Why Did Prehistoric “Trees” Grow Tall?

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 CO₂-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 deep-rooting access to nutrients and the water table are all deemed more fundamental potential drivers than light.

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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 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 CO₂ concentrations are thought to be low compared to most of the Phanerozoic (Berner, 2006). This is important because of the high sensitivity to CO₂ concentration of the Calvin cycle enzyme Rubisco, that is directly responsible for the fixation of the carbon from CO₂into 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 CO₂concentration (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 CO₂ 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 CO₂concentrations.

There have been efforts to unite the two perspectives of extrinsic CO₂ 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 CO₂ 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 CO₂concentrations declined over the Cenozoic (Brodribb & Feild, 2010). To be clear regarding the implications of this hypothesis, typical low productivity ferns – given enough CO₂ – 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. 1 mm mm⁻²seen 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 CO₂ was high, suggesting instead that these plants never had the capacity for the high productivity seen in many angiosperms, regardless of fluctuating CO₂ concentrations (Boyce & Zwieniecki, 2012). One lineage of plants did show the expected increase in minimum vein densities in leaf fossils during times of high CO₂: 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 CO₂ concentrations being restricted to just the flowering plants. Indeed, this is consistent with experiments where living plants are subjected to CO₂ elevated above modern concentrations: angiosperms can show a substantial CO₂ fertilization effect, but this effect is muted in other plants (Boyce & Zwieniecki, 2012). In general, living nonangiosperms subjected to elevated CO₂ still have assimilation rates lower than what can be seen in angiosperms with low ambient CO₂ concentrations. Whether CO₂ 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 Carboniferous, the combination of low CO₂ and high O₂would 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, CO₂concentrations 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 well-supported throughout the Paleozoic origins of tracheophyte-based vegetation.

III. Reaching for the light?

A standard interpretation of the parallel evolution of increasing stature and the tree habit in multiple Devonian tracheophyte 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 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 Archaeopterisroots.

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 CO₂, but should be particularly uncontroversial when CO₂ was low and/or stomatal 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 CO₂ and the Devonian evolution of deep-rooting trees is widely thought to have lowered CO₂ concentrations by enhancing silicate weathering. After tree evolution, plant productivity is thought to remain a key negative feedback on CO₂: more CO₂ leads to more plant productivity, which leads to more root activity and more silicate weathering, thereby dampening the original CO₂ increase (Berner, 2004). This latter feedback may have been considerably muted before angiosperm dominance.