhuber et al. 2006; see also Characters), although the significance of this variation is less than clear, and strong correlations seem hard to come by (Garcia et al. 2010). Many of the connections between genome size and gene and/or genome duplication and subsequent diversification of angiosperms that have been suggested remain to be established.
Perhaps 15% of angiosperm speciation events are associated with genome duplication/polyploidy (see Otto & Whitton 2000 and Meyers & Levin 2006 for general overviews). Polyploidy has occurred many times and at all levels of the tree from species like Sporobolus (Spartina) anglica, formed by allopolyploidization in the 1870s, to the common ancestor of small groups of genera deep within Poaceae and Brassicaceae, or much larger groups such as the asterids, core eudicots and all seed plants. It is increasingly being implicated in the evolution and diversification of angiosperms (e.g. Vision et al. 2000; Bowers et al. 2003; Blanc & Wolfe 2004a; Schlueter et al. 2004; Adams & Wendel 2005; Maere et al. 2005; de Bodt et al. 2005; de Martins et al. 2006; Chapman et al. 2006; Cui et al. 2006; Jaillon, Eury et al. 2007; Soltis et al. 2009; van de Peer et al. 2009b; Duarte et al. 2010; Barker et al. 2010; Jiao et al. 2011; Mühlhausen & Kollmar 2013: myosin motor proteins; Guo et al. 2013).
Gene/genome duplications may facilitate diversification by allowing the subfunctionalisation and neofunctionalisation of genes (e.g. Renny-Byfield et al. 2014). Alternatively, one of the gene copies may be lost (for a nice example, see de Martino et al. 2006), perhaps particularly in important housekeeping genes, which thus revert to being single copy genes (de Smet et al. 2013). Novel regulatory pathways may evolve, and there are other changes (e.g. Guo et al. 2013; Conant 2014: Saccharomyces). Genome duplications may also reduce the probability of extinction by e.g. increasing genetic variation and environmental tolerance (Crow & Wagner 2006 and references; see also van de Peer 2009a; Franzke et al. 2011), and individual mutations are less likely to have an immediate effect. Along these lines, 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 Deccan Traps eruptions/bolide impact, suggesting that polyploids forming then were at a selective advantage because of their hybrid vigour, also having extra genes/alleles available for selection given the changing environment (see also Visser & Molofsky 2014 for possible advantages of polyploids). Species-rich clades and genome duplications have been associated, Soltis et al. (2009: p. 336) linking genome duplications with "a dramatic increase in species richness" in Poaceae, Fabaceae, Brassicaceae and Solanaceae.
However, Wood et al. (2009) suggest that polyploidy affects primarily cladogenesis, less the diversification rate of those clades; polyploidy is quite commonly an evolutionary dead end, with recently-formed polyploid plants speciating less and in particular showing higher extinction rates than diploids (Mayrose et al. 2011, 2014). Scarpino et al. (2014) proposed that the prevalence of polyploidy was the result of a ratchet mechanism, since it is irreversible (but see below), and diploids speciated more frequently. As van de Peer et al. (2009a), Schranz et al. (2012), Estep et al. (2014) and others have pointed out, there is often an appreciable time lag between duplication and subsequent diversification. The distinction between short- and long-term effects helps clarify the discussion between Mayrose et al. (2011, 2014: emphasis on the former) and Soltis et al. (2009, 2014: emphasis on the latter).
Isozyme duplications suggest past polyploidization in clades like Magnoliaceae, Aesculus, Salix/Populus, etc. (Soltis & Soltis 1990). The notably small stomata of some fossils when compared with extant members of these clades also may suggest polyploidization, extinct members perhaps having chromosome numbers half of any of those known in extant members (Masterson 1994: Lauraceae, Magnoliaceae [one point], Platanaceae), this thesis being largely based on the assumption that there is a correlation between stomatal size, DNA content and chromosome number. However, the examples just mentioned are from woody groups that are unlikely to have had herbaceous ancestors, so polyploidy may be less likely in such groups, smaller stomata might be expected given given falling CO2 concentrations, and genome size and stomatal size are not always coupled (see below).
Genome size in angiosperms is correlated positively with cell size and guard cell length (e.g. Franks et al. 2012: correlation of guard cell, nuclear and genome size among north temperate herbs). Stomatal size is negatively correlated with stomatal density; trees, with rather small genomes, have the highest stomatal density (Beaulieu et al. 2008, see also Bainard et al. 2012, c.f. Rupp et al. 2010 for Polystachya [Orchidaceae]). Stomatal size, and hence genome size, may have been inversely correlated with atmospheric CO2 concentration over the last 300 m.y. or so (Franks et al. 2012: Fig. 3 - Fig. 4 has problems with ancestral state reconstructions), so both increasing and decreasing in size; Lomax et al. (2013: c.f. fig. 2A and 2B) thought that maximum genome size (derived from maximum guard cell length) may have been steadily increasing from 360 m.y.a. (the Mississippian), but a time-binned average shows a decrease over the last 250 m.y., there was no signal of increased genome size in the early Caenozoic and grasses (e.g.) have notably small stomata (Franks & Beerling 2009). Franks et al. (2012) do not suggest any mechanism that facilitated changes in genome size. Indeed, Hodgson et al. (2010) suggested that changes in stomatal size could have driven changes in genome size, and they emphasize the complexity of the relationship between stomatal amd genome size. Surprisingly, of the species they examined, stomatal length was highest, at up to around 2µm, for vernal geophytes, not species in shade. However, Jordan et al. (2014) found that in Proteaceae, at least, changes in genome size drove changes in stomatal size, the two often being correlated, but some species showed substantial changes in stomatal size without change in genome size, and this was related to the ecology of the plants involved.
There is often little correlation between genome size and chromosome number and in particular ploidy level (e.g. Leitch & Bennett 2004; Weiss-Schneeweiss et al. 2005; Bennett & Leitch 2005; Lysack et al. 2007, 2009; Schnable et al. 2009; Peruzzi et al. 2009; Bliss & Suzuki 2012; Escudero et al. 2012a: Carex; Vaio et al. 2013; Gorelick et al. 2014; Jordan et al. 2014; c.f. in part Jakob et al. 2005). Overall, the genome of angiosperms has been duplicated several times. Brassica napus, for example, is estimated to be 72x (Chalhoub et al. 2014), yet its diploid chromosome number is only 38 and its genome size is unremarkable (see e.g. Wolfe 2001 for chromosome number reduction). Since genome duplications have been common in seed plants and there are no comparable changes in genome size or chromosome number, these must be decoupled, even if there is sometimes systematic signal in genome size (e.g. Bennett & Leitch 2005; Leitch et al. 2005; Hodgson et al. 2010; Schneider et al. 2015). Furthermore, changes in the amount of repetitive DNA can have major effects on C-values (e.g. Jakob et al. 2004). Bennetzen and Kellogg (1997) floated the idea that increase in genome size might be irreversible, which might be true of some gymnosperms (e.g. Nystedt et al. 2013) but not angiosperms. There is no correlation between chromosome number and genome size in Cycadales, and there chromosome number changes are probably caused by fissions or fusions (Gorelick et al. 2014).
Miscellaneous: Root meristem growth rate seems to be negatively correlated with genome size, and since holoparasites in particular have little need for roots (Gruner et al. 2010), they may show much increased genome sizes (e.g. Piednoël et al. 2012). For the GC content of genomes, which shows interesting correlations with genome size, karyotype morphology (esp. holocentric chromosomes) and some aspects of ecology, see Smarda et al. (2014). In extant plants, seed size is more or less correlated with genome size (Beaulieu et al. 2007a; Linkies et al. 2010) and more so with plant habit. Seed size and plant height are correlated, however, for a possible negative correlation of genome size and plant size, see Beaulieu et al. (2007b).
6E. Diversification on other Plant and Animal Groups associated with Flowering Plants.
Other Embryophytes. What about the diversification of embryophytes other than angiosperms? Mosses and liverworts for the most part seem to have undergone bouts of rapid diversification earlier, but in both there was also extensive diversification in the Caenozoic (Cooper et al. 2012; Feldberg et al. 2014; Laenen et al. 2014). 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). Porellales, largely leaf-epiphytic liverworts, diverged from the terrestrial Jungermanniales somewhere between the Late Carboniferous to Triassic, but they, too, diversified in the Cretaceous and early Caenozoic (Heinrichs et al. 2007; Feldberg et al. 2014; see also Ahonen et al. 2003; Forrest & Crandall-Stotler 2004; Cooper et al. 2012). Indeed, much divergence within liverwort families was Caenozoic (Cooper et al. 2012), but Lejeuneaceae initially diversified in the Cretaceous and neither here nor in Cephaloziineae were there rate changes in the Caenozoic (R. Wilson et al. 2007a, b; Feldberg et al. 2013). Laenen et al. (2014) suggest that, as in gymnosperms, there may also have been massive extinction events.
About one third of all leptosporangiate ferns are epiphytic - ca 3,000 species, about 10% of all epiphytes and the majority of non-angiosperm epiphytes, and they may have diversified around the PETM in the early Caenozoic (Schneider et al. 2004a, b; Schuettpelz 2007; esp. Schuettpelz & Pryer 2009; Watkins et al. 2010). Ferns are particularly important components of the epiphytic vegetation in the rainforests of the Antipodes and Oceania (Dubuisson et al. 2009). Most epiphytic ferns are Polypodiales, and their initial diversification (it happened in several clades) began in the Palaeocene (Schneider et al. 2004a, b; Schuettpelz 2007; Dubuisson et al. 2009; 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), and the adoption of the epiphytic habitat was perhaps facilitated by the evolution of a distinctive new photosystem that allowed them to grow in shady conditions, although that may have been acquired considerably earlier around 179 m.y.a. (Kawai et al. 2003; F.-W. Li et al. 2014). Trichomanes and relatives, Hymenophyllales, diversified in the early Cretaceous, but they are commonly epiphytic on tree ferns, a relatively old clade (Schuettpelz 2007; see also Schuettpelz & Pryer 2009). 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).
Podocarps with flattened foliage units are often shade tolerant and their diversification may have 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 (e.g. de Boer et al. 2012). Gymnosperms may also have been at least locally disadvantaged by the temperature changes happening at around the K/C boundary (Blonder et al. 2014). Diversification within extant genera of both Cycadales and Pinales is quite recent, mid to later Caenozoic (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).
Clearly, there was no simple replacement of gymnosperms, other vascular plants and "bryophytes" by angiosperms during the Cretaceous-Caenozoic. Brodribb (2011) and Brodribb et al. (2012) and others have emphasized that some conifers, Pinaceae in particular, an ECM clade, are extremely successful in high light but other than high-nutrient conditions, a few species dominating a considerable area of the earth's surface, as is discussed below. Clades of embryophytes other than seed plants 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), emphasizing that many of these plants found the environment created by the dominant angiosperms to their liking.
Ants make up only ca 2% of known insect species, with about 13,000 species described. However, they make up one third of insect biomass, and overwhelmingly dominate in samples collected when l.t.r.f. canopies are fogged (86% arthropod biomass, to 94% of arthropod individuals), have far greater biomass than that of terrestrial vertebrates, and are the major consumers of plant resources in the canopy (e.g. Davidson et al. 2003; Rico-Gray & Oliveira 2007; Pie & Tschá 2009; Ward 2014). Ants are are sister to the Apoidea, spheciform wasps + bees (e.g. B. R. Johnson et al. 2013; Ward 2014). 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, 2014). On the other hand, Grimaldi and Engel (2005) date stem ants to only some 120 m.y.a., the oldest fossil stem-group ants being from the Middle Albian some 105 m.y.a. and crown-group ants are ca 95 m.y.o. (LaPolla et al. 2013).
Ants and plants may have coexisted for at least 120 m.y. (Chomicki & Renner 2015), and between 100 and 60 m.y.a. the rise of angiosperm-dominated forests was tracked by ant diversification (Moreau et al. 2006). The early evolution of ants may have been in pretropical forests, moving in to tropical rain forest as it developed (Moreau & Bell 2013; see also Wilson & Hölldobler 2005). The tree-loving Formicinae and Dolichoderinae are canopy-dwellers and eat plant materials (Rico-Gray & Oliveira 2007), and their crown-group ages are late Cretaceous-early Palaeocene, 80-70 and 70-60 m.y.a. respectively (Ward 2014). All authors suggest that extant ant subfamilies are Cretaceous in origin (Moreau & Bell 2013; Ward 2014), and Pie and Tschá (2009) thought that the rate of divergence of the main clades was constant, but within these clades diversification rates varied greatly. However, rather than "coevolution" of ants and angiosperms occuring in the Cretaceous, fossil evidence suggests that the ecological dominance of ants began in the Eocene, 50-35 m.y.a., modern ants first becoming common in the fossil amber record then (e.g. Grimaldi & Agosti 2000; Grimaldi & Engel 2005; Dunn et al. 2007; Rust et al. 2010; LaPolla et al. 2013: over 5% of insects then; Ward 2014; c.f. in part E. O. Wilson & Holldöbler 2005; Moreau et al. 2006; Rico-Gray & Oliveira 2007), perhaps around the PETM (Ward 2014). Early ant fossils are of stem group Sphecomyrminae, a group that appears to have been quite diverse e.g. in the Burmese amber deposits ca 99 m.y.o. (Barden & Grimaldi 2014). Extant members of several basal ant clades live largely underground (Rabeling et al. 2008), although details of the relationships of these ants need clarifying (Ward 2014). Many ground-dwelling ants are carnivores, for example, some basal clades eat termites (Bourguignon et al. 2014).
Ant-plant, ant-fungus, and ant-hemipteran associations are linked (e.g. Oliver et al. 2008) and, along with extrafloral nectaries, play an important role in ant evolution. Hemipterans include Auchenorrhyncha, leaf hoppers, mealy bugs and spittle bugs, and Sternorhyncha, scale insects and aphids. Ants can obtain sugar directly from extra-floral nectaries, and the earliest nectaries known are on the lamina of ca 49.5 m.y.o. Prunus fossils from the Okanogan Highlands of western North America (DeVore & Pigg 2007). Extra-floral nectaries are common in some Pentapetalae, Orchidaceae, etc. (Weber & Keeler 2013); about a third of woody broad-leaved angiosperms and vines in Panamanian forests have extrafloral nectaries or other ant attractants (Schupp & Feener 1991), although these become less frequent with increasing altitude and latitude (Rico-Gray & Oliveira 2007). Ca 41% of ant genera obtain nectar indirectly by way of honeydew produced by their hemipteran associates that tap the host's phloem, an important food/energy source for many arboreal ants which, although small and not that speciose, can be dominant and form huge colonies (e.g. E. O. Wilson & Holldöbler 2005; Oliver et al. 2008). Extrafloral nectaries are a general resource for ants, while associations with ants that take honeydew are more specialised (Rico-Gray & Oliveira 2007). Plants benefit from such associations in about 3/4 of the cases studied (Styrsky & Eubanks 2006). Ants, scale insects, etc., may live together in plant domatia of a variety of morphologies. These associations date to the Miocene and later, within the last 19 m.y., and have evolved around 160 times. Neither plant nor ant clades are often speciose, and the plant clades in particular are scattered phylogenetically (Chomicki & Renner 2015; see also Ueda et al. 2008: Macaranga). Ant-hemipteran associations are commonest in Myrmicinae and Formicinae, ant-honeydew associations in those families and Dolichoderinae (Oliver et al. 2008; Styrsky & Eubanks 2006). Obligate bacterial endosymbionts are well known from Hemiptera and γ-proteobacteria are associated with herbivorous ants, and bacteria play an important role in nitrogen movement in these associations (Davidson et al. 2003; Russell et al. 2009), so interactions can become very complex. Many lycaenid caterpillars also produce substances prized by ants (around 75% of lycaenids are associated with ants), although some eat homoptera or homopteran honeydew; there are some 5,000 lycaenids, and their caterpillars, along with those of their sister-group Riodinidae, have single-celled pore cupola organs, perhaps involved in these ant associations (Pierce et al. 2002); the age of the clade of lycaenids whose members are commonly associated with ants is around 71.7 m.y. (Wahlberg et al. 2013). Ants and plants are also associated in ant gardens in both the Old and New Worlds (Rico-Gray & Oliveira 2007). The ecologically very important leaf-cutting attine ants (ca 40 species) of the New World tropics, are also young, stem and crown group estimates being (16-)13-9(-7) m.y. and (14-)11-8(-6) m.y. respectively (Schultz & Brady 2008). For general information about ant-plant interactions, see Huxley and Cutler (1991) and Rico-Gray and Oliveira (2007).
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 are eaten by ants that do not eat the seeds themselves (c.f. granivorous ants), at the same time aiding 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, many of which are woody, and a number of South African species are also myrmecochorous (Sernander 1906; Berg 1975; Orians & Milewski 2007; Milewski & Bond 1982; Bond et al. 1991; Lengyel et al. 2009, and references). (Gastropods may also be involved in the distribution of seeds with elaiosomes - Türke et al. 2011.) Interestingly, perhaps half the species of stick insects (Phasmatodea) lay eggs that mimic the seeds of myrmecochorous plants (Hughes & Westoby 1992).
A very conservative estimate is that some 11,500 species of angiosperms are myrmecochorous (Lengyel et al. 2009, 2010) and the trait has evolved 100-140 times - 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-Caenozoic phenomenon (Rico-Gray & Oliveira 2007; Forest et al. 2007b; Lengyel et al. 2009, 2010, see also Fokuhl 2008).
Crown-group termites are around 149 m.y.o. (Bourguignon et al. 2014: mitochondrial genomes). Termites are derived from cockroaches and are very important globally in plant decomposition. They depend on plant material for their nutriition, basal clades having protozoa in their guts that can break down lignins (Sugimoto et al. 2000; Bignell et al. 2011; Ni & Tokuda 2013 and references), while Macrotermitinae "cultivate" lignin-decomposing fungi. The speciose primitively soil-eating Termitidae (crown group age ca 54 m.y.a.) become common about the same time as ants, common predators of termites, in the Caenozoic (Bourguignon et al. 2014).
The phytophagous beetle sister taxa, weevils (Curculionoidea) and leaf beetles (Chrysomeloidea), include about half of all herbivorous insects. It has been suggested that hey may have diversified largely in parallel with angiosperms (Farrell 1998), although initially diversifying on gymnosperms in the Jurassic (e.g. Labandeira et al. 1994; Farrell 1998; McKenna et al. 2009). However, an association between phytophagy, whether of gymnosperms or angiosperms, and diversification is questionable (Hunt et al. 2007), and the story needs to be rethought. Chrysomelidae may diversify (86-)79–73(-63) m.y.a. in the Late Cretaceous-Eocene, especially in the early Caenozoic (Gómez-Zurita et al. 2007; also Winkler & Mitter 2008).
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 Caenozoic; most diversification occurred within the last 100 m.y. (see also Engel 2000; Grimaldi & Engel 2005). 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; Litman et al. 2011 and references: note early ages for bee diversification; also Sedivy et al. 2013; c.f. e.g. Moldenke 1979). However, several species of oliolectic bees may pollinate a single plant species, and the floral morphology of the latter is likely to have been rather unspecialized (but see below). As mentioned above, there is no signal of pollinator type in pollen protein content, etc. (Roulston et al. 2000). Xylocopinae entered the Caenozoic as four clades that had diverged about 20 m.y. before, but in the early Caenozoic diversification increased considerably; before the Caenozoic 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 Tertiary diversification (Almeida et al. 2011).
Lepidoptera, butterflies and moths, with ca 160,000 described and perhaps 500,000 total species, are the biggest insect clade almost totally dependent on plants both as adults and as larvae (Powell et al. 1998; Mutanen et al. 2010). Relationships between the main clades are poorly supported, perhaps reflecting very fast initial evolution (Mutanen et al. 2010). Diversification of the paraphyletic non-ditrysian lepidoptera may have begun in the Jurassic and that of the ditrysians (with separate openings for mating and laying eggs) and in the Cretaceous (Labandeira et al. 1997; Wahlberg et al. 2013), or both may be dated to the Cretaceous (Grimaldi 1999; Grimaldi & Engel 2005). Wahlberg et al. (2013) dated the start of diversification of the speciose Macroheterocera group of moths, with ca 100,000 spp., to about 90 m.y. ago.
Papilionoidea (butterflies) are well embedded in monotrysian lepidoptera. Heikkilä et al. (2011) suggested that the main clades (= families) in Papilionoidae diverged quickly in the early Cretaceous, Wahlberg et al. (2009) thought that these clades were largely of late Cretaceous origin and Wahlberg et al (2013) dated butterfly diversification to ca 104 m.y.a. - poverall eudicots radiated ca 100 m.y.a. and lepidoptera in general shortly after ca 90 m.y. ago. 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/P boundary. Overall, much diversification of of Nymphalidae-Nymphalinae and -Papilioninae seems to have occurred 65-33 m.y.a. (Wahlberg 2006; Zakharov et al. 2004). Although diversification of Pieridae may have begun in the Late Cretaceous (112-)95(-82) m.y.a. (Braby et al. 2006), much speciation was Caenozoic (Simonsen et al. 2011 gives a range of divergence times). Caterpillars of these groups tend to show rather high food-plant specificity. Some butterfly (and other herbivore) clades that survived the K/P boundary may initially have eaten several different food plants, but subsequently they diversified on a more restricted set of plants and/or they shifted their food preferences (Janz et al. 2006; Nylin & Wahlberg 2008; Fordyce 2010; Nylin et al. 2014; but c.f. in part Hamm & Fordyce 2015).
Mammals have a substantial fossil history before the Cretaceous, but their crown-group age is around 77.8-76.5 m.y.a. (e.g. dos Reis et al. 2014), with notable diversification in the early Caenozoic (Bininda-Emonds et al. 2007; see also Stadler 2011a). A radiation of multituberculate mammals, now extinct, began ca 85 m.y.a., and their adoption of a more herbivorous diet may be associated with the increasing prominence of angiosperms (G. P. Wilson et al. 2012). Primates initially may have been arboreal omnivores eating plants and their associated insects, but even in the Palaeocene ca 46% were probably frugivores, the figure rising to ca 76% in the Holocene, and the relationship between plants and primates has been described as a "facultative mutualism" (Goméz & Verdú 2012: p. ; Sussman et al. 2013). Although radiation of extant primates began in the late Cretaceous, e.g. 71-63 m.y.a. (Springer et al. 2012), (89.8-)84.8, 78.8(-64.9) m.y.a. (Fabre et al. 2008), (98.6-)87.2(-75.9) m.y.a. (Perelman et al. 2011), nearly all diversification is Caenozoic. "Old" estimates date the split within Anthropoidea/Simiiformes to the later Eocene ca 43.4 m.y.a., crown-group ages within Old World and New World monkeys (Catarrhini and Platyrrhini) being around 31.6 and 24.8 m.y. respectively (Perelman et al. 2011), and recent discoveries in Amazonian Peru of fossil teeth ca 36 m.y.o. similar to those of African anthropoids (Bond et al. 2015) are consistent with these dates and with the movement of (ancestral) platyrrhines from the Old to the New World.
In bats, both frugivory and nectarivory have arisen in parallel, even within 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 occurred between 43.1 and 33.4 m.y.a., probably in the late Eocene, with diversification of the more specialized fruit-, pollen- and nectar-eating bats dated to around 26-16 m.y.a. in the late Oligocene to mid-Miocene (Datzmann et al. 2010; Rojas et al. 2011; Jones et al. 2005; Teeling et al. 2005). Adoption of a plant diet seems to have accelerated bat diversification rates, but not that many species of bats are involved, for instance, there are ca 15 species of nectar-eating pteropodid (Datzmann et al. 2010: see also below).
Birds. Jetz et al. (2012) and Jarvis et al. (2014: skeleton tree) provide phylogenies for all birds; crown group Aves are estimated to be 115.9-94.8 m.y.a. (Lee et al. 2014). Radiation of important seed-dispersing birds such as Columbiformes (pigeons) began some (63.6-)54.4(-46.1) m.y.a. (95% CI) in the earlier Caenozoic (e.g. Tiffney 1986b; Pereira et al. 2007; Jarvis et al. 2014), extant members, Columbidae, being dated to a mere 33.4 m.y.a. (Jetz et al. 2012). Bird pollination is also likely to be a Caenozoic phenomenon, three groups, Trochilidae (humming birds), Nectariniidae (sunbirds, etc.) and Meliphagidae (honey eaters) being most important (Cronk & Ojeda 2008). Hummingbirds diversified only in the Pliocene (Bleiweiss 1998a; McGuire et al. 2007, 2014), while that part of Passeriformes that includes sunbirds and honey eaters did not begin to diversify until the Oligocene around 30 m.y.a. (Jarvis et al. 2014; c.f. estimate in Friis et al. 2011, up to 65 m.y.a.). Parrots (Psittaciformes) is another clade important in both pollination and seed dispersal, but very differing ages have been suggested for its diversification. Wright et al. (2008) offer two sets of ages, based on different geological calibrations; the younger is consistent with the fossil record and the age for Psittaciformes suggested by Jarvis et al. (201); no fossils from the European Palaeogene, with rather rich records, can be placed in extant crown groups (e.g. Mayr 2002, 2009). Older crown group ages are around 82 m.y.a., with the split of the cockatoos from the rest of the family bar the few Strigopoidea being dated to around (82.9-)74.1, 70(-63.9) m.y.a.; corresponding younger ages are around 50 m.y.a. and (51.4-)45, 42.7(-38) m.y.a. respectively (Wight et al. 2008); Jetz et al. (2012) date a rate shift represented by the true parrots, Psittacoidea, to around 35.6 m.y. ago.
6F. Discussion. We can now return to the issue of when l.t.r.f. as we know it appeared. The question is, to what extent can "the ecological opportunities provided by humid megathermal forests" (Feldberg et al. 2014: p. 1) that seem to have driven the diversification of epiphytic ferns, etc., in the Late Cretaceous translate to the existence of l.t.r.f., particularly a l.t.r.f. that might look something like that of today and have a broadly similar complexity of ecological relationships? What were the relationships between animals and plants in such forests in the Late Cretaceous and Palaeogene, what birds, butterflies and bees were involved in pollination, what mammals and birds were involved in fruit dispersal, how important were ants? 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? Dating is critical, so the problems with dating that have frequently been mentioned should be borne in mind.
Tropical rainforest today is characterized by having an annual rainfall of at least 1800 mm, at most three months having less than 100 mm per month. There is little variation in the temperature, the mean for the coldest month being around 18o, and there is (almost) no frost (e.g. Morley 2000; Burnham & Johnson 2004). Much woody angiosperm diversification has been in such forests, and epiphytes and lianes are common there. The most diverse families in neotropical forests of this kind are Fabaceae (by far), Moraceae, Annonaceae, Euphorbiaceae, Malvaceae, Lauraceae, Sapotaceae and Myristicaceae (Burnham & Johnson 2004: from Fig. 2). Areas of current very high diversity like western Amazonia are wet, less seasonal, relatively nutrient-rich, and with a mosaic of ecological conditions - and they are also young, less than 20 m.y.o., indeed, many neotropical clades characteristic of l.t.r.f. are relatively young (Burnham & Johnson 2004; Hoorn et al. 2010).
Somewhat under 25,000 species of flowering plants are epiphytes (Feild et al. 2009a; Boyce et al. 2009, 2010; Schuettpelz & Pryer 2009; Boyce & Lee 2010; Boyce & Leslie 2012). Major clades with epiphytes include Bromeliaceae, all New World and Oligocene or even Pliocene in age, many Orchidaceae-Epidendroideae, Gesneriaceae, and ca 3,000 species of ferns. There are ca 8,700 species of scandent plants in the New World alone (Gentry 1991), and they have an important effect on carbon cycling (increased), storage (reduced) and sequestration (reduced: van der Heijden et al. 2013). There were lianes in the Cretaceous, probably Menispermaceae, common in l.t.r.f. today, and they showed a burst of diversification close to the K/P boundary (Wang et al. 2012). In the Caenozoic Vitaceae-Vitoideae (Smith et al. 2013), Bignoniaceae-Bignonieae (early Eocene to late Oligocene), Sapindaceae-Sapindoideae-Paullinieae (?age) and Celastraceae (?age) become prominent.
Clades of parasitic and myco-heterotrophic angiosperms that currently live in l.t.r.f. or similar conditions are of particular interest. Stem-group Rafflesiaceae, now largely restricted to l.t.r.f., 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). However, stem-group Tetrastigma, on which Rafflesiaceae are parasitic, is only some 58-50 m.y. old. 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/Caenozoic boundary, and fruits of crown-group Vitaceae are known from the Deccan Traps at around/a little before the K/C boundary ca 66 m.y.a. (Manchester et al. 2013). Myco-heterotrophic clades of Dioscoreales often grow in similar habitats, and some are estimated to have diverged (118-)109-79(-68) m.y.a., the myco-heterotrophic habit being established well before the beginning of the Palaeocene (Merckx et al. 2008a, 2010), although the stem age of Gentianaceae-Voyrieae is only (65.2-)54.0, 46.8(-40.1) m.y.a. (Merckx et al. 2013).
Characteristic of l.t.r.f. is the diversity of various animal groups dependent on plants that live there, whether herbivores, gallers, frugivores, decomposers, or pollinators, not to mention animals that eat other animals. 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, many of which were eating plants (see also Hawkins & Porter 2003; Penney 2004; J. S. Wilson et al. 2012b). Thus Pompilidae, wasps which now almost exclusively eat spiders, radiated in the Caenozoic 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), however, the spider-eating archaeid spiders began diversifying around 200 m.y.a. (Wood et al. 2015). Diversification of parasitic and hyperparasitic wasps such as the hyperdiverse Chalcoidea (the chalcid wasps), perhaps half a million species strong and most ultimately dependent on flowering plants, is most intensive in the Caenozoic (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 dehydrogenase in flies; Harry et al. 1996, 1998: fig-breeding Lissocephala). 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), much evolution here is Caenozoic (Guzmán et al. 2013).
In the following paragraphs emphasis is initially placed on direct relationships. 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), although quite how many insect species in particular and arthropods in general there are is unclear. Ølgaard (2000; see also Hamilton et al. 2013) estimated that there were around (2.75-)4.9-6.7(-10) million species, down from the some 30,000,000 estimate based on the early tree-fogging experiments.
There are well over 100,000 species of extant phytophagous beetles in some five clades, particularly the chrysomelids and curculionids, that eat angiosperms. Initial diversification has been dated to the Jurassic, with over 100 extant beetle lineages divergin before the beginning of the Cretaceous 140 m.y.a. (Farrell 1998, but c.f. dates; see also Mayhew 2007; Hunt et al. 2007). Beetle and angiosperm evolution seem not to be tightly linked, and there is no strong association of diversification and the adoption of herbivory, or shifts from gymnosperms to angiosperms as a food source (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 trend 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. (2005b) suggested that diversification of bruchids and Fabaceae may have occurred more or less together.
There is 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). Diversification and overall diversity of phytophagous insect groups may at least initially increase after they adopt new hosts (Janz et al. 2006; c.f. Hamm & Fordyce 2015). Close co-evolution seems to be the exception 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 low diversities and little evolution of their major pollinators (see below).
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; Eriksson et al. 2000a; Moles et al. 2005a). The acquisition of fleshy fruits is not linked to notable increases in diversification of clades with them (Bolmgren & Eriksson 2010 and literature; c.f. Eriksson & Bremer 1991).
If l.t.r.f. is dated to around the end of the Palaeocene some 58-55 m.y.a., one expectation might be that the distinctive fauna that currently inhabits it is of similar age. In the ca 58 m.y.o. Cerrejón flora, although insect damage was quite high, most was from external feeding, and specialized feeding types like leaf mines and galls were uncommon (Wing et al. 2009). Vertebrates are important in the dispersal of the 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.
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 herbivore 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."
During the early Caenozoic, angiosperms with their often dense veinlet reticulum, 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). 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/P boundary (Wheeler & Baas 1991). Such changes may be connected with changes in venation density and water conductance needs, but their interpretation is not easy (see Wheeler & Baas 1993; Philippe et al. 2008). Fast decomposition of angiosperm litter, particularly associated with the deciduous habit (Knoll & James 1987), may also have speeded nutrient cycling and plant growth (Cornwell et al. 2008; Berendse & Scheffer 2009; Liu et al. 2014). 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 Caenozoic, perhaps also another element in angiosperm success.
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 (Feild et al. 2011b). Such forests had a floristic composition overall quite similar to that of contemporary forests (Jaramillo & Cárdenas 2013; see also Wing et al. 2009; Ricklefs & Renner 2012). Dunne et al. (2014) found a "modern" trophic structure in rich forests in Europe in the early Eocene, but exactly when this first appeared and what it implies in the context of animal-plant relationships is unclear. The first fossil record of l.t.r.f. from Asia are from the early Eocene 52-50 m.y.a. of western India (Rust 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. Tropical forests as we think of them, the "modern archetypal tropical rain forest" of Burnham and Johnson (2004: Table 1), with multi-layered vegetation, lianes, epiphytic ferns, bromeliads (New World) and orchids, the trees in particular having large seeds and relatively large leaf blades with dense venation and entire margins, seem to be a Caenozoic (Palaeocene-Eocene) phenomenon (Upchurch & Wolf 1987; Wing 1987; Eriksson et al. 2000a; Morley 2000: general account; Pennington et al. 2006a; Schuettpelz 2006; Boyce et al. 2009: Schuettpelz & Pryer 2009; Crane & Carvell 2007: the early Caenozoic fossil record; Burnham 2009: climbers; Watkins et al. 2010).
Perhaps the extant pollinators of clades that also were to be found in these forests ecologically "took over" older clades in which there were already established animal-plant relationships (suggested by Janzen 1980). Mayr and Wilde (2014) described an Eocene bird, Pumiliornis, probably nectarivorous, in deposits ca 47 m.y.o. that they thought pollinated flowers, and they suggested that the clade of plants it pollinated might now be pollinated by different birds, so a pollinator switch must have occurred (see also below).
Many angiosperm groups have diversified since the Cretaceous, including speciose clades that often include many herbaceous and/or shrubby taxa (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 Caenozoic. Woody Fabaceae are prominent in tropical forests, while core Lamiales with monosymmetric flowers include many species pollinated by recently-evolved generalist pollinators like birds and corbiculate bees. Diversification of Asteraceae (23,000+ species: K.-J. Kim et al. 2005; Funk et al. 2009c for a summary) is also Caenozoic in age. In far older clades like Myristicaceae, crown group diversification is Caenozoic, but the earlier history of the group is largely unknown (J. A. Doyle et al. 2004, 2008; Scharaschkin & Doyle 2005; Richardson et al. 2004; but c.f. in part Couvreur et al. 2011a, c).
Around 53.5% of vascular plants are herbs, which would suggest that there are about 132,000 species of herbaceous flowering plants (Fitzjohn et al. 2014; Ølgaard 2000: 65,000 species). The high assimilation rates facilitated by high venation density may, in conjunction with a shortening of the life cycle, particularly the pre-fertilization gametophytic stage (e.g. Williams 2012b), etc., have enabled the evolution of annual herbs (Boyce & Leslie 2012). This life form is exceedingly uncommon in other vascular plants, fossil or extant (Boyce & Zwieniecki 2012). Maybe species of flowering plants are annuals.
Palaeocene-Eocene diversification in l.t.r.f. took place in a warmer world with flatter temperature gradients and with the continents in rather different places than they are now. Boreotropical migration and extensive long distance dispersal were important in shaping the assembly of tropical forest biomes (Thomas et al. 2015 and references). The role of India in "seeding" tropical diversity is unclear. Early Eocene dipterocarp resins have been found there, and its biota seems not to indicate particular isolation (Rust 2010). More plants (and animals) with dramatically different past and current distributions are being found and suggests that the composition of past floras is hard to predict.
Diversity may have been high in the early Eocene and the forests may have been quite like extant l.t.r.f.. However, what plant-animal associations looked like then is unclear. Major diversification of birds, both pollinators (hummingbirds, various passeriform groups) and fruit-dispersers (pigeons and parrots) (e.g. et al. ; Jarvis et al. 2014; see also Wright et al. 2008 for parrots), the successfull generalist orchid and bumble bees, fruit-eating mammals, especially fruit-eating and nectarivorous bats and fruit eating primates, and arboreal and seed-eating and -dispersing ants (Ward 2014), was in or after the Oligocene ca 40 m.y. ago. Conspicuous elements of today's vegetation like grasslands and savanna are still younger, most being less than 15 m.y. old.
Increased plant productivity and diversity would allow animals that ate, pollinated (e.g. birds, butterflies, bees) or dispersed (e.g. ants, mammals, birds) angiosperms to diversify (see also Boyce et al. 2010). Thus Novotny et al. (2010) noted that congeneric rather than confamilial, etc., plant species tended to share herbivore species, so as phylogenetic diversity increased, so would the number of herbivore species.
Paragraph out of place. 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 angiosperm evolution. It 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.
7. Flowers and Pollination.
Here I think of some general aspects of angiosperm reproduction in a rather conventional way, i.e. as flowers (and fruits) being a key to understanding angiosperm diversification. I outline the general distribution of particular flower "types" with respect to phylogeny. For details about the interaction of particular groups of pollinators with the flowers they pollinate, see below.
7A. Flowers, Pollination and Fertilization. Most narratives of angiosperm evolution focus on flowers and fruits and their influence on speciation. The flower can be considered a key innovation or a group of innovations. and the success of angiosperms has been attributed in considerable part to the evolution of flowers (e.g. Eriksson & Bremer 1992; Dilcher 2000). 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. 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, given a heterogeneous environment, speciation (e.g. Kay et al. 2006; Kay & Sargent 2009).
Adoption of syncarpy was an important evolutionary event (e.g. Friis et al. 2006b). It has evolved seventeen or more times, and a compitum, which allows pollen tubes from one stigma to fertilize the ovules in more than one carpel, evolved in three quarters of these cases (Armbruster et al. 2002). Many members of the ANITA grade (perhaps not Cabombaceae) have an extragynoecial compitum (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 male 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, herkogamy, i.e. protandry or protogyny (the latter is the basal condition for flowering plants). Closed carpels also protect the ovules and 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).
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; Nowack et al. 2007). (Comparable tissue in gymnosperms is the massive female gametophyte.) 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 endosperm is unclear. However, a higher ratio of paternal genes in diploid compared to triploid endosperm (1:1, vs 1:2) 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. 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.
A number of changes in the gametophyte phase of the angiosperm life cycle result in its usually being notably shorter than that of extant gymnosperms (Williams 2012b). The pollen tube growth rate in angiosperms is much higher than that of extant gymnosperms - 80-600 µm/hour in ANITA-grade angiosperms (overall 60[Fagaceae]-20,000 µm/hour) versus 10-20 (Gnetum, the high end of the spectrum) µm/hour in gymnosperms (Hoekstra 1983; esp. Williams 2008, 2009; also Rudall & Bateman 2008). Fertilization occurs within about 24 hours of pollination in most angiosperms as compared to seven days or often far more in extant gymnosperms (Williams 2008). The development of callose plugs and callose in the pollen tube wall probably enables the pollen tube to grow faster, and callose tubes and fast growth rates are both apomorphies of angiosperms. Although callose synthase genes are expressed in at least some gymnosperm pollen, the pollen tube there is cellulose-based (Williams 2008; Parre & Geitmann 2005: mechanical properties of callose; Abercrombie et al. 2011).
Much growth of the gymnosperm female gametophyte occurs after pollination but before fertilization, and although less in Gnetum, even there the ovule increases appreciably in size after pollination. The ovule grows little after fertilization since reserves for the developing ovule have already been sequestered in the large female gametophyte. On the other hand, there is usually little or no increase of angiosperm ovule size after pollination and before fertilization. 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 (Haig & Westoby 1991; Leslie & Boyce 2012; Sakai 2013). Since few reserves are committed to angiosperm ovules with their tiny mature female gametophytes, when unfertilized ovules abort, little is lost, but the converse is true in gymnosperms.
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), and the evolution of carpels faciltates 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). Within gymnosperms, some Gnetales (Ephedra) are mature by about 7 years, however, 20-100 years are ages for other gymnosperms (B. Wang et al. 2015).
7B. Major Clades With Monosymmetric Flowers. Successful animal pollination entails that the pollinator follows a more or less complex and specific set of cues. Early angiosperms seem to have had what would be described as rather generalized flowers (see below). A number of large clades (2,000+ species each) can be characterised by specialized floral features that seem likely to affect diversification/speciation. Five of these major clades, Orchidaceae, Zingiberales, core Lamiales ([[Calceolariaceae + Gesneriaceae] The Rest]), Fabaceae, and Asteraceae, have a preponderance of members with monosymmetric flowers, although reversion to polysymmetric flowers has also occurred, most notably in Fabaceae-Mimosoideae. Together with some rather smaller clades, e.g. Campanulaceae-Lobelioideae, Caprifoliaceae, some Iridaceae, they include almost one third of all angiosperms. 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.
Diversification as a possible result of the acquisition of monosymmetry can be studied on much iner 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. In fact, monosymmetry has evolved hundreds of times (see also Endress & Matthews 2006a; Endress 2008a; Jabbour et al. 2009, esp. 2014), and even within Asteraceae different CYC2c paralogs are involved in the expression of the monosymmetric (ray flower) phenotype (Chapman et al. 2012). The number of origins of monosymmetry hypothesized 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.
Indeed, as more becomes 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 monosymmetric 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, many more or less compact inflorescences are functionally polysymmetric or haplomorphic flowers, the often strongly monosymmetric peripheral flowers in Asteraceae, some Brassicaceae (e.g. Busch & Zachgo 2007), Adoxaceae and Apiaceae being the visual equivalent of petals to the pollinator. Inflorescences may also be the functional equivalent of a single monosymmetric flower, as in Euphorbia-Pedilanthus, etc., while the polysymmetric flowers of Iridaceae may be the functional equivalent of a small inflorescence with three monosymmetric flowers.
Taxa. There are five particularly 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 to few seeds that are 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 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 in the tropics. 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, although some clades have fleshy fruits. 6. Caprifoliaceae comprise some 850 species; the flowers are often rather weakly monosymmetric and the often indehiscent and dry 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 monosymmetric flowers of one sort or another. The fruits have a moderate number of seeds. 9. Polygalaceae, with some 1,050 species most of which have monosymmetric flowers, 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 myrmecochory is common.
The final clade to be mentioned is 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 for the diversity of secondary metabolites they contain. Again, exactly where acquisition of monosymmetry is to be fixed within Asterales is unclear.
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, 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). Oligolectic (specialist) 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 the more polylectic derived megachilids commonly pollinate monosymmetric Fabaceae and Lamiaceae (Westerkamp 1997), or polysymmetric Boraginaceae (Litman et al. 2011; Sedivy et al. 2013).
The polylectic (generalist) euglossine and bumble bees (see below) in particular pollinate flowers with complex, monosymmetric corollas that the animal has to learn to work before visits are effective; Westerkamp and Claßen-Bockhoff (2007) consider such flowers to be the "ultimate response" to bees. Bumble bees in particular appear to have an innate preference for monosymmetric flowers (Leppik 1957; Kalisz et al. 2006; Rodríguez et al. 2004). Birds also visit monosymmetric flowers, and in the gullet-type ornithophilous syndrome stamens in the mouth of the flowers often deposit pollen on the head of the pollinator. The evolution 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; for dichogamy, see e.g. Bertin & Newman 1993; Routley et al. 2004).
Most of the plant clades just mentioned are more or less herbaceous, and among extant lignophytes, the herbaceous habit is known only in angiosperms while the annual habit is not known in other vascular plants. 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 with trees, shrubs, or simply to plants with long life cycles. For instance, within commelinids 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, or at least, depending on the sister group that is chosen. Y. Yang et al. (2015: focus on Caryophyllales) confirmed this, taking into account synonymous and non-synonymous sites in protein-coding genes.
This correlation may be connected with mutation rate or population size and thence to speciation rate (Gaut et al. 2011 and references). There is a general correlation between rates of molecular evolution (substitution rates) and the rate of speciation, 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). Herbs also show an increased rate of climatic niche evolution (Smith & Beaulieu 2009). The evolution of herbs 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). However, in the fire-prone Mediterranean ecosystem neither diversification nor molecular evolution differs between seeders and resprouters, two ways in which plants survive fires, yet seeders, having shorter generation times, should perhaps have diversified more (Verdú et al. 2007).
Trees may have a distinctive evolutionary rhythm, speciating rather slowly; any one species may have quite large numbers of individuals, and although they may be rather dispersed they are long-lived, the species themselves also being rather long-lived (Petit & Hampe 2006). Trees tend to have lower rates of molecular evolution perhaps because growth/mitotic rates slow down in meristems a long way from the ground (Lanfear et al. 2013; Bromham et al. 2015).
To summarize: Much angiosperm diversity, but not necessarily 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 associated with particular clades within those orders (see the euasterids). Interestingly, monosymmetric flowers are uncommon in the Cretaceous (Friis et al. 2011).
7C. Major Clades With Wind-Pollinated Flowers. 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 1. 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). 2. Cyperaceae-Juncaceae, also with more or less reduced flowers and usually with single-seeded fruits, contain about 4,800 species. 3. 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.
In wind-pollinated angiosperms there has been selection for small flowers, monoecy is common, pollen is smallish, smooth and often some kind of porate, and there is a reduction in ovule number per flower, most wind-pollinated taxa having few to a single ovule per flower and single-seeded fruits, coupled with a high pollen:ovule ratio (e.g. Linder 1998; Culley et al. 2002; Friedman & Barrett 2008, 2011). For the evolution of dioecy, see Dufay et al. (2014) and Renner (2014) and references; monoecy and dioecy (ca 15,600 species), woodiness, and the wind pollination syndrome are associated features. D. W. Taylor et al. (2012) suggested that in Fagales, at least, the evolution of monospermous fruits occurred before the evolution of wind pollination, furthermore, many fossil Normapolles plants (Fagales) have perfect flowers and even nectaries (Friis et al. 2011).
Kay and Sargent (2009) noted that Poaceae and Cyperaceae/Juncaceae were exceptions to the rule that animal pollination led to an increase in speciation rate, each clade 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; the relationships of the [Thurniaceae [Cyperaceae + Juncaceae]] are 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.
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 really 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. Ca 1,300 species of bamboos are woody 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 fungal 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 (but not against that by mammalian grazers), 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, have 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).
8C. Wood and Litter Decay. Another element of the ecological impact of angiosperms 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 of 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 are features of many angiosperms, and they are implicated in speedy litter breakdown. Thus 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 higher MA than do angiosperms (Berendse & Scheffer 2009 and references). However, low MA per se is unlikely to be the only factor speeding breakdown of angiosperm remains.
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). Although angiosperm woods are on the whole denser than gymnosperm woods, they decompose faster (Weedon et al. 2009); brown rot fungi, which do not degrade lignin, are more common in conifer forests than lignin-decaying white rot fungi which are common in angiosperm-dominated forests (Boddy & Watkinson 1995), although it should be noted that the distinction between the two is somewhat artificial (Riley et al. 2014; Floudas et al. 2015). 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). Overall patterns of wood decomposition vary in detail, and differences in decay rates depends on the local decay organisms and tree species, and even on the age of the tree (Weedon et al. 2009). The chemistry of woods is complex (e.g. Kögel-Knaber 2002)!
Graminoid litter, i.e. that of Poaceae and Cyperaceae, decomposes more slowly than that of forbs (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 their 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 silicon concentration, and this is especially high in the annual species (Cooke & Leishman 2011b).
Mean annual precipitation 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).
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). Fast decomposition of angiosperm litter, particularly associated with the deciduous habit (Knoll & James 1987), speed up nutrient cycling and plant growth (Cornwell et al. 2008; Berendse & Scheffer 2009). The high photosynthetic rates of most angiosperms allow high growth rates and the nutrients they need are released by the fast decay of their litter; eudicot angiosperms in particular may utilize any flushes of nutrients produced by litter and wood breakdown, they scavenge nutrients effectively (Berendse & Scheffer 2009). The disturbed habitats of early angiosperms 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), 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).
Liu et al. (2014) pointed out that leaves of most magnoliids have a high SLA and decompose relatively slowly, they are "slow return" leaves, compared with other large angiosperms (see also Cornwell et al. 2014). Magnoliid taxa like Piperales with more quickly decomposing leaves are smaller plants (Liu et al. 2014). The litter of ectomycorrhizal trees also 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). 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). Fire also removes dead organic matter and affects the availability of plant nutrients (see elsewhere)
Limited data suggest that root diameter has decreased in in angiosperms (so the SRL increased - root length per unit biomass) other than magnoliids and the ANITA grade, so allowing for more efficient exploration of soil space to satisfy the increased water demands of the plant and more efficient nutrient scavenging in the high latitude/nutrient poor soils where ECM plants are so prominent (although there seem to be no comparisons specifically between ECM and VAM plants); the hair-like roots of Ericaceae with ericoid mycorrhizae at ca 40µm across are perhaps the finest (Comas et al. 2012). There were also changes in wood anatomy during this period (Wheeler & Baas 1991).
8. 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 involving quite small clades of animals and plants. There are two rather different kinds of these asymmetries. One includes small (in terms of species numbers) clades of animals 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 biome functioning globally, 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.8A. Plant-Animal interactions.
POLLINATION - INTRODUCTION.
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'.". They did provide an estimate - around 308,000. However, for questions like "How many species of plants are dispersed by [such and such a group of] bats?", and "How many species are pollinated by [such and such a group of] of bees?", it is very difficult to obtain reliable estimates.
Estimates of the numbers of species of particular groups 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. 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, 2007; Thompson 2009; Crone 2013). Relationships between plant and pollinator are by no means constant (e.g. Aizen et al. 2012; Natalis & Wesselingh 2013), and 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). Some bees visiting flowers may not be effective pollinators at all, but they scavenge pollen remaining after pollination had actually occured, or being otherwise irrelevant to the pollination process, the plant and insect having some kind of commensal relationship (Linsley 1958; Linsley et al. 1973; Michener 1979; Roubik 1989; Roulston et al. 2000: p. 618).
The estimates below are based on very scanty observations sometimes extrapolated to flowers in the same immediate clade with a similar floral morphology; floral syndromes have been used, despite the problems mentioned earlier. Interestingly, 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, perhaps because the bird would have a better chance to "learn" the local flora. Along the same lines, 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). 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. The pollination behaviour of birds on islands may differ from that on the mainland, the birds being more promiscuous in the plants they visit (Traveset et al. 2015: "interaction release"). Nectarivorous birds may visit a variety of flowers usually pollinated by other animals (e.g. Muruyama et al. 2013), while other animals may on occasion pollinate flowers visited by humming birds (e.g. Snow & Snow 1980; Brown & Hopkins 1995; Fleming et al. 2005). All this emphasizes the amount of salt needed when reading the figures below: Estimates of numbers of pollinators rely in part 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 (visited by male bees for fragrances), and Zingiberales, especially Costaceae (ca 19 species of Costus - Salzman et al. 2015) 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 one species of Euglossa might visit 74 species of plants from 41 families - and that at a single locality.
Crown group euglossine diversification probably began 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, 26(-17) m.y.a. (Cardinal & Danforth 2011; Martins et al. 2014).
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.).
Flowers with a diversity of morphologies in temperate and Arctic-Alpine floras in particular are pollinated by bumble bees. Ericaceae, including Rhododendron and Vaccinium, are common in Arctic communities, but practically all conspicuous flowers in these habitats are visited by the bees (e.g. Ranta & Lunberg 1981; Tomono & Sota 1997; Kudo et al. 2011 and references). I have not found estimates for the number of species involved, but it 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. Lamiaceae and many other Lamiales, Fabaceae, particularly Faboideae, and Impatiens (Balsaminaceae) are also often visited (Williams et al. 2009). Most of the 600-700 species of Ranunculaceae-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 bumble 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 and elsewhere visit monosymmetric flowers (Raine & Chittka 2007a, b; Goulson & Darvill 2004), and they can also handle polysymmetric flowers quite easily (Laverty 1994; Sedivy et al. 2013). Many bees are more specialized in pollen collection than in nectar foraging (for nectaring, see Raine et al. 2006); learning to handle pollen flowers is quite difficult even for bumble bees (Strickler 1979; Goulson & Darvill 2004; Benton 2006; Raine & Chittka 2007b; Ghoulson 2010). Bumble bees are effective buzz pollinators (Goulson 2010). Some 4,000 species of angiosperms, mostly core eudicots, are buzz pollinated, and the distinctive floral syndrome has evolved many times (Buchmann & Hurley 1978; Buchmann 1983). ?Other bees doing this.
Local diversity of bumble bees can be quite high, with 4-12 species occuring in one community (Hines 2008 and references), and one fifth or more of the world's bumble bee species (40<) 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 may be considerably more, 100-80 m.y.a. (Hines 2008; see also Martins et al. 2014); Cardinal and Danforth (2011) suggest a somewhat more recent age for crown-group bumble bees of (31-)21(-12) m.y. ago. 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.
Stem-group Apis 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). Other estimates for the age of the group are (30-)22(-16) m.y.o. (Cardinal & Danforth 2011; Martins et al. 2014)
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. (2014a) found Centradini to be paraphyletic, Epicharis diverging (102-)91(-79) m.y.a. and Centris (95-)84(-72) m.y.a., about contemporaneous with the stem-group age of Malpighiaceae, estimated at (100-)86(-73) m.y.a. (Xi et al. 2012b: other estimates are 75-60(-32) m.y.a. (Wikström et al. 2001; Davis & Anderson 2010; Renner & Schaefer 2010). This is 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 Epicharis are (39-)28(-18) m.y.a. and of Centris (58-)44(-36) m.y.a., all (much) younger. The malpig Eoglandulosa warmanensis from the Eocene Claiborne Formation in Tennessee, U.S.A. in deposits of ca 34 m.y.o. has distinctive paired calyx glands and may have been pollinated by such bees (Taylor & Crepet 1987; Friis et al. 2011). However, details of the evolution of the association between the bees and malpigs are not clear.
Some 1600-2,000 species of oil flowers in 11 families are pollinated by females of 365-447 species of bees (Alves-dos Santos et al. 2007; Martins et al. 2013, 2014 for general statistics).
All told, some 12 species of flies pollinate around 108 species of plants, although the latter figure is likely to be a considerable underestimate. Iridaceae figure particularly prominently, with about 34 species being pollinated by Nemestrinidae - but 100 more are thought to be pollinated by the flies (Manning & Goldblatt 1996, 1997; Goldblatt & Manning 2000)!
In the estimates below of numbers of plants visited I have focussed on larger clades of plants and on literature covering flower visitation in particular regions. As a result taxa like Brachychiton are probably included (in the general figures for bird visitation in Australia), as the 40 or more Old World bird-pollinated species of Erythrina (Bruneau et al. 1997), while species like Holmskiodia sanguinea are probably not (see also Porsch 1936 and references for early literature). I also focus on 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 are responsible for some records of "bird-pollinated flowers"; orioles are particularly important pollinators in drier forests (Stiles 1985). For a recent summary of many aspects of bird pollination, see Fleming and Kress (2013).
Humming birds may be trap-liners, generalists, territorial, or "parasites", visiting flowers normally visited by other kinds of humming birds (e.g. Feinsinger & Colwell 1978). The trap-lining hermits, Phaethornithinae, sister to other humming birds (Bleiwiss 1998a), or with topazes, sister to the remainder (McGuire et al. 2014), tend to be more common at lower altitudes in the Andes, and several clades have independently moved into high-altitude habitats (Bleiwiss 1998b; McGuire et al. 2007 and references). Humming birds often visit herbaceous plants, in part because they do not need perches when feeding (e.g. Stiles 1981; Kress & Beach 1994; Fleming & Muchhala 2008).
Some 1,000 or more species of Ericaceae-Vaccinioideae-Vaccinieae and Gesneriaceae-Gesnerioideae (around 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. Just about all sizeable sympetalous families in the humming birds' ranges, including Rubiaceae (especially important) are visited, as are the polypetalous Rosaceae, Melastomataceae and Symplocaceae, ca 27 species of Costus (Costaceae: Salzman et al. 2015), etc. (see e.g. Snow & Snow 1980; Sazima et al. 1996 for other examples).
Humming birds, 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 place, up to 25-30 being recorded from a single local assemblage (Graham et al. 2009, 2012), and the common species at least visit several species of plants. Figures in Fleming et al. (2005) are 3-28 species per site, pollinating 14-51 species of flowers, mostly herbs, 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 the plants (Dziedzioch et al. 2003), while in the Monteverde forest, Costa Rica, 23 species of humming birds (excluding 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; see also Maglianesi et al. 2014). 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 visited by four species of birds. Depending on the birds and plants in the community, different foraging types of humming birds will visit different species of plants (Feinsinger & Colwell 1978); 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; Jarvis et al. 2014). Rather surprisingly, there are fossils assignable to stem- humming birds that apparently were nectar-eaters from Oligocene Europe in deposits ca 34.3 m.y. old and they are quite similar to Trochilinae (Mayr 2004; Louchart et al. 2008); there are also fossils of stem-group humming birds from the Late Eocene of the Caucasus (Louchart et al. 2008). Crown-group humming bird diversification may have begun in South or Central America, e.g. in lowland South America as late as (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 and McDade (2014a) estimated crown-group diversification to have begun (29.9-)28.8(-28.4) m.y. ago.
The overall imbalance of species numbers of humming birds/plants pollinated is probably similar to the euglossine bees just mentioned, with around 338 species of birds pollinating about 5,000 species of plants (over 4,040 species above, but this is still a considerable underestimate), a ratio of almost 12:1. The long-billed hummingbird Ensifera ensifera visits some 37 species of Andean Passiflora supersection Tacsonia alone as well as a few other species (Abrahamczyk et al. 2014).
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 there are around 60,000 species of flowering plants in Amazonia, that would suggest 12,000 species were pollinated by the 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 flora; Stiles (1985) estimated a total of 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 1994 estimate 1,280 species of flowering plants). The numbers offered by Stiles (1985) extrapolated to the whole of Amazonia give a figure of 2,625 humming bird-pollinated species there.
These pollinators belong to two major clades. Lorikeets probably date from the early Caenozoic (see Fleming & Muchhala 2008), e.g. ca 35.6 m.y.a. is the increase of diversification represented by the true parrots (Jetz et al. 2012). All the rest are Passeriformes. 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). Yuhina), Timaliidae, is paraphyletic to white eyes s. str., and the whole clade (= Zosteropidae/Zosteropinae) began diversifying 8.1-6.31 m.y.a., Zosteropidae s. str. diversified 5.6-4.5 m.y.a., and the speciose Zosterops itself a mere ca 1.8 m.y.a. (Moyle et al. 2009). For a phylogeny of Meliphagidae, see Driskell and Christidis (2004), and Barker et al. (2004) suggested that diversification occurred 50-45 m.y.a. in the Eocene (see also Friis et al. 2011). However, Jarvis et al. (2014) estimated that that part of the very speciose Passeriformes which includes all these birds may not have begun diversifying until much more recently in the Oligocene ca 30 m.y. ago.
Plants visited by Old World nectarivorous birds are mostly woody, in part because the birds perch 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 separately.
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 (this includes New Guinea), a figure that he thought was very definitely an upper estimate. Estimates in Fleming & Muchhala (2008) are 56 genera and 242 species, of which over 60% are honeyeaters, but perhaps only about half the honey eaters, ca 80 species, are nectarivorous, individual species varying considerably in their diet (see also Recher 1981).
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 (estimates 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) - and (pers. comm.) estimates around bird-pollinated species in the family. 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 of ca 37 species of 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. (Cheke and Mann  had suggested that honey eaters alone visited about 450 species of flowering plants from 100 families.) The proportion of ornithophilous flowers may be relatively high on that continent since the copious nectar produced incurs little 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 general 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 the old genus Agapetes, with about 95 species in its centre of diversity in southwest China and adjacent Myanmar and India that also often have red, tubular flowers (see also below). In addition, the widespread Aeschynanthus (Gesneriaceae) has red flowers with the gullet syndrome includes around 185 species. There may be some 36 species of bird-pollinated Loranthaceae in China (Qiu & Gilbert 2003) and 165 in Malesia (Barlow 1998). The ca 14 species of the largely New Guinean Tapeinochilus (Costaceae), are likely to be pollinated by sunbirds (O. Gideon, in Salzman et al. 2015). 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 mentioned above, 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 is particularly difficult since one of the common pollinators, the white eye Zosterops lateralis, arrived from Australia in 1855, three other species have suffered serious recent declines, while the stitchbird Notiomystis cincta is in a monotypic family, Notiomystidae, and is unrelated to any of the other passeriforms so far mentioned (Kelly et al. 2010).
In New Caledonia some 17 species of Cunoniaceae, mostly Geissois, have red, brush-type flowers that are thought to be bird-pollinated (Hopkins et al. 2014). Add Metrosideros
Africa, especially The Cape. 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 there are 64 bird-pollinated species of Iridaceae (Goldblatt & Manning 2006) and 13 species of Cyrtanthus (Amaryllidaceae) in southern Africa alone (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 also pollinate 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 African species are pollinated by birds, which, apart from the sugar birds, are mostly Nectariniidae and a few Zosteropidae. The relatively high frequency of ornithophily in the Cape flora may be connected with the prevalence of nutrient-poor soils there, as in Australia (Rebelo 1987; Orians & Milewski 2007).
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 the unrelated 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 alone 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).
Hawaiian-Oceanic Drepanidae are derived from a cardueline ancestor like a rose finch. 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. Pender et al. (2013) date the diversification of both birds and plants to within the last 17 m. years.
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 that 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, 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.
The bats have diversified within the last 30-12 m.y. (Datzmann et al. 2010), crown-group ages of the two clades involved being around (20.8-)17.5(-14.2) and (11.4-)11.1(-10.9) m.y., with stem group ages of ca 21.6 and 20.6 m.y.a. respectively (Baker et al. 2012). Similarly, Fleming et al. (2009) date the evolution of bat-pollinated flowers to the Miocene ca 20 m.y. ago.
Estimates are that in the New World at least 500 species of plants in 27 families (Vogel 1969) or 590 species of plants in 43 families (Dobat & Peikert-Holle 1985) are pollinated by bats. Although other estimates are substantially lower, e.g. 364 species in 44 families (Fleming et al. 2009), such figures 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 and 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) estimate 17 species, 8 known to be bat-pollinated, 9 likely to be so.
IIIB. Pteropodidae. 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) in the macroglossine Pteropodidae (e.g. Fleming et al. 2009). The bats are found from Africa to Australasia and the Pacific (Fleming & Muchhala 2008), and 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).
Bats pollinate fewer than 200 species of flowers in the Old World (Dobat & Peikert-Holle 1985); 168 species in 41 families is the figure in Fleming et al. (2009).
To summarize differences between Old and New World nectarivorous birds and bats and the plants that they pollinate. Humming birds tend to pollinate herbs and epiphytic plants, while in the Old World nectar-feeding birds more frequently pollinate larger trees (e.g. Stiles 1981; Kress & Beach 1994; Fleming & Muchhala 2008). Both humming birds and phyllostomid bats, all 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 relationships 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). Phyllostomid bats are more efficient pollinators than humming birds, transporting larger amounts of pollen; bat-pollinated flowers evolved from bird-pollinated ancestors (Muchhala & Thomson 2010 and references). 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).
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 the issue here (see e.g. Armbruster 2014 for a recent review). Rather, 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 (the term has to be defined precisely when used, e.g. Hembry et al. 2014), mutualism, and the like.
Floral variation and plant-pollinator interactions have long been of central interest to biologists. Thus Stebbins (1970: p. 308) noted that in animals major groups tended to be rather invariant, differing in characters related to survival, and in plants reproductive features showed comparable invariance: 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-type relations between particular flowers and their pollinators implying 1:1 relationships between the two (e.g. Grant & Grant 1965), as pictures of birds with curved bills next to flowers with a similarly-shaped corolla tube suggest. Stebbins (1970), although cautious, conveyed the same general idea, as 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 some 352,000 species of flowering plants (the latter number from Paton et al. 2008). Sekercioglu (2006) suggested that some 600 species of birds visited plants for nectar, 350 more being casual visitors, and that they visited 500 (3.7%) of a total of 13,500 plant genera (his estimate). By extrapolation, and assuming that there are around 352,000 species of flowering plants and that there is no variation in pollen syndrome within a genus(!), some 13,000 species may be bird-pollinated. Bees are quite a diverse group, with some 17,500 species (Michener 2007), but it is particular groups of bees, not notably speciose, that play a disproportionately important role in current plant:bee interactions (see above; c.f. in part Cappellari et al. 2013: Fig 2B, C). Plants involved in such pollination asymmetries are only ca 3% (11,380) of all animal-pollinated plants, although this figure is likely to be a considerable underestimate.
There are marked asymmetries in the numbers of players in plant:pollinator relationships under discussion (e.g. Bronstein 1994: question 2; S. D. Johnson & Steiner 2000; Johnson 2010; Mello et al. 2012), and plant:pollinator ratios of 10:1 are at the low end of the spectrum. Wiens et al. (1983) expected to find similar asymmetrical relationships in plants with wind or water pollination, also in those pollinated by social bees, passerine birds, most flies, and perhaps beetles; they themselves looked at pollination of South African Protea species by small mammals. From the estimates given by Sekercioglu (2006), one species of bird would pollinate around 21 species of plants. In New Caledonia 43 species of native bees are the major pollinators of a flora of over 3,050 species of flowering plants, a plant:bee ratio of 71:1, which must be a considerable overestimate, but bears clarifying, while in New Zealand the ratio was 57:1 (Donovan et al. 2013). In the relatively well-studied Costa Rican flora, Stiles (1981) estimated that 55 species of humming birds pollinated mostly or exclusively around 300 species of plants. The long-billed humming bird Ensifera ensifera pollinates 37 species of the Andean Passiflora supersection Tacsonia - and some other plants (Abrahamczyk et al. 2014). 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, although he thought that the 15:1 plant:bird ratio was particularly high. Promerops is particularly attracted to 80 or more Cape Proteaceae, while perhaps 37 species, mostly other than Proteaceae, depend for their pollination on the malachite sunbird, Nectarinia famosa (Geerts & Pauw 2009). Long-tongued dipteran Nemestrinidae 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 alone 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 (Johnson & Bond 1994). In Western Australia, the New Holland honeyeater, Phylidonyris novaehollandiae, visits flowers of 142 species of plants in 32 genera and ten families (Brown et al. 1997). 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. For example, even if a single polylectic (generalist) bee species, or colony, or even an individual bee, may visit many species of plants, on any one trip a bee may be much more selective (e.g. Heinrich 1976; Chittka & Thomson 1997; Heard 1999; Hagbery & Nieh 2012 for general pollen/nectar constancy), and the bees may be locally functionally mono- or oligolectic (specialist). Similarly, the other pollinators mentioned may be widely distributed, and at any one place the plant:pollinator ratio is rather lower than the figures from, say, the whole of Costa Rica, might suggest (e.g. Rebelo 1987).
Understanding the relative timing of plant and pollinator diversification is important when thinking about the evolution of plant:pollinator relationships. If fossils are any guide, humming birds evolved before the plants they currently pollinate. Stem-group, but quite highly derived humming birds are first known from Europe (e.g. Mayr 2004; Louchard et al. 2008; Mayr & de Pietri 2014), but there is no evidence that both the birds and plants they pollinated co-evolved in some way there and then moved to the New World. Crown-group diversification in hummingbirds is estimated at (24.7-)22.4(-20.3) m.y.a. (see above). Diversification in 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). In the apparently less tight association of aroids with scarab beetles, the beetles diversified well before the plants (Schiestl & Dötterl 2012). However, not all dates are mismatches. Although the sword-billed humming bird 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., but we do not know when the sword bill itself evolved. Seven species of migratory humming birds pollinate ca 130 species of plants in the western United States alone, particularly at high elevations (Grant 1994; Grant & Grant 1968; Brown & Kodric-Brown 1979). These associations are dated to 9-5 m.y.a. (Abrahamczyk & Renner in Abrahamczyk et al. 2015). The fifteen species of humming birds that occur in the West Indies pollinate some 101 species (90 endemic) of plants in associations also dated 9-5 m.y.a. (Abrahamczyk et al. 2015), bird and plant diversifications being roughly contemporaneous (Abrahamczyk et al. 2015). New World Piper, whose seeds are dispersed by Carollia, a phyllostomid bat, presents problems. 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), a long time after the beginning of diversification of Piper that has been variously estimated at 111-34 m.y.a. (e.g. Martínez et al. 2014), so how this apparently close relationship developed is unclear (Fleming 2004).
The synchronous timing even in some classic examples of apparently strict floral co-evolution is breaking down. Examples are the yucca:yucca moth and orchid:orchid bee associations. 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 strict 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). 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., the dates being from three immediately unrelated clades of bee-pollinated orchids (Ramírez et al. 2011). Figs may be an exception (Cruaud et al. 2012a, b and literature). However, more than one species of wasps pollinates a single species of Ficus in about 30% or more cases. Co-speciation is possible in dioecious figs, less so in monoecious figs where co-pollinating species of wasp are not closely related in about two thirds of the cases (Yang et al. 2015 and references).
Ideas of hyperdominance may be applicable when thinking about such asymmetries. 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). Thus 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).
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). Individual plant:polylectic pollinator interactions may be very 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). Plants and hummingbirds may appear be mutually adapted, there having been "complementary trait evolution" (Maglianesi et al. 2014: p. 3325). But that characters are complementary in plant and pollinator does not mean that they are equally labile in the two. Many of these asymmetries involve 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). Similarly, Wiens et al. (1983) 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, while Stiles (1981) contrasted the behavioural flexibility of the pollinator (humming birds in this case) with the evolutionary flexibility of the plant.
In several of these quite small but very successful groups of pollinators that pollinate many species of plants it is difficult to maintain that much evolution of the pollinator is occurring at all (see esp. Thompson 2009; Guimarães et al. 2011). Plants exploit pre-existing perceptual/sensory biases of the pollinator, effectively manipulating their behaviour, and 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; Shrestha et al. 2013; Hembry et al 2014; c.f. Strong et al. 1984). Thus Dyer et al. (2012) found that flower reflectance curves in Australia matched those in the northern hemisphere, and had probably evolved to match colour discrimination by hymenopteran pollinators; the evolution of the hymenopteran visual system predates angiosperm evolution, and colour perception is not an apomorphy for bees (Chittka 1996). Long-tongued euglossine bees that pollinate a variety of Zingiberales, for example, have less specialized on these flowers than the plants have specialized on long-tongued pollinators (Borrell 2005; see also S. D. Johnson 2010). Sensory exploitation also occurs in pollination by deception (e.g. Schaefer & Ruxton 2009; Moré et al. 2013), but of course benefits there are one-sided.
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) is consistent with such ideas. Many plant:pollinator relationships are relatively recent, plant diversification being (substantially) later than pollinator diversification.
If the effects on the pollinator in such interactions were 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). In southern Africa a number of species of plants belonging to unrelated families depend on the services of a small group of nemestrinid pollinators (S. D. Johnson 2010; see also Huang & Shi 2013 and above), and Pauw et al. (2009) described rather diffuse co-evolution between individual species of these flies and and a group of species with long-tubed flowers. Interactions here take place in a complex geographical mosaic, with some of the flies having considerable infraspecific variation in proboscis length and a number of pollination ecotypes (e.g. Pauw et al. 2008; Newman et al. 2014; van der Niet et al. 2014; Anderson et al. 2014; see also Bascompte & Jordano 2007).
The challenge when thinking about floral evolution and pollinator preferences is to understand how the various changes in the animal partner that we now see as the features of a supergeneralist/"specialized" pollinator (Guimarães et al. 2011) arose. Co-evolution that involves at least some degree of cospeciation would suggest that both plants and pollinators diversified, there being some kind of mutual evolution and speciation. However, there is little evidence for such co-evolution 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; Placentini & Varassin 2007; Ollerton et al. 2009a; Fleming & Kress 2012: pp. 182-188), or for plant:pollinator relationships to involve reciprocal bursts of speciation (Hembry et al. 2014). Mutual co-evolution in the sense of Janzen (1980) may occur, with the complex geographical patterns of infraspecific variation in pollinators that have been documented providing the context for this (see also Cotton 1998: humming birds). On the other hand, the major plant visited may determine the pollinator morphology, other species evolving to "fit", advergent evolution (Anderson & Johnson 2009; Pauw et al. 2009; S. D. Johnson 2010).
A plant may change pollinators, even if its floral morphology remains largely unchanged. For example, the earliest 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, sunbirds and humming birds (Mayr & Wilde 2014). Whether any extant clade of bird-pollinated plants dates back to 47 m.y.a. is debatable, but if they do and they remain bird pollinated, they would have had to switch their partners (Mayr & Wilde 2014; see also Janzen 1980). Flowers pollinated by humming birds may have evolved in the Old World (examples given include Ericaceae-Agapetes and Bignoniaceae-Tecomaria capensis), but such flowers are now pollinated by sunbirds, Nectariniidae (Mayr 2005, 2009). A suggested age for the whole [Styphelioideae + Vaccinioideae] clade is only ca 37.8 m.y. (Wagstaff et al. 2010), while diversification of Nectariniidae may have occurred 45 m.y.a. in the Eocene (Barker et al. 2004). Jarvis et al. (2014) estimated that that part of the very speciose Passeriformes to which Nectariniidae belong may not have begun diversifying until the Oligocene ca 30 m.y. ago. The current plant:pollinator relationships have become superposed as it were on an earlier set of relationships, and how mutual these relationships might have been is unclear.
Parallel cladogenesis, plants diversifying earlier that their bird or bat pollinators, but with an overall similar pattern of cladogenesis, has also been invoked (Fleming & Muchhala 2008: plant family ages used). Fleming and Kress (2013: esp. table 5:3) list a number of examples of pollination and frugivory where they think particular plant groups become ""colonized" by a group of animals which then radiates in parallel with the plants" (ibid., p. 183). Examples they give include phyllostomid bats with Agavaceae and columnar cacti, Hawaiian Campanulaceae with honeycreepers, Asian Loranthaceae with Dicaeidae, frugivorous phyllostomid bats with Piper, Araceae, Cyclanthaceae, and Ficus, and Southeast Asian hornbills/birds of paradise with Meliaceae/Myristicaceae. However, it is unclear how parallel cladogenesis might work (see Fleming & Kress 2013: Fig. 5.4b).
Thinking about asymmetries in pollinator:plant relationships leads to a series of apparent paradoxes (see also Johnson & Steiner 2000). Snow and Snow (1980) noted that although a particular species of plant might have but a single humming bird pollinator, i.e., it was a specialist, a very specialized bird might pollinate several species of plants, i.e. it was a generalist. Similarly, specialized fruit-eating phyllostomid bats are generalists when looking at bat:plant networks (Mello et al. 2011a). The flowers visited by polylectic pollinators like humming birds and bumble bees are indeed specialized, often being monosymmetric, with concealed nectar, and so on. The morphology and behaviour of polylectic pollinators is by no means "primitive" or generalized. 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 that enable individuals to learn how to pollinate diverse flower morphologies ranging from simple to complex, and bumble bees can thermoregulate (e.g. Heinrich 1976; Laverty 1994; Raine & Chittka 2007a, b). However, in such situations one tends to think of both plant and pollinator as being specialists (for pollination/dispersal syndromes and guilds, see also characters).
Ollerton et al. (2007) distinguished between phenotypic generalization and specialization, thinking about the plant, and ecological and functional specialization, thinking about the pollinator, ecological generalization, emphasizing the numbers of pollinators, and functional generalization, their (difficult to quantify) diversity. Thus a species pollinated by 100 species of flies might be ecologically generalized yet funtionally specialized. As Ollerton et al. (2007: p. 725) noted, functionally and phenotypically specialised South American humming bird flowers might be visited by more than one species of bird (also functionally and phenotypically specialized), and so were "to some degree ecological generalists", the birds likewise being ecological generalists.
However, Rebelo (1987) suggested that both plants and pollinating birds in the South African fynbos were generalists, similarly, 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. Pauw and Stanway (2014) found that pollinators in some South African communities studied were often specialists, 154/217 species visiting only one species of plant, but the plants were generalists, 38/62 species being visited by more than two species of pollinator; how the former figures might change if other communities were studied is unclear.
Oligolectic bees 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 often refers to pollen-collecting behaviour, not nectaring, where bees tend to be more catholic - Waser et al. 1996). The bees may have few obvious morphological adaptations for pollination (Michez et al. 2012), and the flowers they visit are often what would be described as unspecialized and apparently accessible to a wide variety of pollinators, with radial symmetry, poorly concealed nectar, etc., although oligolectic bees may also pollinate monosymmetric flowers (e.g. Bawa 1990; Sedivy et al. 2008). Oligolectic bees, which are often solitary, are in general most diverse in arid often extratropical regions, 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 like deserts, the Great Basin, and parts of California and Chile there are many species of oligolectic/specialist bees (e.g. Waser et al. 1996) that 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). Such specialist pollinators may be less effective in and necessary for pollination than are generalists (e.g. Ehrenfeld 1979; Olesen 1997 and references). For example, the creosote bush, Larrea tridentata (Zygophyllaceae), common in the American southwest and with an open and "unspecialized" floral morphology, 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). Similarly, 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).
The plesiomorphic condition for pollination specificity in bees seems to be oligolecty (Danforth et al. 2006; Sipes et al. 2006; Michez et al. 2008); 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). Oligolecty may facilitate the evolution of large numbers of sympatric species of plants because each is pollinated by different species of pollinators (e.g. Linsley & MacSwain 1958), however, the behaviour of many polylectic pollinators would have the same effect, and anyhow, as just mentioned, several oligolectic pollinators may visit the one species of plant. Floral specialization has increased over evolutionary time, and unspecialised flowers probably pollinated by several species of oligolectic bees or other pollinators precede specialised flowers pollinated by one or a few species of polylectic pollinators. Monosymmetric flowers in which precise interactions between plant and pollinator are needed for effective pollination are largely a Caenozoic phenomenon, and they are likely to have polylectic pollinators. 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).
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. 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), and in the Mediterranean, Bombus and Apis were the most generalized visitors since they visited the most plant species (Olesen et al. 2007). In the humid tropics polylectic bees, which often live longer, are proportionally more common 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.
Many species of plants have specialized flowers and many species of bees, for example, visit a relatively few species of plants. Pollinator-plant relationships are not nested in any simple fashion: Specialist flowers interact more with polylectic pollinators, while generalist flowers often interact both with oligolectic and polylectic pollinators (e.g. James et al. 2012; c.f. Bascompte et al. 2003; Pawar 2014). 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 the pollinator may affect some of the plants it pollinates more seriously. The 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) 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 2013; esp. Suweis et al. 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 and frugivores being keystone clades that show phylogenetic niche conservatism (e.g. Fleming et al. 2005; S. D. Johnson 2010: see below) readily spring to mind.
9A2. Seed Dispersal.
Bats in which plant material is a major component of the diet are phyllostomids (New World) and pteropodids (Old World), and together they account for about 350 species, about 30% of all bat species (Baker et al. 2012).
Major diversification of fruit-eating phyllostomid bats, a clade of 68 species and twenty genera, began (27-)22(-18) m.y.a. in the late Oligocene to mid-Miocene (Datzmann et al. 2010; see also Rojas et al. 2011) or (18.6-)17.0(-15.4 m.y.a. (Baker et al. 2012), the stem-group age being around 17.0 m.y.a. (Baker et al. 2012). Of the more obligate frugivores Carollia has a stem-group age of about 17.6 m.y., while that of the [Stenoderma + Ariteus] clade, 8 species in eight genera, is ca 10.3 m.y.a., with a crown-group age of (6.2-)5.4(-4.6.) m.y.a. (Baker et al. 2012, q.v. for other estimates, all broadly similar). Bats can be very abundant, and species of New World phyllostomids are wide-ranging compared to Old World pteropodids (Muscarella & Fleming 2008).
Old World fruit-eating bats (pteropodids) tend to disperse seeds of later-successional trees in families like Sapotaceae, Meliaceae, Arecaceae and Rubiaceae (Muscarella & Fleming 2008), and thethese tend to be canopy trees with larger fruits. Pteropodids tend to be larger (less so in New Guinea) and they more commonly fly long distances (Cristoffer & Peres 2003). Crown dates for pteropodids are around (29-)24(-20) m.y. (Teeling et al. 2005) or (30.3-)25.1(-22.7) m.y. (Bininda-Emons et al. 2007).
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).8B. Carbon Sequestration.
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 by fixing and/or sequestering 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). The monodominance discussed here is more extreme, a single species representing 60% or more of the canopy individuals and/or basal area (Connell & Lowman 1989; see also Peh et al. 2011), and it is sometimes extended to include members of the one 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". Even if they are not strictly successional, some of the vegetation types mentioned may have been affected by human activities, as is discussed later.
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 150 "oligarchic" species (from several families) occured per hectare in Peru, and although they represented over 50% of the individuals, no species was close to being a monodominant, even by the somewhat relaxed definition sometimes adopted below. Building on this work, ter Steege et al. (2013) found that half the individuals with stems at least 10 cm across in Amazonian rainforests were accounted for by only 227 species in 41 families in 11 orders; they called these species "hyperdominants" (they would be hypodominants following classical ideas of dominance). In any one plot 32 of these species represented about 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. Fauset et al. (2015), also looking at these Amazonian forests, found that about 1% of the trees (ca 160 species) were responsible for around 50% of the above-ground carbon storage/biomass production, but again, single species or even species from the one family had relatively small effects. The maximum percentage of biomass represented by a single species was a mere 1.93% (VAM/ECM Eperua falcata:Fabaceae) and the maximum total biomass of any one family in the top 20 biomass accumulators was 4.96% (Fabaceae, 1/4 the species).
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). Different countries may have different definitions of "woodland", "grassland", "peat soils", and the like, and the distinctions between communities such as sea-grass, marine salt-marsh and mangrove 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.
C4 photosynthesis, 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). Perhaps the immediate drivers of the evolution of this distinctive syndrome are 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, but we still understand rather little about details of its origin and spread (see also Cowling 2013). For more details of the evolution of C4 photosynthesis, see e.g. Kellogg (2013a), 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). Grasses in general have a great effect on soils and weathering (see below). Grassland soils are notably moister than corresponding woodland soils, so leading to increased weathering and increased C sequestration, yet somewhat paradoxically grasslands support a drier climate, their transpiration being relatively low; woodlands have a lower albedo and transpire more, so their soil is drier. Evidence from palaeosols suggests that grasses replaced woodland (Retallack 2001, 2013a). Grassland grasses have dense root systems, and savanna trees allocate relatively more carbon to below-ground biomass than do forest trees, while in both Cerrado and African savanna 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).
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; the residence time for the carbon is much longer, largely because of the cooler temperatures.
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, Schizachyrum, Hyparrhenia), with some -- species, are prominent among the dominants (Estep et al. 2014).
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). 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).
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); and there can be impressive single-site fungal diversity (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, but c.f. van der Heijden et al. 2015).
The almost 4,000 species of Ericaceae with ericoid mycorrhizae (ERM), ectendomycorrhizae, are not included in the totals above. Vrålstad (2004), Villareal et al. (2004), Brundrett (2004), Tedersoo et al. (2010b) and others (see also above) 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), although unlike ECM fungi, ERM fungi are also more or less saprotrophic (Kohler et al. 2015). ERM are included in the discussion below, but orchid mycorrhizae (see Orchidaceae), 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 are generally woody, although there are some herbaceous ECM taxa, perhaps particularly in Arctic-Alpine environments (e.g. Newsham et al. 2009). ECM/ERM plants tend to dominate the communities in which they grow, although these communities are often 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). Many ECM plants are large individuals, each representing a substantial amount of standing biomass, and, very importantly, the soil is often acid and litter commonly accumulates, and peat formation is common (e.g. Yu et al. 2010; Page et al. 2011). 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, species of Vaccinium can be very abundant locally in montane forests in Malesia, and Rhododendron species can dominate locally in the Himalayas-Yunnan region.
Many vegetation types dominated by particular ECM species also include other ECM/ERM plants. Thus in the Mediterranean Maquis, ECM Cistaceae (close to Dipterocarpaceae), Fagaceae and Pinaceae are all important components of the vegetation. There are extensive oak-pine ECM forests in the eastern United States and Mexico, 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, and 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.
Many ECM plants have a distinctive ecological syndrome: They are trees, often locally dominant and casting deep shade; 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 deep leaf litter and accumulating humus (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 and Veller et al. 2015 for mast fruiting). Fabaceae-Detarieae have most of these features, but not all are mast fruiters, and not all Fabaceae that do have most of them, are ECM plants (see also Torti et al. 1997, 2001). Furthermore, 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, and 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). (Mast fruiting has been described from a number of trees and lianes from tropical French Guiana in South America, but these are not known to be ECM plants nor to be particularly dominant in the communities where they grow [Norden et al. 2007].)
Whether or not the establishment of conspecific seedlings is less affected than might be expected in ECM forests needs more study, but some evidence points in that direction; if confirmed, it would be consistent with the dominance shown by many ECM trees. In temperate forests the regeneration of the more abundant species (not necessarily ECM) may show weaker negative density dependence that that of the less common species (D. J. Johnson et al. 2012a, b; c.f. Dickie et al. 2012), perhaps enhancing their dominance, although this is not a general latitudinal effect (Comita et al. 2014). Whether the common species in ECM-dominated communities behave similarly is largely unknown, although this may be so in the ECM network in Dicymbe forests in Guyana described by McGuire (2007a, b). 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).
ECM, ERM, and their seed-plant associates together form the 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 plants like and VAM plants do not, and ERM Ericaceae are noted for producing nitrogen-poor litter that is slow to decompose (e.g. Read 1991); litter accumulation is also notable in tropical ECM communities (Torti et al. 2001). In Rhododendron, at least, nitrogen in stable protein-tannin complexes formed by the plant are more easily accessed by its own ERM associates than by ECM or VAM roots (Wurzburger & Hendrick 2009). Nitrogen mobilization is also affected by the polyphenols in the litter (e.g. Northup et al. 1995). Brown rot fungi are associated with conifer forests in partixcular, but they are unable to destroy lignin, which acculates in large amounts and binds nitrogen and cations (Eastwood 2011 and references). 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 make the kind of soil to suit themselves.
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 nutrient-poor humus unsuitable for VAM plants which are often faster-growing and need nitrogen. ECM and ERM plants can 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) 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, whether deciduous or evergreen (Pérez-Harguindeguy et al. 2000; Cornelissen et al. 2001; Alexander & Lee 2005; Cornwell et al. 2008; Lang et al. 2011) and conifer litter decomposes more slowly than that of angiosperms (e.g. Wardle et al. 2008; Cornwell et al. 2008b; Weedon et al. 2009); litter from ERM plants may be the most recalcitrant (Read 1991; Cornelissen et al. 2001; Alexander & Lee 2005).
Although aspects of this story, particularly the generality of any foliar traits of ECM plants (Koele et al. 2012; Liu et al. 2014 for Fagaceae), are questionable, the result of plant 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). 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.
There is a another aspect of ECM activities which affects global carbon balances. 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 other plants (e.g. L. L. Taylor et al. 2009). 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, 2014). 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). These low molecular weight organic acids can mobilize cations such as Ca++ and Mg++, increase phosphorus availability, etc. (Taylor et al. 2012); 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). 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). Quirk et al. (2014) showed that plants allocated more carbon to ECM than to VAM, and that ECM caused correspondingly higher rates of calcium silicate dissolution from basalt, a rate proportionally reduced when atmospheric CO2 concentrations were low. 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), and it is not for nothing that ECM fungi have been dubbed "rock-eating fungi" (Jongmans et al. 1997).
Dipterocarpaceae (Pakaraimaeoideae - blue; Monotoideae - green; Dipterocarpiodeae - red) dominate large areas of Southeast Asian l.t.r.f., forming extensive areas of peatlands. Most Dipterocarpoideae are Malesian, and in particular Bornean, and they are also abundant away from peatlands; 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 (11.5 x 106 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 ECM Fabaceae-Detarieae (see below).
Dipterocarpaceae occupy about 56% of the total tropical peatland area, close to 250,000 km2, about 6.2% of the global peatland area, and they dominate on huge peat lenses (Page et al. 2011, 2012; Richards 1996). This peat contains an estimated 68.5 Gt carbon, some 77% of the tropical and 11-19% of the global totals for peatlands (Page et al. 2011: above-ground biomass not included). 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 also include a substantial component of other ECM trees. (Other estimates are 84 Gt C in tropical peat - Rydin & Jeglum 2013 and references; also Immirizi & Maltby 1992; Rieley et al. 1996, etc., including estimates of pre-human peatland areas). 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. Peat deposits started to form in the late Pleistocene 40,000 y.a., and now the peat may be 25 m deep (Page et al. 2004, 2012; see Raes et al. 2014 for dipterocarps on the Sunda Shelf during glacial maxima).
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 west Amazonian forests largely similar in soil, precipitation, etc. (Banin et al. 2014). From these points of view, dipterocarp forests represent an extreme in the ecological spectrum represented by ECM plants. Amazonian peatlands sequester perhaps 9.7 Gt carbon, 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 largely unknown (Lähteenoja 2011; Lähteenoja et al. 2011).
Fabaceae are not generally thought of as being ECM plants, but Old World Detarieae, which dominate millions of square kilometres in Africa (blue in map), are ECM plants (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 3.27-3.75 x 106 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 inland from the coast from Sierra Leone to western Gabon, and again in the periphery of the Zaire basin (White 1983). 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, 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). Dicymbe has a remarkably high basal area of 38.4-52.5 m2 per hectare, around 25(-40) m2 being more normal figures (Henkel 2003).
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, listed by ter Steege et al. (2013) as being "hyperdominants", the ECM Eperua falcata (see Peh et al. 2011), along with E. leucantha (mycorrhizal status?), Detarieae, are notable as being 50% more abundant (usually far more) than any other non-palm on the list. However, biomass figures were not given. Peltogyne (Detarieae: ?mycorrhizal status) is a rare Amazonian monodominant, and 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). For further discussion on Amazonian "hyperdominance", see above.
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), while in mixed ECM temperate forests the half-life of conifer wood was about 20 years, but 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). However, Faison and Foster (2014) qualify earlier literature reports, i.a. noting that some of the apparent dominance of chestnut is likely to have been quite recent, being the result of coppicing after being cut down by early Europeans. In any event, it has 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 ECM trees.
Pinaceae (red in map above) are the major component of boreal/subarctic forests; there are also Salicaceae and Betulaceae, also ECM, while ERM Ericaceae are often common in the understory (e.g. Read 1991; Villareal et al. 2004; Vrålstad et al. 2002; Vrålstad 2004; Kranabetter & MacKenzie 2010). 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, 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).
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. 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). In younger forests cord-forming basidiomycete ECM were commoner, mycelial biomass turnover was fairly rapid, and little carbon was stored, in older forests ERM, with their decay-resistent melanized hyphae, were associated with increased carbon sequestration (Clemmensen et al. 2014). Indeed, the factors affecting carbon storage are complex. Pinaceae, for example, in boreal forests do not all behave the same. There is massive accumulation of non-flammable litter under genera like Tsuga and Picea while the litter of Pinus is much more flammable, burns more easily, and accumulates much less readily (Cornwell et al. 2015 and references). Furthermore, brown-rot fungi are commonly associated with Pinaceae, and these decompose wood less thoroughly than white-rot fungi, being unable to break down lignin (Riley et al. 2014; Floudas et al. 2015 and references: no sharp distinction between these two types of fungi).
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±5 x 1015 g and 9.7±2 x 1015 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.
ERM Ericaceae, a clade including Epacridaceae, Prionotaceae, Empetraceae and Vacciniaceae, are characteristic and often very common in heathlands world-wide (green in map above, inc. tundra: Specht 1979a; Read 1996: also Grubbiaceae and Diapensiaceae), 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 (Grubbiaceae also grow here) and Australia (see also articles in Specht 1979b). Tundra vegetation 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).
Tundra, Boreal Forests and Permafrost. ECM/ERM plants are abundant in boreal forests and tundra in particular, but also in many temperate forests, that are so abundant. Tundra-type habitats are often dominated by Ericaceae, Vaccinium and Empetrum being two of the seven prominent biomass accumulators there (Chapin & Körner 1995; Gardes & Dahlberg 1996; Kranabetter & MacKenzie 2010), and Read (1993) characterized the tundra by the prevalence of ericoid mycorrhizae. Three of the other major biomass accumulators, Salix, Betula and Dryas, are also ECM plants, while two Cyperaceae (Eriophorum, Carex: see below) are the others (see also Timling & Taylor 2012 for mycorrhizal diversity). ECM Polygonum (Bistorta) viviparum is a perennial herbaceous tundra plant, both as a pioneer and a prominent component of established vegatation (e.g. Gardes & Dahlberg 1996; Michelsen et al. 1998; Brevik et al. 2010). The mycorrhizal status of Diapensiaceae (Ericales) needs clarification; the family is not immediately related to Ericaceae, and only a single species, Diapensia lapponica, with a circumpolar distribution, grows in the tundra.
There is long-term storage of carbon in the extensive peat deposits in tundra, boreal forests, and heathlands. Estimates in MacDonald et al. (2006) are that northern peatlands stored 188-455 Pg carbon; Yu et al. (2010) thought that 547 gigatons of carbon were stored there, with an additional 15 gt in Patagonian peatlands; or some 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). Ericaceae 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). Soils contain most of the carbon in tundra ecosystems (e.g. Gorham 1991), and although the net primary productivity of Ericaceae may be high, they are only one the major sequesters of carbon in peat soil. We shall see that mosses, especially Sphagnum, are also important contributors to peat.
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. (2002, q.v. for detail; c.f. Tarnocai et al. 2009); areas with some, but less than 50%, permafrost are also extensive, but are not included. The permafrost area includes extensive bogs dominated by Sphagnum and Cyperaceae (e.g. Camill et al. 2001), and there are extensive areas of thick, carbon-rich sediment (yedoma), deltaic deposits, etc., and much of the carbon is below 200 cm (Tarnocai et al. 2009; Schuur et al. 2015). Tarnocai et al. (2009) estimated permafrost to occupy about 18 x 106 km2, about 16% of the global soil area. Figures for carbon storage in the tundra are about 158 PgC (Carvalhais et al. 2014: tables S1 and S2) and for that in permafrost areas 1,035±150 PgC (references in Schuur et al. 2015), the latter figure being about one third the global total (Jobb´gy et al. 2000: to 3 m depth). Ecosystem turnover times for carbon are longer in cooler climates: Times for tropical, temperate and boreal forests, and tundra are ca 14.2, 23.5, 53.3, and 65.2 years respectively, and above 75o N the mean turnover time is ca 255 years (Carvelhais et al. 2014).
Mosses are very important components of the tundra and boreal forests, and 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 tundra and boreal bryophytes and vascular plants (Verhoeven & Liefveld 1997: secondary metabolites; Lang et al. 2009; Lindo et al. 2013; Sistla et al. 2013; Rydin & Jeglum 2013). Sphagnum-dominated poor fens in northern Alberta may not be very productive, but respiration tends to be low, the plants start photosynthesizing early in the year, etc., so net carbon production may be higher than in, for example, Carex-dominated rich fens with their shorter growing seasons (Flanagan 2014; see also Ragoebarsing et al. 2005; Larmola et al. 2010; Hájek 2014; Bragina et al. 2104). Interestingly, the ERM ascomycete Oidiodendron maius is saprotrophic and can break down Sphagnum peat (Kohler et al. 2015).
The ecological role of Cyperaceae is poorly understood (Barrett 2013). Members of the family are often particularly common in rich fens 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; see also Flanagan 2014 and above), 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 single species of ECM Cyperaceae. Thus there are some 450,000 km2 of meadows between 3,000 and 5960 m altitude on the Tibetan plateau that are dominated by the ECM Kobresia pygmaea (Miehe et al. 2008, see also Zhou 2001). ECM species of Kobresia are widespread and sometimes dominant in other alpine, Arctic and tundra habitats (e.g. Gardes & Dahlberg 1996; Muhlmann & Peintner 2008; Newsham et al. 2009; Gao & Yang 2010).
Seagrasses, Mangroves, and Tidal Saltmarshes.
Sea-grasses, mangroves and tidal salt marshes all have carbon burial rates well over 100 g C M2 y-1, 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 can be for thousands of years, well over ten times as long as that in l.t.r.f. (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 30 x 106 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 amount of carbon in the sea-grass plant (= ramet) itself is small, that stored in the "soil", which can form mats up to 11 m thick, as 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, 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 22.8 x 106 (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 17.7-60.0 x 106 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, somewhat over 0.5% of the global total (Fourqueran et al. 2012; see Charpy-Roubaud & Soumia 1990 for estimates of benthic algal productivity). Carbon may be sequestered for 4,000 years or more in the anoxic sea-grass beds (Orem et al. 1999; Serrano et al. 2011, 2013).
To summarize. The sea-grass ecosystem 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).
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. ago. 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 (see Feller et al. 2010 for a good summary). 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 22.0-25.5 x 106 hectares (estimated, from Valiela et al. 2001, current figures corrected by 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 g C m2y-1, global primary productivity is 417 Tg C y-1, but with a rather lower net ecosystem production (221 g C m2 y-1, 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 where it made up 15% of the organic carbon accumulating in marine sediments globally; 10% of terrestrially-derived dissolved organic carbon in the oceans comes from mangroves (Dittmar et al. 2006). 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 13.8-15.2 x 106 ha). Mangrove peat can become very thick, and carbon in Caribbean peat has been dated to around 7,500 years old (McKee et al. 2007). (For salt and water balance in mangroves, see Reef and Lovelock (2015) and other papers in Ann. Bot. 115(3). 2015.)
In many parts of the world estuarine and salt marsh vegetation have been very considerably affected by human activity. This is reflected in changes in their floristic composition because of agricultural runoff, drainage or grazing, decreased extent because of reduced sedimentation or increased extent because of increased sedimentation caused by human-induced erosion (e.g. Chapman 1984; Brush & Hilgartner 2000; Kirwan et al. 2011; Mariotti & Fagherazzi 2013).
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 (2.2-40 x 106 ha in extent) are given by Mcleod et al. (2011): 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 g C m2y-1 and global primary productivity of 1438 Tg C y-1, while their net ecosystem production was 1585 g C m2 y-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.
Understanding ecophysiological relationships earlier in the Caenozoic, let alone in the Mesozoic, presents major challenges. There are three immediate issues that arise when thinking of the possible changes of carbon sequestration over time. 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 area estimates (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). Land clearance and the resultant increase in sediment in rivers facilitate the development of salt marshes in their estuaries (e.g. Kirwan et al. 2011; Chmura 2011), while agricultural nutrients in runoff negatively affect 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 can 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 above-ground carbon in forest throughout the whole Indo-East Malesian area is 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 grazing pressure associated with the spread of the Tibetan empire in the seventh century CE facilitated the development of the widespread ECM Kobresia pygmaea-dominated community of Tibet (Miehe et al. 2008, see also Zhou 2001).
The focus here is as far as possible on pre-agricultural vegetation, although 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 thinking about ecosphere effects of the vegetation over time is very difficult. How have the ecosystems with small groups of species that have 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.
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. 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); 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. As conditions change, different species may assume importance - and the history of the Caenozoic 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.
Over the last few hundred years human activities and changing climate may have had little effect on ECM activity, at least. 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 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). ECM trees remain important in Californian forests, even if tree size has changed and the ECM species are different (McIntyre et al. 2015).
However, 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). Many forest communities found in North America are Holocene in age, 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 "no-analog communities", communities with species combinations unlike those of any current communities, while Veloz et al. (2012) emphasize "no-analog climates". Similarly, realised niches may change, and, given enough time, fundamental niches may change, too.
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 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).
Further back in time, differences increase. 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 Caenozoic (e.g. R. Sage et al. 2012; Pennington et al. 2006b; Simon et al. 2009; Simon & Pennington 2012). The boreal biome, now dominated by ECM taxa, is dated to 10-4 m.y.a. (references in Fine & Ree 2006), and diversification of Sphagnum, now such a prominent and ecologically important component of boreal forest and tundra vegetation, is dated to the middle Miocene ca 14 m.y.a. (Shaw et al. 2010a; Shaw & Devos 2014; Johnson et al. 2015; see Graham et al. 2013 for Sphagnum-like fossils in Ordovician rocks 455-460 m.y.o.), evidence for this is wanting. Betula, now conspicuous in northern forests, has probably diversified within the last 10 m.y. (Xing et al. 2014).
The floristic composition of vegetation became much more "modern" in the latter part of the Caenozoic, 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, and the present is at beast an imperfect guide to the past (e.g. Meseguer et al. 2014b).
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), 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 in west North America. Mangrove peat, perhaps from a community dominated by Nypa, is known from the earlier Cenzoic of Guyana (Leidelmeyer 1966).
Latitudinal diversity curves were almost flat or even peaking in more temperate areas in the Mesozoic and early Caenozoic, the current curves, with diversity peaking near the Equator, are a phenomenon of a post-Eocene globe with strong 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 grow together, and 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). However, 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 the distribution of such trees in the early Caenozoic is an interesting unknown (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). 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 high latitudes (Daly et al. 2011: also Cupressaceae there, conflict between evidence from pollen and macrofossils), 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). Pseudolarix was widely distributed in the northern hemisphere at latitudes above 400 in the Early Cretaceous (Barremian, 115 m.y.a.), and the post-Oligocene cooling trend and Late Miocene-Pliocene mountain building would favour Pinaceae (LePage 2003). With the climatic deterioration of the Late Eocene-Oligocene, Pinus moved back to mid latitudes while persisting at higher latitudes (Miller 1993). In the Oligocene it moved into western Malesia (e.g. Muller 1972).
Plants with distinctive pollen assignable to the Normapolles complex and comparable with that of extant Fagales (but not Nothofagaceae or Fagaceae) were both diverse and ecologically prominent in the northern hemisphere from the Turonian-Campanian 94-80 m.y.a. (but c.f. Batten 1981, 1989; Clarke et al. 2011 for cautionary comments). The pollen peaked in the Coniacian-Santonian ca 88 m.y.a. being found in much of the area 20-45oN Cretaceous palaeolatitudes from eastern North America to west central Asia (Kedves 1989; Vakhrameev 1991; Sims et al. 1999; Friis et al. 2003a, esp. 2006a, 2010b and references). Elsewhere in the Northern hemisphere Aquilapollenites and Wodehouseia pollen, of uncertain affinities - Aquilapollenites has been variously linked with Santalales, Apiaceae and Caprifoliaceae-Morinoideae (Farabee 1993) - predominated, and in tropical Gondwanan areas pollen of Arecaceae was common. A temperate Gondwanan pollen province was characterized by Nothofagites pollen, probably from Nothofagus, also Fagales (e.g. Pacltová 1981 for a review; Kedves & Diniz 1983; Friis et al. 2006b, 2010b; Nichols & Johnson 2008). Nothofagus is thought to have dominated in mid-Eocene forest on Wilkes Land ca 660 S (Contreras et al. 2013). Pollen suggest that Fagaceae were diverse 42-40 m.y.a. in western Greenland (Grímsson et al. 2015). However, there has been little discussion about any ECM-associated activities of these plants.
The ecosystem functions emphasized here are carbon sequestration and to a lesser extent net primary productivity, but the two are not necessarily linked (Lähteenoja 2011). Carbon estimates can be of above-ground biomass, or in soils and peats, while 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 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), but above- and below-ground biomass, nutrient cycling and productivity all vary considerably.
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. ECM/ERM communities may not be notably productive, and those in the boreal zone in particular (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). 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 ECM-dominated 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). Bornean Dipterocarps show very high levels of above-ground wood production when compared with other species in the same community, and also when compared with forests in the western Amazon (Ecuador, Peru) that are similar in soils, precipitation, etc.; dipterocarps were more productive by as half as much again 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 Caenozoic (Pagani et al. 2009; L. L. Taylor et al. 2009, 2011; Quirk et al. 2014). 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, all three forming a functional whole (e.g. Landeweert et al. 2001; L. L. Taylor et al. 2009; Bonfante & Anca 2009).
Communities in which ECM clades dominate often grow under quite extreme environmental conditions, whether of substrate or climate (Read 1991). ECM Pinaceae (as well as other Pinales, which are endomycorrhizal), successfully compete with angiosperms, but not in the most productive environments (Brodribb et al. 2012), and the marine and estuarine environments inhabited by mangroves and sea-grasses are physiologically extreme for angiosperms.
In the more ecophysiological interactions under discussion, one or a few clades largely dominate important aspects of community/ecosystem functioning, thus relatively few clades of ECM plants occupy perhaps 50% of the earth's forested areas (L. L. Taylor et al. 2011). 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.
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, the ECM habit has originated several times in the N-fixing clade.
ECM associations have formed perhaps 78-82 times in fungi, especially in ascomycetes and basiodiomycetes, but also Zygomycota, with more to be discovered especially in tropical and south temperate areas (Tedersoo & Smith 2013); over 40 families of seed plants, most notably in Pinaceae and the N-fixing clade, 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). 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) (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. Kohler et al. (2015) suggest that ECM associations with plants have developed in the last ca 175 m.y., while a clade of ECM, brown rot, and one white rot fungus is dated to ca 115 m.y. ago.
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). Estimates of the age of crown-group Pinaceae range from (271-)153(-136) m.y.o. (Gernandt et al. 2008; Magallón et al. 2013) to 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. There are massive amounts of dipterocarp resin from India in the Early Eocene around 52-50 m.y.a. (Rust et al. 2010), diversification in Fabaceae is very largely Caenozoic, while the clade within Ericaceae for which ERM are an apomorphy is ca 65 m.y.o. (Wagstaff et al. 2010).
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; Quirk et al. 2012, 2014). If the present and past are connected, Normapolles and Nothofagites plants, along with most Fagales, were ECM; fossil remains of these plants are abundant in Late Cretaceous and early Cainozoic rocks (Friis et al. 2011 for a summary), and 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). ECM plants may even have progressively supplanted VAM plants at weathering hotspots from some time in the Cretaceous (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).
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 have been 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 (Plaziat et al. 2001; Ricklefs et al. 2006 for some dates; but see Martínez-Millán 2010 for Pelliciera). Nypa, today found only in the Indo-Malesian area, is known from 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).
The related ideas of keystone species and ecosystem engineers, species that directly or indirectly 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. The clades under discussion have major effects at ecological scales from the local community up to the global ecosystem. They 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 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), and 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, whether keystone clades or ecosystem engineers, they are not sharply distinguishable from all other clades in terms of their effects on the environment. The term "phylogenetic conservatism" has been used in various ways in the literature on phylogenetic community ecology (Mouquet et al. 2012a), while for demolition of the simple idea that there are keystone species - species "important for something", see Hurlbert (1997). 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.
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).
Overall, the implications of these asymmetries in relationships between animals, plants, and the environment, are complex, but it is clear that species numbers 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 the animals associated with them, at all levels.
10. In Conclusion.
Innovations in reproductive biology characterise the evolution of new plant groups, allowing increases in diversity in part by greater subdivision of the environment (e.g. Niklas et al. 1983). 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 plant species richness that are such a distinctive feature of the environment (Palmer 1994).
A focus has been 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 they arose (e.g. Marazzi & Sanderson 2010). Thus clades with 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), are often more diverse in terms of extant species than their sister clades lacking these distinctive features. Interestingly, Malpighiales and Ericales, disproportionately common among the small trees of the understory of tropical rain forests (Davis et al. 2005a), include taxa with many kinds of flowers and fruits. 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.
It is indeed a challenge to think about the evolution of the morphological and other novelties that are the focus here. 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), and Donoghue and Sanderson (2015) and Bouchenak-Khelladi et al. (2015) look at diversification and its relation to where characters that might be involved in that diversification actually change on the tree. Indeed, Hedges et al. (2015) suggest that speciation and diversification are largely dominated by random events, while adaptive changes are something else again.
In many very speciose clades, including angiosperms as a whole, patterns of clade numbers do not suggest an immediate diversification after the acquisition of putative key innovations (see also above). Characters that seem to facilitate diversification but that evolve well before the diversification they are supposed to facilitate may be best thought of as exaptions (de Queiroz 2002; see also 2015), and this may be appropriate for several of the characters considered to be key innovations of angiosperms or of major clades within it. There seem to be no immediate changes in diversification rates when flowers evolved; these occurred later (Feild & Arens 2007). Similarly, the venation density and spacing of ANITA-grade angiosperms is rather similar to that of non-angiosperm lignophytes and their xylem with its vessels functionally not that different from that of vessel-less Pinales. 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." Flowers may become important in facilitating diversification only with the evolution of bees (Cappellari et al. 2013).
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). CYC-like genes are widely involved in symmetry changes, especially in core eudicots (X. Yang et al. 2012; Preston & Hileman 2012), but direct links remain to be established. Howarth and Donoghue (2004, esp. 2005) note possible connections between changes in such genes and changes in floral form in Dipsacales. Indeed, crown-group Caprifoliaceae-Valerianoideae may be 60-55 m.y. old (Bell & Donoghue 2005a), but diversification in the Andean paramo, which has resulted in ca 1/7th of the species currently recognized in the clade, happened less than 5 m.y.a. after their arrival in South America (Bell & Donoghue 2005b; Moore & Donoghue 2007, see also Viburnum) and 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 was probably 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.).
Key innovations are rarely simple features, rather, they may involve a complex suite of changes (e.g. Horn et al. 2012: Euphorbia subgenus Chamaesyce; Schranz et al. 2012; Donoghue & Sanderson 2015; see also Stebbins 1951). 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. 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). C4 photosynthesis, and the effects of genome duplications all fit this model.
Nearly all angiosperm characters are highly homoplastic, arising in parallel and being lost many times and characterising both large and small clades, and particular features are rarely consistently key innovations. The evolution of extra-floral nectaries may be deemed a key innovation in some Senna (Fabaceae) but the loss of such nectaries may equally be a key innovation in related taxa (Marazzi & Sanderson 2010). Similarly, Weber and Agrawal (2014) found that the acquisition of defensive metabolites increased diversification in 4/6 of the clades on which they focussed, and some wind-pollinated clades are very speciose. Parallelism and convergence, homoplasy, are everywhere one looks, even in early land plant evolution (e.g. Boyce 2010; Endress & Matthews 2012). 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 commonly occur even 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).
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 combinations; Mathews and Kramer (2012) review floral and in particular ovule development across seed plants from this point of view, and this is true of vegetative features, too, as in the distinctive leaves of the Inverted Repeat Loss Clade of Fabaceae.
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 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. Genes can be transferred via grafts in host-parasite connections, chloroplasts can move via grafts between 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!).
The idea of evolutionary "tendencies" persists (e.g. Endress & Matthews 2012), similar discussions having recurred 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, sedges and core Caryophyllales 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).
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 in which angiosperms are also involved, 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. 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 there that the environment does not change.
The evolution of the first angiosperms took place under ecological conditions rather different from those under which they prospered later; then continents were drifting apart, there were high atmospheric carbon dioxide concentrations and rising sea levels, and ever-wet tropical humid climates were rather restricted. Even if "basal" clades that are now species poor were much more diverse in their early history (Magallón & Castillo 2009; Friis et al. 2011 and references), conditions then were unlike those of today. Angiosperm-dominated vegetation is largely of Caenozoic age, so the early Caenozoic environment - warm, not seasonal, few fires, the beginning of the diversification of pollinators, herbivores and frugivores - provide the context for thinking about its evolution. Subsequent diversification occurred as temperatures and atmospheric CO2 concentrations were dropping, seasonality increasing, and, especially more recently, fires were increasing. Climate has been changing dramatically throughout the history of crown-group angiosperms, spurred by angiosperms themselves and their ECM associates (e.g. Knoll & James 1987; Volk 1989; Boyce et al. 2010).
Establishing an immediate connection between acquisition of an apomorphy or group of apomorphies and diversification is difficult. 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. 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). 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. Phylogenetic niche conservatism or 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 Caenozoic, 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 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, vascular evolution and other ecophysiologically important features like the evolution of ectomycorrhizal associations have helped shape the evolution of biomes within which diversification has occurred. Biome change continues, the evolution of extensive 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, but at various levels and contexts, species number asymmetries seem the rule.
[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: (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. 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.
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, 5-8, basally slightly connate, 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, i.e. the plants are ambophilous (Thien et al. 2003; see Culley et al. 2002 for ambophily). Stigmatic exudate may join all the stigmas of a single flower together, so pollen landing on a single stigma can pollinate ovules in more than one carpel, 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 & Ryerson 2009), 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).