Nitrogen-based symbioses, phosphorus availability, and accounting for a modern world more productive than the Paleozoic.

Evolution of high-productivity angiosperms has been regarded as a driver of Mesozoic ecosystem restructuring. However, terrestrial productivity is limited by availability of rock-derived nutrients such as phosphorus for which permanent increases in weathering would violate mass balance requirements of the long-term carbon cycle. The potential reality of productivity increases sustained since the Mesozoic is supported here with documentation of a dramatic increase in the evolution of nitrogen-fixing or nitrogen-scavenging symbioses, including more than 100 lineages of ectomycorrhizal and lichen-forming fungi and plants with specialized microbial associations. Given this evidence of broadly increased nitrogen availability, we explore via carbon cycle modeling how enhanced phosphorus availability might be sustained without violating mass balance requirements. Volcanism is the dominant carbon input, dictating peaks in weathering outputs up to twice modern values. However, times of weathering rate suppression may be more important for setting system behavior, and the late Paleozoic was the only extended period over which rates are expected to have remained lower than modern. Modeling results are consistent with terrestrial organic matter deposition that accompanied Paleozoic vascular plant evolution having suppressed weathering fluxes by providing an alternative sink of atmospheric CO2 . Suppression would have then been progressively lifted as the crustal reservoir's holding capacity for terrestrial organic matter saturated back toward steady state with deposition of new organic matter balanced by erosion of older organic deposits. Although not an absolute increase, weathering fluxes returning to early Paleozoic conditions would represent a novel regime for the complex land biota that evolved in the interim. Volcanism-based peaks in Mesozoic weathering far surpass the modern rates that sustain a complex diversity of nitrogen-based symbioses; only in the late Paleozoic might these ecologies have been suppressed by significantly lower rates. Thus, angiosperms are posited to be another effect rather than proximal cause of Mesozoic upheaval.

What we talk about when we talk about the long-term carbon cycle.

The terrestrial biota is a crucial part of the long-term carbon cycle via the deposition of biomass as coal and other sedimentary organic matter and the impact of plants, fungi, and microbial life on the weathering of silicate minerals. Understanding these processes and their changes through time requires both geochemical modeling of the system as well as expertise in the living and fossil biotas and their ecological interactions, but details of these components are often lost in translation between disciplines. Here, we highlight misconceptions of the long-term carbon cycle that most frequently infiltrate the literature and hamper progress: mass balance requirements, the nature and duration of perturbations, opposing timescale constraints on biological and geological processes, and the role of models.

Lepidoptera demonstrate the relevance of Murray's Law to circulatory systems with tidal flow.

BACKGROUND: Murray's Law, which describes the branching architecture of bifurcating tubes, predicts the morphology of vessels in many amniotes and plants. Here, we use insects to explore the universality of Murray's Law and to evaluate its predictive power for the wing venation of Lepidoptera, one of the most diverse insect orders. Lepidoptera are particularly relevant to the universality of Murray's Law because their wing veins have tidal, or oscillatory, flow of air and hemolymph. We examined over one thousand wings representing 667 species of Lepidoptera. RESULTS: We found that veins with a diameter above approximately 50 microns conform to Murray's Law, with veins below 50 microns in diameter becoming less and less likely to conform to Murray's Law as they narrow. The minute veins that are most likely to deviate from Murray's Law are also the most likely to have atrophied, which prevents efficient fluid transport regardless of branching architecture. However, the veins of many taxa continue to branch distally to the areas where they atrophied, and these too conform to Murray's Law at larger diameters (e.g., Sesiidae). CONCLUSIONS: This finding suggests that conformity to Murray's Law in larger taxa may reflect requirements for structural support as much as fluid transport, or may indicate that selective pressures for fluid transport are stronger during the pupal stage-during wing development prior to vein atrophy-than the adult stage. Our results increase the taxonomic scope of Murray's Law and provide greater clarity about the relevance of body size.

Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size.

Maintaining high rates of photosynthesis in leaves requires efficient movement of CO2 from the atmosphere to the mesophyll cells inside the leaf where CO2 is converted into sugar. CO2 diffusion inside the leaf depends directly on the structure of the mesophyll cells and their surrounding airspace, which have been difficult to characterize because of their inherently three-dimensional organization. Yet faster CO2 diffusion inside the leaf was probably critical in elevating rates of photosynthesis that occurred among angiosperm lineages. Here we characterize the three-dimensional surface area of the leaf mesophyll across vascular plants. We show that genome size determines the sizes and packing densities of cells in all leaf tissues and that smaller cells enable more mesophyll surface area to be packed into the leaf volume, facilitating higher CO2 diffusion. Measurements and modelling revealed that the spongy mesophyll layer better facilitates gaseous phase diffusion while the palisade mesophyll layer better facilitates liquid-phase diffusion. Our results demonstrate that genome downsizing among the angiosperms was critical to restructuring the entire pathway of CO2 diffusion into and through the leaf, maintaining high rates of CO2 supply to the leaf mesophyll despite declining atmospheric CO2 levels during the Cretaceous.

The macroevolutionary dynamics of symbiotic and phenotypic diversification in lichens.

Symbioses are evolutionarily pervasive and play fundamental roles in structuring ecosystems, yet our understanding of their macroevolutionary origins, persistence, and consequences is incomplete. We traced the macroevolutionary history of symbiotic and phenotypic diversification in an iconic symbiosis, lichens. By inferring the most comprehensive time-scaled phylogeny of lichen-forming fungi (LFF) to date (over 3,300 species), we identified shifts among symbiont classes that broadly coincided with the convergent evolution of phylogenetically or functionally similar associations in diverse lineages (plants, fungi, bacteria). While a relatively recent loss of lichenization in Lecanoromycetes was previously identified, our work instead suggests lichenization was abandoned far earlier, interrupting what had previously been considered a direct switch between trebouxiophycean and trentepohlialean algal symbionts. Consequently, some of the most diverse clades of LFF are instead derived from nonlichenized ancestors and re-evolved lichenization with Trentepohliales algae, a clade that also facilitated lichenization in unrelated lineages of LFF. Furthermore, while symbiont identity and symbiotic phenotype influence the ecology and physiology of lichens, they are not correlated with rates of lineage birth and death, suggesting more complex dynamics underly lichen diversification. Finally, diversification patterns of LFF differed from those of wood-rotting and ectomycorrhizal taxa, likely reflecting contrasts in their fundamental biological properties. Together, our work provides a timeline for the ecological contributions of lichens, and reshapes our understanding of symbiotic persistence in a classic model of symbiosis.

Arborescent lycopsid periderm production was limited.

Late Paleozoic arborescent lycopsids have been thought to have grown from sporelings into large trees through the production of a periderm cylinder, particularly massive in the proximal portion of the trunk and tapering distally, with this rind of bark providing most of their structural support. Here, we argue that physiological limitations would have prohibited the production of thick periderm and test this hypothesis using multiple independent lines of evidence derived from anatomical permineralization and surface impression fossils that allow both direct and indirect measurement of periderm radial thickness. Across all six genera of Pennsylvanian arborescent lycopsids that were investigated, all evidence indicates limited periderm production: typically < 5 cm, always < 15 cm, even in trunks that would have reached 1 m or more in diameter. The large amount of arborescent lycopsid periderm in Middle Pennsylvanian coals represents taphonomic enrichment rather than a true anatomical signal, complicating interpretation of their biology including biomechanics and early ontogeny.

No support for the emergence of lichens prior to the evolution of vascular plants.

The early-successional status of lichens in modern terrestrial ecosystems, together with the role lichen-mediated weathering plays in the carbon cycle, have contributed to the long and widely held assumption that lichens occupied early terrestrial ecosystems prior to the evolution of vascular plants and drove global change during this time. Their poor preservation potential and the classification of ambiguous fossils as lichens or other fungal-algal associations have further reinforced this view. As unambiguous fossil data are lacking to demonstrate the presence of lichens prior to vascular plants, we utilize an alternate approach to assess their historic presence in early terrestrial ecosystems. Here, we analyze new time-calibrated phylogenies of ascomycete fungi and chlorophytan algae, that intensively sample lineages with lichen symbionts. Age estimates for several interacting clades show broad congruence and demonstrate that fungal origins of lichenization postdate the earliest tracheophytes. Coupled with the absence of unambiguous fossil data, our work finds no support for lichens having mediated global change during the Neoproterozoic-early Paleozoic prior to vascular plants. We conclude by discussing our findings in the context of Neoproterozoic-Paleozoic terrestrial ecosystem evolution and the paleoecological context in which vascular plants evolved.

A left-handed fern twiner in a Permian swamp forest.

The twining habit is a climbing strategy that helps slender plants grow upward by using circumnutation around other plants. In geological history, climbing may have already been present in the first Middle Devonian forests, as indicated by possible climbers among aneurophytalean progymnosperms [1] and lycopsids [2]. By the late Carboniferous, climbing was both more common and diverse - preserved in swamp forests with modes of attachment ranging from aerial roots to appendages modified into hooks and tendrils on the leaves [3]. However, all of these diagnoses of a climbing habit are based upon either indirect morphological characteristics of the purported climber or on direct physical contact with a host plant, but without direct preservation of twining [3,4]. Permineralized epiphytes have been preserved in the Carboniferous [5], but the interpretation of scars purported to have been caused by twiners that have been found on trunk compressions of potential host-plants has been questioned [5] (see Supplemental Information). Direct preservation of a climber engaged in true twining around a host has only been documented in the Miocene Shanwang Formation of Eastern China, albeit with the identity of the twiner difficult to establish and likely to be a self-twiner [6]. Here, we report a climbing fern engaged in left-handed twining around a seed plant from the early Permian Wuda Tuff fossil Lagerstätte of Inner Mongolia, China [7]. Moreover, the host plant is likely to also be a climber based on its overall form. Such a climber-climbing-a-climber phenomenon signals the potential ecological complexity of late Paleozoic forests.

Competition for epidermal space in the evolution of leaves with high physiological rates.

Leaves with high photosynthetic capacity require high transpiration capacity. Consequently, hydraulic conductance, stomatal conductance, and assimilation capacities should be positively correlated. These traits make independent demands on anatomical space, particularly due to the propensity for veins to have bundle sheath extensions that exclude stomata from the local epidermis. We measured density and area occupation of bundle sheath extensions, density and size of stomata and subsidiary cells, and venation density for a sample of extant angiosperms and fossil and living nonangiosperm tracheophytes. For most nonangiosperms, even modest increases in vein density and stomatal conductance would require substantial reconfigurations of anatomy. One characteristic of the angiosperm syndrome (e.g. small cell sizes, etc.) is hierarchical vein networks that allow expression of bundle sheath extensions in some, but not all veins, contrasting with all-or-nothing alternatives available with the single-order vein networks in most nonangiosperms. Bundle sheath modulation is associated with higher vein densities in three independent groups with hierarchical venation: angiosperms, Gnetum (gymnosperm) and Dipteris (fern). Anatomical and developmental constraints likely contribute to the stability in leaf characteristics - and ecophysiology - seen through time in different lineages and contribute to the uniqueness of angiosperms in achieving the highest vein densities, stomatal densities, and physiological rates.

The prospects for constraining productivity through time with the whole-plant physiology of fossils.

Anatomically preserved fossils allow estimation of hydraulic parameters, potentially providing constraints on interpreting whole-plant physiology. However, different organ systems have typically been considered in isolation - a problem given common mismatches of high and low conductance components coupled in the hydraulic path of the same plant. A recent paper addressed the issue of how to handle resistance mismatches in fossil plant hydraulics, focusing on Carboniferous medullosan seed plants and arborescent lycopsids. Among other problems, however, a fundamental error was made: the transpiration stream consists of resistances in series (where resistances are additive and the component with the largest resistance can dominate the behavior of the system), but emphasis was instead placed on the lowest resistance, effectively treating the system as resistances in parallel (where the component with the smallest resistance will dominate the behavior). Instead of possessing high assimilation capacities to match high specific stem conductances, it is argued here that individual high conductance components in these Paleozoic plants are nonetheless associated with low whole-plant productivity, just as can be commonly seen in living plants. Resolution of how to handle these issues may have broad implications for the Earth system including geobiological feedbacks to rock weathering, atmospheric composition, and climate.

Phanerozoic pO2 and the early evolution of terrestrial animals.

Concurrent gaps in the Late Devonian/Mississippian fossil records of insects and tetrapods (i.e. Romer's Gap) have been attributed to physiological suppression by low atmospheric pO2 Here, updated stable isotope inputs inform a reconstruction of Phanerozoic oxygen levels that contradicts the low oxygen hypothesis (and contradicts the purported role of oxygen in the evolution of gigantic insects during the late Palaeozoic), but reconciles isotope-based calculations with other proxies, like charcoal. Furthermore, statistical analysis demonstrates that the gap between the first Devonian insect and earliest diverse insect assemblages of the Pennsylvanian (Bashkirian Stage) requires no special explanation if insects were neither diverse nor abundant prior to the evolution of wings. Rather than tracking physiological constraint, the fossil record may accurately record the transformative evolutionary impact of insect flight.

The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging.

The mesophyll surface area exposed to intercellular air space per leaf area (Sm ) is closely associated with CO2 diffusion and photosynthetic rates. Sm is typically estimated from two-dimensional (2D) leaf sections and corrected for the three-dimensional (3D) geometry of mesophyll cells, leading to potential differences between the estimated and actual cell surface area. Here, we examined how 2D methods used for estimating Sm compare with 3D values obtained from high-resolution X-ray microcomputed tomography (microCT) for 23 plant species, with broad phylogenetic and anatomical coverage. Relative to 3D, uncorrected 2D Sm estimates were, on average, 15-30% lower. Two of the four 2D Sm methods typically fell within 10% of 3D values. For most species, only a few 2D slices were needed to accurately estimate Sm within 10% of the whole leaf sample median. However, leaves with reticulate vein networks required more sections because of a more heterogeneous vein coverage across slices. These results provide the first comparison of the accuracy of 2D methods in estimating the complex 3D geometry of internal leaf surfaces. Because microCT is not readily available, we provide guidance for using standard light microscopy techniques, as well as recommending standardization of reporting Sm values.

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.

Contents I. II. III. IV. V. Acknowledgements References 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.

Stomatal design principles in synthetic and real leaves.

Stomata are portals in plant leaves that control gas exchange for photosynthesis, a process fundamental to life on Earth. Gas fluxes and plant productivity depend on external factors such as light, water and CO2 availability and on the geometrical properties of the stoma pores. The link between stoma geometry and environmental factors has informed a wide range of scientific fields-from agriculture to climate science, where observed variations in stoma size and density are used to infer prehistoric atmospheric CO2 content. However, the physical mechanisms and design principles responsible for major trends in stomatal patterning are not well understood. Here, we use a combination of biomimetic experiments and theory to rationalize the observed changes in stoma geometry. We show that the observed correlations between stoma size and density are consistent with the hypothesis that plants favour efficient use of space and maximum control of dynamic gas conductivity, and that the capacity for gas exchange in plants has remained constant over at least the last 325 Myr. Our analysis provides a new measure to gauge the relative performance of species based on their stomatal characteristics.

Delayed fungal evolution did not cause the Paleozoic peak in coal production.

Organic carbon burial plays a critical role in Earth systems, influencing atmospheric O2 and CO2 concentrations and, thereby, climate. The Carboniferous Period of the Paleozoic is so named for massive, widespread coal deposits. A widely accepted explanation for this peak in coal production is a temporal lag between the evolution of abundant lignin production in woody plants and the subsequent evolution of lignin-degrading Agaricomycetes fungi, resulting in a period when vast amounts of lignin-rich plant material accumulated. Here, we reject this evolutionary lag hypothesis, based on assessment of phylogenomic, geochemical, paleontological, and stratigraphic evidence. Lignin-degrading Agaricomycetes may have been present before the Carboniferous, and lignin degradation was likely never restricted to them and their class II peroxidases, because lignin modification is known to occur via other enzymatic mechanisms in other fungal and bacterial lineages. Furthermore, a large proportion of Carboniferous coal horizons are dominated by unlignified lycopsid periderm with equivalent coal accumulation rates continuing through several transitions between floral dominance by lignin-poor lycopsids and lignin-rich tree ferns and seed plants. Thus, biochemical composition had little relevance to coal accumulation. Throughout the fossil record, evidence of decay is pervasive in all organic matter exposed subaerially during deposition, and high coal accumulation rates have continued to the present wherever environmental conditions permit. Rather than a consequence of a temporal decoupling of evolutionary innovations between fungi and plants, Paleozoic coal abundance was likely the result of a unique combination of everwet tropical conditions and extensive depositional systems during the assembly of Pangea.

Forest productivity and water stress in Amazonia: observations from GOSAT chlorophyll fluorescence.

It is unclear to what extent seasonal water stress impacts on plant productivity over Amazonia. Using new Greenhouse gases Observing SATellite (GOSAT) satellite measurements of sun-induced chlorophyll fluorescence, we show that midday fluorescence varies with water availability, both of which decrease in the dry season over Amazonian regions with substantial dry season length, suggesting a parallel decrease in gross primary production (GPP). Using additional SeaWinds Scatterometer onboard QuikSCAT satellite measurements of canopy water content, we found a concomitant decrease in daily storage of canopy water content within branches and leaves during the dry season, supporting our conclusion. A large part (r(2) = 0.75) of the variance in observed monthly midday fluorescence from GOSAT is explained by water stress over moderately stressed evergreen forests over Amazonia, which is reproduced by model simulations that include a full physiological representation of photosynthesis and fluorescence. The strong relationship between GOSAT and model fluorescence (r(2) = 0.79) was obtained using a fixed leaf area index, indicating that GPP changes are more related to environmental conditions than chlorophyll contents. When the dry season extended to drought in 2010 over Amazonia, midday basin-wide GPP was reduced by 15 per cent compared with 2009.

Leaf fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm evolution.

Declining CO(2) over the Cretaceous has been suggested as an evolutionary driver of the high leaf vein densities (7-28 mm mm(-2)) that are unique to the angiosperms throughout all of Earth history. Photosynthetic modeling indicated the link between high vein density and productivity documented in the modern low-CO(2) regime would be lost as CO(2) concentrations increased but also implied that plants with very low vein densities (less than 3 mm mm(-2)) should experience substantial disadvantages with high CO(2). Thus, the hypothesized relationship between CO(2) and plant evolution can be tested through analysis of the concurrent histories of alternative lineages, because an extrinsic driver like atmospheric CO(2) should affect all plants and not just the flowering plants. No such relationship is seen. Regardless of CO(2) concentrations, low vein densities are equally common among nonangiosperms throughout history and common enough to include forest canopies and not just obligate shade species that will always be of limited productivity. Modeling results can be reconciled with the fossil record if maximum assimilation rates of nonflowering plants are capped well below those of flowering plants, capturing biochemical and physiological differences that would be consistent with extant plants but previously unrecognized in the fossil record. Although previous photosynthetic modeling suggested that productivity would double or triple with each Phanerozoic transition from low to high CO(2), productivity changes are likely to have been limited before a substantial increase accompanying the evolution of flowering plants.

The evolution and functional significance of leaf shape in the angiosperms.

Angiosperm leaves manifest a remarkable diversity of shapes that range from developmental sequences within a shoot and within crown response to microenvironment to variation among species within and between communities and among orders or families. It is generally assumed that because photosynthetic leaves are critical to plant growth and survival, variation in their shape reflects natural selection operating on function. Several non-mutually exclusive theories have been proposed to explain leaf shape diversity. These include: thermoregulation of leaves especially in arid and hot environments, hydraulic constraints, patterns of leaf expansion in deciduous species, biomechanical constraints, adaptations to avoid herbivory, adaptations to optimise light interception and even that leaf shape variation is a response to selection on flower form. However, the relative importance, or likelihood, of each of these factors is unclear. Here we review the evolutionary context of leaf shape diversification, discuss the proximal mechanisms that generate the diversity in extant systems, and consider the evidence for each the above hypotheses in the context of the functional significance of leaf shape. The synthesis of these broad ranging areas helps to identify points of conceptual convergence for ongoing discussion and integrated directions for future research.

An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity.

Movement of water from soil to atmosphere by plant transpiration can feed precipitation, but is limited by the hydraulic capacities of plants, which have not been uniform through time. The flowering plants that dominate modern vegetation possess transpiration capacities that are dramatically higher than any other plants, living or extinct. Transpiration operates at the level of the leaf, however, and how the impact of this physiological revolution scales up to the landscape and larger environment remains unclear. Here, climate modelling demonstrates that angiosperms help ensure aseasonally high levels of precipitation in the modern tropics. Most strikingly, replacement of angiosperm with non-angiosperm vegetation would result in a hotter, drier and more seasonal Amazon basin, decreasing the overall area of ever-wet rainforest by 80 per cent. Thus, flowering plant ecological dominance has strongly altered climate and the global hydrological cycle. Because tropical biodiversity is closely tied to precipitation and rainforest area, angiosperm climate modification may have promoted diversification of the angiosperms themselves, as well as radiations of diverse vertebrate and invertebrate animal lineages and of epiphytic plants. Their exceptional potential for environmental modification may have contributed to divergent responses to similar climates and global perturbations, like mass extinctions, before and after angiosperm evolution.