Tansley insight. Review. C. Kevin Boyce 1, Ying Fan 2 and Maciej A. Zwieniecki 3. Contents. Summary. I. Introduction

Transcription

1 Review Tansley insight Did trees grow up to the light, up to the wind, or down to the water? How modern high productivity colors perception of early plant evolution Author for correspondence: C. Kevin Boyce Tel: Received: 7 September 2016 Accepted: 6 November 2016 C. Kevin Boyce 1, Ying Fan 2 and Maciej A. Zwieniecki 3 1 Geological Sciences, Stanford University, Stanford, CA 94305, USA; 2 Earth & Planetary Sciences, Rutgers University, New Brunswick, NJ 08544, USA; 3 Plant Sciences, University of California at Davis, Davis, CA 95616, USA Contents Summary 552 I. Introduction 552 II. Productivity before the angiosperm radiation 553 V. Conclusions 555 Acknowledgements 556 References 556 III. Reaching for the light? 554 IV. Why trees? 555 doi: /nph Key words: arborescence, hydraulic physiology, Paleozoic, photosynthesis, plant ecology, root, tracheophyte, water table. Summary Flowering plants can be far more productive than other living land plants. Evidence is reviewed that productivity would have been uniformly lower and less CO 2 -responsive before angiosperm evolution, particularly during the early evolution of vascular plants and forests in the Devonian and Carboniferous. This introduces important challenges because paleoecological interpretations have been rooted in understanding of modern angiosperm-dominated ecosystems. One key example is tree evolution: although often thought to reflect competition for light, light limitation is unlikely for plants with such low photosynthetic potential. Instead, during this early evolution, the capacities of trees for enhanced propagule dispersal, greater leaf area, and deeprooting access to nutrients and the water table are all deemed more fundamental potential drivers than light. I. Introduction Modern ecology must necessarily be the foundation of our understanding of paleoecology (e.g. Behrensmeyer et al., 1992). However, modern plant ecology is largely angiosperm ecology because the flowering plants are overwhelmingly dominant in the extant vegetation. Although only present for about a quarter of land plant evolutionary history, angiosperms now make up the large majority of the biomass in most terrestrial environments and the large majority of the tracheophyte species in all of them (Kreft & Jetz, 2007). Given how distinct angiosperm physiology can be, the present flora may represent an unreliable key to the past for the 300- Myr fossil history of vascular plant ecology and physiology before the angiosperm radiation. Productivity can be a key consideration for understanding plant form and ecology, but different estimates of maximum rates of productivity can conflict wildly for any point in the geological past, including values that are both substantially higher and lower than the modern. Here, we review evidence for consistently low terrestrial productivity before angiosperm evolution and evaluate how this revises basic, widely held expectations 552

2 New Phytologist Tansley insight Review 553 regarding the early evolution of plant form and ecology that implicitly assume at least modern levels of productivity, if not substantially higher levels (Boyce & DiMichele, 2016). A particular focus will be the evolution of arborescence. II. Productivity before the angiosperm radiation Is modern productivity high or low when compared across vascular plant history? Conflicting answers have resulted from emphasis on either extrinsic environmental forcing or intrinsic plant biology. On the one hand, modern atmospheric CO 2 concentrations are thought to be low compared to most of the Phanerozoic (Berner, 2006). This is important because of the high sensitivity to CO 2 concentration of the Calvin cycle enzyme Rubisco, that is directly responsible for the fixation of the carbon from CO 2 into a reduced organic form. Thus, productivity in the geological past has been expected to have been about twice modern levels for much or most of the last 300 million yr, based upon estimates from fossils of stomatal conductance coupled to extrinsic forcing from modeling outputs of atmospheric CO 2 concentration (Beerling & Woodward, 1997; Franks & Beerling, 2009; Brodribb & Feild, 2010). On the other hand, flowering plant biology has been recognized to be distinct from that of other plants, so that it might be expected that productivity was consistently lower before angiosperm evolution (Bond, 1989; Boyce et al., 2009; Bond & Scott, 2010). In particular, stomata must close and photosynthesis halt if the water lost in gas exchange cannot be replaced quickly enough from the vasculature; thus, photosynthetic capacity will be tightly correlated with hydraulic capacity (Brodribb et al., 2007; Boyce et al., 2009; Zwieniecki & Boyce, 2014a). A higher vein density means a shorter transport path for water through high-resistance mesophyll between vein and stomata. Thus, the density of leaf veins is an important determinant of hydraulic capacity, and flowering plants have mean and maximum vein densities about four times higher than all other plants, extant or extinct (Boyce et al., 2009). Thus, past productivity might be expected to have averaged either twice or only half of modern values depending on whether extrinsic CO 2 or intrinsic biology is emphasized. However, these two literatures are not entirely in conflict. The characteristics actually measurable in fossils, vein density and stomatal traits, are congruent: stomatal conductance also was found to be substantially higher in flowering plants (Franks & Beerling, 2009), as with vein density. Therefore, differences in interpretation devolve to what is assumed about the capacity of Rubisco to accommodate and use high CO 2 concentrations. There have been efforts to unite the two perspectives of extrinsic CO 2 vs intrinsic physiology as determinants of productivity and potential drivers of plant evolution. The incorporation of leaf vein density into standard photosynthetic models based on stomatal conductance and atmospheric composition led to the suggestion that the pre-angiosperm vegetation was highly productive due to high Mesozoic CO 2 concentrations, but it was specifically the angiosperms that managed to maintain relatively high productivity via the evolution of high leaf vein density and other traits as CO 2 concentrations declined over the Cenozoic (Brodribb & Feild, 2010). To be clear regarding the implications of this hypothesis, typical low productivity ferns given enough CO 2 would be expected to have been more productive than modern sunflowers and other crops so long as they maintained leaf vein densities above c. 2 mm mm 2 ; that is, marginally above the minimum of c. 1mmmm 2 seen across vascular plant history and well within the range of possibility shared by all vascular plants. Looking to test this hypothesis, the lower bound of fossil vein densities was investigated through time and was found to be invariantly c. 1 mm mm 2, rather than increasing when CO 2 was high, suggesting instead that these plants never had the capacity for the high productivity seen in many angiosperms, regardless of fluctuating CO 2 concentrations (Boyce & Zwieniecki, 2012). One lineage of plants did show the expected increase in minimum vein densities in leaf fossils during times of high CO 2 : the angiosperms (Boyce & Zwieniecki, 2012; referring to Fig. 1 in Feild et al., 2011). Thus, the fossil record is consistent with high productivity and a strong response to CO 2 concentrations being restricted to just the flowering plants. Indeed, this is consistent with experiments where living plants are subjected to CO 2 elevated above modern concentrations: angiosperms can show a substantial CO 2 fertilization effect, but this effect is muted in other plants (Boyce & Zwieniecki, 2012). In general, living nonangiosperms subjected to elevated CO 2 still have assimilation rates lower than what can be seen in angiosperms with low ambient CO 2 concentrations. Whether CO 2 is elevated or not, both the fossil record and living plants indicate that productivity was consistently low before angiosperm evolution. Low productivity before modern angiosperms would have important implications for the evolution of plant ecology (Fig. 1). Broadly defined ecological guilds of competitor and ruderal are dependent on high productivity (Grime, 2002). Indeed, perennial herbs are abundant, but annuals are effectively absent outside of the angiosperms throughout > 400 Myr of tracheophyte history (Boyce & Leslie, 2012). With exclusively low photosynthetic potential, a smaller range of ecological strategies would be available with all plants more closely overlapping the traits associated with stress tolerance in the modern world: slow growing, long-lived forms with low reproductive output. Some modern nonangiosperms can be deemed competitors, despite low productivity per unit leaf area because of other anatomical innovations. For example, conifers can accumulate large numbers of long-lived leaves and bracken fern produces dense and decay-resistant leaf litter that prevents establishment of angiosperm seedlings. Thus, modest ecological disparity can be achieved among nonangiosperm vascular plants via anatomical disparity despite a relatively narrow range of photosynthetic potential. This mechanism may underlie the striking ecological segregation between different phylogenetic lineages seen in Carboniferous landscapes (DiMichele & Phillips, 1996): if differences in potential productivity are minimal, then phylogenetically conserved differences in anatomy can take on outsized importance in establishing ecology in a way not seen among later angiosperms that are labile in both productivity and anatomy. Even if room for debate might remain regarding the productivity of Mesozoic vegetation, agreement is widespread that productivity should have been low during the early evolution of vascular plants in the Silurian, Devonian and Carboniferous. In the

3 554 Review Tansley insight New Phytologist Maximum assimilation (µmol m 2 s 1 ) Nonangiosperms Angiosperms Stress-tolerators Competitors Ruderals Vein density (mm mm 2 ) Intensity of competition S Carboniferous, the combination of low CO 2 and high O 2 would have removed any possibility of atmospheric forcing of high productivity (Beerling & Woodward, 1997; Franks & Beerling, 2009; Boyce & Zwieniecki, 2012), so that the modern relationship between vein density and assimilation capacity should have held (Fig. 2). Before the Carboniferous, CO 2 concentrations were high, but fossil stomatal conductance estimates were so low as to prevent any expectation of high productivity (Beerling & Woodward, 1997; Franks & Beerling, 2009). Thus, low productivity is wellsupported throughout the Paleozoic origins of tracheophyte-based vegetation. III. Reaching for the light? C S A standard interpretation of the parallel evolution of increasing stature and the tree habit in multiple Devonian tracheophyte C C S R C R Intensity of stress Intensity of disturbance Fig. 1 Leaf structure, productivity and potential ecology. Upper: assimilation rates correlate with leaf vein density (replotted from Brodribb et al., 2007) due to the limitations imposed by hydraulics on gas exchange. Some gymnosperms can assimilate more than might be expected from their low vein densities due to transfusion tissue or hydrophilic fibers (Zwieniecki & Boyce, 2014b), but do not approach the maximum assimilation rates of angiosperms. Lower: with both competitor (C) and ruderal (R) strategies dependent on high productivity, the potential range of ecological strategies (redrawn from Grime, 2002) would have been limited before angiosperm evolution. For both panels, orange shading indicates the limited range accessible by nonangiosperms vs the full range accessible by angiosperms (blue). R Atmospheric CO 2 (ppm) O S D C P T J K Pg Ng (Ma) Paleozoic Carboniferous fossils Nonseed plants Calamitales Annularia (10) Asterophyllites (8) Sphenophyllales (8) Marattiales (11) Zygopteridales (3) Other eusporangiates (6) Leptosporangiate (3) Seed plants Lyginopteridales (11) Callistophytales (1) Medullosales (15) Cordaitales (5) *Duckmantian (28) * Shade Mesozoic Modern angiosperms Canopy GEOCARB III GEOCARBSULF Pioneers Cenozoic Vein density (mm mm 2 ) Fig. 2 Constraints on Paleozoic ecology from CO 2 and leaf structure. Upper: alternative modeling outputs of atmospheric CO 2 concentrations through time (replotted from Berner, 2006). Low Carboniferous CO 2 also consistent with more recent proxy and sensitivity analyses (Royer et al., 2014). Lower: vein density measurements of Carboniferous tracheophyte lineages, all from the British coal measures, with full range, median 50% (darker shading), and mean (black line). Number of sampled species included in parentheses (for details, see Supporting Information Table S1). Because the Duckmantian (or Westphalian B, equivalent to the latest Bashkirian, indicated by asterisk in upper panel) lasted < 1 Myr, this subsample of fossils approximates a single, reasonably complete vegetation. Inclusion of arborescent lycopsids would be inappropriate due to the 3D complexity of their leaves; however, low productivity is consistent with all aspects of their biology (Boyce & DiMichele, 2016). Two anomalously high sphenopsid values included here (one each in Asterophyllites and Sphenophyllales) represent scale-like, linear forms that may, or may not, have been photosynthetic. Vein density ranges for different modern angiosperm ecologies (Feild et al., 2011) included for comparison. Timescale covered in the upper panel: O, Ordovician; S, Silurian; D, Devonian; C, Carboniferous; P, Permian; T, Triassic; J, Jurassic; K, Cretaceous; Pg, Paleogene; Ng, Neogene; Ma, Myr ago. lineages is one of competition for light (Beck, 1971; Knoll & Niklas, 1987; Stewart & Rothwell, 1993; Niklas, 1997; Berry & Fairon-Demaret, 2001; Kenrick & Davis, 2004; Meyer-Berthaud et al., 2010). The original evolutionary succession, thus, is treated implicitly as an analogue of modern ecological succession with

4 New Phytologist Tansley insight Review 555 Devonian herbaceous plants equated with modern early successional herbs of exposed environments that are shaded out by later trees. With this basic assumption of benefit from sun exposure and detriment from being shaded by neighbors, the fundamental premise is that early plants were light-limited. Is light limitation a reasonable assumption? Extensive sampling of vein density in Carboniferous forests illustrates the problem: all Carboniferous plants are at or below the vein densities associated with obligate shade-requiring angiosperms in the modern world (Fig. 2). The low vein densities of nonangiosperms result in direct ecological constraints (Zwieniecki & Boyce, 2014a). Ferns have thin leaves potentially capable of high photosynthetic gas exchange, but their hydraulic constraints tend to limit them to low stomatal conductances and sheltered environments with decreased risk of desiccation, but thereby less opportunity for photosynthesis as well. (Low vein density basal angiosperms are similarly constrained (Feild et al., 2004).) Gymnosperms can endure greater sun exposure by virtue of having thicker leaves, but those thick leaves limit gas exchange potential by increasing diffusive pathlengths, preventing full use of the light received. It is only derived angiosperms with high vein density that can take thin leaves with high gas exchange potential and maintain them in direct sunlight at the top of the canopy. Thus, individual Paleozoic plants may have been better or worse at enduring full sun exposure, but none would have had the capacity to use as much of the light they received as modern angiosperms. IV. Why trees? Without competition for light, what could have driven the evolution of trees? A variety of possibilities may have contributed (e.g. Niklas, 1994, 1997; Meyer-Berthaud & Decombeix, 2007), none of which are mutually exclusive. Indeed, with trees evolving independently at least seven times by the Carboniferous (Taylor et al., 2009), a unitary explanation might even be inappropriate. Increased height is advantageous for wind dispersal of propagules (Stewart & Rothwell, 1993; Niklas, 1997). Simply being larger can also be advantageous, producing more sporangia (Kenrick & Davis, 2004) and allowing the accumulation of many long-lived leaves of low individual productivity (Bond, 1989). Some archaeopterid progymnosperms did apparently have longer-lived leaves that persisted on older branches (e.g. Beck, 1971), although other early arborescent forms were rosette trees (e.g. the cladoxylopsids, even though lacking proper fronds: Stein et al., 2007; Meyer-Berthaud et al., 2010), which tend to have lower leaf area indices (Boyce et al., 2009). In theory, an active evolutionary driver for tree evolution might not have been needed: with vascular plants starting at the lower limits of their potential body sizes (Boyce, 2008), a diversification involving random evolutionary walks would lead to passive diffusion into larger sizes. That argument, borrowed from paleozoology (Stanley, 1973; McShea, 1994), does not strictly translate to plants because trees are not simply scaled-up versions of small herbs. However, uniquely botanical arguments may apply instead: for plants, survival entails growth. Because plants have cell walls that prevent any shifting cell contacts, production of new cells requires production of new tissue and organs in peripheral meristems, not just the in situ replacement of old cells in existing tissues as in animals. Photosynthetic cells have a finite lifespan, requiring continued production of new leaves, which requires continued production of new stem. Growth can be minimized by the suppression of stem internode elongation, but it cannot be halted without leading to plant death. A palm, for example, cannot choose to stop growing once emergent above any potentially shading canopy. Thus, any transition from the ancestral rhizomatous growth to an upright axis bearing leaves or lateral branches will lead to increased height, particularly given the propensity of low productivity plants to involve longer lifespans (Grime, 2002). Vascular plants first occupied waterway margins where the water table would have been at or near the surface (Hotton et al., 2001), with water more or less permanently available. Evolutionary transitions from horizontal to upright growth may have been pivotal for expansion of vascular plant occupation to both wetter and drier habitats: in wetlands, raising photosynthetic tissues above potential gas exchange limitations from prolonged or periodic submergence (e.g. arborescent lycopsids) and, in drier environments, allowing access to lower water tables and nutrients via deep rooting (e.g. progymnosperms/seed plants). For the latter case, modern maximum rooting depths follow the depth of the water table where/when the latter is accessible (Fan, 2015), providing an important water source through periods of water stress (Naumburg et al., 2005). However, horizontal rhizomes without persistent aerial axes grow distally and senesce proximally, providing a limited window for growth of their homorhizically produced roots and, thus, a smaller maximum rooting depth. Clonal trees illustrate that the important distinction is not necessarily unipolar vs bipolar growth, but rather sustained growth in a single spot: Carboniferous Calamites was rhizomatous, but each clonal tree lived for a number of years, allowing for deep-rooting with persistent woody roots (Taylor et al., 2009). The sustained localized, vertical growth needed for a deep and permanent rootstock also results in trees and shrubs. The Devonian first appearance of deep rooting is widely associated with tree evolution (Algeo & Scheckler, 1998; Berner, 2004), but polarity of causation has never been established. Tree evolution at least in some cases should perhaps instead be looked at as a consequence of deep rooting. Some of these ideas may be evaluated with future investigations of fossil roots (e.g. Algeo et al., 2001; Pfefferkorn & Wang, 2009) that exhibit forms consistent with water table interactions as documented in living roots (e.g. Armstrong et al., 1976). Even the classic, often reproduced illustration of increasing rooting depth over the Devonian (Fig. 3 in Algeo & Scheckler, 1998) shows interaction with a deeper, but fluctuating water table in its reconstruction of the horizontal tiering of late Devonian Archaeopteris roots. V. Conclusions Before angiosperm evolution, productivity is argued to have been consistently lower than modern levels. This conclusion is supported even during times of high atmospheric CO 2, but should be particularly uncontroversial when CO 2 was low and/or stomatal

5 556 Review Tansley insight New Phytologist conductance was limiting, encompassing the entire early diversification of vascular plants and first evolution of forests. Thus, any paleontological interpretation that implicitly assumes high productivity such as an expectation of annual life cycles or biotic competition for resources such as light should be treated with caution. When considering the fossil record, analogy to the modern world is unavoidable. However, multiple competing analogies will always be available. Trees and shrubs do not exist exclusively in closed canopy forests: they also are in modern dry and seasonally dry environments that are fully open and where competition for light cannot be an issue. There, the low productivity plants that tolerate the stresses of these environments have long lifespans and, as plants, continue to grow over those long lifespans with not all of that growth being visible aboveground. A final consideration: although productivity surely matters for the ecophysiology of the plants themselves, does it also matter for the Earth system as a whole? Land plant productivity has pervasive effects on terrestrial food webs and diversity, but the influence via river runoff on evolutionary patterns in the marine biota is likely to be minimal (Boyce & Lee, 2011). A strong impact on the carbon cycle also is uncertain. First, more photosynthesis may be offset by more turnover without guaranteeing more standing biomass; that is, more productive leaves tend to have shorter lifespans (Wright et al., 2004). In any case, biomass is typically in relative steady state, so that it has no impact on the long-term carbon cycle (Berner, 2004). Second, productivity levels also should not necessarily be expected to impact rates of organic matter accumulation via burial. Organic preservation is ultimately constrained by the distribution of appropriate depositional environments, in turn determined by climate and global tectonics (Nelsen et al., 2016). However, the potential impact of plant productivity on long-term carbon cycling extends beyond biomass accumulation or preservation; the weathering of silicate rocks is an important sink of atmospheric CO 2 and the Devonian evolution of deep-rooting trees is widely thought to have lowered CO 2 concentrations by enhancing silicate weathering. After tree evolution, plant productivity is thought to remain a key negative feedback on CO 2 : more CO 2 leads to more plant productivity, which leads to more root activity and more silicate weathering, thereby dampening the original CO 2 increase (Berner, 2004). This latter feedback may have been considerably muted before angiosperm dominance. Acknowledgements S. E. Scheckler and W. A. DiMichele provided helpful discussion. This work was supported by the National Science Foundation (grant no. EAR to C.K.B. and M.A.Z.). References Algeo TJ, Scheckler SE Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events. Philosophical Transactions of the Royal Society B 353: Algeo TJ, Scheckler SE, Maynard JB Effects of the Middle to Late Devonian spread of vascular land plants on weathering regimes, marine biotas, and global climate. In: Gensel PG, Edwards D, eds. Plants invade the land: evolutionary and environmental perspectives. New York, NY, USA: Columbia University Press, Armstrong W, Booth TC, Priestley P, Read DJ The relationship between soil aeration, stability and growth of sitka spruce (Picea sitchensis (Bong.) Carr.) on upland peaty gleys. Journal of Applied Ecology 13: Beck CB On the anatomy and morphology of lateral branch systems of Archaeopteris. American Journal of Botany 58: Beerling DJ, Woodward FI Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record. Botanical Journal of the Linnean Society 124: Behrensmeyer AK, Damuth JD, DiMichele WA, Potts R, Sues H-D, Wing SL Terrestrial ecosystems through time. Chicago, IL, USA: University of Chicago Press. Berner RA The Phanerozoic carbon cycle: CO 2 and O 2. Oxford, UK: Oxford University Press. Berner RA GEOCARBSULF: a combined model for Phanerozoic atmospheric O 2 and CO 2. Geochimica et Cosmochimica Acta 70: Berry CM, Fairon-Demaret M The Middle Devonian flora revisited. In: Gensel PG, Edwards D, eds. Plants invade the land: evolutionary and environmental perspectives. New York, NY, USA: Columbia University Press, Bond WJ The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence. Biological Journal of the Linnean Society 36: Bond WJ, Scott AC Fire and the spread of flowering plants in the Cretaceous. New Phytologist 188: Boyce CK How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34: Boyce CK, Brodribb T, Feild TS, Zwieniecki MA Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B 276: Boyce CK, DiMichele WA Arborescent lycopsid productivity and lifespan: constraining the possibilities. Review of Palaeobotany and Palynology 227: Boyce CK, Lee J-E Could land plant evolution have fed the marine revolution? Paleontological Research 15: Boyce CK, Leslie AB The paleontological context of angiosperm vegetative evolution. International Journal of Plant Science 173: Boyce CK, Zwieniecki MA Leaf fossil record suggests limited influence of atmospheric CO 2 on terrestrial productivity prior to angiosperm evolution. Proceedings of the National Academy of Sciences, USA 109: Brodribb TJ, Feild TS Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13: Brodribb TJ, Feild TS, Jordan GJ Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144: DiMichele WA, Phillips TL Clades, ecological amplitudes, and ecomorphs: phylogenetic effects and persistence of primitive plant communities in the Pennsylvanian-age tropical wetlands. Palaeogeography, Palaeoclimatology, Palaeoecology 127: Fan Y Groundwater in the Earth s critical zone: relevance to large-scale patterns and processes. Water Resources Research 51: Feild TS, Arens NC, Doyle JA, Dawson TE, Donoghue MJ Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30: Feild TS, Brodribb TJ, Iglesias A, Chatelet DS, Baresch A, Upchurch GR Jr, Gomez B, Mohr BAR, Coiffard C, Kvacek J et al Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences, USA 108: Franks PJ, Beerling DJ CO 2 -forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7: Grime JP Plant strategies, vegetation processes, and ecosystem properties, 2 nd edn. Hoboken, NJ, USA: Wiley. Hotton CL, Hueber FM, Griffing DH, Bridge JS Early terrestrial plant environments: an example from the Emsian of Gaspe, Canada. In: Gensel PG, Edwards D, eds. Plants invade the land: evolutionary and environmental perspectives. New York, NY, USA: Columbia University Press, Kenrick P, Davis P Fossil plants. London, UK: Natural History Museum. Knoll AH, Niklas KJ Adaptation, plant evolution, and the fossil record. Review of Palaeobotany and Palynology 50:

6 New Phytologist Tansley insight Review 557 Kreft H, Jetz W Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences, USA 104: McShea DW Mechanisms of large-scale evolutionary trends. Evolution 48: Meyer-Berthaud B, Decombeix A-L A tree without leaves. Nature 446: Meyer-Berthaud B, Soria A, Decombeix A-L The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. Special Publications of the Geological Society of London 339: Naumburg E, Mata-Conzalez R, Hunter RG, Mclendon T, Martin DW Phreatophytic vegetation and groundwater fluctuations: a review of current research and application of ecosystem response modeling with an emphasis on Great Basin vegetation. Environmental Management 35: Nelsen MP, DiMichele WA, Peters SE, Boyce CK Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proceedings of the National Academy of Sciences, USA 113: Niklas KJ Morphological evolution through complex domains of fitness. Proceedings of the National Academy of Sciences, USA 91: Niklas KJ The evolutionary biology of plants. Chicago, IL, USA: University of Chicago Press. Pfefferkorn HW, Wang J Stigmariopsis, Stigmaria asiatica, and the survival of the Sigillaria brardii-ichthyolepis group in the tropics of the late Pennsylvanian and Early Permian. Palaeoworld 18: Royer DL, Donnadieu Y, Park J, Kowalczyk J, Godderis Y Error analysis of CO 2 and O 2 estimates from the long-term geochemical model GEOCARBSULF. American Journal of Science 314: Stanley SM An explanation for Cope s rule. Evolution 27: Stein WE, Mannolini F, VanAller Hernick L, Landing E, Berry CM Giant cladoxylopsid trees resolve the enigma of the Earth s earliest forest stumps at Gilboa. Nature 446: Stewart WN, Rothwell GW Paleobotany and the evolution of plants, 2 nd edn. Cambridge, UK: Cambridge University Press. Taylor TN, Taylor EL, Krings M Paleobotany: the biology and evolution of fossil plants, 2 nd edn. Burlington, MA, USA: Academic Press. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender- Bares J, Chapin T, Cornelissen JHC, Diemer M et al The worldwide leaf economics spectrum. Nature 428: Zwieniecki MA, Boyce CK. 2014a. Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proceedings of the Royal Society B 281: e Zwieniecki MA, Boyce CK. 2014b. The role of cellulose fibers in Gnetum gnemon leaf hydraulics. International Journal of Plant Sciences 175: Supporting Information Additional Supporting Information may be found online in the Supporting Information tab for this article: Table S1 Lineage-specific leaf vein densities of Carboniferous fossils of Great Britain Please note: Wiley Blackwell are not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. New Phytologist is an electronic (online-only) journal owned by the New Phytologist Trust, a not-for-profit organization dedicated to the promotion of plant science, facilitating projects from symposia to free access for our Tansley reviews. Regular papers, Letters, Research reviews, Rapid reports and both Modelling/Theory and Methods papers are encouraged. We are committed to rapid processing, from online submission through to publication as ready via Early View our average time to decision is <26 days. There are no page or colour charges and a PDF version will be provided for each article. The journal is available online at Wiley Online Library. Visit to search the articles and register for table of contents alerts. If you have any questions, do get in touch with Central Office (np-centraloffice@lancaster.ac.uk) or, if it is more convenient, our USA Office (np-usaoffice@lancaster.ac.uk) For submission instructions, subscription and all the latest information visit See also the Commentary on this article by Friedman, 215: